10 1016@j FBR 2015 05 001

f u n g a l b i o l o g y r e v i e w s x x x ( 2 0 1 5 ) 1 e3 5
journal homepage: www.elsevier.com/locate/fbr
Review
How do Agaricomycetes shape their fruiting

bodies? 1. Morphological aspects of development
€
Ursula KUES*, Mo
nica NAVARRO-GONZALEZ1
€ sgen-Institute, Georg-August-University G€ottingen,

Molecular Wood Biotechnology and Technical Mycology, Bu
€ sgenweg 2, D-37077 G€ottingen, Germany
Bu
article info abstract
Article history: Fruiting body formation in Agaricomycetes (Agaricomycotina) represents the most complex
Received 24 September 2014 developmental processes known in the fungal kingdom. Shapes range from simple resupi-
Received in revised form nate forms with open hymenia through to closed puff-balls and false truffles with internally
7 May 2015 hidden hymenia and include brackets and stiped mushrooms, which may have open caps
Accepted 8 May 2015 throughout or which open during development, where the hymenia cover the surfaces of
gills or pores. Mushroom shapes and features do not necessarily reflect close or distant
Keywords: phylogenetic relationships. Thus, morphological characteristics have lost some of their
Cell types former significance in taxonomy. The onset and progress of courses of processes in mush-
Development room formation are determined by the sum of various genetic, physiological and environ-
Evolution mental factors. Shapes of mushrooms can be dramatically changed by mutations and by
Fruiting body morphology adverse environmental conditions. Events in normal fruiting body formation may run in
Taxonomy parallel or behind each other in the form of ‘subroutines’ that have different degrees of inde-
Tissue differentiation pendency to each other. Alterations in details or in places and orders of distinct subroutines
and omissions can result in abnormal mushrooms. Developmental processes, time courses
and tissue structures have been described in more details for a few model species (such as
the hemiangiocarpous Coprinopsis cinerea and the gymnocarpous Schizophyllum commune)
and some species of commercial interest (e.g. the gymnocarpous Auricularia auricula-judae
and the hemiangiocarpous Agaricus bisporus). Morphological descriptions of fruiting body
development in these four species are summarized here. Agaricomycetes have relatively
large genomes with more than 10,000 different genes, many of which are expressed during
the fruiting process in specific pseudoparenchymatous tissues (plectenchyma) or possibly
only in individual cells within a tissue and at specific times. To understand the distinct func-
tions of all these genes in space and time will require very fine dissection and analysis of
distinct mushroom tissues and cells in future studies.
ª 2015 The British Mycological Society. Published by Elsevier Ltd. All rights reserved.
* Corresponding author.
E-mail address: ukuees@gwdg.de (U. Ku € es).
1
Present address: Laboratory of Fungal Biotechnology, Faculty of Chemical Engineering, Beneme rita Universidad Auto
noma de Puebla,
Cd. Universitaria 18 sur y Av. San Claudio, Col. San Manuel. 72570 Puebla, Mexico.
http://dx.doi.org/10.1016/j.fbr.2015.05.001
1749-4613/ª 2015 The British Mycological Society. Published by Elsevier Ltd. All rights reserved.
lez, M., How do Agaricomycetes shape their fruiting bodies? 1.

€ es, U., Navarro-Gonza
Please cite this article in press as: Ku
Morphological aspects of development, Fungal Biology Reviews (2015), http://dx.doi.org/10.1016/j.fbr.2015.05.001
2 U. Ku lez
€ es, M. Navarro-Gonza
1. Introduction and the Agaricomycetes (Hibbett, 2006). All three classes

contain species that form fruiting bodies. The mushroom-
Mushrooms are defined as macrofungi with epigeous (above forming species in the Tremellomycetes and Dacrymycetes
ground) or hypogeous (below ground) distinct fruiting bodies are paraphyletic jelly fungi to the Auriculariales and the Seba-
which can be seen by the naked eye and picked by hand cinales from the Agaricomycetes (Hibbett et al., 2007). The
(Chang and Miles, 1989). More specifically, the term mushroom gelatinous to cartilaginous basidiomes of Tremellomycetes
is also used for the fruiting bodies themselves, or alternatively (Bandoni and Ginns, 1998; Esser, 2000; Vizzini, 2007;
the term toadstools where these are poisonous. Some ascomy- Millanes et al., 2011; Weiss et al., 2014) and Dacrymycetes
cetes such as in the genera Helvella, Morchella, Peziza and Tuber (Sierra and Cifuentes, 2005; Shirouzu et al., 2009;
produce mushrooms but most of the large fruiting bodies Oberwinkler, 2014) are less complex structured compared to
emerge from mycelia of Agaricomycotina in the phylum of Basi- the elaborately textured fruiting bodies of most of the Agari-
diomycota, especially from mycelia of the class of Agaricomy- comycetes (Cooke and Berkeley, 1875; Breitenbach and
cetes (Breitenbach and Kra € nzlin, 1984, 1986, 1991, 1995). Kra€ nzlin, 1986, 1991, 1995; Figs 1e5). The focus of this review
Notably, fruiting bodies of basidiomycetes are the most complex is on fruiting body formation in Agaricomycetes given the
structures found in the fungal kingdom (Oberwinkler, 2012). frequency and variable complexity of the structures in this
Three distinct classes are currently distinguished in the grouping and that this grouping is the best explored from a
Agaricomycotina: the Tremellomycetes, the Dacrymycetes research viewpoint.
Fig. 1 e Selected examples of fruiting bodies of Agaricomycotina, Agaricomycetes. Gilled pileate-stipitate mushrooms of the
hemiangiocarpous agarics A. Amanita pantherina with a typical annulus enlacing the stipe, B. Laccaria laccata and C. Copri-
nellus disseminatus. Pileate-stipitate mushrooms of the gymnocarpous polypores D. Polyporus brumalis and E. Boletus luridus.
F. Sessile-pileate mushroom of the bracket fungus Ganoderma applanatum, G. resupinate basidiome of Ceriporia viridans, H.
coralloid fruiting body of Clavulinopsis corniculata, and I. gasteroid fruiting body of Calvatia sp.. Insets show photos of typical
basidia (holobasidia) with exogenous basidiospores (A., B., E., F.), overviews on pore shapes (D., G.), longitudinal section of a
complete mushroom (E.), and longitudinal (E.) and cross sections (E., F.) through trama with pores. Mushrooms were
observed in the surroundings of the Go € ttingen University and species were determined with the help of the books of
Breitenbach and Kra € nzlin (1986, 1991, 1995).

Morphology of fruiting bodies of Agaricomycetes 3
Fig. 2 e Gymnocarpous fruiting bodies of Auricularia auricula-judae on an elder twig found on the grounds of the Go € ttingen
University. A. View on the abhymenial hairy top surface (ontogenetically the lower surface, dorsal side), B. view on under-
neath surface with the smooth hymenium (ontogenetically the upper surface, ventral side), C. mushroom cross section with
distinct zones, and section views of D. Zona pilosa with hair-like cells, E. Zona compacta with difficult to distinguished
narrow hyphae, F. Zona subcompacta superioris of a network of somewhat wider hyphae, G. the gelatinous loosely inter-
woven Zona intermedia with widest hyphae which frequently undergo anastomoses and sometimes produce globose
cellular structures (possibly a kind of chlamydospores?; see insets), H. Zona subcompacta inferioris of a network of some-
what wider hyphae, I. young hymenium with sterile hyphidia and young phragmobasidia, J. mature hymenium with sterile
hyphidia and phragmobasidia, K. four-celled transversely septated phragmobasidia, and L. single- and two-celled basidio-
spores. The samples in D. to L. have been stained by 0.1 % methylene-blue aqueous solution for better contrast.
(Fig. 1AeE). Fruiting bodies are structures in which meiotic

2. General shapes spores are found. Meiotic basidiospores emerge exogenously
on short sterigmata on the basidia (Fig. 1A,B,E,F), specialized
Mushrooms of basidiomycetes differ considerably in shape cells in which karyogamy and meiosis occurs and which are
and structure. Most prominent are pileate-stipitate fruiting often produced within a hymenium, the differentiated spore-
bodies that have an umbrella-shaped cap (pileus) on a stalk forming mycelial layer. This spore-bearing layer is localized

4 U. Ku lez
Fig. 3 e Hemiangiocarpous fruiting body development of Coprinopsis cinerea. A. Progress of fruiting body development of
strain AmutBmut under standard fruiting conditions as described in Granado et al. (1997). Structures were harvested on daily
basis directly at onset of the respective 12 h light phases (indicated by the left border of the white bars; days of developmental
age are numbered by 0d to 7d). Outer views and longitudinal sections of structures are shown. K/ M / Spores denotes time
points of karyogamy (at the morning of 6d), meiosis (during the following light phase) and spore maturation (during the
following night phase). B. Enlarged view of a primary hyphal knot. C. Sclerotium that will develop from a primary hyphal
knot if cultures are kept in dark or being too old to initiate fruiting. D. Cross-section through the secondary hyphal knot. E.
Structure of a ‘dark stipe’ (overview). F. Longitudinal section through the upper third of a ‘dark stipe’ revealing an under-
developed cap and the extended stipe growth. G. Top view on the slimmer and more protruding basidia (most basidiospores
fallen off) surrounded by larger vaculoated sterile hyphidia. H. Side-views of basidia with mature basidiospores on sterig-
mata. I. Fruiting body cap in autolysis releasing spores in liquid droplets. J. Longitudinal view of a mature primordium (P5)
with fully established cap and stipe tissues. At this stage, the hymenium is fully developed and is undergoing light-induced
karyogamy. The cap is covered by a loose layer of disheveled cells of the universal veil (v) and consists of three mayor layers
of tissues (upper cortical pileipellis of dense hyphae, inner plectenchymatic trama of the pileus, lower denser cortical layer).
It is still attached to the stipe by cells of a ring-like partial veil (arrows). K. Cross-section through cap of a P5 primordium
showing adnate to adnexed primary gills (pg) with their edges with tramal plectenchyma attaching still to the stipe and

in the gilled Agaricales on the surface of the lamellae under- involve plectological differentiation. All other basidiome types
neath the mushroom’s umbrella (Fig. 1A,B) or develops in the are factual fruiting bodies and include extensive plectological
Boletales, Polyporales, and other poroid clades within the differentiation that shapes the different mushroom forms
caps as the outer hyphal sheath around pores (Fig. 1DeF) through production of varied pseudoparenchymatous tissues
which are unclosed to the ground to allow easy outwards of intertwined hyphae (plectenchyma) and that can give rise
release of the mature basidiospores. Hymenial surfaces to multiple types of intertwined hyphal cell shapes and sizes
may be exposed throughout their development and also dur- with distinct functions. The meticulous compilations of pho-
ing spore production and maturation (gymnocarp basi- tographs and drawings on mushroom structures, tissues and
diomes; Fig. 1G,H; Fig. 2B,C), or they may be protected differentiated cells in the books by Cle mençon (1997, 2004,
during development by specific mycelial layers (veils; 2012) document such variability impressively. For character
Fig. 1A; Fig. 3A,J; Fig. 4CeF,H,N) and then exposed at spore evolution studies, Hibbett (2004, 2007) applied as an alterna-
maturation (hemiangiocarpous fruiting bodies; Fig. 3A; tive a simpler system of only five major morphotypes to
Fig. 4L,M,SeU), or they may be protected throughout (angio- describe the majority of Agaricomycotina basidiomes, i.e.
carpous basidiomes; Fig. 1I). The hymenium in gasteroid ba- pileate-stipitate, gasteroid, resupinate, pileate-sessil (bracket
sidiomycetes is enclosed within an internal mycelial fungi and other forms that have a cap but no stipe),
plectenchyma (gleba) until after the spores have matured coralloid-clavariod (club or candelabra-shaped) and consid-
and are released by rupture of the peridium which is the ered some of Cle mençon (2004, 2012) types as intermediates.
outer protective layer of their fruiting bodies (Fig. 1I). Mush- Focussing on fleshy fruiting bodies, Watling and Moore
rooms can be fleshy, short-lived and easily decaying (1994) distinguish 10 basic ways as how to make a mushroom,
(Fig. 1AeC), tough, gelatinous-elastic and in dried form hard taking into account periods of hymenia inclusion and disposal
and steady (Fig. 2A,B), or they can be firm, of leathery, corky (throughout, at the beginning or at later stages of develop-
or woody appearance, and persistent (Fig. 1F; Fig. 5AeE). ment) and development of veil tissues for hymenium protec-
Certain species have fruiting bodies without stipes (Fig. 1F; tion (universal veil enveloping the whole primordium; inner/
Fig. 2A) or only very stunted stalks if at all (Fig. 5BeE,V) and partial veil connecting cap and stipe and conferring extra pro-
others with resupinate basidiomes are reduced to (crusteous) tection over the hymenium; reduced forms of veils; secondary
mycelial layers spreading on the surface of a substrate tissue development from pileus and/or stipe or basal regions
mençon (2004, 2012) groups fruiting bodies of
(Fig. 1G). Cle to enclose the hymenium or the whole primordium analo-
Agaricomycotina into nine main types, i. by general position gously to a universal veil).
of the hymenium and ii. by initial geotrophic forces acting on
the initiating hyphae of the structures (negative geotrophic:
columnar, cantharelloid, stipito-pileate, sequestrate; positive 3. Mushroom shapes in taxonomy
geotrophic: mucronelloid/hydnoid, cyphelloid; without geot-
ropism: mycelial, corticioid, dimidiate). Configurations of Formerly, the combination of the basidiome type and the
hymenophores (defined in the sense of an organ of a mush- hymenophore configuration served in a morphology-based
room bearing the hymenium; Donk, 1964) such as smooth, systematics of the clades of Hymenomycetes (now known as
tubular, lamellar or spinose are not considered in subphylum Agaricomycotina) and Homobasidiomycetes
Clemençon’s morphological classification of basidiomes, un- (now assembled together with the orders Auriculariales and
like in schemes established and used for basidiomycetous Sebacinales into the class Agaricomycetes). However, molecu-
taxonomy by other mycologist since the early days of Per- lar DNA analyses revealed the morphological criteria to be un-
soon and Fries (see historical introduction in Hibbett, 2007 reliable for taxonomy and definition of natural evolutionary
and Larsson, 2007). Fruiting body macromorphology turned positions (Hibbett, 2006, 2007; Hibbett et al., 2007). Gasteroid
however out to be a controversial criterion for cladistics, (sequestrate, secotioid) and resupinate species for instance
especially at the family level and above (Hibbett et al., 2014; have been developed multiple times within the Agaricales
see below). Orders and most families cannot be clearly and Russulales (Thiers, 1984; Hibbett et al., 1997; Peintner
defined and morphological diagnoses for taxonomy of such et al., 2001; Hibbett and Binder, 2002; Desjardin, 2003; Miller
clades have thus been omitted from the latest edition of et al., 2006; Albee-Scott, 2007; Lebel and Tonkin, 2007; Larsson
the ‘Dictionary of the Fungi’ (Kirk et al., 2011). and Jeppson, 2008; Gube, 2009; Henkel et al., 2010; Justo et al.,
mençon’s classification of basidiomes as organs car-
Cle 2010; Kinoshita et al., 2012; Lebel, 2013; Lebel and Vellinga,
rying basidia and producing basidiospores can serve to under- 2013) and reductions such as to coral and club-shaped forms
stand basic types of carpogenesis. Mycelial basidiomes are and transitions to poroid hymenophores from agaricoid
simplest with basidia produced in a more or less continuous shapes are also observed (Hibbett and Vilgalys, 1993; Pine
loose hymenium and such are of the only type that does not et al., 1999; Moncalvo et al., 2002; Matheny et al., 2006;
secondary gills with fully enclosed edges (sg), the outer edge of the pileus (p), and some disheveled veil cells (v). The arrow
points to an example of a cystidia-cystesia-bridge between two neighbouring gills. L. Enlarged view on hymenia of two
neighbouring gills with a cystidia-cystesia-bridge (arrow) born in the layer of hymenial palisade-like cells of which some will
develop into larger club-shaped basidia. The dense layer beneath are generative hyphae (subhymenium) and the more loose
plectenchyma present the inner trama of the gills. Sections in D. and J.eL. are stained by 0.1 % toluidine-blue in 0.2 M Na-
phosphate-buffer, pH 7.0.

6 U. Ku lez
Fig. 4 e Hemiangiocarpous mushroom development of Agaricus bisporus. A. Pinheads (stage 1) and B. young fruiting bodies at
the button stage (stage 2) as developed in a mushroom home grower kit. C. View of an older button stage from below at the
time the veil starts to stretch. D. View on the connection of cap margin and stipe through partial veil tissue in the late button
state and E. at the start of tearing the veil at the beginning of stage 4. F. View on inner surface of the partial veil (‘gill chamber
floor’) at the late button state and a cross-section through the stipe. Note the grooves as places where lamellae touched the
partial veil and the inner core and the broad outer tissue region of the stipe. G. Cross-section through the cap at the button
stage showing full extension of the free primary gills between pileus tissue and the stipe and shorter secondary and tertiary
lamellae in between. H. Somewhat older still closed cup (stage 3, just before entering stage 4 for tearing the veil) with
stretched partial veil in a longitudinal section revealing the whitish-beige thick inner pileus and stipe tissues, the ar-
rangements of the brown lamellae, and the annular cavity covered by a white partial veil. I. View on the outer margin of
pileus tissues and the outer melanized skin with brown melanized hyphae (from a cross-section of an older button stage). J.
View on surface of primary and secondary gills at an older button stage with maturing basidia glowing by light reflection. K.
At this stage, basidia with pairs of brownish oval basidiospores (s) in different maturity stages can already be found in

Hibbett, 2007). The lamellate pileate-stipitate genus Camaro- 2013). An extraordinary richness of shapes (coral and club-
phyllopsis is derived within clavarioid fungi (Birkebak et al., shaped basidiomes, stinkhorns, earthstars, cannon ball fruit-
2013). The lamellate hymenium has been generated multiple ing bodies, gilled and toothed sporophores, false truffles,
times and gilled species are found in the polyporoid, bolete resupinate forms) exists in the orders Geastrales, Gomphales,
and other clades outside the Agaricales (Hibbett and Hysterangiales, and Phallales of the Phallomycetidae. Occur-
Vilgalys, 1993; Hibbett et al., 1997; Vellinga, 2004; Justo and rence of the different fruiting body shapes is highly polyphy-
Hibbett, 2011; Seelan et al., 2015). Gilled species have thus letic (Hosaka et al., 2006; Giachini et al., 2010; Kasuja et al.,
been excluded from the mainly lamellate Agaricales and 2012).
poroid, gasteroid and other forms were required to be Close sister species in the agaric genus Moniliophthora pro-
included (Moncalvo et al., 2002; Thorn et al., 2005; Matheny duce typical agaricoid mushrooms with normal 4-spored un-
et al., 2006). Polyphyletic are also reductions to cyphelloid divided holobasidia (Moniliophthora perniciosa), respectively
forms with cup-to barrel-shaped or tubular fruiting bodies pseudostromal basidiomata (Moniliophthora roreri) with sporo-
that have smooth hymenophores lining the inner concave phores (interpreted as ‘modified basidia’) presenting chains
cup surface. Reductions are known from pileate gilled agarics of globose to subglobose thickwalled spores which can un-
and poroid and crust-like species. The split-gill fungus Schizo- dergo stages of meiosis and germinate like probasidia of
phyllum commune with a cyphelloid mode of hymenium pro- smuts and rusts into unusual four-celled cross-divided
duction (Fig. 5; Section 6) and Fistulina hepatica with phragmobasidium-like structures (Delgado and Cook, 1976;
hymenophores of a tubular, pore-like appearance are closest Evans et al., 2002, 2003, 2013; Aime and Phillips-Mora, 2005).
relatives (Floudas et al., 2015). Furthermore, the unique marine Resupinate basidiomes, usually with undivided holobasidia,
gasteroid Nia vibrissa originates by transformation from eua- are actually found across all major lineages of the Agaricomy-
garic cyphelloid taxa (Binder et al., 2001; Bodensteiner et al., cetes (Binder et al., 2005, 2010; Matheny et al., 2006; Miller
2004; Thorn et al., 2005). et al., 2006; Larsson, 2007; Uehling et al., 2012a,b; Birkebak
Gasteroid species exist also in mainly poroid clades such as et al., 2013). The study of Binder et al. (2010) on early lineages
the Boletales (Thiers, 1984; Hughey et al., 2000; Binder and within the subclass Agaricomycetidae (order Jaapiales) sug-
Bresinsky, 2002; Lebel et al., 2012). Gasteroid evolutions tend gests resupinate to be an ancestral fruiting body morphology
to be terminal positions of development (Thiers, 1984; Lebel from which more complex forms radiated with multiple
et al., 2012; Oberwinkler, 2012). Evolution of angiocarpous gains and losses of complex forms. A strong trend in evolu-
fruiting bodies from non-gasteroid clades correlates with tion with three- to six-fold higher likelihood seems to go to-
loss of ballistospory (Thiers, 1984; Hibbett et al., 1997; Wilson wards development of pileate-erect forms (pileate-stipitate
et al., 2011), which is the active spore discharge mechanism mushrooms, coral fungi, bracket fungi, puffballs/false truf-
employing Buller’s drops at the proximal tips of basidiospores fles), although reversions into resupinate forms are repeat-
that is innate to the basidiomycetes (Buller, 1909; Pringle et al., edly observed (Hibbett and Binder, 2002; Hibbett, 2004;
2005). Indeed, loss of ballistospory appears to be the only cri- Oberwinkler, 2012). Pileate-stipitate fruiting bodies evolved
terion shared between the diverse evolutionary lineages of several times, such as from different resupinate ancestors
gasteroid species (Reijnders, 2000). Loss of ballistospory is (Binder et al., 2010; Sjo € kvist et al., 2012) and from coralloid-
considered a reason why reversions from enclosed basi- clavariod lineages (Matheny et al., 2006; Birkebak et al.,
diomes to gymnocarp forms are not observed (Hibbett et al., 2013). Gasteroids appear to be more recent acquisitions
1997). Species with different types of fruiting bodies including from non-gasteroid ancestors, be it from gilled mushrooms,
gasteroid forms occur also in clades of the Polyporales (Wilson polyporoids or coral fungi (Wilson et al., 2011; Kinoshita
et al., 2011; Miettinen et al., 2012) e 16 transitions between et al., 2012). Evolution into gasteroid forms initially may occur
poroid and hydnoid (with teeth-like hymenium) fruiting quickly on simple genetic bases (Bruns et al., 1989; Hibbett
bodies were revealed in the Steccherinaceae alone, a family et al., 1994). However, net diversification rates of gasteroid
which contains species with resupinate, bracket-shaped and forms exceed those of the non-gasteroid forms (Wilson
also stipitate basidiomes (Miettinen et al., 2012). Cantharelloid et al., 2011). Pileate-sessile and coralloid-clavaroid shapes
and clavarioid fungi are of polyphyletic origin and nest be- appear to be the most labile forms, pileate-stipitate configu-
tween species of diverse other shapes of basidiocarps (Pine rations are relatively stable and resupinates are not particu-
et al., 1999; Binder et al., 2005; Hibbett, 2007; Birkebak et al., larly labile (Hibbett, 2004).
between resting basidioles (less clear beige-appearing cells) and developing basidoles (b; round cells of lighter colour) on the
hymenial surface of a gill. L. View on a mushroom with the partial veil torn (cup shortly after stage 4) and M. young cup stage,
giving sight on the dark-coloured lamellae developed within an inner cavity. Note the annulus of veil tissue left behind on
the stipe. N. Larger view into the annular cavity of a longitudinal section of a mushroom at the switch from button to closed
cup stage, showing the extension of free primary lamellae up to close to the stipe and the connection of the already slightly
stretched partial veil to cap and stipe. O.eR. Enlarged views of cross-sections of a cap of similar age showing O. and P. the
outer connection of primary and higher order gills with the cap tissue and Q. and R. the upmost free inner edges of primary
gills which connect at the upper side to the corticial hyphal cells lining the upper annular cavity between pileus and stipe. S.
Views on lamellae into an open cap (stage 5) of a normal mushroom and T. and U. into the open caps of conjoined mush-
rooms. Gills in the fusion zones are interconnected into convoluted plates (O.).

8 U. Ku lez
Fig. 5 e Structure of gymnocarpous fruiting bodies of Schizophyllum commune, the split gill fungus. A. Sessile mature
mushrooms grown on bark and bast of a beech trunk about 1 year after felling. B.eE. Views of a mature fruiting body (stage V
fruiting body) collected from the wild: B.,C., Upper surface, i.e. dorsal, respectively originally lower side of the structure; D., E.
view from beneath, i.e. the ventral and originally upper side of the structure showing the pseudolamellae, in B., D. dry
enrolled and C., E. moist unfolded state. Cross-sections through a mature mushroom F., G. in dry and H. moist state. Primary
pseudolamellae distinguish from secondary pseudolamellae in that they are fully divided by white thick-walled hyphae
originating from the abhymenial surface. Note in F. in the bisected mushroom the hymenium-lined tubes generated by
outward enrolling of halves of neighbouring pseudolamella. Outer edges of split pseudolamellae with white thick-walled
hyphae I. in dry and J. moist condition. K. The outer edge of mushroom tissues with bundles of abhymenial hairs is enrolled
over the youngest hymenia in a fruiting body in dry condition. L. Under moist condition, the hymenia are freely exposed on
the stretched outer edges of the mushroom. M.eP. Early developmental stages in fruiting body development: M. Hyphal
knots (stage I aggregates); N., O. young stalks (stage II aggregates); P. stalk (fully grown stage II aggregate). The structures in
M. to P. were grown in the laboratory on infested twigs of lilac and cherry in moist glass chambers at room temperature

hymenial areas (‘cauliflower’) (Raper and Krongelb, 1958;

4. Slight genetic changes can lead to new, Brasier, 1970; Schwalb, 1974, 1978). On occasions, different
completely different morphologies while large fruiting body shapes have lead to different genus denomina-
sets of genes are involved in fruiting tions of interrelated organisms. The false-truffle Rhizopogon
subcaerulescens is shown by molecular data to be a very recent
The many different blueprints that exist for formation of transition from a closely related species of the pileate-stipitate
mushrooms (Watling and Moore, 1994; Cle mençon, 1997, genus Suillus. Variations in only a small number of develop-
2004, 2012) might be taken to indicate that at a genetic level mental genes, e.g. of regulators, explain best the accelerated
different sets of genes might have evolved for the production rate of morphological changes relative to the conserved mo-
of different mushroom shapes. However, the repeated conver- lecular rate (Bruns et al., 1989). Likewise, the secotioid bolete
sion in evolution in multiple lines from one basidiocarp Gastrosuillus laricinus with enclosed mushrooms is now
configuration to another suggests this is most likely not to considered to be a recent mutant form of Suillus grevillei with
be the case. Genetic changes with such severe consequences which it shares an identical ITS sequence and with which it
might be expected to be at a regulator level, involving differen- co-occurs in location (Baura et al., 1992; Kretzer and Bruns,
tial orchestration of larger sets of developmental genes. 1997). Similar lines of evidences suggest that the hypogeous
For example, a single-gene gasteroid mutant of the gilled angiocarpous Macowanites messapicoides is a mutant of the
polypore Lentinus tigrinus (Hibbett et al., 1994) shows that a gilled Russula messapica (Martın et al., 1999).
small genetic change can result in dramatic morphological More than two decades ago, Reijnders (1991) was the first
changes and redirection from one type of basidiome into to address the question of whether ontogenic steps in devel-
another. Spontaneous gasteroid variants and a variant that opment of multicellular fruiting bodies of diverse shapes in
produces giant spherical masses with no further internal dif- the Basidiomycetes are brought about by the same processes
ferentiation were also reported for Agaricus bisporus (Fritsche, and similar genes. A most striking recent report on the
1968, 1972; Fritsche and von Sengbusch, 1969). Phenotypic var- dimorphic maize smut Ustilago maydis from the subphylum
iants with pileate-stipitate or with sequestrate fruiting bodies, Ustilagomycotina states that the fungus can form under
variably with two- or with four-spored basidia, have been discrete artificial conditions highly organized enclosed basi-
described for the agaric Inocybe multifolia (Braaten et al., diocarps with three distinct types of tissues, i.e. an outer
2013). A single mutation revoluta in the lamellated agaric Copri- layer of skeletal hyphae (i.) and an underneath layer of
nopsis cinerea resulted in a heavily convoluted brain-like cap generative hyphae (ii.) that give rise to the inner hymenium
topography with revolute pileus margins (Chiu and Moore, (iii.) with club-shaped non-septate holobasidia with four
1990). Abnormal mutants of the bracket fungus S. commune exogenous basidiospores (Cabrera-Ponce et al., 2012; Leo n-
exist in nature with dominant or recessive mutations such Ramirez et al., 2014) reminiscent of the typical basidia for
as causing loss of gill formation (‘bug’s ear’), production of instance in the Agaricales, Boletales and Polyporales of the
elongated stipe-like structures (‘medusa’) and of mycelial Agaricomycetes (Fig. 1A,B,E,F). In nature in contrast, diploid
masses with limited and irregular distributed exposed teliospores are produced from U. maydis hyphal tips in
under good ventilation and full sun light through the days. Normal development went rarely further than the stage shown in
P. when chambers were moved into shadow behind partially closed shutters. Q. and R. Under poor light conditions or poor
aeration, the hyphal tips of the stalks grow tuft-like out. S. Cushions are formed that T. when cut in two halves reveal in the
inner the stalk. U. Apical pit (stage III primordium) established under favorite conditions (light, aeration) with inwards
growth of outer hyphae to cover the central area of first hymenium formation. The inset in the left lower corner shows the
apex of a structure at the beginning of apical pit formation when the outer hyphae of a stalk grew above its inner hyphae and
thus created a dent in the center of the apex. V. View from below (ventral) on young laterally extending fruiting bodies (stage
IV fruiting bodies; from right to left: cup stage with yet no pseudolamella; young mushroom with a first primary pseudo-
lamella; young mushroom with several primary pseudolamellae) grown on a freshly cut plane of an infested branch of beech
after 5 days of incubation at room temperature with ventilation in a moist chamber in full sun light. The inset shows a
transition from the cup stage with three pseudolamellae beginning to develop at the outer edge of the mushroom. W. View
from below (ventral) on a circularly growing young mushroom forming pseudolamellae on all sides and a very young state at
initiation of pseudolamellae formation. X. View on the outer edge of a stage IV fruiting body with freshly initiated secondary
pseudolamellae. Y. Cross-section through on older mushroom stained by 0.1 % toluidine-blue in 0.1 M Na-acetate buffer, pH
4.4. A secondarily formed, already split pseudolamellae (2nd) with inner trama (t) of mostly parallel-vertically growing
stronger hyphae with air-spaces in between, the subhymenial layer of heavily cross-linked hyphae and its outer hymenial
layers of palisade cells (h) is seen in the center of the photo. The inner trama of this pseudolamella is linked to the mostly
horizontally growing hyphae in the trama of the pileus (pt). The surface of the pileus consists of the loosely grouped
thick-walled hairy hyphae (s) and underneath the pileipellis, a dense darker stained cutis (c). A younger pseudolamella (3rd)
with still closed outer edge and parts of a primary pseudolamella with throughout an inner layer of loose thick-walled hy-
phae is present at the left to the secondary pseudolamellae. The toluidine-blueestained upper inset shows an enlarged view
on a hymenium with palisade cells, some of which carry basidiospores (b), and the subhymenial cells (sh) underneath. The
lower toluidine-blueestained inset displays a view on the connection between pileus and an initially formed pseudolamella
(1st), illustrating that the layer of hairy abhymenial cells and the cutis below continue into the inner of the pseudolamella.

10 U. Ku lez
tumors in planta (Snetselaar and Mims, 1994; Banuett and nutrition, stress response, redox status, cell wall biogenesis,
Herskowitz, 1996). The teliospores overwinter and then membrane metabolism, etc., and there are also many genes
germinate to undergo meiosis and partition of the germ of unknown function (Ohm et al., 2011; Erdmann et al., 2012;
tube into four-celled transverse-divided phragmobasidia Knabe et al., 2013; Ku € es, 2015). Mushroom forming Agaricomy-
(promycelia) from which the basidiospores bud off cetes have over 10,000 genes, many of which are expressed in
(O’Donnell and McLaughlin, 1984a, b). The report by distinct stages of fruiting and need to be regulated according
Cabrera-Ponce et al. (2012) implies that U. maydis likely pos- to their precise situation (e.g. Martin et al., 2008; Pires et al.,
sesses basic gene sets for tissue formation and of basidio- 2009; Burns et al., 2010; Ohm et al., 2010; Stajich et al., 2010;
spore production in a manner as found in the majority of Anderson et al., 2012; Morin et al., 2012; Cheng et al., 2013;
the Agaricomycetes. Contrariwise, the phragmobasidia-like Eastwood et al., 2013; Plaza et al., 2014; Zhou et al., 2014;
structures observed in pseudotramal basidiomata of M. roreri Cheng et al., 2015; Ku € es et al., 2015; Ku € es and Navarro-
(Evans et al. 2002, 2003, 2013) might indicate that Agaricomy- Gonza lez, in preparation). Little is it known about how all
cetes share with U. maydis the set of genes that the smut uses these genes may contribute to fruiting. Analysis of mutants
for phragmobasidia formation. It is indeed not excluded that with defects in fruiting and of transformants with silenced
genes being appointed in normal holobasidia formation in or knocked-out genes identified further transcription factors
the Agaricomycetes are corresponding to genes being and other modulators of gene expression (Muraguchi et al.,
appointed in normal phragmobasidia formation in smuts 2008a, b; Nakazawa et al., 2010; Ando et al., 2013), gene func-
and in rusts, respectively. Actually, phragmobasidia are tions in the cell cycle (de Sena-Toma s et al., 2013; Shiyoa
observed also in basic lines of Agaricomycotina, including et al., 2013), genes for cell wall modification (van Wetter
certain in the Agaricomycetes (Fig. 2IeK; Hibbett, 2006; et al., 2000), genes in lipid metabolism (Liu et al., 2006), and
Oberwinkler, 2012). Holobasidia in contrast occur also in na- genes for enzymes with yet to define substrates and products
ture in lines of the Ustilagomycotina and in taxa of the Puc- (Muraguchi and Kamada, 1998, 2000; Arima et al., 2004).
ciniomycotina (Aime et al., 2006; Begerow et al., 2006; The canon of genes found experimentally to affect steps in
Oberwinkler, 2012) and appear to be of polyphyletic second- fruiting is steadily increasing, with functions in regulation and
ary origins (Zmitrovich and Wasser, 2012). Furthermore, sim- signaling, cell cycle control, cell wall metabolism, lipid and
ple stipitate-capitate and resupinate basidiocarps of minute membrane metabolism, secondary metabolism, and others.
size have also been described in distinct families of the Puc- A detailed account on these and on other genes of potential in-
ciniomycotina (Oberwinkler and Bandoni, 1982; Aime et al., fluence on fruiting will be presented in a follow-up paper to
2006; Oberwinkler, 2012). Larger multicellular basidiocarps this review (Ku € es and Navarro-Gonza lez, in preparation). Ge-
are known within the Pucciniomycotina from species of nomes of species with differently shaped mushrooms (jelly
the genus Septobasidium (Reid and Manimohan, 1985; Henk mushrooms, resupinate fruiting bodies, brackets, pileate-
and Vilgalys, 2007; Kumar et al., 2007). It will therefore be stipitate basidiomes; Grigoriev et al., 2013) were searched
interesting to discover how much is shared at the genetic with sequences from products of these identified genes. The
level in the production of basidiocarps between the Agarico- crude picture that arises from this analysis is that genes that
mycotina, the Ustilagomycotina and the Pucciniomycotina, act in fruiting are mostly well conserved between Agaricomy-
respectively (Ku € es and Navarro-Gonza lez, in preparation). cetes, to certain degrees in Tremellomycetes and Dacrymy-
Mating-type genes encoding homeodomain transcription cetes and the dimorphic smut U. maydis, and to low degrees
factors and pheromones and pheromone receptors, respec- in yeast-like Ustilagomycotina and Pucciniomycotina and in
tively are known to be master regulators of initiation of fruit- the ascomycete Neurospora crassa that was included in the
ing body development and control of fruiting body maturation study as a representative of the second branch of dikarya
(Tymon et al., 1992; Ku € es et al., 1998, 2002b). In accordance, (Ku€ es and Navarro-Gonza lez, in preparation). The data sup-
genes in the mating-type pathways and in communication be- port the notion of Stajich et al. (2009) that multicellularity
tween the mating-type loci also play a role (Ku € es, 2015; Ku
€ es and tissue differentiation in the Dikarya developed indepen-
and Navarro-Gonza lez, in preparation). Inactivation of dently in the basidiomycetes and in the ascomycetes (Labbe
selected genes for other transcription factors fully blocked or et al., 2014).
arrested development in S. commune at early stage in some
cases and enhanced frequencies in initiation in others (Ohm
et al. 2010, 2011). Inactivation or alterations of elements of 5. Environmental and physiological influ-
additional signaling pathways such as of light or of nutrient ences on mushroom shapes
sensing lead also to blocks in developments, increase in initi-
ation of fruiting or in some instances to morphological As discussed above, molecular phylogeny indicates that
changes (Bottoli, 2001; Yamagishi et al., 2002, 2004; mushroom shapes and stipe, pileus, and hymenium mor-
Terashima et al., 2005; Schubert et al., 2006; Srivilai, 2006; phologies are highly plastic characters. Environment and
Kuratani et al., 2010; Stajich et al., 2010; Nakazawa et al., prevailing physiological conditions determine generally
2011; Ohm et al., 2013; Knabe et al., 2013). Multiple sets of genes whether fruiting body development will initiate and
are affected in expression by the mating-type genes, by € es and Liu, 2000; Ku
whether it will complete (Ku € es and Nav-
fruiting-regulating transcription factors and by inter-related arro-Gonza lez, in preparation). They may play further
signaling pathways. These genes belong to multiple func- important roles in the expressed morphological phenotype
tional categories such regulation, signaling, energy and of a mushroom.

Plasticity of mushroom shapes within species Badalyan et al., 2011). Hybrid caps with lamellae with bulbous
bodies and lamellae with typical basidia and basidiospores
Bracket fungi such as Bjerkandera adusta, Irpex lacteus, Heteroba- observed in culture of a same strain identify them to be alterna-
sidion annosum or Phellinus vorax may form resupinate or inter- tive final routes of basidiome development (Navarro-Gonza lez,
mediate effused-reflexed basidiomes as an alternative to 2008). Another case of modified sterile basidiomes with spore-
pileate fruiting bodies (Donk, 1964; Breitenbach and less heads of structured tissues (known as stilboids) concerns
Kra€ nzlin, 1986), indicating a less strict routine of development the agaric Mycena citricolor and its anamorph Decapitatus flavidus
and flexibility for morphological adaptations. Other species mençon, 1997, 2004, 2012; Redhead et al., 2000). Nothoclavu-
(Cle
such as the corticoids Corticium bombycinum and Corticirama lina ditopa is an anamorphic version of the agaric Arthrosporella
sp., the polyporoid Hyphoderma setigerum, or Pterulicium xylo- ditopa and forms pileus-free clavaroid structures that bear ar-
gena and Parapterulicium subarbusculum from the Agaricales throspores on their surface as do the stipes of normal-shaped
can produce both resupinate and clavaroid fruiting body mushrooms with pileus (Singer, 1986; Stalpers et al., 1991).
forms, possibly as a local response to gravity (Donk, 1964). Spontaneous errors of tissue conjoining between caps of
Monstrous spherical fruiting bodies with irregular hymenial two distinct structures might be a cause for twin mushrooms
tubes all over the surface occur in nature in the polypore Abor- with split stipes observed in various agarics and boletes
tiporus biennis as well as the more common fan-shaped struc- (Magnus, 1906; Buller, 1922; Ulbrich, 1933b; Umar and Van
tures with pores underneath the caps (Buller, 1922). Multiple Griensven, 1997a), such as in the case of the A. bisporus fruiting
mushroom shapes in unusual large sizes (fleshy stipes with bodies shown in Fig. 4T,U whose lamellae are manifold
underdeveloped caps, stunted fleshy caps) were observed in dysplastic interconnected. Twin-mushrooms bifurcated at
nitrogen-rich manure bed cultures of the in nature normally their common base of stems have been described in nature
slender, long-stemmed and gilled fairy ring fungus Marasmius for the bird’s nest fungus Cyathus stercoreus (Brodie, 1977).
rufescens (Buller, 1922). Types and amounts of carbohydrates Furthermore, individuals of A. bisporus, Laccaria laccata, Pholiota
define the complexity of branching patterns in ranks and squarrosa, Tricholoma nudum, and Clitocybe nebularis were
whorls on the main axis of the clavarioid fruiting bodies of recorded where (partially) inverted gilled caps and also whole
Artomyces pyxidatus from the Agaricales. Abnormal swollen inverted mushrooms grow on top of the pileus of otherwise
plump non-branched fruiting bodies appear in cultivation on normal fruiting bodies (Magnus, 1906; Buller, 1922;
arabinose and sucrose (James and McLaughlin, 1988). Buschmann, 1960; Ramel et al., 1998; Umar and van
Abnormal gasteroid and morchelloid forms were observed Griensven, 1999). Double and triple mushrooms mounted up-
in nature for the agarics Galerina pseudomycenopsis and Psilo- right in pagoda-like manner are documented from nature in
cybe semilanceata (Watling and Martın, 2001, 2003) and along- the agarics Agaricus procereus, Lepista nuda, and Melanoleuca mel-
side to normal pileate-stipitate fruiting bodies in pure aleuca, from Clitocybe species, and in several Cyathus and Nidula
laboratory cultures of the agarics Volvariella bombycina (Chiu bird’s nest fungi (v. Wettstein, 1887; Magnus, 1906; Buller, 1992;
et al., 1989), Psilocybe coprophila (McKnight, 1953), Psilocybe mex- Brodie, 1958; Ramel and Webster, 1995; van der Aa, 1997).
icana (Singer, 1986) and Psilocybe merdaria (Watling, 1971).
Abnormal morchelloid forms occur in nature also in Clitocybe, Mis-shaping by environmental stress
Collybia, Hydrocybe, and Tubaria species, Amanita pantherina,
Hygrophorus nemoreus, and several other agarics, as well as in Rosecomb is a syndrome of the button mushroom A. bisporus
Boletales such as Paxillus involutus (Ulbrich, 1926, 1933a; and other agaricoid species (e.g. Psilocybe cubensis) observed
Benedix, 1967). Agaricoid fruiting body variations with opened upon exposition to environmental stressors (e.g. exposure to
lamellated caps and stipes can appear in pot cultures of the mineral oil fumes or mechanical damage to the partial veil
ectomycorrhizal species Hydnangium sublamellatum whereas (velum partiale) of developing primordia) that results in large
in field collections of the holotype angiocarpous truffle-like hordes of malformed mushrooms with split stipes and with
mushrooms were evident with an internal heavily convoluted mis-shaped and -located lamella and caps and even convo-
hymenium and a small bulbous stipe tightly clasped by the luted pore-like hymenia (‘lamellar dysplasia’) on the pileus
enclosed cap (Bougher et al., 1993). surface (Magnus, 1906; Stamets and Chilton, 1983; Flegg and
Wood, 1985; Umar and Van Griensven, 1999; Noble et al.,
Mis-shaping by physiology and formation of sterile structures 2003). Elevated CO2 concentrations lead in the agaric Pleurotus
ostreatus and allies to size reductions and deformations of caps
Normal-shaped pileate-stipitate mushrooms together with a and to elongated stipes, eventually also to thickened plump
multitude of mis-shaped fructifications with split stipes, with short stipes with cap rudiments (Kinugawa et al., 1994; Jang
stipes that punch the caps and continue to grow above the et al., 2003; Kong, 2004). Slender elongated stipes with reduced
cap, and with split, crippled and otherwise deformed caps are pilei were also observed under higher CO2 concentrations in
observed in cultures of a Coprinellus species (Navarro- cultures of other agarics including the edible A. bisporus
Gonza lez et al., 2006; Navarro-Gonza lez, 2008). Some species (Stoller, 1952; Turner, 1977; Flegg and Wood, 1985), Flammulina
such as the agaric Coprinopsis clastophylla give rise in nature velutipes (Kinugawa et al., 1994), Hypholoma capnoides (Gramss,
and also in pure culture to sterile fruiting-body-like structures 1978), and Lentinula edodes (Jablonsky , 1981), as well as of
(described under the anamorph name Rhacophyllus lilacinus) stipitate-pileate polypores (Plunkett, 1956). Larger undifferen-
that instead of basidia and basidiospores contain large bulbous tiated spherical aggregates (Fig. 5QeT) arise under CO2 stress
bodies (Maniotis, 1964; Pegler, 1986; Cle mençon, 1997, 2004, in the bracket fungi S. commune (Volz and Niederpruem,
2012; Redhead et al., 2000; Navarro-Gonza lez et al., 2006; 1970) and Grifola frondosa (Gramss, 1978). Another interesting

12 U. Ku lez
example of phenotypic plasticity was observed in Lentinellus short-lived mushrooms in C. cinerea and F. velutipes to put caps
cochleatus. At low temperature, this fungus from the Russu- and gills back into desired position (Moore, 1991; Haindl and
lales produces coralloid fruiting body forms instead of Monzer, 1994; Greening et al., 1997; Kern et al., 1997). To the
pileate-stipitate gilled mushrooms (Miller, 1971; Hibbett, same end, many fallen bracket fungi simply grow out in right
2007). High humidity allows in the bracket fungus Gloeophyl- direction to earth a new conk from the elder mushroom
lum sepiarium substantial formation of upturned irregularly (Buller, 1922; Kaneko and Sagara, 2001; Bunyard, 2012). Envi-
folded hymenophores over an underdeveloped cap (States, ronmental plasticity by gravity is further documented by the
1972, 1975). Multiple layers of interfolded lamellated lobes loss of the dorsiventral directionality of mushrooms in the
arise under humid weather on caps of Clitocybe species bracket Pycnoporus cinnabarinus under clinostat conditions.
(Benedix, 1960, 1967). Weather conditions can be responsible Instead, pulvinate aggregates fully covered with the tubular
for abnormal development, for example cold temperature hymenophore were obtained. Also under clinostat-growth,
can result in the production of sporeless pale mushrooms in the normal gill location in S. commune reversed from the
several species of Strophariaceae (Watling and Martın, 2003). ventral to the dorsal surface (Hasselbring, 1907).
Insufficient illumination can also result in the production
of slender elongated stipes with no or only underdeveloped Mis-shaping by biological infections and injuries
spore-free pilei in various agarics (Fig. 3E,F; Rogers, 1973;
Triratana, 1976; Kaneko and Sagara, 2002; Sakamoto et al., Transmissible virus infections have been deduced to be
2004, 2007; Chaisaena, 2008; Miyazaki et al., 2011) as well as another cause for mis-placements of hymenia to the upper
in pileate-stipitate Polyporales (Buller, 1905, 1909; Kitamoto surface of caps, for instance in the agarics Armillaria mellea,
et al., 1968; Horikoshi et al., 1974). Neolentinus suffrutescens of Laccaria amethystina and Pholiota mutabilis (Blattny et al., 1971,
the Polyporales thereby shows an extraordinarily morpholog- 1973). Infections by the mycopathogenic ascomycete Lecanicil-
ical flexibility with which it reacts on insufficient light. The lium fungicola is cause of dry bubble disease in A. bisporus cul-
species not only gives rise to elongated stipes with no, rudi- tures that among other symptoms leads to bent or split stipes
mentary or abnormal caps but also to multiple branched (blowout) and outgrowth of infected structures into a spher-
stipes with epileate apexes or with rudimentary pilei with or ical mass of host and pathogen hyphae with little or no tissue
without aborted gills (Buller, 1905; Lingelsheim, 1917). These differentiation (Largeteau and Savoie, 2008, 2010). Mycogone
highly branched structures have been assessed by shape as perniciosa is a parasitic ascomycete that can bring about a
clavaroid fruiting bodies (Pine et al., 1999). Antler-like mis- wet bubble disease with severe malformations of A. bisporus
shaped fruiting bodies may be produced by S. commune in mushrooms (Umar and Van Griensven, 1999). Attack of the
weak light (Ju € rgens, 1958). The polyporous species Grifola fron- mycopathogenic ascomycete Hyphomyces lactifluorum has
dosa misses in dark to form the large cluster of multiple caps been described by Buller (1922) to suppress gill formation in
on the mycelial aggregate serving in light as base to the Lactarius piperatus underneath the caps. Based on molecular
normal cluster of caps (Miyazaki et al., 2011). Abnormal orbic- and microbiological data, individuals of the stipitate Gastro-
ular caps covered throughout with interlacing gills were cybe lateritia with gelatinous, hardly or never expanding caps
observed under continuous illumination in cultures of the observed in nature are now considered to be specimens of a
lamellated L. tigrinus (Bobbitt and Crang, 1974, 1975). pileate-stipitate Conocybe species in the section Candidae that
Gravity also has morphogenetic effects. A change in direc- are just abnormal since diseased by a bacterium Chryseobacte-
tion of specimens can bring about more or less drastic trans- rium sp. (Hallen et al., 2003; Hausknecht and Krisai-Greilhuber,
formations. Swelling and tilting of gills has been observed in 2006). Other reported incidences of mal-formation in nature
the agarics F. velutipes, Hypsizygous marmoreus and Hebeloma include creation of aberrant puffball-like structures of the
radicosum, swelling and waving of caps in F. velutipes and H. pileate-stipitate Entoloma abortivum induced by growth in hy-
marmoreus and stipe twisting in F. velutipes (Kaneko and phal alliance with A. mellea sensu lato (Watling, 1974) or, as
Sagara, 2001, 2002). P. ostreatus reacts with de- and redifferen- reinterpreted in younger literature, rather by remodeling the
tation of gills: Mesh-like shallow gills arise on swollen stipes normally also pileate-stipitate Armillaria fruiting bodies
when caps are directed downwards, new shallow gills can through intrusion of hyphae of E. abortivum (Czederpiltz
appear on the morphologically upper surface of caps, the fruit- et al., 2001). Species of the agaric genus Squamanita parasite
ing body may bend to adjust gills into a right position, and on basidiocarps of a number of other agarics, deform the hosts
eventually, new primordia may develop on tissues of the older and induce gall formation, and on occasion chimeric mush-
structure (Kaneko and Sagara, 2001). Lenzites betulina also de- rooms arise (Ba € ßler, 1959; Redhead et al., 1994; Matheny and
velops new primordia on older tissue and gills proliferate in Griffith, 2010; Leach, 2013; Cortes-Pe
rez et al. 2014).
a morchelloid honeycombed manner (Lohwag, 1955). A. bispo- Injuries can also lead to malformations. Loss of the veil
rus responds on change in direction with one-sided extension covering the hymenial chamber in young developing A. bispo-
growth and structural splitting of the stipe in order to achieve rus structures for example favours irregular outgrowth of
via a strong stipe curvature a lifting back of parts of further pore-like hymenia instead of the normal lamellar plates
developing gills into the vertical position envisaged for spore with outer layers of hymenia (Umar and Van Griensven, 1999).
release. Those parts of the caps situated at the non-extended
side of the stipe abort to give the required space for sufficient Subroutines in mushroom formation
bending of the stipe by the inequal outgrowth (Moore, 1998b).
Gravitrophic bending by differential length increase of cells in The many examples of broad variation and plasticity in mac-
the lower half of horizontally placed stipes is observed for the romorphology within a species and even within individuals

indicates once again that the morphological manifestation of and Esser, 1976; Prillinger and Six, 1983) and loosely aggre-
developmental variants are likely to be the result of a differen- gated hyphal tufts with two-spored basidia on the surface in
tial interplay of an extant larger set of genes acting in steps monokaryotic cultures of G. sepiarium (States, 1975). Basidia
within the complex program of mushroom formation. Fungal may even evolve directly from little differentiated vegetative
morphogenesis is evidently organized in an array of indepen- mycelium as has been observed for instance in A. mellea
dent but coordinated developmental processes that have been (Kniep, 1911) and G. sepiarium (States, 1975). Mycelia of the
called ‘subroutines’ by Moore and colleagues (Chiu et al., 1989; agaric Lyophyllum tylicolor directly developed basidia and ba-
Moore, 1998a). These subroutines can run in parallel or in sidiospores on special broad hyphae (resembling hyphae of
sequence and the order of which determines the final the inner plectenchymatic trama of the lamella) when culti-
outcome. Subroutines can be defined on different levels e vated in dim light on glass slides (Yamanaka and Sagara,
development of specific organs (such as cap or stipe or gill 1990). Without forming a typical basidiocarp with cap and
etc.), different types of tissues within an organ (outer cortical stipe, basidia with basidiospores emerged on further undiffer-
layer, inner trama, etc.), different cell types (such as fertile entiated mycelial aggregates of the pileate-stipitate M. perni-
basidia, sterile hyphidia as little modified terminal hyphae ciosa (Bastos and Andebrhan, 1987). An example of fruiting
in the hymenium, sterile cystidia, etc.) and even cell compo- in culture of a naturally resupinate species is available with
nents (e.g. nuclei) with regards of one-, two- or threedimen- Phellinus contiguus grouping within the Hymenochaetales.
sional directions of growth (Moore, 1998b). They are Normal and abnormal poroid hymenophores formed on agar
genetically determined but can physiologically as well as envi- in upside-down incubated Petri dishes, thick irregular aggre-
ronmentally be influenced. Omissions of one or the other sub- gated tissue in upwards placed Petri dishes, indicating in
routine or chances within a subroutine will not inevitably fully this species an effect of gravity on the choice of tissue differ-
break down the whole process of fruiting whose ultimate bio- entiation. Poroid tissues and hymenium construction in agar
logical target is genetic recombination and the production of cultures did not differ from those of specimens from nature
meiotic basidiospores. Noteworthy for commercial mush- but a characteristic mycelial layer (subiculum) beneath the
room cultivation, a block in basidiospore production for tubes and typical basidiome margin tissues were missing in
example can still give perfectly shaped mushrooms and these artificial culture (Butler, 1988, 1992a, 1995; Butler and Wood,
can overcome the problems of spore-induced allergies for 1988). Light was required for pore tissue formation and pro-
mushroom growers and consumers (Hasebe et al., 1991; Ku € es duction of sterile, pointed and thick, brown-walled hyphal
et al., 2007; Okuda et al., 2013). ends termed seta (‘stiff hairs’) and of fertile basidia with basid-
Degrees of independency of subroutines in fruiting may be iospores (Butler, 1992a,b, 2000).
recognized in artificial cultures. Under poorly understood
environmental constraints in artificial culture, no or only
initial parts of the complex tissue differentiation programs 6. Tissue and cell differentiation
of complete fruiting body development might occur that nor-
mally culminate in meiosis and basidiospore formation. This As much as the macromorphology of mushrooms can differ
might not be too surprising considering the fact that particu- between species (Fig. 1), the micromorphology can differ
even more (Cle mençon, 1997, 2004, 2012; Breitenbach and
larly later stages in fruiting involving basidium differentia-
Kra€ nzlin, 1986, 1991, 1995, Fig.s 2 and 3). Bistis et al. (2003) list
tion, karyogamy, meiosis and basidiospore formation are
most complex energy- and nutrient-demanding processes 15 different cell types for the sexual phase of the ascomycete
(Straatsma et al., 2013). As a result of intense research efforts, N. crassa, starting from the first cell (ascogonium) initiating
the number of species that can be successfully induced to fruit the fruiting process to the complete description of the mature
and produce normally shaped mushrooms in culture is fruiting body (i.e. a perithecium with asci and ascospores in its
steadily increasing (Yamada et al., 2001; Yamanaka, 2005; inner). We are not aware that for any of the Agaricomycotina
Ru€ hl and Ku € es, 2007; Flores et al., 2008; Fu et al., 2011; such an account of cells occurring during the whole develop-
Pleszczyn ska et al., 2013; Colavolpe and Alberto, 2014). Howev- mental process of fruiting and in the mature basidiocarp has
er, also only later parts of the complete routine might occur in ever been made. However, the descriptions of selected species
culture. For example, atypical cap-less fruiting structures below reveal that many more cell types are often involved in
(AFSs) with an unusual coralloid and incomplete poroid resu- fruiting body formation in the Agaricomycetes.
pinate hymenial tissue with basidia and basidiospores arose
from mycelia in artificial agar culture of several strains of Auricularia auricula-judae, Auriculariaceae, Auriculariales,
the bracket fungus Ganoderma lucidum (Seo et al., 1995a,b). Auricularomycetidae
‘Sparassis’ types of abnormalities (named after the unique
brain-like shape of the cauliflower mushroom Sparassis crispa Looking at a comparably simple-structured matured mush-
and allies) refer to flat erect, more or less tightly packed and room such as of the gelatinous dorsiventral constructed
involuted plates of hymenophores that can emerge in several Auricularia auricula-judae from the Auriculariales (Fig. 2), six
polyporous species directly from a common primordial hy- different tissue layers are apparent in cross-sections of the
phal aggregate without the development of any characteristic mature fruiting bodies (Fig. 2C): i. a rough zone of hairs on
pileus (Cartwright, 1929; Siepmann, 1970; States, 1975). Clav- the upper abhymenial surface (Zona pilosa, presenting the
arioid and coralloid erect structures and resupinate poroid hy- dorsal, i.e. ontogenically lower surface; Fig. 2A,D), ii. a very
menia were further observed in cultures of monokaryons of compact zone of difficult to distinguish narrow elements
the normally pileate-stipitate species Polyporus ciliatus (Stahl (Zona compacta; Fig. 2E), iii. a zone of less compact

14 U. Ku lez
plectenchyma of wider hyphae in a gelatinous matrix (Zona conditions including a period of illumination, primary hyphal
subcompacta superioris; Fig. 2F), iv. a zone of loose plecten- knots will alternatively pursue the pathway of fruiting
chyma of widest hyphae (in our specimen with sometimes (Kamada et al., 1978; Moore, 1981; Ku € es et al., 1998, 2002b).
swollen round cells at the hyphal ends; Fig. 2G insets) in a Although fruiting body development can be induced on plain
gelatinous matrix (Zona laxa intermedia; Fig. 2G), v. another vegetative mycelium, some strains can produce mycelial
zone of more compact plectenchyma of wider hyphae (Zona strands that as anchors in substrate may favor initiation of
subcompacta inferioris; Fig. 2H), and vi. the hymenium fruiting body development (Badalyan et al., 2011).
formed by palisades of sterile little modified hyphidia (in liter- In subsequent fruiting body development, further branch-
ature often referred to as paraphyses) and young or mature ing and hyphal swelling occur, aggregation of hyphae and also
four-celled transverse septated phragmobasidia (Fig. 2IeK) anastomosis (fusion of hyphal cells) to finally result in a dense
with single-celled or septate basidiospores (Fig. 2L) found on globose structure (secondary hyphal knot/secondary nodule,
the lower smooth hymenial surface of the mature mushroom ca. 0.2 mm in Ø; see Fig. 3A,D). The core of the secondary hy-
which corresponds to the ventral, i.e. ontogenically upper sur- phal knot consists of tightly interwoven and heavily
face (Fig. 2B; Lowy, 1951, 1952; Esser, 2000; Musngi et al., 2005). branched, still unspecialized hyphae of firstly more or less
From this overview documented in Fig. 2, at least 8 up to 15 uniform appearance. It is covered by a coat (basically a young
different cell types contribute to the mature mushroom struc- universal veil) of larger outward directed vacuolated hyphae
ture of the jelly fungus A. auricula-judae. Further cell types (Matthews and Niederpruem, 1972; van der Valk and
occur during development. Fruiting body formation is gymno- Marchant, 1978; Muraguchi et al. 1999; Liu, 2001; Velagapudi,
carpous and divides into five stages: i. formation of a first 2006; Lakkireddy et al., 2011). Hyphal cells in the knot can
tightly arranged hyphal patch (2e5 mm in diameter), ii. con- lack clamp cells at their septa, have reduced chitin content
version into a 2e7 mm-sized ball-form stage of two types of and an altered helical arrangement of chitin microfibrils in
inner irregularly intermingled trama hyphae within a brown the cell walls (Kamada and Tsuru, 1993). Within the upper
gelatinous mass and an outer layer of white hairs, iii. the core of the secondary hyphal knot (in older literature some-
pileus-initiating stage giving rise to a violet-brown gelatinous times called initial or also undifferentiated primordium or pri-
head that replaces the white hairs (‘pileus initial’), iv. the mordial bud; van der Valk and Marchant, 1978; Lu, 1974a;
pileus-forming stage in which the gelatinous head expands Moore et al., 1979; Ku € es, 2000), cap and stipe tissue differenti-
into a concave form of which the upper surface becomes the ation starts in approximate isocarpous manner (i.e., all tissue
hymenial layer, and v. the pileus-maturing stage in which differentiation occurs at more or less the same time;
the non-differentiated trama hyphae reorganize into distinct Matthews and Niederpruem, 1973).
zones of the basidiocarp. Basidia are formed only in the It is difficult to compare reports and provide precise details
pileus-maturing stage (Cheng and Tu, 1978). When the mush- of further stages in development from the scientific literature.
room extends further in size, the originally upper located, This is due to the use of subjective time frames and reference
ventral hymenium eventually will become positioned to the points and periods of observation, imprecise definitions of
bottom and the originally lower, dorsal abhymenial surface timings, incomplete accounts of development, difficulties to
to the top, relative to the earth (Fig. 2A,B). recognize early stages, poor dissections into distinct steps,
overlapping and confusional nomenclature even between pa-
Coprinopsis cinerea, Psathyralleceae, Agaricales, pers of same authors, and possibly also the fact that cultures
Agaricomycetidae contain with time many aborted stages of different develop-
mental phases. Different culture conditions and different ge-
In other species, there are definitely more cell types. Fruiting netic backgrounds may also play a role (Tsusue , 1969; Iten,
body development of the best studied hemiangiocarpous 1970; Kamada et al., 1978; Moore et al., 1979; McLaughlin,
agaric model mushroom C. cinerea (previously reviewed by 1982; Rosin and Moore, 1985a,b; Hammad et al., 1993a; Ku € es,
Moore et al., 1979; Moore, 1998a; Ku € es, 2000; Kamada, 2002) 2000; Lu, 2000; Liu, 2001; Liu et al., 2006). Starting from the un-
starts with a loose microscopic small hyphal agglomeration differentiated secondary hyphal knots, two to four days are
(primary hyphal knot/primary nodule, ca. 0.1 mm in size; variably given in the literature as times required for comple-
Fig. 3A,B). The primary hyphal knot is formed on a single or tion of primordia formation or, quite often, timing and kinds
a few neighbouring vegetative hyphae by localized intense of early events are left open (Borris, 1934; Takemaru and
production of multiple randomly oriented short hyphal Kamada, 1972; Morimoto and Oda, 1973; Kamada et al., 1978;
branches that show restricted tip growth (Matthews and Moore et al., 1979; Ballou and Holton, 1985; Muraguchi and
Niederpruem, 1972; Boulianne et al., 2000; Liu, 2001; Kamada, 1998; Boulianne et al., 2000; Ku € es, 2000; Lu, 2000;
Lakkireddy et al., 2011). Considering this very initial stage, Kamada, 2002; Walser et al., 2003; Ku € es et al., 2004; Liu, 2001;
there are thus already two or more different cell types Kamada et al., 2010; Shioya et al., 2013).
involved: a single or more main hyphae of indefinite unidirec- According to our current understanding deduced from ob-
tional growth that locally bear in three-dimensional manner servations on series of hundreds of cultures grown under
short stunted side branches of first and higher orders with standard fruiting conditions (Granado et al., 1997) of the self-
irregular inflated hyphal cells. Primary hyphal knots arise in compatible C. cinerea homokaryon AmutBmut (Swamy et al.,
cultures in the dark and transform in dark into small sclerotia 1984; Kertesz-Chaloupkova et al., 1998), development from
which are multi-cellular round brown-coloured resting bodies the secondary hyphal knot up to the prekaryogamy primor-
(Moore and Jirjis, 1976; Ku€ es et al., 1998, 2002a,b; Badalyan dium with largely established tissues ready to perceive a light
et al., 2011, Fig. 3C). Under appropriate environmental signal for induction of karyogamy in the basidia (here defined

€ es et al., 2007; Navarro-

as P4) takes place within 4 d (Fig. 3A; Ku primordia differentiation can be recognized at the upper third
Gonza lez, 2008) and has been specified more precisely in the in the prepileus region which will develop into the pileus
early steps of primordia development compared to the former trama (dense plectenchyma filling the inner of the pileus)
comprehensive description of fruiting body development in and in the middle part of the knot where cells will line up to
Ku€ es (2000). Primordia development progresses continuously give rise to stipe tissue (Matthews and Niederpruem, 1973).
over the time of the days and this can result in short period The lower mass of cells remains unchanged as randomly ori-
in different and more advanced tissue appearances. There- ented basal plectenchyma of isodiametric cells to serve as a
fore, we take here the moments of switching-on the light at basal bulb (‘primordial shaft’; Muraguchi and Kamada, 1998).
a new day as reference points for unambiguously defining The clear shape of a minute mushroom embedded in a
distinct primordial stages, with P1 being the stage reached at comparably thick layer of veil cells becomes visible within a
the early morning the day after secondary hyphal knots day, already at a size of 0.5 mm in more or less still round P1
occurred, P2 two days after, etc. up to P5 5 d after (Fig. 3A), primordia (Fig. 3A). The pileus core consists of densely packed
and we try our best to connect descriptions from the literature cells, the lower edges of the young pileus are darker stained
into this scheme. The primordium grows over this time in and the stipe is apparent by more stretched parallel hyphae
size, on artificial medium (Granado et al., 1997) up to about (Matthews and Niederpruem, 1973; Moore et al., 1979; Moore,
3e6 mm prior to karyogamy (P4) and then to about 5e7 mm 1995, 1998a; Navarro-Gonza lez, 2008).
when undergoing karyogamy at the mature primordia stage In further light-induced development from P1, the young
P5 (Fig. 3A,J). One more light phase and part of the following primordium stretches in length into a pear-shaped figure
night is required for maturation of the about 4e5 cm sized (P2, ca. 1e2 mm; Fig. 3A; corresponding approximately to
fruiting bodies (Fig. 3A; Ku € es et al., 2007; Navarro-Gonza lez, day 0 primordia of Lu, 1974a and to an interim step in stage
2008). On the natural substrate horse dung, primordia (about 0 carpophore initial development of Moore et al., 1979 and
9e11 mm at P5) and resulting mushrooms (8e12 cm and Ku€ es, 2000) by downwards outgrowth of chains (tapering in
more) will commonly be much larger but not fundamentally size) of septate but clamp-less multi-nucleated larger vacuo-
different in structure (Moore et al., 1979; Walser et al., 2003; lated veil cells from the top of the structure, by tissue prolifer-
Ku€ es et al., 2004; Navarro-Gonza lez et al., 2011). Nutritional ef- ation at the lower cap margins resulting in increase in cap
fects may account for occurrence of dwarf fruiting bodies of size, and by some length growth of the parallel oriented hy-
sizes as small as about 1 cm (known once under a separate phae of the stipe (Fig. 3A; Buller, 1924; Matthews and
species name Coprinus radiatus, not to be confused with the Niederpruem, 1973; Lu, 1974a; Reijnders, 1979; Muraguchi
valid different species Coprinopsis radiata; Ku € es, 2000) with a and Kamada, 1998; Navarro-Gonza lez, 2008). At the apex of
same principle body plan but with reduced numbers of gills the cap at the P2 state, homogenous zones of larger outer
and of differentiated cells in the gills, along with smaller cell veil cells demarcate clearly from a layer of dense young
sizes such as of veil cells and basidiospores (Buller, 1922). cortical pileus cells (pileipellis; cap cuticle) bordering the inner
Studying the course of fruiting body development in C. plectenchymatic pileus tissue. By downwards marginal, cen-
cinerea, which has a classical mushroom morphology, trifugal growth of the cap at the zone of cell division (meriste-
under fixed environmental conditions (Granado et al., moid; Reijnders, 1979), the lower parts of the cap enclose the
1997) including distinct light and dark periods (reflecting a top of the stipe that consists of less dense tissue of wider
dayenight cycle) clearly has distinct advantages. Light and vertically-oriented parallel dikaryotic cells in the core and
also dark control defined steps in development (Ku € es, 2000; thinner multinucleate clamp-less hyphal cells at the outer
Lu, 2000; Ku € es et al., 2007; Kamada et al., 2010), therefore the margin. Gill rudiments are formed at the P2 stage. Their differ-
whole process is highly synchronous in time and order. entiation starts from the bottom of the cap zone and moves
Consequently, individual temporal stages of tissue differenti- upwards (Lu, 1974a). Somewhat below the apex of the cap, a
ation and individual cellular events present within a structure dense band of young tissue surrounds the central stipe as
are easily predictable according to time and outside observa- beginning of gill differentiation and inner delimination of
tions (Fig. 3A). As already stated above, secondary hyphal the pileus. Further downwards, vertical dome-shaped ridges
knot formation is light induced. However, light is also needed unfold from the dense band of subhymenial tissue into the
for further progress in fruiting body development. If light is pileus tissue. At the bottom of the cap, these ridges are
missing, the secondary hyphal knot will turn into an ‘elon- enlarging into rudimentary primary gills (‘gill domains’) which
gated stipe’ with an underdeveloped cap, a slender stipe-like attach at their outer edges to the trama of the stipe (Lu, 1974a,
structure also variedly known as ‘dark stipe’ or ‘etiolated 1991; Moore, 1987; Navarro-Gonza lez, 2008). Growth of ridges
stipe’ (Fig. 3E,F; Borris 1934; Tsusue , 1969; Morimoto and starts with hyphae that radiate from the pileus trama in
Oda, 1973; Elliott, 1994; Ku € es et al., 1998; Fischer and Ku € es, opposing directions and give rise to a layer of densely packed
2003; Terashima et al., 2005; Chaisaena, 2008). Illumination is cells on the two flanks of an evolving ridge (Rosin and Moore,
also needed to continue in fruiting body development further 1985a). Initially, the outer cell layers of two neighbouring
from stages P1, P2, P3 and P4 (Fig. 3A). If after any of these ridges attach to each other. According to Lu (1991, 2006), gill
stages light is missing, the basal stipe plectenchyma of the cavities are then carved out by cell degeneration through
young primordia will proliferate to result also in a ‘dark stipe’ autophagic cell death, starting near the stipe by splitting the
with arrested cap development (Tsusue , 1969; Lu, 1974a; rim between neighbouring dome-shaped ridges and moving
Kamada et al., 1978; Chaisaena, 2008). further in direction radially away from the stipe into the pileus
Progressing from the originally homogeneous secondary tissue (rupthymenial gill differentiation). Slightly preceding
hyphal knots, first histologically distinct zones in course of the splitting reactions, cells from the dense outer layer of

16 U. Ku lez
the ridges begin to vertically elongate to give rise to a dense (Morimoto and Oda, 1973; Navarro-Gonza lez, 2008). Cap tissue
palisade of oblong, equally sized binucleate cells (young growth by cell proliferation, especially for length and height
hymenial layer, protohymenium) on the two outer flanks of growth of primary and higher order gills happening in the
the arising rudimentary gills. During continued outwards sup-apical region of the cap in centrifugal direction
growth of the gill cavities, further protohymenium differenti- (Reijnders, 1979), is largely finished at the day of P4 primordia
ates continuously from hyphae that divert from trama tissue and gill tissue differentiation is further advanced (Lu, 1974a).
from the young pileus to cover the enlarging rudimentary gills The further apically swollen, still dikaryotic probasidia are
at the outer flanking sides throughout by the young dense ready to receive a light signal to induce karyogamy (Lu,
hymenial layer and eventually also the bottom of the elon- 1974a, 2000). Randomly interspersed between the masses of
gating gill cavity. Plate-like small primary gills result whose probasidia in the hymenia, the also club-shaped but larger,
inner less dense plectenchymas remain connected to the typically binucleate cystidia are now recognized as alternate
pileus trama and to the outer young cortical tissue layers of differentiation of hymenial palisade cells arisen from the
the stipe (Lu, 1974a; Rosin and Moore, 1985a; Navarro- same subhymenial branches as the probasidia (seen in
Gonza lez, 2008). Fig. 3K,L at later stage). Facial cystidia (pleurocystidia) pro-
With continuing growth of the primordium and enhanced trude into the gill cavity and strongly attach to a probasidium
size increase of the cap, primary gills enlarge further longitu- in the flanking hymenium of the adjacent gill (Moore and
dinally and in vertical height of their flanks. The primordium Pukkila, 1985; Rosin and Moore, 1985a; Horner and Moore,
adopts thereby a terete shape (P3, 2e3 mm in size; Fig. 3A; cor- 1987; Chiu and Moore, 1993; Navarro-Gonza lez, 2008), possibly
responding approximately to Lu’s day 1 primordia and to to act as space generators for basidiospore development
smallest of Rosin’s and Moore’s stage 1 primordia; Lu, 1974a; (Moore, 1995), as tension ties (Chiu and Moore, 1990; Moore,
Rosin and Moore 1985a; Ku € es, 2000; Navarro-Gonza lez, 2008). 1998a) or as distance pieces for structural stabilisation
Due to further outgrowth of chains of large veil cells with (Buller, 1924), aeration and humidity control (Smith, 1966).
the enlarging of the cap (Buller, 1924; Muraguchi and The contact between a cystidium and a probasidium in the
Kamada, 1998), the pileal veil at the P3 state is slightly tousled. opposing hymenium causes the latter cell to vaculoate and
A first rim becomes visible on the outer surface marking the to differentiate into a cystesium, instead of to further progress
border between cap and stipe and the margin of cap veil tissue the pathway of basidium development (Buller, 1922, 1924;
of large vacuolated clamp-less cells (Fig. 3A). With increasing Rosin and Moore, 1985b; Horner and Moore, 1987; Bourne
outer cap girth in development from the P2 to the P3 structure, et al., 1996). Facial cystidia spanning a same gill cavity may
empty spaces arise between riving primary gills since these do originate from the same or from opposing hymenia. The num-
not vary much in thickness over height and length. Spaces are ber of cystidia on the flanks of primary and higher order gills is
filled by secondary and higher order gills that are initiated in similar (in total 8 % of the original palisade cells). However,
between primary gills by bifurcation of splitting the pileus higher order gills carry increased numbers of cystidia at their
trama (Moore, 1987; Lu, 1991). Moore (1995, 1998a) postulates outer edges, possibly for reinforcement of the free gill apices
a ‘gill organizer’ located in the outermost rim of a broadening in space (Horner and Moore, 1987; Moore, 1987; Chiu and
gill cavity to arrange the formation of a tip of a new gill of Moore, 1993). The inner stipes in P4 structures contain now
higher order. As primary gills, also the gills of higher order two types of parallel hyphae, narrow and inflated (Rosin and
extend at the roots of the gill cavities radially outwards into Moore, 1985a; Hammad et al., 1993a,b; Navarro-Gonza lez,
the undifferentiated pileus trama. By then two outward mov- 2008).
ing intrusions into the pileus trama for shaping the higher or- Increase in size subsequent to the P4 stage is mostly via cell
der gill, an outwards extending gill cavity is then Y-shaped. inflation (Moore et al., 1979; Hammad et al., 1993a; further re-
Gills of higher order differ from primary gills in that they are view in Ku € es, 2000) although sizable somatic cell divisions,
covered throughout with a hymenium including their edges confined mainly to the stipe (Lu, 1974a), still continue at least
(Moore, 1987; Chiu and Moore, 1990; Navarro-Gonza lez, up to 8 h prior to karyogamy when the premeiotic S-phase
2008). In addition, some of the primary gills bifurcate zipper- starts which is also prekaryogamic (Lu and Jeng, 1975). First,
like from their inner trama in centrifugal direction into two the gill cells increase in size, thereby stretching the lamellae
descendant gills whose roots are both attached to the stipe in length and height. This will only happen to continue,
(Chiu and Moore, 1990). The masses of oblong palisade cells when a light signal was received to induce nuclear fusion in
in the young hymenia of gills in P3 structures begin to trans- the binucleate probasidia (Lu, 1974a; Morimoto and Oda,
form into a layer of densely arranged club-shaped probasidia 1974; Kamada et al., 1978; Navarro-Gonza lez, 2008). The light
(young basidioles; Rosin and Moore, 1985a; Navarro- signal possibly targets at premeiotic S-phase replication. It
Gonza lez, 2008). takes about 2 h to initiate in all probasidia the replication
P4 primordia (3e6 mm in size; Fig. 3A; corresponding to and 8 h to complete the S-phase (Lu, 1974b, 1982, 2000; Lu
Lu’s day 2 primordia and larger Rosin’s and Moore’s stage 1 and Jeng, 1975). Onset of nuclear fusion (stage karyogamy as
primordia; Lu, 1974a; Rosin and Moore, 1985a; Ku € es, 2000; defined in the sense of Lu, i.e. that 5 % of all basidia entered
Navarro-Gonza lez, 2008) are dumbbell-shaped by a second the process; Raju and Lu, 1970; Lu, 1974b, 2000) happens at
deeper rim marking the place of first loosening of outer veil the following morning in the P5 primordium (P5, 5e7 mm in
tissue at the border of cap and stipe. The lower part of the size; Fig. 3A,J; corresponding to Lu’s day 3 primordia and to
veil might thus be perceived as a reduced volva around the the interims phase between Rosin’s and Moore’s prokaryo-
base of the stipe. The layer of veil cells covering the cap ap- gamic stage 1 and meiotic stage 2 primordia; Lu, 1974a, 1982,
pears scrubby due to the growing chains of elongated veil cells 2000; Rosin and Moore, 1985a; Ku € es, 2000; Navarro-Gonza lez,

2008). Except for the cystidia and cystesia, virtually all cells in et al. 1979; Ku€ es, 2000; Navarro-Gonza lez, 2008). Cell inflation
the hymenia of P5 structures (Fig. 3K,L) present expanding of different zones of the young fruiting structure in cap and
basidia that will undergo karyogamy and subsequently stipe is coordinated and proportional to each other
meiosis (Raju and Lu, 1970; Navarro-Gonza lez, 2008). At the (Hammad et al., 1993a). First, the stipe extends only slowly,
P5 stage the cap is enlarged in diameter relative to that of exclusively through cell elongation. Hyphae in the outer cortex
the stipe and the shape resembles a light bulb (Fig. 3A,J). The regions of the premeiotic stipe are all narrow. Parts of the inner
veil of the cap looks heavily disheveled by radially splitting premeiotic stipe cells are inflated, multinucleate and often
the chains of veil cells into fibrous scales. The indentation be- clampless, but a majority of hyphae across the stipe diameter
tween cap and stipe is more profound (Fig. 3A,J) due to further and along the length of the stipe are also narrow (Lu, 1974a;
marginal bracing of the outer veil of the cap and by the begin- Stephenson and Gooday, 1984; Hammad et al., 1993b). Minor
ning of rupturing of the inner partial veil (lipsanenchyma; premeiotic stipe elongation depends on the stipe being in con-
Reijnders, 1991), the connecting plectenchyma between cap tact with the enlarging cap. After meiosis (P5 þ 12 h) rapid stipe
and stipe (Buller, 1924; Moore et al., 1979; Navarro-Gonza lez, elongation continues also without the cap, although the extent
2008). Thereby, the connection between primary gills and of postmeiotic stipe elongation is still influenced by contact
stipes has already become somewhat loosened which initiates with the cap. Slow and rapid stipe elongation happens most
the formation of an annular cavity in the boundary between actively at the upper mid-region in the upper half of the young
cap and stipe tissues. At the outer lower margin of the cap, stipe, i.e. in the zone that in the primordia is covered by the
the adnate to adnexed primary gills might have already fully cap. The primordial shaft but also the cells at the outmost
detached from the stipe and hymenial tissue can extend apex of the stipe (at the pileus/stipe junction) are not involved
over the freed edge of the gills. In particular, several marginal (Gooday, 1974; Cox and Niederpruem, 1975; Kamada and Tsuji,
multinucleate and more oval cystidia (cheilocystidia) are 1979; Hammad et al., 1993a). Stipe elongation is due to exten-
generated from multi-nucleate tramal gill hyphae as closure sion of component cells that rapidly stretch by massive diffuse
of the lamella edges when primary gills pull away from the cell wall expansion (Gooday, 1975, Kamada and Takemaru,
stipe (Buller, 1924; Jones and McHardy, 1985; Rosin and 1977; Kamada, 1994). Inflated hyphae swell further and, in
Moore, 1985a; Horner and Moore, 1987; Chiu and Moore, 1993). addition, parts of the narrow hyphae also inflate. Postmeiotic
During the seventh day of development, fruiting body for- stipes contain less narrow hyphae and more broader vacuo-
mation proceeds very fast in multiple events adjusted in lated hyphae in the mid to outer regions of the stipe up to
timing to the processes occurring in and on the basidia (for the outmost layer that continues to consist of a protective
detailed review see Ku € es, 2000). The processes in the basidia coating of narrow hyphae (Hamada et al. 1993b; Greening
are remarkably synchronous, i.e. 70e75 % of all basidia will et al., 1997). Over the diameter of the stipe, mostly cells of a
be always in the same developmental phase, with the cells mid-to inner-cortex location expand (Hammad et al., 1993b).
at the lower gill margin and at the edge closer to the stipe be- The inequal distribution of inflating cells over the stipe diam-
ing always most advanced in development. As previously the eter causes a change of the stipe from a solid cylinder to a hol-
gill formation, also basidia maturation within the gills moves low tube. The inner part of the hollow extended stipe is first
along two gradients, outwards away from the stipe and up- filled with a brown gelatinous substance but this disappears
wards to the apex of the cap (Raju and Lu, 1970; Lu, 1982; with time (Cox and Niederpruem, 1975; Hammad et al.,
Hammad et al., 1993a; Navarro-Gonza lez, 2008). Karyogamy 1993b; Navarro-Gonza lez, 2008). Hyphae that cover the inner
within the basidia will complete over the whole gill surface af- lumen of the extended stipe are also narrow and are suggested
ter about 6 h (P5 þ 6 h). Meiosis directly follows karyogamy to serve possibly as insulation and/or as places of excretion of
and takes about 8e9 h for all steps, to finish towards the end the gel-like material (Hammad et al., 1993b). Allover from P5,
of the light phase (P5 þ 11 h; Kimaru and Takemaru, 1955; the stipe elongates 8e10 times in the last 20 h of development
Raju and Lu, 1970; Lu, 1982, 2000; Hammad et al., 1993a; (Iten, 1970; Gooday, 1974, 1975; Cox and Niederpruem, 1975;
Celerin et al. 2000; Navarro-Gonza lez, 2008; Burns et al., Moore and Pukkila, 1985; Hammad et al., 1993a; Kamada,
2010). First sterigmata emerge 8 h after onset of karyogamy. 1994; Navarro-Gonza lez, 2008).
They develop prior to the end of meiosis (P5 þ 8e11 h). Basid- In the cap, parallel to meiosis, the gills start to separate
iospores bud off within the following 2e3 h (P5 þ 10e14 h) for from each other as consequence of cell inflation
the haploid nuclei resulting from meiosis to then migrate into (P5 þ 2e11 h; Rosin’s and Moore’s stage 2 primordia; Rosin
(P5 þ 12e19 h). Basidiospores are matured and stained black and Moore 1985a; Hammad et al., 1993a; Navarro-Gonza lez,
by incorporation of pigments in the outer spore cell wall layer 2008). Towards the end of meiosis at the start of sterigmata
within 7 h (P5 þ 12e19 h), which in the scheme of Fig. 3A is formation on the inflating basidia (P5 þ 8e11 h), the partial
shortly after the middle of the last night phase (Kimaru and veil fully ruptures, leaving behind another outer ring of tissue
Takemaru, 1995; Iten, 1970; Iten and Matile, 1970; at the top of the primordial shaft (Moore et al., 1979; Hammad
McLaughlin 1973, 1977, 1982; Hammad et al., 1993a; Navarro- et al., 1993a; Navarro-Gonza lez, 2008). The edges of primary
Gonza lez, 2008; for a more detailed review of basidiospore pro- gills carry now well-differentiated cheilocystidia and those of
duction and maturation, see Ku € es, 2000). neighbouring primary gills attach to each other (Buller, 1924;
Over the seventh day of development, the fully established Chiu and Moore, 1993). Next to club-shaped basidia and fully
primordium constantly increases in size due to cell inflation developed pleurocystidium-cystesium connections, imma-
resulting in the formation of an immature fruiting body of ture fruits at the end of the light phase (P5 þ 12 h) contain in
about 15e20 mm by the end of the light phase (P5 þ 12 h, cor- the hymenia also sterile dikaryotic hyphidia (in the C. cinerea
responding to Moore’s et al. stage 3 immature fruits; Moore literature often referred to as paraphyses; Buller, 1924; Iten

18 U. Ku lez
and Matile, 1970; Rosin and Moore, 1985b; Ku € es, 2000). Hyphi- and ordinary hyphidia (Buller, 1924). Notably, meiosis and
dia emerge as outgrowths of binucleate subbasidial cells dur- basidiospore formation is not required for fruiting body matu-
ing early meiosis and protrude through hyphal tip growth ration. Defects in meiosis or in subsequent sporulation leads
from their subhymenial location of generation into the young still to fully erected, normal-shaped mushrooms that however
hymenium to enclose in groups of about four to six a single have caps of whitish appearance (‘white caps’) due to lack of
basidium and to spatially separate basidia from each other. spore formation or coloration and such white caps still may un-
Postmeiotic inflation of hyphidia makes a major contribution dergo autolysis (Zolan et al., 1988; Kanda et al., 1989; Lu et al.,
to cap extension and may contribute to overall gill structure 2003; Namekawa et al., 2005; Sugawara et al., 2008).
stability (Raju and Lu, 1970; Lu, 1974a; Rosin and Moore, Summing up from all the descriptions to estimate numbers
1985b; Horner and Moore, 1987; Navarro-Gonza lez, 2008). of different cell types during the development in C. cinerea, i.
Depending on the strain, larger hyphidia surrounding a facial there are at least four cells types in primary and secondary hy-
cystidium (‘clasping-cells’) might rise in size above the general phal knots, ii. at least two cell types can be counted for the
hymenial surface, both on the hymenium of origin of a cysti- outer veil (the original smaller veil cells of the young primor-
dium and on the hymenium of attachment of a cystidium to dium and the large veil cells that grow downwards in chains
cystesia (Buller, 1924; Chiu and Moore, 1990). Moreover, there from the apex of the developing primordium), and iii. three
are two types of basidia distinguished by length, short and for the primordial and mature pileus (with an outer dense
long, that alternate in order over the gill surfaces (Buller, cortical layer, an inner more loose plectenchyma and a lower
1924; McLaughlin, 1982; Jones and McHardy, 1985; Horner denser layer of hyphae that connects to the gills; Fig. 3K,L). iv.
and Moore, 1987; Bourne et al. 1996). Hyphidia and slightly Further in gill generation, there are cells that undergo auto-
shifted in time the bimorphic swollen basidia vacuolate with phagic cell death for producing space for gills and there are
basidiospore production and maturation (Iten, 1970; Iten and pileus hyphae that are engaged in gill extension movement
Matile, 1970; McLaughlin, 1982). With basidiospore formation and in new gill generation, respectively. v. The structure of
and maturation (P5 þ 12e18 h; corresponding to Moore’s the grown lamellae (Fig. 3K,L) is determined by cells of an in-
et al. stage 4 immature fruits; Moore et al. 1979; Ku € es, 2000), first ner tramal plectenchyma, by subhymenial generative hyphae
the stipe elongation (see above) and then the cap expansion for production of palisade cells that transfer either into short
accelerates. With time, the pileus opens like an umbrella by and long basidia with basidiospores or into pleurocystidia or
cracking the cystidium-cystesium connections between the cystesia, respectively, by subbasidial cells for production of or-
gills, centripetally starting from the periphery of the pileus dinary hyphidia and enlarged clasping-cells, and by cheilocys-
(Buller, 1924; Chiu and Moore, 1993; Muraguchi et al., 2008a). tidia at their apexes. vi. Cap and stipe are separated at the
At the outer periphery of the cap also for rapid expansion, in- lower margin of the pileus by larger cells of the partial veil.
ner and cortical pileus tissue situated at the outer base of the vii. The stipe consists at the primordial shaft of the isodia-
gills loosen and crack, respectively. This in consequence splits metric cells surrounded by a volva of veil cells, and in the up-
all gills V-shaped from the outside (Muraguchi et al., 2008a) for per parts of narrow hyphae of the outer cortex, of narrow and
easy radially unfolding the umbrella. The thus ‘plicate’ cap inflated hyphae in the internal tissue and of narrow hyphae of
rapidly opens in the last 3 h of rapid stipe elongation the inner boundary, and there are small dense cells at the
(P5 þ 18e20 h) and flattens more or less into a plane stipe apex connecting to the cap (Fig. 3J). viii. Specific tissue re-
(P5 þ 18e23 h; Buller, 1924; Muraguchi and Kamada, 1998; gions above the gills in the inner pileus trama loosen to pro-
Muraguchi et al., 1999, 2008a; Navarro-Gonza lez, 2008). With duce vacant spaces and to subsequently crack at these
stretching the pleats in the cap surface, the pileal veil will places the outer cortical layer for generation of outer pleats
fall apart into loose fugacious scales that are either left in the cap for umbrella unfolding. Counting all the different
speckled over the cap surface, peel off or degenerate. Scales cell types and tissues noticed throughout the whole develop-
of the partial veil in contrast are deposited in flocks on the sur- mental process, over 30 different cell types might be recog-
face of the cortex of the elongating stipe (Buller, 1924; nized by form, position, time and function. However, since
Hammad et al., 1993a; Navarro-Gonza lez et al., 2008). the whole process might not have been yet well followed up
The fruiting body (ca. 4e5 cm in size on artificial medium; in all microscopic details, there might still be more. For exam-
Fig. 3A) is fully erected and the cap with matured blackish ba- ples, distinctive differences in numbers of nuclei per cell and
sidiospores (Fig. 3G,H) is fully opened 2e3 h after the middle differential responses on stains and antibodies of cells of
of the last dark phase (P5 þ 20e21 h). During and upon cap same appearance in cap and in stipe tissues support the
opening, mature basidiospores might at first be discharged un- view of existence of further physiologically distinct cell types
der usage of Buller’s drops, particularly at the firstly opened in the fruiting bodies of C. cinerea (Lu, 1974a; Chui and Moore,
pileus periphery (Buller, 1924; Iten, 1970; McLaughlin and 1993; Hammad et al., 1993b; Boulianne et al. 2000; Walser et al.
Beckett, 1987) but, C. cinerea being an inkcap fungus, the major- 2005).
ity of all spores is released within few hours after maturity in
liquid droplets resulting from enzymatic cap autolysis with hy- Agaricus bisporus, Agaricaceae, Agaricales,
drolases originating from the hyphidia vacuoles. Cap autolysis Agaricomycetidae
starts at the edges of the gills, centripetally from the pileus pe-
riphery to the inner pileus-disc, and takes about 4e5 h Some central aspects of the hemiangiocarpous development
(P5 þ 21e26 h; Fig. 3I; Iten, 1970; Iten and Matile, 1970; further of A. bisporus resemble those of C. cinerea (Walser et al., 2003)
review in Ku € es, 2000), with cheilocystidia being the first to auto- but there are important differences in the initiation of fruiting
digest, and then the pleurocystidia in advance of the basidia and particularly in gill formation and structure, in tissue

development by parallel hyphal growth in absence of any An outer visible demarcation between cap and stipe marks
anastomoses in A. bisporus, and there are differences in order the position of the hymenial split and the stipo-hymenial
of events. Specifically in the button mushroom, fruiting body junction (Cle mençon, 1997, 2004, 2012; Umar and Van
formation necessitates first the formation of thick fluffy Griensven, 1997a) in the differentiating primordia with a
mycelial cords of parallel running hyphae of pseudoparenchy- distinct ‘waist’ (DPW; Eastwood et al., 2013). The cap with
matous structure (Mathew, 1961; Heckman et al., 1989; Umar pileus margin and the beginning stipe with the ‘bulbus’ (basal
and Van Griensven, 1998), close to which or on which then plectenchymal tissue) beneath are then clearly distinguish-
the primary hyphal knots develop in mucilaginous material able underneath the young outer skin, although the tissues
by frequent branching of short stunted sharply curved hyphae of the different organs are not yet sharply separated from
that grow out in all directions (Angeli-Papa and Eyme, 1978; each other with exception of the palisade layers
Heckman et al., 1989; Umar and Van Griensven, 1997a, 1998; mençon, 1997, 2004, 2012; Umar and Van Griensven,
(Cle
Morin et al., 2012; Eastwood et al., 2013). By further growth, 1997a). At this primordial stage, development may arrest for
loose hyphal interwining and aggregation (in absence of anas- some time (Straatsma et al., 2013). In spite of the usual asyn-
tomoses), the primary hyphal knots rise in size (1e2 mm) to chronous start of primordia development within cultures
the circular compact secondary nodules of undifferentiated (Wood, 1976; Noble et al., 2003) and the possibility to reversibly
inner hyphal tissue that is under protection of an outer layer arrest in primordia development (Straatsma et al., 2013), the
of more loose hyphae, as the precursor of the universal veil overall course of events up to maturation is nevertheless
covering the older structures as a peel (Atkinson, 1906; remarkably conserved in timing (Eastwood et al., 2013;
Hayes, 1978; Cle mençon, 1997, 2004, 2012; Umar and Van Straatsma et al., 2013).
Griensven, 1997a, 1999). If development continues, active structures further in-
Within the growing spherical secondary hyphal knots crease continuously in size by both cell proliferation and
(2e4 mm; smooth undifferentiated primordia, SUP; cellular expansion. The hyphae at the margin of the cap heavi-
Eastwood et al., 2013), cap and stipe differentiation initiates ly branch and grow radially outwards to enlarge both the
(‘histo-organogenetic stage’), employing steps of cell prolifer- pileus as well as the cavity in size. With time, the enlarging
ations and later on also cell degeneration (Umar and Van downwards oriented cap margin bends round in direction to-
Griensven, 1997a,b). The central tissues divide first into wards the stipe and nestles to the partial veil evolving between
distinct more or less equal upper and lower parts of dense cap and stipe. The partial veil differentiates through hyphal
plectenchyma (Atkinson, 1906; Cle mençon, 1997, 2004, 2012; growth from the plectenchyma positioned at the base of the
Umar and Van Griensven, 1999), which marks a transition annular cavity. At a primordium size of about 1 cm, lamella
stage for the next phase of specific tissue differentiation (de initials grew down into the cavity until the edges of the gills
Groot et al., 1997). Parallel orientated hyphae appear then in touch the surface of the partial veil (Fig. 4F). Lamellae grow
the region that will give the upper part of the stipe (Angeli- in height by cell proliferation at their base attached to the
Papa and Eyme, 1978; Cle mençon, 1997, 2004, 2012). Signs of pileus. Primary lamellae fold up lateral from the stipe to the
cap and stipe are clearly visible at a size of about 4e5 mm, outside of the cap and elongate radially with the marginal
but a velum connecting cap and stipe is not yet differentiated growth of the pileus. Short secondary or higher order gills
(stage 1, ‘pinheads’; De Bary, 1884; Hammond and Nichols, intercalate at the margin of the pileus into expanding inter-
1975, Fig. 4A). In the steadily enlarging structures at a size of lamellar spaces (Fig. 4G,O,Q). The trama of the comparably
about 5e7 mm (elongated differentiated primordial struc- thin lamellae of A. bisporus spans across only 12e14 parallel
tures, EDP; Eastwood et al., 2013), cell degeneration at the growing hyphae. Thickening of lamellae is achieved by
base of the young cap initiates a prehymenial almost verti- strengthening the subhymenial layer. Generative hyphae
cally positioned annular cavity (hymenial split) which eventu- laterally bending out of the inner trama of parallel growing hy-
ally results in the beginnings of lamella formation (Umar and phae will intensely ramify to give a subhymenium from which
Van Griensven, 1997a). First, hyphae grow downwards from then the mass of the oblong basidioles (young basidia) as ter-
the prepileus plectenchyma into the arising tiny annular cav- minal cells arise (De Bary, 1884; Atkinson, 1906; Buller 1922;
ity as precursors of the prehymenial palisades and of the later Levine, 1922; Hein, 1930; Cle mençon, 1997, 2004, 2012).
pileus edge. Around the enlarging cavities, prehymenial pali- With further cap growth, the partial veil becomes visible
sades are next recognized, born in groups of slightly inwards from the outside (Fig. 4CeE; De Bary, 1884; Hammond and
oriented hyphal tips from tramal prepileus tissue. Small re- Nichols, 1975; de Groot et al. 1997). With growth of the cap to
gions of loose plectenchyma in between groups of palisades about 2e3 cm, the lower edges of the cap are closely posi-
present the rudimentary future lamellar tramas that connect tioned to the stipe. The velum connecting cap and stipe re-
to tramal hyphae of the young stipe and the young pileus. mains still closed and unstretched (‘button stage’, stage 2;
Gill cavities will arise within the groups of palisades which Hammond and Nichols, 1975; Hayes, 1978, Fig. 4BeD). Within
then enclose as rudiments of adjacent hymenia an interhy- the enclosed growing cap, the lamellae matured. Mature gills
phal space as the beginning gill cavity. Palisades growing on are brown stained by gradual darkening of cell saps by pink-
the surface of resulting young lamellar plates are precursors red quinonoid pigments (Fig. 4G,H,J,NeQ; Buller, 1922;
of basidia. They differ in size with smallest cells found at Claydon, 1985). They are composed of inner elongate tramal
the edges of the plates (Atkinson, 1906; Levine, 1922; cells, extensively branched subhymenial cells and the outer
Clemençon, 1997, 2004, 2012; Umar and Van Griensven, hymenium as continuous layer over the whole gill surface of
1997a,b). Stipe cells enlarge in parallel to the beginning of basidioles (Fig. 4J,K) that differentiated from the palisadal cells
pileus differentiation (Clemençon, 1997, 2004, 2012). of the young hymenium (Buller, 1922; Flegg and Wood, 1985).

20 U. Ku lez
The closed ‘buttons’ form already basidiospores (Fig. 4K) as do further growth in diameter to over 20 cm (‘open flats’ with
the more advanced ‘closed cups’ (Elliott, 1977), larger sized convex upper cap surface and gill surface flat, stage 6; ‘flats’
structures of up to about 5 cm with a stretched but still closed with gill surface curving upwards, stage 7; Hammond and
velum (stage 3; Hammond and Nichols, 1975; Hayes, 1978, Nichols, 1975). Growth can even happen after a sporophore
Fig. 4E,H). Importantly, basidia in A. bisporus do not mature is harvested at the button or a later stage (Gruen, 1963; Umar
synchronously. Unlike in C. cinerea, the hymenium of A. bispo- and Van Griensven, 1997b; Braaksma et al., 1998). Cap growth
rus lacks any extra structural cells and consists solely of the depends on nutrient resources provided by the stipe (Ajlouni
cylindrical slightly club-shaped clampless basidioles. Basi- et al., 1992) and regulation by lamellar growth factors of cap
dioles in matured gills contain fused nuclei. However, parts trama expansion (Gruen, 1963). Ultimately, the cap turns
but by far not all of the basidioles will successively replace into in the ‘stage of senescence’ in which cap tissues pigment
any matured and upon spore release collapsed basidia. and slowly degenerate, along with the mycelial cords (Burton
Many others of the basidioles in contrast arrest permanently et al., 1997; Umar and Van Griensven, 1997b). Tyrosinases and
in meiotic prophase, appear to have only structural function serine-proteases expressed in specific stipe and cap tissues
and have in early literature therefore been distinguished play a role in this (Burton et al., 1997; van Leewen and
from further developing basidioles as sterile paraphyses Wichers, 1999; Heneghan et al., 2009).
(Buller, 1922; Manocha, 1965; Saksena et al., 1976; Allen et al., In summary, we do not have such an extensive description
1992). Basidiospores are first released at ‘open cup stages’ of the morphology and developmental events in fruiting in A.
when the partial veil tears (cup opening or stage 4; Fig. 4E) bisporus as in C. cinerea, which is the best studied mushroom of
and is finally fully torn (open cup or stage 5, respectively; € es, 2000). There appear to be less cell types in
all (Section 6.; Ku
Hammond and Nichols, 1975; Hayes, 1978, Fig. 4L,M) and the basidiomes of A. bisporus as compared to C. cinerea, not only by
gills become visible and the convex cap with a thick white i. the less structured gills with only inner trama, subhymenial
layer of pileus plectenchymal trama (Fig. 4G,H) and a thin hyphal cells, basidioles of different age and function and basi-
outer brown (Fig. 4C,I,L) or, depending on races, white- dia with the tick-walled globose basidiospores (Buller, 1922;
colored peel further expands. A majority of individuals pro- Manocha, 1965). ii. The outer peel tissue consists of long,
duce predominantly two dikaryotic spores at a basidium clampless, parallel growing hyphae (Breitenbach and
(Fig. 4K) but four-spored variants with homokaryotic basidio- Kra € nzlin, 1995). iii. Also the short-lived partial veil is
spores are also known and rarer mixed spore combinations composed of parallel arranged and overlapping hydrophobic
are sometimes also observed (Buller, 1909, 1922; Elliott, 1977; hyphae (De Bary, 1884; Umar and van Griensven, 1997a,
Callac et al., 1993, 2003). Hyphae in the brown peel are mela- 1999). iv. The thick pileus trama contains only one type of
nized (Knaus et al., 2013, Fig. 4I). broad, irregularly shaped, cytoplasmic-rich and loosely con-
Primordial development up to the stage 2 and then stage 4 nected unstained hyphal cells (Manocha, 1965; Angeli-Papa
(as defined by Hammond and Nichols, 1975, Fig. 4AeC) in A. and Eyme, 1978; Cle mençon, 1997, 2004, 2012). However, there
bisporus takes about 10 and 12 d, respectively (de Groot et al., is a zonal heterogeneity in expression of certain developmen-
1996, 1997; Morin et al., 2012). Stipe elongation occurs during tally regulated genes in the inner pileus trama and in more
this time, first at the lower part of the stipe not covered by outer trama localized beneath the pileipellis (de Groot et al.,
the cap, in order to lift the developing mushroom up from 1999). Already in the young mushroom stages, there is a pig-
the substrate. Subsequently, during mushroom maturation mented thin layer of cap trama to which the gills attach and
from stage 2 to stage 4, stipe elongation increases proportion- that with age extends as a demarcation layer also to the upper
ally with cap expansion, then largely by cell expansion stipe tissues (Gruen, 1963; Cle mençon, 1997, 2004, 2012,
through diffuse cell wall extension in the upper part of the Fig. 4H,O,P). Differential tinting of cells by leucofuchsin, crys-
stipe above the partial veil but also by some cell proliferation tal violet or azur A observed in pileus and in stipe tissues sug-
(see stretched stipe and stretched partial veil in Fig. 4E,H). Dur- gests degrees of discrimination by function, such as the
ing cap and stipe expansion, the chitin content in cell walls stained ones to function as reserve cells (Umar and Van
rises and amounts of cell wall glucan decrease (Gruen, 1963; Griensven, 1997a, 1999) or for secretion (Cle mençon, 1997,
Hammond, 1979). Stipe growth is positively influenced by 2004, 2012). v. In the stipe of the young mushroom, three prin-
cap and by lamellae tissues (Gruen, 1963). Stipes extend to ciple types of multi-nucleated hyphae are distinguished, large
about 2e3 times of the length they have at the button stage. vacuolated and thin threadlike hyphae in the inner stipe tis-
An inner core can be distinguished from an outer thick layer sues and closely-packed vertical thinner but also vacuolated
in the young stipe (Fig. 4F,G). Therefore, the inner matured hyphae forming an outer cortical layer over the core regions
stipes may be hollow or stuffed with loose hyphae. A collar of the stipe (Manocha, 1965; Craig et al., 1979; Umar and Van
of velum tissue (‘annulus’; Fig. 4L,M,T) is left behind around Griensven, 1997a). A stipe differs over its length in distribu-
the extended stipe at about two-thirds of its total height. tion, orientation and density of internal hyphae. In the closed
Below the superior larger annulus, a slight inferior ring is and opening cup stages, the outer and inner tissues at the base
sometimes visible (Fig. 4M) which together mark the upper consist of an irregular mass of densely-packed thin branching
and lower border of attachment of the partial veil to the stipe, hyphae. The extreme top of a stipe is made up of similar tissue
respectively (Buller, 1922; Gruen, 1963; Craig et al., 1977). but the cells at the top are generally shorter than those at the
The mature open mushrooms (Fig. 4SeT) have a longer life base. Hyphae at the upper core region covered by the cap are
span than those of C. cinerea. Spore formation and shedding in vacuolated and more loosely-packed, they grow vertically,
A. bisporus continues for several further days (‘spore-shedding branch and are responsible for stipe elongation during fruiting
stage’) during which the flourishing cap may increase by body maturation. Hyphae at the covered part and the upper

uncovered regions at the middle of the stipe are also vertical Schwalb (1978). The authors therefore summarized develop-
but are poorly branched, larger and more densely packed ment of S. commune in a simplified two-phase system, with
(Craig et al., 1977, 1979). vi. As a further type of cells within phase I describing all processes up to first pseudolamellae for-
growing and mature mushrooms, white branching and mation in the young cup (up to stage IV of young mushrooms;
loosely arranged hydrophobic repair hyphae can be formed Leonard and Dick, 1968; Schwalb, 1978) and the growing
upon injuries (Umar and van Griensven, 1997a). Summing matured fruiting body as the phase II. A later applied system
up, the mature mushroom may thus contain more than 15 in the study of Ruiters and Wessels (1989) used the age of
or 16 distinct cell types and there are probably at least 7 extra structures in h (12, 24, 48, 96 h) in the course of light-
cell types (cell types in the hyphal strands and within the hy- induced development in dark-grown cultures, which
phal knots; prepileus cells undergoing specific cell death, mer- happened to approximate the scheme of the five stages as
istemoic prepileus cells producing cap margins, palisades and defined by Leonard and Dick (1968) and Schwalb (1978). Since
trama of lamellae, respectively, and the meristemoic cells giv- a finer system will be easier for best understanding of overall
ing rise to the partial veil) that in addition occur throughout progress in development and morphology, we will follow here
development. the terminology of the latter authors. However, the reader
might note that also more than five stages in development
Schizophyllum commune, Schizophyllaceae, Agaricales, might be distinguished by even finer dissection of the process
Agaricomycetidae into further recognisable events or subroutines.
From the upper end of S. commune stage I aggregates (sensu
S. commune is a second well established model species for Leonard and Dick, 1968; Schwalb, 1978), multiple strong aerial
studying fruiting in the Agaricomycetes (Wessels, 1999; hyphae can grow upwards in synchronous parallel manner to
Walser et al., 2003; Wo € sten and Wessels, 2006; Ohm et al., form a tighter aggregate of organized structure and subspher-
2010). Development in this gymnocarpous species is also high- ical to cylindrical shape (Fig. 5NeP; stage II aggregate, also
ly organized but it is not as strictly divided in steps by time as known as stalk; Leonard and Dick, 1968; Watling and
in C. cinerea or also not as much as in A. bisporus. S. commune Sweeny, 1971; Schwalb, 1978; van der Valk and Marchant,
forms sessile or slightly stalked cyphelloid fruiting bodies 1978; Wessels, 1992). The aerial hyphae in these stalks show
(Fig. 5AeE,V) and follows a unique and very different morpho- retarded apical growth. Growth of inner hyphae of stage II ag-
genetic pathway than the two other Agaricales species. This gregates may start from stage I aggregates or aggregated
pathway has been sub-divided into five successive steps strands, whereas hyphae at the outer borders can grow in
(Leonard and Dick, 1968; Schwalb, 1978). from surrounding areas (Fig. 5N,O; Essig, 1922; Leonard and
In artificial agar culture, light-induced asymmetrical col- Dick, 1968; Schwalb, 1978; van der Valk and Marchant, 1978).
ony growth precedes fruiting (Raudaskoski and Viitanen, Inner tissue in the established stalk of parallel growing hy-
1982; Ohm et al., 2013). Fruiting in S. commune starts within phae (Fig. 5P) shows no differentiation into visually distinct
such irregular colony, preferentially at the margins cell types (Adams, 1918; Essig, 1922; Volz and Niederpruem,
(Niederpruem and Jersild, 1972), also with the local formation 1969; Knabe et al., 2013).
of small hyphal knots of no defined regular shape that consist From a large number of initiated aggregates, typically only
of loosely intertwined thin hyphae with clamps (stage I aggre- a few will reach maturity (Adams, 1918; Essig, 1922; own ob-
gate; Leonard and Dick, 1968; Schwalb, 1978). Similar hyphal servations). Under unfortunate conditions (such as too little
knots develop also on wood and bark surfaces as natural sub- light or too high CO2), the stage I aggregates or the hyphae at
strates (Fig. 5M). Stimulated by light and aeration (Perkins, the apexes of stalks may grow out fountain-like into aborting
1969; Raudaskoski and Viitanen, 1982; Raudaskoski and larger spherical aggregates with little tissue differentiation
Salonen, 1984), such primary aggregates develop from (Fig. 5QeT; Volz and Niederpruem, 1970). Under conditions
growth-retarded apical hyphae under increased outgrowth favouring fruiting (sufficient light, low CO2; Perkins, 1969;
of subapical hyphae. Aggregates tend to form in clusters and Raudaskoski and Viitanen, 1982), hyphal growth eventually
hyphae thereby may also assemble into aggregated strands becomes directed towards the apical center of the young
(Adams, 1918; Volz and Niederpruem, 1969; Raudaskoski and growing structure, with the inner hyphae being more sup-
Vauras, 1982) on which later rows of fruiting bodies might be pressed in growth and thus shorter than the hyphae at the pe-
formed (Fig. 5V; Volz and Niederpruem, 1969). S. commune riphery (Fig. 5U, see inset). The long outer hyphae in the stalks
stage I aggregates (Fig. 5M) resemble in appearance primary grow first inwards and then downwards into the center of the
hyphal knots of C. cinerea (Fig. 3A,B). enlarging primordium (Volz and Niederpruem, 1969; van der
As in A. bisporus and C. cinerea, there is no overall consistent Valk and Marchant, 1978; Wessels, 1992), thereby eventually
nomenclature in the literature for the different developmental forming a curled apical perimeter (Volz and Niederpruem,
stages of S. commune. The more compact spherical bodies pre- 1969), a macroscopically visible apical pit that covers the cen-
sented as stage I aggregates of S. commune in Ohm et al. (2010) tral apical depression (stage III primordium; Fig. 5U; Leonard
appear more alike secondary hyphal knots of C. cinerea and Dick, 1968; Watling and Sweeny, 1971; Schwalb, 1978). Un-
(Fig. 3A, D) and might be a non-elongated kind of type II aggre- der continuous illumination, stage III structures may also
gates of S. commune in the sense of Leonard and Dick (1968) form in similar manner directly on a substrate surface as
and Schwalb (1978). Wessels et al. (1985) pointed out that sessile structures from stage II aggregates, without producing
morphological events in fruiting body development are not an elongated stalk (Perkins, 1969; Raudaskoski and Vauras,
as strictly separated in time from each other as could be un- 1982; Wessels, 1992), possibly employing the compact spher-
derstood from the scheme of Leonard and Dick (1968) and ical bodies presented in Ohm et al. (2010) as stage I aggregates.

22 U. Ku lez
Formation of a larger elongated stage II aggregate prior to the 1978; called cup stage in Wessels, 1992 who included under
stage III primordium will apparently be influenced by the rela- the term also advanced apical stage III primordia still lacking
tive position of the structure to its growth surface (Volz and pseudolamellae). Depending on lateral or radial outgrowth of
Niederpruem, 1969) and by the moisture in the substratum the young pileus, pseudolamellae arise only on the sideward
and the air (Essig, 1922). extending side (Fig. 5V) or distributed over the whole bound-
In the very outer hyphae of the very young stage III primor- ary of a structure (Fig. 5W).
dium, local swellings become visible (van der Valk and Stipe and cap in the growing fruiting bodies are not
Marchant, 1978; Wessels, 1992) and tip cells of the outer hy- distinctly deliminated from each other. The base of the stipe
phae collapse and appear to autolyze (Volz and consists of a disorganized region of bulbous cells that may in-
Niederpruem, 1969). Importantly, at the bottom floor central crease in size and number but the overall basal region of the
of the apical depression of the young stage III primordium, a stipe does not enlarge much further. Growth of the parallel
layer of equally sized parallel palisade-shaped cells estab- hyphae in the central and upper area of the stipe leads to for-
lishes as the very early hymenium with precursors of basidia. mation of groups of parallel hyphae with air spaces in be-
These palisadal cells are short branches from subjacent multi- tween. Anastomoses between parallel hyphae occur with
branched hyphae of pileus trama (Adams, 1918; Essig, 1922; time. This results with older age in a pseudoparenchymatous
Volz and Niederpruem, 1969; van der Valk and Marchant, appearance of the stipe. Groups of parallel growing hyphae
1978; Raudaskoski and Vauras, 1982; Cle mençon, 1997, 2004, continue from the stipe into the basidiocarp trama and, even-
2012; Wo € sten and Wessels, 2006; Knabe et al., 2013). Formation tually, as a continuation also into the trama of pseudolamellae
of the young hymenium initiates already very early, in parallel once these are forming (Fig. 5Y; Volz and Niederpruem, 1969).
to the development of the apical rim (Watling and Sweeny, Pseudolamellae are analogous organs to the lamellae in C. cin-
1971; Raudaskoski and Vauras, 1982; Wessels et al., 1985) and erea and A. bisporus since their mode of generation and the
prior to production of a subhymenial layer of a loose arrange- origin of their hymenium from the cyphelloid cup surface dif-
ment of narrower hyphae (Volz and Niederpruem, 1969). fers from agaric gill and hymenia formation (Watling and
Additional discrete key events can mark the further growth Sweeny, 1971, Section 6.).
processes in stage III primordia. As development continues, Formation of the first pseudolamellae starts at the outer
the apical cavity of the cyphelloid primordium widens up by edge of the young ventral hymenium that can be as small as lit-
peripheral expansion of the central hymenial disc, first into tle more than 1 mm in diameter. Hyphae from the inner trama
an open plain cup-like pileus structure, still without the typical tissue grow out in ventral direction into adjacent tissues and
‘split gills’ (Fig. 5V, outer right structure; an advanced apical pit lift and eventually break the existing hymenial layer into splits
stage; Leonard and Dick, 1968; Watling and Sweeny, 1971; which extend in outwards direction (Fig. 5V,W and compare in
Schwalb, 1978; in Ohm et al., 2010 referred to as stage II Fig. 5Y the analogous processes in generation of 3rd and 2nd
primordia). The outer dorsal whitish tissue of the marginally pseudolamellae, respectively). At both sides of the generated
growing structure adopts a hairy tomentous appearance splits, the originally continuous preexisting hymenial layer as-
(Fig. 5FeH,K) and consists of strong thick-walled clampless hy- sembles away from the plane of the growing mushrooms, in
phal cells that can carry crystalline deposits and that are born order to form the outside layers on firstly shallow plates with
from peripheral cells of the pileus (Linder, 1933; Volz and some inner tramal hyphae in between (Fig. 5Y, compare in
Niederpruem, 1969). The young cup-shaped fruiting body can the cross-section the respective structure of the 2nd pseudola-
already sporulate but continues to grow in size by hyphal pro- mella). Once these shallow plates with the outwards extending
liferation at the outer edges of the cap. The cellular splits join to the mushroom outer edges, they will then radially
morphology of the growing outer edges remains much the grow (Fig. 5D,E,K,LVeX) by peripheral proliferation of all
same as in the older parts of the primordium (Hasselbring, different layers of pileus hyphae (hymenium, trama and outer
1907; Essig, 1922; Wessels, 1965; Watling and Sweeny, 1971). hairy tomentum). Incorporation of also the whitish thick-
Marginal growth of the pileus of the stage III primordia and walled hairy hyphae from the outer dorsal surface makes the
the resulting older fruiting structures is indeterminate and prolonging plates wider and results in longitudinally-two-
perennial. Further size growth of the young pileus occurs typi- divided pseudolamellae. Older pseudolamellae completely
cally unilaterally, the direction of which is determined by the segment the fruiting bodies through all tissue layers
position of the fruiting body relative to its substrate (Fig. 5A,V). (Fig. 5FeH,L and Y, lower inset showing the base of a 1st pseu-
Such sidewards outgrowth moves the dorsal hairy side (‘tri- dolamella; Buller, 1922; Volz and Niederpruem, 1969; Watling
choderm’) of the mushroom to become then the upper side and Sweeny, 1971). Pseudolamellae extend in height and
and the ventral hymenium the lower side of the enlarging length purely by hyphal proliferation at the margins of the
mushroom, relative to the earth (Fig. 5A). Structures that are mushrooms and not by inflation. Radially, they grow together
vertically hanging with their hymenium downwards-faced with the complete outer edge of the fruiting body, under broad-
from the beginning will instead adopt by growth a radial sym- ening the hymenium-lined cyphelloid cavities in between
metry (Fig. 5W; Hasselbring, 1907; Essig, 1922; Volz and them. To further use the rising space, three to five shallower
Niederpruem, 1969). With increasing size of the stage III pri- and shorter pseudolamellae arise secondarily in between two
mordium, while sporulation continues, the typical ‘split gills’ initial pseudolamellae (Fig. 5FeH,Y; Buller, 1909). Outgrowth
(forked pseudolamellae; Fig. 5FeL,Y) are formed by infoldings of younger pseudolamellae with differentiation of new hyme-
into the inner cup (e.g. see inset in Fig. 5V; young mature nia for basidiospore production is asynchronous and repeats
mushroom; stage IV young differentiated fruiting body; from time to time with the enlarging size of the fruiting
Leonard and Dick, 1968; Watling and Sweeny, 1971; Schwalb, body. The younger hymenial plates initiate in similar manner

than the first pseudolamellae, through outgrowth from the in- stage, the growth retarded inner hyphae of the stalk and the
ner pileus trama with resulting splits (see 2nd pseudolamella in bulbous cells at the stipe base, iv. the collapsing cells at the
Fig. 5Y) moving towards the outer mushroom margins outer edge of the apical pit, v. the thick-walled hyphae and
(Fig. 5L,X; Buller, 1909; Watling and Sweeny, 1971). In youngest the generative hyphae of the subhymenium and the outer
age, edges of pseudolamellae are still closed with a continuous hairs of the pileus all of which continue into pseudolamellae;
hymenial cover (see 3rd pseudolamella in Fig. 5Y). vi. the denser interwoven hyphae of the pileipellis (Fig. 5Y), vii.
Occasionally, a thorough rupture of a pseudolamella the inner hyphae cells for outgrowth of pseudolamellae, viii.
through the dorsal surface of the pileus might cause the forma- the primary and secondary basidia with basidiospores of the
tion of new fruiting body lobes (see arrows in Fig. 5C,E and hymenium (Essig, 1922; Linder, 1933; Niederpruem and
Fig. 5A for mature mushrooms). Alternatively, cushions of Wessels, 1969; Volz and Niederpruem, 1969, 1970; van der
interconnected fruiting body lobes can originate as early out- Valk and Marchant, 1978; Knabe et al., 2013, Fig. 5). In sum,
growths from a same aggregate or aggregated strand (Fig. 5V, we recognize at least 15 different cell types in S. commune.
outer left mushroom?). Unilateral outer size growth and repet- Distinct patterns of locations of different fruiting-specific
itive formation of ‘split gills’ eventually result in large fan- RNA species within immature and mature fruiting structures
shaped mature fruiting bodies with one or more lobes, with suggest also for S. commune that functionally there could be
the hymenia being directed down to the earth (stage V fully more cell types than identified so far by morphology (Ruiters
grown mushroom; Fig. 5AeE; Leonard and Dick, 1968; and Wessels, 1989; Wessels, 1993).
Watling and Sweeny, 1971; Schwalb, 1978; Ohm et al., 2013).
As already indicated, the outer hymenia of the older pseu-
dolamellae connect to the hymenium of the cyphelloid struc- 7. Conclusions and broader outlooks
ture’s plane and the inner pseudolamellar trama is
continuous with the pileus trama and with the outer whitish Nearly 21,000 different species are known within the Agarico-
thick-walled hairy pileus tissue. Inner broader thick-walled mycetes which are distributed over 17 different orders, with
hyphae in the trama are also thick-walled and grow more or the Agaricales containing the most with over 13,000 species
less parallel to each other, with air spaces in between (Kirk et al., 2011). Fruiting bodies have meticulously been
(Fig. 5Y). Diameters of parallel tramal hyphae decrease from described for many species by macro- and microscopic in-
the interior towards the outsides of the pseudolamellae. spections for identification and taxonomical purposes (e.g.
They are interconnected by multiple anastomoses, particu- Breitenbach and Kra € nzlin, 1986, 1991, 1995) and, yet for less
larly also the multiple-branched and coiled narrower hyphae species, also for understanding their structures and develop-
beneath the hymenium, probably to reinforce as subhymenial ment (Clemençon, 1997, 2004, 2012). The Agaricomycetes are
underlay the hymenium. The loosely arranged thick-walled rich in different basidiome shapes (Fig. 1; Section 2.) of often
hyphae in the middle of the pseudolamellae are in contrast quite contrasting looks within orders, families and even
comparably little interconnected. New hymenial layers of genera. It is now well established that macro- and microscopic
palisade-shaped cells emerge on both sides of the out- characters of fruiting bodies do not necessarily reflect a degree
growing pseudolamellae but not on their apexes which have of closer or distant phylogenetic relatedness (Hibbett et al.,
frayed margins by pullulating loosely connected whitish 2014; Section 3.).
thick-walled tramal hyphae (Fig. 5F,I,J,Y). This allows the Although there are distinct main body plans of fruiting
forked pseudolamellae in dry stage to split into two halves, bodies for the different species, these are not absolute. The
roll up and cover the hymenia and the outer mushroom mar- multitude of exceptions from standard mushroom forms and
gins (Fig. 5F,G,I,K), whereas in humid conditions the two the broad range of reasons behind such exemptions (the diver-
halves enroll to give the hymenium free for spore release sity of environmental cues, physiological states and muta-
(Fig. 5H,J,L; Buller, 1909; Essig, 1922; Linder, 1933; Watling tions; Sections 4. and 5.) show a high level of plasticity in
and Sweeny, 1971; Cle mençon 1997, 2004, 2012). Within 1 h shaping fruiting bodies. Such broad plasticity is best achieved
upon moistening of a dried fruiting body, spore discharge be- and explained by separating different modules for the entire
gins (Essig, 1922). The xerophytic mushrooms in dried state process as proposed in the concept of ‘subroutines’ by Moore
can overcome decades (>50 y) without loss of viability and and colleagues (Section 5.). Modifying some details in the
the ability to sporulate (Ainsworth, 1962). Under suitable envi- different subroutines could then have dramatic effects. At a ge-
ronmental conditions, basidiospore formation is not synchro- netic level, modifications might be accomplished by changes in
nous and only few basidia will mature at a time. Basidia sets of genes involved in relative expression to each other, by
collapse after karyogamy, meiosis and sporulation and are gain of (a) new gene(s) or by loss of (a) gene(s). Achieving in
replaced by new binucleate probasidia which emerge repeti- such way the extensive morphological plasticity as observed
tively as subbasidial branches growing out from the clamp over the closely and distantly related species and within the
connections of the older basidia in a cymose manner species can imply that most or even all of the genes for the
(Niederpruem et al., 1971; Niederpruem and Jersild, 1972). basic main body plans were likely early present in the lines
Various cell types can also be counted during the develop- of the Agaricomycetes, or to parts possibly even in the early
ment of the S. commune fruiting body and in its different tis- Agaricomycotina and the Basidiomycetes in general (further
sues. In summary, they include: i. the undifferentiated review in Ku € es and Navarro-Gonza lez, in preparation).
thinner hyphae in the nodulus with functionally different api- Mechanisms of pattern formation have to be understood
cal and subapical cells, ii. the stronger, parallel inner and and how these are modified through evolution and environ-
outer growing and eventually bending hyphae in the stalk ment (Hibbett, 2007). How is evolution of fruiting body

24 U. Ku lez
development driven? What features are ancestral and what comprehensively (Section 6.) document for instance already
are derived? Scholarly studies on these evolutionary foremost three distinct ways to produce vertical plates beneath the
questions are still scarce. So far, the multiple evolutionary or- cap with hymenia for spore production. Pseudolamellae for-
igins of the resupinate fruiting bodies and the appearances mation in S. commune is in ontology clearly distinct from that
and diversifications of ‘gasteromycetation’ are somewhat bet- of the other two Agaricales and present an apparently analo-
ter addressed in this regard (Section 3.), with time estimates gous developmental process to genuine gill construction.
from ancient origin of hundreds of million years ago to quite However, how much in distinct and in alike-looking steps in
recent as is short as in the first third of the last century gill formation in C. cinerea and in A. bisporus is homologous
(Bruns et al., 1989; Peintner et al., 2001; Desjardin, 2003, and how much is analogous? To rely and conclude simply on
Hallen et al., 2003; Vellinga, 2004; Hosaka et al., 2006). However, look of hymenophores or on comparative views of their ontol-
it is quite possible that different mechanistic instruments are ogies can all easily be misleading, as has been particularized
included in these comparisons which lead to a same end for lamellate species in the Polyporales (Hibbett et al., 1993).
result in gross morphology, for example in the convergent The question of homologies and analogies can also be
evolution of ‘gasteromycetation’. further transferred onto the level of single cells. The co-
The evolution of changes in morphology might be easier to existence of phragmo- and holobasidia in clades of Basidio-
address in more specific traits associated with later, finer as- mycetes has already been addressed above (Sections 3., 4.
pects of the development of organs and tissues, such as inde- and 6.). Looking more closely at the basidioles as specific
pendent hymenophore transitions from circular pores to fertile cells within the hymenia, the three Agaricales dis-
angular pores, subporiod lamellae and full lamellae in the cussed in Section 6. distinguish all from each other. In C. cin-
genus Lentinus (Seelan et al., 2015). Nagy et al. (2011, 2013) erea and A. bisporus, basidioles arise in the hymenia as
concentrated on emergence of deliquescence (‘coprinoidiza- primary terminal cells of branches from ramified tramal hy-
tion’), i.e. cap autolysis as a derived mushroom character in phae curved out from inner trama (Buller, 1922; Rosin and
the Psathyrellaceae. The feature evolved at least four times Moore, 1985b; Cle mençon, 1997, 2004, 2012). While basidia
independently in the family from most recent common ances- maturation and basidiospore formation in C. cinerea is syn-
tors with non-deliquescent fruiting bodies. The authors found chronous (Lu, 1974a; Navarro-Gonza lez, 2008), basidia matu-
that deliquescence in the family evolved first, followed by ration and sporulation in A. bisporus occurs consecutively
correlated and elevated gain of further adaptative characters over the time (Hammond and Nichols, 1975; Elliott, 1977). In
such as sterile hyphidia (denoted pseudoparaphyses in their S. commune in contrast, most basidioles are formed in succes-
papers), voluminous hymenial cystidia (pleurocystidia), sion as out-growths of subbasidial hyphal cells and basidia
bimorphic basidia and a plicate cap surface (characters such maturation and sporulation thus occurs consecutively over
as all occurring in the ephemeral C. cinerea; Section 6.). The the time (Niederpruem et al., 1971; Niederpruem and Jersild,
non-deliquescent ancestors of the Psathyrellaceae had 1972). With a static primary basidiole population and synchro-
possibly evolved to make these derived changes more likely nized karyogamy, meiosis and basidiospore production in C.
to happen, but the genetic mechanisms behind these changes cinerea, the sterile binucleate hyphidia branch from the subba-
remain elusive. Are these polyphyletic physiological and sidial hyphal cells out instead of any secondary basidioles,
morphological changes in the Psathyrellaceae based on events once meiosis occurred in the existing basidioles (Rosin and
in homologous genes or are they caused by modifications in Moore, 1985b) and, importantly, these hyphidia do not un-
unrelated genes with resulting analogous phenotypic effects? dergo karyogamy and meiosis (Lu, 1974a; Rosin and Moore,
Notably, outside of the Psathyrellaceae, there are also a few 1985b). Hyphidia in the Psathyrellacaeae might thus be spe-
other examples of deliquescent fruiting bodies in the Agarica- cific transformations from cells being originally secondary
ceae and the Bolbitiaceae. The order of autolysis relative to basidioles, whereas the also sterile binucleate pleurocystidia
spore discharge differs in these compared to the Psathyrella- and cystesia are transformations of some of the primary basi-
ceae, prior and after, respectively (Singer, 1986; Hallen et al., dioles (Rosin and Moore, 1985a; Horner and Moore, 1987; Chiu
2003). This different timing is interpreted as possible existence and Moore, 1993; Nagy et al., 2011) and the multinucleate chei-
of distinct mechanisms and origins of deliquescence (Hallen locystidia at the freed ends of primary gills are cells of non-
et al., 2003; Nagy et al., 2011). hymenial tramal origin (Buller, 1924; Chiu and Moore, 1993).
As shown by the examples presented in this review, In A. bisporus as the third species of the presented Agaricales,
shaping of mushrooms principally follows defined routes (Sec- all basidioles enter meiosis with some of them carrying on one
tion 6.) but allows also an enormous flexibility for a species to after the other in sexual development whereas many others
react to changing environmental conditions and to establish persist continuously in prophase I to undertake the structural
genetic variation (Sections 4. and 5.). Selected model organ- job hyphidia have in C. cinerea (Buller, 1922; Allen et al., 1992).
isms can help to provide insights and understanding of both In conclusion, ontogeny and fate of hymenial cells and their
the ontogenetic and the phylogenetic plasticity in fruiting nuclei in the three species have all clear overlaps but also all
body morphologies. A wealth of literature is available on clear differences (Chiu and Moore, 1993). The gills and hyme-
mushroom development (Cle mençon, 1997, 2004, 2012) and nia in these three species have evidently elements of both, ho-
how closely related species might differ in major or minor de- mologies and analogies.
tails (for more insight into Agaricales see the books of Including A. auricula-judae, in the four species we have
Reijnders, 1963 and Singer, 1986). A deeply detailed picture described here in more detail, there are about 10 to more
of different steps throughout development has only emerged than 30 different cell types which contribute to the develop-
for certain species. The specimens described here more ment and the ultimate shape and function of a mushroom,

with the two gymnocarpous organisms having less cell types genetics. Molecular biological studies on individual genes
than the two hemiangiocarpous species (Section 6.). In other and outcomes of advanced modern ‘omics’ technologies
species, there might possibly be even more and there are have to be accurately conjoined with detailed enough excel-
certainly many other types of cells by which species distin- lent descriptions of morphology, cytology and ontology, to a
guish from each other. For example, three principle types of level and preciseness which we currently may not always or
main hyphal systems are described for tramal tissues of basi- not in all instances have at hand, even not for the established
diomes: Monomitic systems with only generative hyphae model species. Within and between the different species, we
(thin-walled, septate, branched, longitudinal or interwoven), need to come to easy to follow common concepts of descrip-
dimitic systems with generative and skeletal hyphae (thick- tions in simple terminology to avoid confusion and possible
walled, aseptate, unbranched, longitudinal), and trimitic sys- discouragement from reading the multifaceted and highly
tems with generative, skeletal, and binding hyphae (thick- specific literature in the field.
walled, aseptate, highly branched, interwoven, narrow).
These systems take into account similar hyphal shapes
to have similar functions. Generative hyphae are those that
ultimately give rise to the basidia and directly or indirectly Acknowledgements
to all other structures. Skeletal hyphae are giving rigidity to
a structure, and binding hyphae function in connecting the This paper has been dedicated to Prof. Karl Esser on the occa-
types of hyphae together. Originally applied to the sturdy pol- sion of his 90th birthday. We are indebted to members of our
ypores (Corner, 1932a,b), similar di- and trimitic hyphal sys- group, Susanna Badalyan and Alla Shnyreva for many chal-
tems have been observed in some of the Agaricales lenging discussions on mushroom development, to Matthias
(Redhead, 1987; Norvell, 1998; Cle mençon, 2005) whereas the Gube for advice on S. commune, to Karin Lange, Wassana Chai-
majority of fleshy Agaricales are monomitic and possess saena, Weeradej Khonsuntia and Kiran Lakkireddy for support
only generative hyphae (Singer, 1986; Pegler, 1996). in sample collecting, tissue sectioning, and photographing, to
Further visual differences between hyphae might exist ac- Neil Gow and Nick Read for the invitation to write this review
cording to the presence or absence of clamp cells and different and their long-lasting patience in waiting for the product, and
colouration and numbers of nuclei per hyphal cell (Corner, to Paul Dyer for language improvements. Work by MNG on
1932a,b; Cunningham, 1955; Moore 1998a), hyphae might be fruiting body development of C. cinerea was supported by CON-
narrow or inflated and functionally differentiated hyphal cells ACYT (Mexican Council for Science and Technology) in frame
terminal or intercalary localized, and there can be intermedi- of a PhD scholarship.
ate hyphal forms and composite forms (e.g. skeleto-
binding ¼ skeletoligative hyphae) (Pegler, 1996). Moreover,
functionally there might be more types of hyphae and hyphal references
cells in fruiting body tissues to be expected than what is visu-
ally recognized. The distinctive positions of two morpholog-
ical types of hyphae (narrow and inflated) in the stipes of C. Adams, J.F., 1918. Origin and development of the lamellae in
Schizophyllum commune. Mem. Torrey Bot. Club 17, 326e333.
cinerea are an excellent example for existence of this possibil-
Aime, M.C., Phillips-Mora, W., 2005. The causal agents of witches’
ity (Hammad et al., 1993b; Moore, 1998b). Not to be ignored, an
broom and frosty pod rot of cacao (chocolate, Theobroma cacoa)
additional range of specialized morphologically modified cells form a new lineage of Marasmiaceae. Mycologia 97, 1012e1022.
exists in different species as specific adaptations that Aime, M.C., Matheny, P.B., Henk, D.A., Frieders, E.M., Nilsson, R.H.,
contribute to mushroom structures, with different morpho- Piepenbring, M., McLaughlin, F.J., Szabo, L.J., Begerow, D.,
logical subforms, different positions (on the surface or in the Sampaio, J.P., Bauer, R., Weiß, M., Oberwinkler, F., Hibbett, D.,
inner tissues of caps or stipes, within hymenia) and different 2006. An overview of the higher level classification of Pucci-
niomycotina based on combined analyses of nuclear large and
cellular origins, such as cystidia, seta (‘stiff hairs’), dendroid
small subunit rDNA sequences. Mycologia 98, 896e905.
structures, lactifers (latex carrying hyphae), oleiferous ele-
Ainsworth, G.C., 1962. Longevity of Schizophyllum commune. Na-
ments (with resinous substances) to name just some (Lentz, ture 195, 1120e1121.
1954; Cunningham, 1955; Pegler, 1996). What are analogous Ajlouni, S.O., Beelman, R.B., Thompson, D.B., Mau, J.-L., 1992.
structures, which are homologous, what indeed is truly new Stipe trimming at harvest increases shelf-life of fresh mush-
and what in contrast is possibly lost between species? rooms (Agaricus bisporus). J. Food Sci. 57, 1361e1363.
The high variability of generic and individual mushroom Albee-Scott, S.R., 2007. Does secotioid inertia drive the evolution
of false-truffles? Mycol. Res. 111, 1030e1039.
shapes, of generic and fine structures and of locations of their
Allen, J., Moore, D., Elliott, T.J., 1992. Persistent meiotic arrest in
organs, tissues and types of cells, and of the developmental basidia of Agaricus bisporus. Mycol. Res. 96, 125e127.
patterns which with these are formed make it very difficult Anderson, E., Burns, C., Zolan, M.E., 2012. Global gene expression
or even impossible to define a fundamental basic concept of in Coprinopsis cinerea meiotic mutants reflects checkpoint ar-
how to shape a mushroom (Cle mençon, 2004, 2012). Still, as rest. G3-Gen. Genom. Genet. 10, 1213e1221.
hard as it is, we need to establish a framework to come closer Ando, Y., Nakazawa, T., Oka, K., Nakahori, K., Kamada, T., 2013.
Cc.snf5, a gene encoding a putative component of the SWI/SNF
to an understanding of mushroom development and tissue
chromatin remodeling complex, is essential for sexual devel-
differentiation in the Agaricomycetes and other Basidiomy-
opment in the agaricomycete Coprinopsis cinerea. Fungal Genet.
cetes. Thus, we have to further study and compare a few Biol. 50, 82e89.
selected, easy to handle and easy to manipulate species. Prog- Angeli-Papa, J., Eyme, J., 1978. Ultrastructural changes during
ress will be made through the application of molecular development of Agaricus bisporus and Agaricus sylvicola. In:

26 U. Ku lez
Chang, S.T., Hayes, W.A. (Eds.), The Biology and Cultivation of Bobbitt, T.F., Crang, R.E., 1974. Light effects on fruiting in Panus
Edible Mushrooms. Academic Press, New York, NY, pp. 53e81. tigrinus var. tigrinus. Can. J. Bot. 52, 255e257.
Arima, T., Yamamoto, N., Hirata, A., Kawano, S., Kamada, T., 2004. Bobbitt, T.F., Crang, R.E., 1975. Basidiocarp development of the
The eln3 gene involved in fruiting body morphogenesis of Copri- two varieties of Panus tigrinus and their light-induced
nus cinereus encodes a putative membrane protein with a general abnormal forms. Mycologia 67, 182e187.
glycosyltransferase domain. Fungal Genet. Biol. 41, 805e812. Borriss, H., 1934. Beitra € ge zur Wachstums- und Entwicklungs-
Atkinson, G.F., 1906. The development of Agaricus campestris. Bot. physiologie der Fruchtko € rper von Coprinus lagopus. Planta 22,
Gaz. 42, 241e264. 28e69.
Badalyan, S.M., Navarro-Gonza lez, M., Ku€ es, U., 2011. Taxonomic Bottoli, A.P.F., 2001. Metabolic and Environmental Control of
significance of anamorphic characteristics in the life cycle of Development in Coprinus cinereus. ETH Zurich, Zurich,
coprinoid mushrooms. In: Savoie, J.-M., Foulongne-Oriol, M., Switzerland. PhD thesis.
Largeteau, M., Barroso, G. (Eds.), Proceedings of the 7th Inter- Bougher, N.L., Tommerup, I.C., Malajczuk, N., 1993. Broad varia-
national Conference on Mushroom Biology and Mushroom tion in developmental and mature basidiome morphology of
Products (ICMBMP7) 2011, Vol. 1. INRA Bordeaux, Bordeaux, the ectomycorrhizal fungus Hydnangium sublamellatum sp.
France, pp. 140e154. nov. bridges morphologically based generic concepts of Hyd-
Ballou, L.R., Holton, R.W., 1985. Synchronous initiation and nangium, Podohydnangium and Laccaria. Mycol. Res. 97,
sporulation of fruitbodies by Coprinus cinereus on a defined 613e619.
medium. Mycologia 77, 103e108. Boulianne, R.P., Liu, Y., Aebi, M., Lu, B.C., Ku € es, U., 2000. Fruiting
Bandoni, R., Ginns, J., 1998. Notes on the Tremella mesenterica and body development in Coprinus cinereus: regulated expression of
allied species. Can. J. Bot. 76, 1544e1557. two galectins secreted by a non-classical pathway. Microbiol.
Banuett, F., Herskowitz, I., 1996. Discrete developmental stages 146, 1841e1853.
during teliospore formation in the corn smut fungus, Ustilago Bourne, A.N., Chiu, S.W., Moore, D., 1996. Experimental ap-
maydis. Development 112, 2965e2976. proaches to the study of pattern formation in Coprinus cinereus.
€ ßler, K., 1959. Squamanita Imbach in der Rheinpfalz gefunden.
Ba In: Chiu, S.W., Moore, D. (Eds.), Patterns in Fungal Develop-
Z. Pilzk. 25, 113e115. ment. Cambridge University Press, Cambridge, UK,
Bastos, C.N., Andebrhan, T., 1987. In vitro production of basidio- pp. 126e155.
spores of Crinipellis perniciosa, the causative agent of witches’ Braaksma, A., Von Doon, A.A., Kieft, H., Van Aelst, A.C., 1998.
broom disease of cocao. Trans. Br. Mycol. Soc. 88, 406e409. Effects of pre- and post-harvest development on Agaricus bis-
Baura, G., Szaro, T.M., Bruns, T.D., 1992. Gastrosuillus laricinus is a porus proteases. J. Hort. Sci. 63, 103e108.
recent derivative of Suillus grevillei: molecular evidence. My- Braaten, C.C., Matheny, P.B., Viess, D.L., Wood, M.G.,
cologia 84, 592e597. Williams, J.H., Bougher, N.L., 2013. Two new species of Inocybe
Begerow, D., Stoll, M., Bauer, R., 2006. A phylogenetic hypothesis from Australia and North America that include novel secotioid
of Ustilaginomycotina based on multiple gene analyses and forms. Botany 92, 9e22.
morphological data. Mycologia 98, 906e916. Brasier, C.M., 1970. Variation in a natural population of Schizo-
Benedix, E.H., 1960. Eine seltene Prolifikation von Clitocybe clavipes phyllum commune. Am. Natur. 104, 191e204.
(Pers. ex Fr.) Que l. Z. Pilzkd. 26, 4e8. Breitenbach, J., Kra € nzlin, F., 1984. Pilze der Schweiz, Vol. 1. My-
Benedix, E.H., 1967. Bemerkenswerte Prolifikationen bei Bla € tter- kologia Luzern, Luzern, Switzerland.
pilzen. Feddes Rep. 74, 201e207. Breitenbach, J., Kra € nzlin, F., 1986. Pilze der Schweiz, Vol. 2. My-
Binder, M., Bresinsky, A., 2002. Derivation of a polymorphic line- kologia Luzern, Luzern, Switzerland.
age of Gasteromycetes from boletoid ancestors. Mycologia 94, Breitenbach, J., Kra € nzlin, F., 1991. Pilze der Schweiz, Vol. 3. My-
85e98. kologia Luzern, Luzern, Switzerland.
Binder, M., Hibbett, D.S., Molitoris, H.P., 2001. Phylogenetic rela- Breitenbach, J., Kra € nzlin, F., 1995. Pilze der Schweiz, Vol. 4. My-
tionships of the marine gasteromycete Nia vibrissa. Mycologia kologia Luzern, Luzern, Switzerland.
93, 679e688. Brodie, H.J., 1958. Renewal of growth and occurence of twin fruit
Binder, M., Hibbett, D.S., Larsson, K.-H., Langer, E., Langer, G., bodies in the Nidulariaceae. Svenks Bot. Tidsk. 52, 371e378.
2005. The phylogenetic distribution of resupinate forms across Brodie, H.J., 1977. Twin fruit bodies in a slender-stemmed form of
the major clades of mushroom-forming fungi (Homobasidio- Cyathus stercoreus. Mycologia 69, 199e203.
mycetes). Syst. Biodiv. 3, 113e157. Bruns, T.D., Fogel, R., White, T.J., Palmer, J.D., 1989. Accelerated
Binder, M., Larsson, K.H., Matheny, P.B., Hibbett, D.S., 2010. evolution of a false-truffle from a mushroom ancestor. Nature
Amylocorticiales ord. nov and Jaapiales ord. nov.: early 339, 140e142.
diverging clades of Agaricomycetidae dominated by corticoid Buller, A.H.R., 1905. The reactions of the fruit-bodies of Lentinus
forms. Mycologia 102, 865e880. lepideus, Fr., to external stimuli. Ann. Bot. 19, 427e438.
Birkebak, J.M., Mayor, J.R., Ryberg, K.M., Matheny, P.B., 2013. A Buller, A.H.R., 1909. Researches on fungi, Vol. I. Longmans, Green
systematic, morphological and ecological overview of the and Co, London, UK.
Clavariaceae (Agaricales). Mycologia 105, 896e911. Buller, A.H.R., 1922. Researches on fungi, Vol. II. Longmans, Green
Bistis, G.N., Perkins, D.D., Read, N.D., 2003. Different cell types in and Co, London, UK.
Neurospora crassa. Fungal Genet. Newsl. 50, 17e19. Buller, A.H.R., 1924. Researches on fungi, Vol. III. Longmans,
Blattny , C., Kasala, B., Pila t, A., Santilliova -Svovbodova , J., Green and Co, London, UK.
Semerdz ieva, M., 1971. Proliferation of Armillariella mellea Bunyard, B.A., 2012. Which way is up? Fungi 5, 26e28.
(Vahl in Fl. Dan. ex Fr.) P. Karst. probably caused by a virus. Burns, C., Stajich, J.E., Rechtsteiner, A., Casselton, L.A.,

Cesk Mykol. 25, 66e74.
a Hanlon, S.E., Wilke, S.K., Savytskyy, O.P., Gathman, A.C.,
Blattny lik, O., Veselsky
, C., Kra , J., Kasala, B., Herzova , H., 1973. Lilly, W.W., Lieb, J.D., Zolan, M.E., Pukkila, P.J., 2010. Analysis
Particles resembling virions accompanying the proliferation of of the basidiomycete Coprinopsis cinerea reveals conservation
agaric mushrooms. Cesk Mykol. 27, 1e5.
a of the core meiotic expression program over half a billion
Bodensteiner, P., Binder, M., Moncalvo, J.-M., Agerer, R., years of evolution. PLoS Genet. 6, e1001135.
Hibbett, D.S., 2004. Phylogenetic relationships of cyphelloid Burton, K.S., Partis, M.D., Wood, D.A., Thurston, C.F., 1997.
homobasidiomycetes. Mol. Phyl. Evol. 33, 501e515. Accumulation of serine protease in senescent sporophores of

the cultivated mushroom, Agaricus bisporus. Mycol. Res. 101, mençon, H., 1997. Anatomie der Hymenomyceten. Eine
Cle
146e152. Einfu € hrung in die Cytologie und Plectologie der Krustenpilze,
Buschmann, A., 1960. Ein abnormer Fruchtko € rper von Pholiota Porlinge, Keulenpilze, Leistlinge, Bla € tterpilze und Ro € hrlinge. F.
squarrosa. Mitt. Naturwiss. Ver. Steiermark 90, 22e24. Flu€ ck-Wirth, Teufen, Switzerland.
Butler, G.G., 1988. Pattern of pore morphogenesis in the resupi- mençon, H., 2004. Cytology and Plectology of the Hymeno-
Cle
nate basidiome of Phellinus contiguous. Trans. Br. Mycol. Soc. mycetes. J. Cramer, Berlin, Germany.
91, 677e686. mençon, H., 2005. Basidiome development of Xeromphalina
Cle
Butler, G.M., 1992a. Location of hyphal differentiation in the agar campanella (Tricholomatales, Basidiomycetes). Persoonia 18,
pore field of the basidiome of Phellinus contiguous. Mycol. Res. 449e470.
313e317. mençon, H., 2012. Cytology and Plectology of the Hymeno-
Cle
Butler, G.M., 1992b. Capacity for differentiation of setae and other mycetes, second revised ed. J. Cramer in der Gebr. Borntraeger
hyphal types of the basidiome in explants from cultures of the Verlagsbuchhandlung, Stuttgart, Germany.
polypore Phellinus contiguus. Mycol. Res. 96, 949e955. Colavolpe, M.B., Alberto, E., 2014. Cultivation requirements and
Butler, G.M., 1995. Induction of precocious fruiting by a diffusible substrate degradation of the edible mushroom Gymnopilus
factor in the polypore Phellinus contiguus. Mycol. Res. 99, 325e329. pampeanus. A novel species for mushroom cultivation. Sci.
Butler, G.M., 2000. Morphology, rate and spatial density of seta Hort. 180, 161e166.
differentiation during in vitro development of the fruit body of Cooke, M.C., Berkeley, M.J., 1875. Fungi: Their Nature and Uses. S.
Phellinus contiguus. Mycol. Res. 104, 1493e1500. Appleton and Company, New York, NY.
Butler, G.M., Wood, A.E., 1988. Effects of environmental factors on Corner, E.J.H., 1932a. A Fomes with two systems of hyphae. Trans.
basidiome development in the resupinate polypore Phellinus Br. Mycol. Soc. 17, 51e81.
contiguus. Trans. Br. Myol. Soc. 90, 75e83. Corner, E.J.H., 1932b. The fruit-body of Polystictus xanthopus Fr.
Cabrera-Ponce, J.L., Leo n-Ramırez, C.G., Verver-Vargas, A., Palma- Ann. Bot. 46, 71e111.
Tirado, L., Ruiz-Herrera, J., 2012. Metamorphosis of the Basi- Corte s-Pe rez, A., Guzma n, G., Ramırez-Guillen, F., 2014. Squama-
diomycota Ustilago maydis: transformation of yeast-like cells nita umbonata (Fungi, Agaricales, Tricholomataceae), primer
into basidiocarps. Fungal Genet. Biol. 49, 765e771. registro en Me xico. Act. Bot. Mex. 108, 105e111.
Callac, P., Billette, C., Imbernon, M., Kerrigan, R.W., 1993. A new Cox, R.J., Niederpruem, D.J., 1975. Differentiation in Coprinus la-
tetrasporic variety of Agaricus bisporus occurs below sea level gopus. III. Expansion of excised fruit-bodies. Arch. Microbiol.
in the Sonoran desert of California. Mycologia 85, 835e851. 105, 257e260.
Callac, P., de Haut, I.J., Imbernon, M., Guinberteau, J., Craig, G.D., Gull, K., Wood, D.A., 1977. Stipe elongation in Agaricus.
Desmerger, C., Theochari, I., 2003. A novel homothallic variety J. Gen. Microbiol. 102, 337e347.
of Agaricus bisporus comprises rare tetrasporic isolates from Craig, G.D., Newsam, R.J., Gull, K., Wood, D.A., 1979. An ultra-
Europe. Mycologia 95, 222e231. structural and autoradiographic study of stipe elongation in
Cartwright, K.S.G., 1929. Notes on basidiomycetes grown in cul- Agaricus bisporus. Protoplasma 98, 15e29.
ture. Trans. Br. Mycol. Soc. 14, 300e305. Cunningham, G.H., 1955. Taxonomic problems of some hyme-
Celerin, M., Merino, S.T., Stone, J.E., Menzie, A.M., Zolan, M.E., nomyctes. Trans. Roy. Soc. N. Z. 82, 893e901.
2000. Multiple roles of Spo11 in meiotic chromosome Czederpiltz, D.L.L., Volk, T.J., Burdsall Jr., H.H., 2001. Field obser-
behavior. EMBO J. 19, 2739e2750. vation and inoculation experiments to determine the nature
Chaisaena, W., 2008. Light Effects on Fruiting Body Development of the carpophoroids associated with Entoloma abortivum and
of Wildtype in Comparison to Light-insensitive Mutant Strains Armillaria. Mycologia 93, 841e851.
of the Basidiomycete Coprinopsis cinerea, Grazing of Mites De Bary, A., 1884. Vergleichende Morphologie und Biologie der
(Tyrophagus putrescentiae) on the Strains and Production Pilze. Mycetozoen und Bakterien. Verlag von Wilhelm Engel-
of Volatile Organic Compounds during Fruiting Body Devel- mann, Leipzig, Germany.
opment. University of Go € ttingen, Go
€ ttingen, Germany. PhD De Groot, P.W.J., Schaap, P.J., Sonnenberg, A.S.M., Visser, J., Van
thesis. Griensven, L.J.L.D., 1996. The Agaricus bisporus hypA gene en-
Chang, S.T., Miles, P.G., 1989. Edible Mushrooms and Their Cul- codes a hydrophobin and specifically accumulates in peel
tivations. CRC Press Incorporation, Boca Raton, FL. tissue of mushroom caps during fruit body development. J.
Cheng, C.K., Au, C.H., Wilke, S.K., Stajich, J.E., Zolan, M.E., Mol. Biol. 257, 1008e1016.
Pukkila, P.J., Kwan, H.S., 2013. 50 -Serial analysis of gene De Groot, P.W.J., Schaap, P.J., Van Griensven, L.J.L.D., Visser, J.,
expression studies reveal a transcriptomic switch during 1997. Isolation of developmentally regulated genes from the
fruiting body development in Coprinopsis cinerea. BMC Genom. edible mushroom Agaricus bisporus. Microbiol. 143, 1993e2001.
14, 195. De Groot, P.W.J., Roeven, R.T.P., Van Griensven, L.J.L.D., Visser, J.,
Cheng, S., Tu, C.C., 1978. Ontogeny and development of the Schaap, P.J., 1999. Different temporal and spatial expression of
fruiting body of Auricularia polytricha. Mushroom Sci. X, two hydrophobin-encoding genes of the edible mushroom
713e722. Agaricus bisporus. Microbiol. 145, 1105e1113.
Cheng, X., Hui, J.H.L., Lee, Y.Y., Law, P.T.W., Kwan, H.S., 2015. A Delgado, J.C., Cook, A.A., 1976. Nuclear condition of the basidia,
‘developmental hourglass’ in fungi. Mol. Biol. Evol. 32, basidospores, and mycelium of Marasmius pernicious. Can. J.
1556e1566. http://dx.doi.org/10.1093/molbev/msv047. Bot. 54, 66e72.
Chiu, S.W., Moore, D., 1990. A mechanism for gill pattern forma- Desjardin, D.E., 2003. A unique ballistosporic hypogeous seques-
tion in Coprinus cinereus. Mycol. Res. 94, 320e326. trate Lactarius from California. Mycologia 95, 148e155.
Chiu, S.W., Moore, D., 1993. Cell form, function and lineage in the de Sena-Toma s, C., Navarro-Gonza lez, M., Ku rez-
€ es, U., Pe
hymenium of Coprinus cinereus and Volvariella bombycina. My- Martın, M.J., 2013. A DNA damage checkpoint pathway coor-
col. Res. 97, 221e226. dinates the division of dikaryotic cells in the ink cap mush-
Chiu, S.W., Moore, D., Chang, S.T., 1989. Basidiome polymor- room Coprinopsis cinerea. Genetics 195, 47e57.
phism in Volvariella bombycina. Mycol. Res. 92, 69e77. Donk, M.A., 1964. A conspectus of the families of Aphyllophor-
Claydon, N., 1985. Secondary metabolic products of selected ales. Persoonia 3, 199e324.
agarics. In: Moore, D., Casselton, L.A., Wood, D.A., Eastwood, D.C., Herman, B., Noble, R., Dobrovin-Pennington, A.,
Frankland, J.C. (Eds.), Developmental biology of higher fungi. Sreenivasaprasad, S., Burton, K.S., 2013. Environmental regu-
Cambridge University Press, Cambridge, UK, pp. 561e579. lation of reproductive phase change in Agaricus bisporus by 1-

28 U. Ku lez
octen-3-ol, temperature and CO2. Fungal Genet. Biol. 55, Greening, J.P., Sa nchez, C., Moore, D., 1997. Coordinated cell
53e66. elongation alone drives tropic bending in stems of the mush-
Elliott, C.G., 1994. Reproduction in Fungi. Genetical and Physio- room fruit body of Coprinus cinereus. Can. J. Bot. 75, 1175e1181.
logical Aspects. Chapman & Hall, London, UK. Grigoriev, I.V., Nikitin, R., Haridas, S., Kuo, A., Ohm, R., Otillar, R.,
Elliott, T.J., 1977. Basidiospore numbers in Agaricus bisporus Riley, R., Salamov, A., Zhao, X., Korzeniewski, F., Smirnova, T.,
(Lange) Imbach. J. Bac. 129, 525e526. Nordberg, H., Dubchak, I., Shabalov, I., 2013. MycoCosm portal:
Erdmann, S., Freihorst, D., Raudaskoski, M., Schmidt-Heck, W., gearing up for 1000 fungal genomes. Nucl. Acids Res. 42,
Jung, E.M., Senftleben, D., Kothe, E., 2012. Transcriptome and D699eD704.
functional analysis of mating in the basidiomycete Schizo- Gruen, H.E., 1963. Endogenous growth regulation in carpophores
phyllum commune. Eukaryot. Cell 11, 571e589. of Agaricus bisporus. Plant Phys. 38, 652e665.
Esser, K., 2000. Kryptogamen. Praktikum und Lehrbuch. 1. Cya- Gube, M., 2009. Ontogeny and Phylogeny of Gasteroid Members of
nobakterien, Algen, Pilze, Flechten, third ed. Springer, Berlin, Agaricaceae (Basidiomycetes). Friedrich-Schiller-University,
Heidelberg, Germany. Jena, Germany. PhD thesis.
Essig, F.M., 1922. The morphology, development and economic Haindl, E., Monzer, J., 1994. Elongation growth and gravitrophic
aspects of Schizophyllum commune Fries. Uni. Calif. Publ. Bot. 7, curvature in the Flammulina velutipes (Agaricales) fruiting
447e498. body. Exp. Mycol. 18, 150e158.
Evans, H.C., Holmes, K.A., Phillipps, W., Wilkinson, M.J., 2002. Hallen, H.E., Watling, R., Adams, G.C., 2003. Taxonomy and
What’s in a name: Crinipellis, the final resting place for the toxicity of Conocybe lactea and related species. Mycol. Res. 107,
frosty pod rot pathogen of cocoa? Mycologist 16, 148e152. 969e979.
Evans, H.C., Holmes, K.A., Reid, A.P., 2003. Phylogeny of the frosty Hammad, F., Ji, J., Watling, R., Moore, D., 1993a. Cell population in
pod rot pathogen of cacao. Plant Pathol. 52, 476e485. Coprinus cinereus: co-ordination of cell inflation throughout the
Evans, H.C., Bezerra, J.L., Barreto, R.W., 2013. Of mushrooms and maturing basidiome. Mycol. Res. 97, 269e274.
chocolate trees: aetiology and phylogeny of witches’ broom Hammad, F., Watling, R., Moore, D., 1993b. Cell population in
and frosty pod diseases of cacao. Plant Pathol. 62, 728e740. Coprinus cinereus: narrow and inflated hyphae. Mycol. Res. 97,
Fischer, R., Ku € es, U., 2003. Developmental processes in filamen- 275e282.
tous fungi. In: Prade, R.A., Bohnert, H.J. (Eds.), Genomics of Hammond, J.B.W., 1979. Changes in composition of harvested
plants and fungi. Marcel Dekker, New York, NY, pp. 41e118. mushrooms. Phytochem. 18, 415e418.
Flegg, F.B., Wood, D.A., 1985. Growth and fruiting. In: Flegg, F.B., Hammond, J.B.W., Nichols, R., 1975. Changes in respiration and
Spencer, D.M., Wood, D.A. (Eds.), The Biology and Technology soluble carbohydrates during the post-harvest storage of
of the Cultivated Mushroom. John Wiley, Chichester, UK, mushrooms (Agaricus bisporus). J. Sci. Fd. Agric. 26, 835e842.
pp. 141e178. Hasebe, K., Murakami, S., Tsuneda, A., 1991. Cytology and ge-
Flores, R., Dıaz, G., Honrubia, M., 2008. Mycorrhizal synthesis and netics of a sporeless mutant of Lentinus edodes. Mycologia 83,
basidioma primordium formation between Abies guatemalensis 354e359.
and Laccaria bicolor. Nova Hed. 87, 153e160. Hasselbring, H., 1907. Gravity as a form-stimulus of fungi. Bot.
Floudas, D., Held, B.W., Riley, R., Nagy, L.G., Koehler, G., Gaz. 43, 251e258.
Ransdell, A.S., Younus, H., Chow, J., Chiniquy, J., Lipzen, A., Hausknecht, A., Krisai-Greilhuber, I., 2006. Infrageneric division
Tritt, A., Sun, H., Haridas, S., LaButti, K., Ohm, R.A., Ku € es, U., €
of the genus Conocybe e a classical approach. Osterr. Z. Pilzk.
Blanchette, R.A., Grigoriev, I.V., Minto, R.E., Hibbett, D.S., 2015. 15, 187e212.
Evolution of novel wood decay mechanisms in Agaricales re- Hayes, W.A., 1978. Biological nature. In: Chang, S.T., Hayes, W.A.
vealed by the genome sequences of Fistulina hepatica and (Eds.), The Biology and Cultivation of Edible Mushrooms. Ac-
Cylindrobasidium torrendii. Fungal Genet. Biol. 76, 78e92. ademic Press, New York, NY, pp. 192e217.
Fritsche, G., 1968. Zu € chterische Arbeiten an „59c“, einem Cham- Heckman, C.A., Pelok, S.D., Kimpel, S.A., Wu, L.-C., 1989. Scanning
pignonstamm mit neuer Fruchtko € rperform. I. Steigerung des electron microscope studies on fruitbody primordium forma-
Ertrages. Theor. Appl. Genet. 38, 28e37. tion in Agaricus bisporus. Mycologia 81, 717e727.
Fritsche, G., 1972. Zu € chterische Arbeiten an „59c“, einem Cham- Hein, I., 1930. Studies on morphogenesis in Agaricus (Psalliota)
pignonstamm mit neuer Fruchtko € rperform. II. Cytologische campestris. Am. J. Bot. 17, 882e915.
Untersuchungen. Theor. Appl. Genet. 42, 44e50. Heneghan, M.N., Porta, C., Zhang, C., Burton, K.S., Challen, M.P.,
Fritsche, G., von Sengbusch, R., 1969. Klumpenfo € rmige Cham- Bailey, A.M., Foster, G.D., 2009. Characterization of serine
pignonfruchtko € rper. Naturwiss. 56, 30e33. proteinase expression in Agaricus bisporus and Coprinopsis cin-
Fu, S.C., Zhang, M.Y., Shang, X.D., Chen, M.J., Tan, Q., 2011. An erea by using green fluorescent protein and the A. bisporus
axenic culture system for fruiting body formation by an edible SPR1 promoter. Appl. Microbiol. Biotechnol. 75, 792e801.
Bolete phylogenetically related to culinary-medicinal penny Henk, D.A., Vilgalys, R., 2007. Molecular phylogeny suggests a
bun mushroom, Boletus edulis Bull.:Fr. strains from China. Int. single origin of insect symbiosis in the Pucciniomycetes with
J. Med. Mushrooms 13, 387e395. support for some relationships within the genus Septobasi-
Giachini, A.J., Hosaka, K., Nouhra, E., Spatafora, J., Trappe, J.M., dium. Am. J. Bot. 94, 1515e1526.
2010. Phylogenetic relationships of the Gomphales based on Henkel, T.W., Smith, M.E., Aime, M.C., 2010. Guyanagaster, a new
nuc-25S-rDNA, mit-12S-rDNA, and mit-atp6-DNA combined wood-decaying sequestrate fungal genus related to Armillaria
sequences. Fungal Biol. 114, 224e234. (Physalariaceae, Agaricales, Basidiomycota). Am. J. Bot. 97,
Gooday, G.W., 1974. Control of development of excised fruit 1474e1484.
bodies and stipes of C. cinereus. Trans. Br. Mycol. Soc. 62, Hibbett, D.S., 2004. Trends in morphological evolution in homo-
391e399. basidiomycetes inferred using maximum likelihood: A com-
Gooday, G.W., 1975. The control of differentiation in fruit bodies parison of binary and multistate approaches. Syst. Biol.
of Coprinus cinereus. Rep. Tottori Mycol. Inst. 12, 151e160. 889e903.
Gramss, G., 1978. Die Fruchtko € rperbildung ho € herer Pilze II. Hibbett, D.S., 2006. A phylogenetic overview of the Agaricomy-
Holzzersto € rende Basidiomyceten. Z. Mykol. 45, 195e208. cotina. Mycologia 98, 917e925.
Granado, J.D., Kertesz-Chaloupkova , K., Aebi, M., Ku€ es, U., 1997. Hibbett, D.S., 2007. After the gold rush, or before the flood?
Restriction enzyme-mediated DNA integration in Coprinus Evolutionary morphology of mushroom-forming fungi (Agar-
cinereus. Mol. Gen. Genet. 256, 28e36. icomycetes) in the 21st century. Mycol. Res. 111, 1001e1008.

Hibbett, D.S., Binder, M., 2002. Evolution of complex fruiting body fruitbody morphology on various environmental conditions in
morphologies in homobasidiomycetes. Proc. Roy. Soc. Lond. B Pleurotus ostreatus. Mycobiology 31, 145e150.
269, 1963e1969. Jones, D., McHardy, W.J., 1985. Scanning electron microscopy of
Hibbett, D.S., Vilgalys, R., 1993. Phylogenetic relationships of cryofixed and critical point-dried Coprinus cinereus. Micron
Lentinus (Basidiomycotina) inferred from molecular and Microsc. Acta 16, 115e123.
morphological characters. Syst. Bot. 18, 409e433. € rgens, C., 1958. Physiologische und genetische Untersuchungen
Ju
Hibbett, D.S., Murakami, S., Tsuneda, A., 1993. Hymenophore u€ ber die Fruchtko € rperbildung bei Schizophyllum commune.
development and evolution in Lentinus. Mycologia 85, 428e443. Arch. Mikrobiol. 31, 388e421.
Hibbett, D.S., Tsuneda, A., Murakami, S., 1994. The secoid form of Justo, A., Hibbett, D., 2011. Phylogenetic classification of Trametes
Lentinus tigrinus - Genetics and development of a fungal (Basidiomycota, Polyporales) based on a five-marker dataset.
morphological innovation. Am. J. Bot. 81, 466e478. Taxon 60, 1567e1583.
Hibbett, D.S., Pine, E.M., Langer, E., Langer, G., Donoghue, M.J., Justo, A., Morgenstern, I., Hallen-Adams, H.E., Hibbett, D.S., 2010.
1997. Evolution of gilled mushrooms and puffballs inferred Convergent evolution of sequestrate forms in Amanita under
from ribosomal DNA sequences. Proc. Natl. Acad. Sci. U. S. A. Mediterreanean climate conditions. Mycologia 102, 675e688.
94, 12002e12006. Kamada, T., 1994. Stipe elongation in fruit bodies. In:
Hibbett, D.S., Binder, M., Bischoff, J.F., Blackwell, M., Cannon, P.F., Wessels, J.G.H., Meinhardt, F. (Eds.), The Mycota, Growth,
Eriksson, O.E., Huhndorf, S., James, T., Kirk, P.M., Lu € cking, R., Differentiation and Sexuality, Vol. I. Springer-Verlag, Berlin,
Lumbsch, H.T., Lutzoni, F., Matheny, P.B., McLaughlin, D.J., Germany, pp. 367e380.
Powell, M.J., Redhead, S., Schoch, C.L., Spatafora, J.W., Kamada, T., 2002. Molecular genetics of sexual development in
Stalpers, J.A., Vilgalys, R., Aime, M.C., Aptroot, A., Bauer, R., the mushroom Coprinus cinereus. BioEssays 24, 449e459.
Begerow, D., Benny, G.L., Castlebury, L.A., Crous, P.W., Dai, Y.- Kamada, T., Takemaru, 1977. Stipe elongation during basidiocarp
C., Gams, W., Geiser, D.M., Griffith, G.W., Gueidan, C., maturation in Coprinus macrorhizus: mechanical properties of
Hawksworth, D.L., Hestmark, G., Hosaka, K., Humber, R.A., the stipe cell wall. Plant Cell Physiol. 18, 831e840.
Hyde, K.D., Ironside, J.E., Ko ~ ljalg, U., Kurtzman, C.P., Kamada, T., Tsuji, M., 1979. Darkness-related factor affecting
Larsson, K.-H., Lichtwardt, R., Longcore, J., Mia˛dlikowska, J., basidiocarp maturation in Coprinus macrorhizus. Plant Cell
Miller, A., Moncalvo, J.-M., Mozley-Standridge, S., Physiol. 20, 1445e1448.
Oberwinkler, F., Parmasto, E., Reeb, V., Rogers, J.D., Roux, C., Kamada, T., Tsuru, M., 1993. The onset of the helical arrangement
Ryvarden, L., Sampaio, J.P., Schu € ßler, A., Sugiyama, J., of chitin microfibrils in fruit-body development of Coprinus
Thorn, R.G., Tibell, L., Untereiner, W.A., Walker, C., Wang, Z., cinereus. Mycol. Res. 97, 884e888.
Weir, A., Weiss, M., White, M.M., Winka, K., Yao, Y.-J., Kamada, T., Kurita, R., Takemaru, T., 1978. Effects of light on
Zhang, N., 2007. A higher-level phylogenetic classification of basidiocarp maturation in Coprinus macrorhizus. Plant Cell
the Fungi. Mycol. Res. 111, 509e547. Physiol. 19, 263e275.
Hibbett, D.S., Bauer, R., Binder, M., Giachini, A.J., Hosaka, K., Kamada, T., Sano, H., Nakazawa, T., Nakahori, K., 2010. Regula-
Justo, A., Larsson, E., Larsson, K.H., Lawrey, J.D., Moettinen, O., tion of fruiting body photomorphogenesis in Coprinopsis cin-
Nagy, L.G., Nilsson, R.H., Weiss, M., Thorn, R.G., 2014. Agari- erea. Fungal Genet. Biol. 47, 917e921.
comycetes. In: McLaughlin, D.J., Spatafora, J.W. (Eds.), The Kanda, T., Goto, A., Sawa, K., Arakawa, H., Yasuda, Y.,
Mycota, Systematics and Evolution. Part A., second ed., Vol. 7. Takemaru, T., 1989. Isolation and characterisation of recessive
Springer, Heidelberg, Germany, pp. 373e429. sporeless mutants in the basidiomycete Coprinus cinereus. Mol.
Horikoshi, T., Kitamoto, Y., Kasai, Z., 1974. Effect of light on the Gen. Genet. 216, 526e529.
initiation of pileus formation in a basidiomycete, Favolus ar- Kaneko, A., Sagara, N., 2001. Responses of lignicolous-agaric
cularius. Plant Cell Pysiol. 15, 903e911. fruit-bodies to light and gravity: a study to overview the fruit-
Horner, J., Moore, D., 1987. Cystidial morphogenetic field in the body development in hymenomycetes. Mycoscience 42,
hymenium of Coprinus cinereus. Trans. Br. Mycol. Soc. 88, 301e310.
479e488. Kaneko, A., Sagara, N., 2002. Responses of Hebeloma radicosum
Hosaka, K., Bates, S.T., Beever, R.E., Castellano, M.A., fruit-bodies to light and gravity: negatively gravitropic and
Colgan III, W., Dominguez, L.S., Nourhra, E.R., Geml, J., nonphototrophic growth. Mycoscience 43, 7e13.
Giachini, A.J., Kebbey, S.R., Simpson, N.R., Spatafora, J.W., Kasuya, T., Hosaka, K., Uno, K., Kakishima, M., 2012. Phylogenetic
Trappe, J.M., 2006. Molecular phylogenies of the gomphoid- placement of Geastrum melanocephalum and polyphyly of
phalloid fungi with an establishment of the new subclass Geastrum triplex. Mycoscience 53, 411e426.
Phallomycetidae and two new orders. Mycologia 98, Kern, V.D., Mendgen, K., Hock, B., 1997. Flammulina as a model
949e959. system for fungal graviresponses. Planta 203, S23eS32.
Hughey, B.D., Adams, G.C., Bruns, T.D., Hibbett, D.S., 2000. Phy- Kertesz-Chaloupkova , K., Walser, P.J., Granado, J.D., Aebi, M.,
logeny of Calostoma, the gelatinous-stalked puffball, based on Ku € es, U., 1998. Blue light overrides repression of asexual
nuclear and mitochondrial ribosomal DNA sequences. Myco- sporulation by mating type genes in the basidiomycete Copri-
logia 92, 94e104. nus cinereus. Fungal Genet. Biol. 23, 95e109.
Iten, 1970. Zur Funktion hydrolytischer Enzyme bei der Autolyse Kimaru, K., Takemaru, T., 1955. Cytological studies of fungi: I.
von Coprinus. Ber. Schweiz. Bot. Ges. 79, 175e198. Basidial development of Coprinus macrorhizus Rea f. microsporus
Iten, W., Matile, P., 1970. Role of chitinase and other lysosomal Hongo. Biol. J. Okayama Uni. 2, 51e61.
enzymes of Coprinus lagopus in the autolysis of fruiting bodies. Kinugawa, K., Suzuki, A., Takamatsu, Y., Kato, M., Tanaka, K.,
J. Gen. Microbiol. 61, 301e309. 1994. Effects of concentrated carbon dioxide on the fruiting of
Jablonsky , I., 1981. Einfluß von Milieufaktoren auf die Ent- several cultivated basidiomycetes (II). Mycoscience 35,
wicklung und Ausbeute der Fruchtko € rper von Lentinus edodes 345e352.
(Berk.) Sing. Z. Mykol. 47, 291e299. Kinoshita, A., Sasaki, H., Nara, K., 2012. Multiple origins
James, S.W., McLaughlin, D.J., 1988. The influence of carbohydrate of sequestrate basidiomes within Entoloma inferred
source and concentration and light on fruitbody development from molecular phylogenetic analysis. Fungal Biol. 116,
in Clavicorona pyxidata. Mycologia 80, 89e98. 1250e1262.
Jang, K.-Y., Jhune, C.-S., Park, J.-S., Cho, S.-M., Weon, H.-Y., Kirk, P.M., Cannon, P.F., Minter, D.W., Stalpers, J.A., 2011. Dictio-
Cheong, J.-C., Choi, S.-G., Sung, J.-M., 2003. Characterization of nary of the Fungi, 10th ed. CABI Europe, Wallingford, UK.

30 U. Ku lez
Kitamoto, Y., Takahashi, M., Kasai, Z., 1968. Light-induced for- Lakkireddy, K.K.R., Navarro-Gonza lez, M., Velagapudi, R.,
mation of fruit-bodies in a basidiomycete, Favolus arcularius Ku € es, U., 2011. Proteins expressed during hyphal aggregation
(Fr.) Ames. Plant Cell Physiol. 9, 797e805. for fruiting body formation in Basidiomycetes. In: Savoie, J.-
Knabe, N., Jung, E.-M., Freihorst, D., Hennicke, F., Horton, J.S., M., Foulongne-Oriol, M., Largeteau, M., Barroso, G. (Eds.), Pro-
Kothe, E., 2013. A central role for Ras1 in morphogenesis of the ceedings of the 7th International Conference on Mushroom
basidiomycete Schizophyllum commune. Eukaryot. Cell 12, Biology and Mushroom Products (ICMBMP7) 2011, Vol. 2. INRA
941e952. Bordeaux, Bordeaux, France, pp. 82e95.
Knaus, K., Blab, G.A., Agronskaia, A.V., van den Heuvel, D.J., Largeteau, M.L., Savoie, J.-M., 2008. Effect of the fungal pathogen
Gerritsen, H.C., Wo € sten, H.A.B., 2013. Monitoring the metabolic Verticillium fungicola on fruiting initiation of its host, Agaricus
state of fungal hyphae and the presence of melanin by nonlinear bisporus. Mycol. Res. 112, 825e828.
spectral imaging. Appl. Environ. Microbiol. 79, 6345e6350. Largeteau, M.L., Savoie, J.-M., 2010. Microbially induced diseases of
€
Kniep, H., 1911. Uber das Auftreten von Basidien im einkernigen Agaricus bisporus: biochemical mechanisms and impact on
Mycel von Armillaria mellea Fl. Dan. Z. Bot. 3, 529e553. commercial production. Appl. Microbiol. Biotechnol. 86, 63e73.
Kong, W.-S., 2004. Descriptions of commercially important Larsson, E., Jeppson, M., 2008. Phylogenetic relationships among
Pleurotus species. In: MushWorld (Ed.), Mushroom Growers’s species and genera of Lycoperdaceae based on ITS and LSU
Handbook 1: Oyster Mushrooom Cultivation. MushWorld, sequence data from north European taxa. Mycol. Res. 112,
Seoul, Korea, pp. 54e61. 4e22.
Kretzer, A., Bruns, T.D., 1997. Molecular revisitation of the genus Larsson, K.-H., 2007. Re-thinking the classification of corticioid
Gastrosuillus. Mycologia 89, 586e589. fungi. Mycol. Res. 111, 1040e1063.
€ es, U., 2000. Life history and developmental processes in the
Ku Leach, J., 2013. Squamanita odorata found in Britain. Field Mycol.
basidiomycete Coprinus cinereus. Microbiol. Mol. Biol. Rev. 64, 14, 53e55.
316e353. Lebel, T., 2013. Two new species of sequestrate Agaricus (section
€ es, U., 2015. From two to many: multiple mating types in ba-
Ku Minores) from Australia. Mycol. Prog. 12, 699e707.
sidiomycetes. Fungal Biol. Rev. (special issue). Lebel, T., Tonkin, J.E., 2007. Australasian species of Macowanites
€ es, U., Liu, Y., 2000. Fruiting body production in basidiomy-
Ku are sequestrate species of Russula (Russulaceae, Basidiomy-
cetes. Appl. Microbiol. Biotechnol. 54, 141e152. cotina). Aust. Syst. Bot. 20, 355e381.
€ es, U., Granado, J.D., Hermann, R., Boulianne, R.P., Kertesz-
Ku Lebel, T., Vellinga, E.C., 2013. Description and affinities of a
Chaloupkova , K., Aebi, M., 1998. The A mating type and blue sequestrate Lepiota (Agaricaceae) from Australia. Mycol. Prog.
light regulate all known differentiation processes in the 12, 525e532.
basidiomycete Coprinus cinereus. Mol. Gen. Genet. 260, 81e91. Lebel, T., Orihara, T., Maekawa, N., 2012. The sequestrate genus
€ es, U., Polak, E., Bottoli, A.P.F., Hollenstein, M., Walser, P.J.,
Ku Rosbeeva T.Lebel & Orihara gen. nov. (Boleteacae) from Aus-
Boulianne, R.P., Hermann, R., Aebi, M., 2002a. Vegetative tralasia and Japan: new species and new combinations. Fungal
development in Coprinus cinereus. In: Osiewacz, H.D. (Ed.), Div. 52, 49e71.
Molecular biology of fungal development. Marcel Dekker, Inc., Lentz, P.L., 1954. Modified hyphae of hymenomycetes. Bot. Rev.
New York, NY, pp. 133e163. 20, 135e199.
€ es, U., Walser, P., Klaus, M.J., Aebi, M., 2002b. Influence of
Ku n-Ramirez, C.G., Sa
Leo nchez-Arreguın, J.A., Cabrera-Ponce, J.L.,
activated A and B mating-type pathways on the develop- Ruiz-Herrera, J., 2014. Role of white collar proteins in the Ba-
mental processes in the basidiomycete Coprinus cinereus. Mol. sidiomycota fungus Ustilago maydis. In: Deshpande, M.V., Ruiz-
Genet. Genom. 268, 262e271. Herrera, J., Gour, H.N., Giri, A.P., Ghormade, V., Tupe, S.G.
€ es, U., Ku
Ku € nzler, M., Bottoli, A.P.F., Walser, P.J., Granado, J.D., (Eds.), Biotechnology: Beyond Borders. CSIR-National Chemi-
Liu, Y., Bertossa, R.C., Ciardo, D., Clergeot, P.-H., Loos, S., cal Laboratory, Pune, India, pp. 39e49.
Ruprich-Robert, G., Aebi, M., 2004. Mushroom development in Levine, M., 1922. The origin and development of lamellae in
higher basidiomycetes; implications for human and animal Agaricus campestris and in certain species of Coprinus. Am. J.
health. In: Kushwaha, R.K.S. (Ed.), Fungi in human and in Bot. 9, 509e533.
animal health. Scientific Publishers, Jodhpur, India, pp. Leonard, T.J., Dick, S., 1968. Chemical induction of haploid fruit-
431e469. ing bodies in Schizophyllum commune. Proc. Natl. Acad. Sci. U. S.
Ku lez, M., Srivilai, P., Chaisaena, W., A. 59, 745e751.
Velagapudi, R., 2007. Mushroom biology and genetics. In: Linder, D.H., 1933. The genus Schizophyllum. I. Species of the
Ku€ es, U. (Ed.), Wood Production, Wood Technology, and Western Hemisphere. Am. J. Bot. 20, 552e564.
Biotechnological Impacts. Universita € tsverlag Go€ ttingen, Lingelsheim, A., 1917. Abnorme Fruchtko € rper von Lentinus squa-
Go€ ttingen, Germany, pp. 587e607. mosus (Schaeff.) Schro € t. (Agaricus lepideus Fr.). Beih. Bot. Cent.
€ es, U., Nelson, D.R., Liu, C., Yu, G.-J., Zhang, J., Li, J., Wang, X.-
Ku 34, 205e207.
C., Sun, H., 2015. Genome analysis of medicinal Ganoderma Liu, Y., 2001. Fruiting Body Initiation in the Basidiomycete Copri-
spp. with plant-pathogenic and saprotrophic life-styles. nus cinereus. ETH Zurich, Zurich, Switzerland. PhD thesis.
Phytochem 114, 18e37. http://dx.doi.org/10.1016/j.phytochem. Liu, Y., Srivilai, P., Loos, S., Aebi, M., Ku € es, U., 2006. An essential
2014.11.019. gene for fruiting body initiation in the basidiomycete Copri-
Kumar, T.K.A., Celio, G.J., Matheny, P.B., MyLaughlin, D.J., nopsis cinerea is homologous to bacterial cyclopropane fatty
Hibbett, D.S., Manimohan, P., 2007. Phylogenetic relationships acid synthase genes. Genetics 172, 873e884.
of Auriculoscypha based on ultrastructural and molecular Lohwag, K., 1955. Wachstumsversuche mit Lenzites betulina (L.) FR.
studies. Mycol. Res. 111, 268e274. €
Osterr. Bot. Zeitschr. 102, 524e528.
Kuratani, M., Tanaka, K., Terashima, K., Muraguchi, H., Lowy, B., 1951. A morphological basis for classifying the species of
Nakazawa, T., Nakahori, K., Kamada, T., 2010. The dst2 gene Auricularia. Mycologia 43, 351e358.
essential for photomorphogenesis of Coprinopsis cinerea en- Lowy, B., 1952. The genus Auricularia. Mycologia 44, 656e690.
codes a protein with a FAD-binding-4 domain. Fungal Genet. Lu, B.C., 1974a. Meiosis in Coprinus. V. The role of light on basi-
Biol. 47, 152e158. diocarp initiation, mitosis, and hymenium differentiation in
Labbe, J., Uehling, J., Payen, T., Plett, J., 2014. Fungal biology: Coprinus lagopus. Can. J. Bot. 52, 299e305.
compiling genomes and exploiting them. New Phytol. 203, Lu, B.C., 1974b. Meiosis in Coprinus: VI. The control of initiation of
359e361. meiosis. Can. J. Genet. Cytol. 16, 155e164.

Lu, B.C., 1982. Replication of deoxyribonucleic acid and crossing McLaughlin, D.C., 1973. Ultrastructure of sterigma growth and
over in Coprinus. In: Wells, K., Wells, E.K. (Eds.), Basidium and basidiospore formation in Coprinus and Boletus. Can. J. Bot. 51,
Basidiocarp. Evolution, Cytology, Function, and Development. 145e150.
Springer, New York, Heidelberg, Berlin, pp. 93e112. McLaughlin, D.C., 1977. Basidiospore initiation and early devel-
Lu, B.C., 1991. Cell degeneration and gill remodeling during basi- opment in Coprinus cinereus. Am. J. Bot. 64, 1e16.
diocarp development in the fungus Coprinus cinereus. Can. J. McLaughlin, D.C., 1982. Ultrastructure and cytochemistry of ba-
Bot. 69, 1161e1169. sidial and basidiospore development. In: Wells, K., Wells, E.K.
Lu, B.C., 2000. The control of meiosis progression in the fungus (Eds.), Basidium and Basidiocarp. Evolution, Cytology, Func-
Coprinus cinereus by light/dark cycles. Fungal Genet. Biol. 31, tion, and Development. Springer, New York, Heidelberg, Ber-
33e41. lin, pp. 37e74.
Lu, B.C.K., 2006. Programmed cell death in fungi. In: Ku € es, U., McLaughlin, D.C., Beckett, A., 1987. Low temperature scanning
Fischer, R. (Eds.), The Mycota, Growth, Differentiation and electron microscopy of discharged basidiospores of Coprinus
Sexuality, second ed., Vol. I. Springer, Berlin, Heidelberg, cinereus. Mycologia 79, 158e161.
Germany, pp. 167e187. Miettinen, O., Larsson, E., Sjo € kvist, E., Larsson, K.-H., 2012.
Lu, B.C., Jeng, D.Y., 1975. Meioisis in Coprinus. VII. The prekar- Comprehensive taxon sampling reveals unaccounted diver-
yogamy S-phase and the postkaryogamy DNA replication in C. sity and morphological plasticity in a group of dimitic poly-
lagopus. J. Cell Sci. 17, 461e470. pores (Polyporales, Basidiomycota). Cladistics 28, 251e270.
Lu, B.C., Gallo, N., Ku € es, U., 2003. White-cap mutants and meiotic Miller, O.K., 1971. The relationship of cultural characters to the
apoptosis in the basidiomycete Coprinus cinereus. Fungal taxonomy of the agarics. In: Petersen, R.H. (Ed.), Evolution in
Genet. Biol. 39, 82e93. the Higher Basidiomycetes. University of Tennessee Press,
Magnus, W., 1906. Uber € die Formbildung der Hutpilze. Arch. Bio- Knoxville, TN, pp. 197e215.
ntol. 1, 86e161. Miller, S.L., Larsson, E., Larsson, K.-H., Verbeken, A., Nuytinck, J.,
Maniotis, J., 1964. The coprinoid state of Rhacophillus lilacinus. Am. 2006. Prespectives in the new Russuales. Mycologia 98,
J. Bot. 51, 485e494. 960e970.
Manocha, M.S., 1965. Fine structure of the Agaricus carpophore. Millanes, A.M., Diederich, P., Ekman, S., Wedin, M., 2011. Phy-
Can. J. Bot. 43, 1329e1333. logeny and character evolution in the jelly fungi (Tremellomy-
Martin, F., Aerts, A., Ahre n, D., Brun, A., Danchin, E.G.J., cetes, Basidiomycota, Fungi). Mol. Phyl. Evol. 61, 12e28.
Duchaussoy, F., Gibon, J., Kohler, A., Lindquist, E., Pereda, V., Miyazaki, Y., Masuno, K., Abe, M., Nishizawa, H., Matsumoto, T.,
Salamov, A., Shapiro, H.J., Wuyts, J., Blaudez, D., Bue e, M., Kunitomo, S., Sakata, H., Nakamura, K., Koyama, T., Ito, M.,
Brokstein, P., Canba € ck, B., Cohen, D., Courty, P.E., Kazama, H., Suzuko, D., Obatake, Y., Sano, H., Nakamura, M.,
Coutinho, P.M., Delaruelle, C., Detter, J.C., Deveau, A., Miyazaki, K., Sakamoto, Y., Kaneko, S., Kamada, T., 2011.
DiFazio, S., Duplessis, S., Fraissinet-Tachet, L., Lucic, E., Frey- Light-stimulative effects on the cultivation of edible mush-
Klett, P., Fourrey, C., Feussner, I., Gay, G., Grimwood, J., rooms by using blue LED. In: Savoie, J.-M., Foulongne-Oriol, M.,
Hoegger, P.J., Jain, P., Kilaru, S., Labbe , J., Lin, Y.C., Legue , V., Le Largeteau, M., Barroso, G. (Eds.), Proceedings of the 7th Inter-
Tacon, F., Marmeisse, R., Melayah, D., Montanini, B., national Conference on Mushroom Biology and Mushroom
Muratet, M., Nehls, U., Niculita-Hirzel, H., Oudet-Le Secq, M.P., Products (ICMBMP7) 2011, Vol. 2. INRA Bordeaux, Bordeaux,
Peter, M., Quesneville, H., Rajashekar, B., Reich, M., France, pp. 58e67.
Rouhier, N., Schmutz, J., Yin, T., Chalot, M., Henrissat, B., Moncalvo, J.-M., Vilgalys, R., Redhead, S.A., Johnson, J.E.,
Ku € es, U., Lucas, S., Van de Peer, Y., Podila, G.K., Polle, A., James, T.Y., Aime, M.C., Hofstetter, V., Verdiun, S., Larsson, E.,
Pukkila, P.J., Richardson, P.M., Rouze , P., Sanders, I.R., Baroni, T.J., Thorn, R.G., Jacobsson, S., Cle mençon, H.,
Stajich, J.E., Tunlid, A., Tuskan, G., Grigoriev, I.V., 2008. The Miller Jr., O.K., 2002. One hundred and seventeen clades of
genome of Laccaria bicolor provides insights into mycorrhizal euagarics. Mol. Phyl. Evol. 23, 357e400.
symbiosis. Nature 452, 88e92. Morimoto, N., Oda, Y., 1973. Effects of light on fruitbody forma-
Martın, M.P., Ho € gberg, N., Llistosella, J., 1999. Macowanites messa- tion in a basidiomycete, Coprinus macrorhizus. Plant Cell
picoides, a hypogeous relative of Russula messapica. Mycol. Res. Physiol. 14, 217e225.
103, 203e208. Morimoto, N., Oda, Y., 1974. Photo-induced karyogamy in a
Matheny, P.B., Curtis, J.M., Hofstetter, V., Aime, M.C., basidiomycete, Coprinus macrorhizus. Plant Cell Physiol. 15,
Moncalvo, J.M., Ge, Z.W., Yang, Z.L., Slot, J.C., Ammirati, J.F., 183e186.
Baroni, T.J., Bougher, N.L., Hughes, K.W., Lodge, D.J., Morin, E., Kohler, A., Baker, A.R., Foulongne-Oriol, M.,
Kerrigan, R.W., Seidl, M.T., Aanen, D.K., DeNitis, M., Lombard, V., Nagy, L.G., Ohm, R.A., Patyshakuliyeva, A.,
Daniele, G.M., Desjardin, D.E., Kropp, B.R., Norvell, L.L., Brun, A., Aerts, A.L., Bailey, A.M., Billette, C., Coutinho, P.M.,
Parker, A., Vellinga, E.C., Vilgalys, R., Hibbett, D.S., 2006. Major Deakin, G., Doddapaneni, H., Floudas, D., Grimwood, J.,
clades of Agaricales: a multilocus phylogenetic overview. Hilden, K., Ku€ es, U., LaButti, K.M., Lapidus, A., Lindquist, E.A.,
Mycologia 98, 982e995. Lucas, S.M., Murat, C., Riley, R.W., Salamov, A.A., Schmutz, J.,
Matheny, P.B., Griffith, G.W., 2010. Mycoparasitism between Subramanian, V., Wo € sten, H.A.B., Xu, J.P., Eastwood, D.C.,
Squamanita paradoxa and Cystoderma amianthinum (Cystoder- Cullen, D., de Vries, R.P., Lundell, T., Hibbett, D.S.,
mateae, Agaricales). Mycoscience 51, 456e461. Henrissat, B., Burton, K.S., Kerrigan, R.W., Challen, M.P.,
Mathew, K.T., 1961. Morphogenesis of mycelial strands in the Grigoriev, I.V., Martin, F., 2012. Genome sequence of the but-
cultivated mushroom, Agaricus bisporus. Trans. Br. Mycol. Soc. ton mushroom Agaricus bisporus reveals mechanisms govern-
44, 285e290. ing adaptation to humic-rich ecological niche. Proc. Natl.
Matthews, T.R., Niederpruem, D.J., 1972. Differentiation in Copri- Acad. Sci. U. S. A. 109, 17501e17506.
nus lagopus. I. Control of fruiting and cytology of initial events. Moore, D., 1981. Developmental genetics of Coprinus cinereus: ge-
Arch. Mikrobiol. 87, 257e268. netic evidence that carpophores and sclerotia share a com-
Matthews, T.R., Niederpruem, D.J., 1973. Differentiation in Copri- mon pathway of initiation. Curr. Genet. 3, 145e150.
nus lagopus. II. Histology and ultrastructural aspects of devel- Moore, D., 1987. The formation of agaric gills. Trans. Br. Mycol.
oping primordia. Arch. Mikrobiol. 88, 169e180. Soc. 89, 105e108.
McKnight, K., 1953. An unusual species of Psilocybe. Mycologia 45, Moore, D., 1991. Perception and response to gravity in higher
793e794. fungi e a critical appraisal. New Phytol. 117, 3e23.

32 U. Ku lez
Moore, D., 1995. Tissue formation. In: Gow, N.A.R., Gadd, G.M. Universidad Pu blica de Navarra, Pamplona, Spain,
(Eds.), The growing fungus. Chapman & Hall, London, UK, pp. 113e122.
pp. 423e465. Navarro-Gonza lez, M., Arndt, M., Zomorrodi, M., Majcherczyk, A.,
Moore, D., 1998a. Fungal Morphogenesis. Cambridge University Ku€ es, U., 2011. Regulation of fruiting body formation in Copri-
Press, Cambridge, UK. nopsis cinerea. In: Savoie, J.-M., Foulongne-Oriol, M.,
Moore, D., 1998b. Mushrooms upright, sideways and inside-out. Largeteau, M., Barroso, G. (Eds.), Proceedings of the 7th Inter-
Mycol. Res. 102, 641e657. national Conference on Mushroom Biology and Mushroom
Moore, D., Jirjis, R.I., 1976. Regulation of sclerotium production by Products (ICMBMP7) 2011, Vol. 1. INRA Bordeaux, Bordeaux,
primary metabolites in Coprinus cinereus (¼ C. lagopus sensu France, pp. 175e186.
Lewis). Trans. Br. Mycol. Soc. 66, 377e382. Niederpruem, D.J., Jersild, R.A., 1972. Cellular aspects of
Moore, D., Pukkila, P.J., 1985. Coprinus cinereus: an ideal organism morphogenesis in the mushroom Schizophyllum commune. CRC
for studies of genetics and developmental biology. J. Biol. Edu. Crit. Rev. Microbiol. 1, 545e576.
19, 31e40. Niederpruem, D.J., Wessels, J.G., 1969. Cytodifferentiation and
Moore, D., Elhiti, M.M.Y., Butler, R.D., 1979. Morphogenesis of morphogenesis in Schizophyllum commune. Bac. Rev. 33,
the carpophore of Coprinus cinereus. New Phytol. 83, 505e535.
695e722. Niederpruem, D.J., Jersild, R.A., Lane, P.L., 1971. Direct micro-
Muraguchi, H., Kamada, T., 1998. The ich1 gene of the mushroom scopic studies of clamp connection formation in growing hy-
Coprinus cinereus is essential for pileus formation in fruiting. phae of Schizophyllum commune. Arch. Mikrobiol. 78, 268e280.
Development 125, 3133e3141. Noble, R., Fermor, T.R., Lincoln, S., Dobrovin-Pennington, A.,
Muraguchi, H., Kamada, T., 2000. A mutation in the eln2 gene Evered, C., Mead, A., Li, R., 2003. Primordia initiation of
encoding a cytochrome P450 of Coprinus cinereus affects mushroom (Agaricus bisporus) strains on axenic casing mate-
mushroom morphogenesis. Fungal Genet. Biol. 29, 49e59. rials. Mycologia 95, 620e629.
Muraguchi, H., Takemaru, T., Kamada, T., 1999. Isolation and Norvell, L.L., 1998. Observations on development, morphology
characterization of developmental variants in fruiting using a and biology in Phaeocollybia. Mycol. Res. 102, 615e630.
homokaryotic fruiting strain of Coprinus cinereus. Mycoscience Oberwinkler, F., 2012. Evolutionary trends in Basidiomycota.
40, 227e233. STAPFIA 96, 45e104.
Muraguchi, H., Fujita, T., Kishibe, Y., Konno, K., Ueda, N., Oberwinkler, F., 2014. Dacrymycetes. In: McLaughlin, D.J.,
Nakahori, K., Yanagi, S.O., Kamada, T., 2008a. The exp1 gene Spatafora, J.W. (Eds.), The Mycota, Systematics and Evolu-
essential for pileus expansion and autolysis of the inky cap tion. Part A., second ed., Vol. 7. Springer, Heidelberg, Ger-
mushroom Coprinopsis cinerea (Coprinus cinereus) encodes an many, pp. 357e372.
HMG protein. Fungal Genet. Biol. 45, 890e896. Oberwinkler, F., Bandoni, R.J., 1982. A taxonomic survey of the
Muraguchi, H., Abe, K., Nakagawa, M., Nakamura, K., Yanagi, S.O., gasteroid, auricularoid Heterobasidiomycetes. Can. J. Bot. 60,
2008b. Identification and characterization of structural main- 1726e1750.
tenance of chromosome 1 (smc1) mutants of Coprinopsis cin- O’Donnell, K.L., McLaughlin, D.J., 1984a. Ultrastructure of meiosis
erea. Mol. Gen. Genom. 280, 223e232. in Ustilago maydis. Mycologia 76, 468e485.
Musngi, R.B., Abella, E.A., Lalap, A.L., Reyes, R.G., 2005. Four spe- O’Donnell, K.L., McLaughlin, D.J., 1984b. Postmeiotic mitosis,
cies of wild Auricularia in central Luzon, Phillipines as sources basidiospore development, and septation in Ustilago maydis.
of cell lines for researchers and mushroom growers. J. Agric. Mycologia 76, 486e502.
Technol. 1, 279e299. Ohm, R.A., de Jong, J.F., Lugones, L.G., Aerts, A., Kothe, E.,
Nagy, L.G., Walther, G., Ha zi, J., Va
gvo€ lgyi, C., Papp, T., 2011. Un- Stajich, J.E., de Vries, R.P., Record, E., Levasseur, A., Baker, S.E.,
derstanding the evolutionary process of fungal fruiting bodies: Bartholomew, K.A., Gathman, A.C., Lombard, V., Henrissat, B.,
correlated evolution and divergence times in the Psathyrella- Knabe, N., Ku € es, U., Lilly, W.W., Lindquist, E., Lucas, S.,
ceae. Syst. Biol. 60, 303e317. Magnuson, J.K., Piumi, F., Raudaskoski, M., Salamov, A.,
Nagy, L.G., Va gvo € lgyi, C., Papp, T., 2013. Morphological charac- Schmutz, J., Schwarze, F.W.M.R., vanKuyk, P.A., Horton, J.S.,
terization of clades of the Psathyrellaceae (Agaricales) inferred Grigoriev, I.V., Wo € sten, H.A.B., 2010. Genome sequence of the
from a multigene phylogeny. Mycol. Prog. 12, 505e517. model mushroom Schizophyllum commune. Nat. Biotech. 28,
Nakazawa, T., Tatsuta, Y., Fujita, T., Nakahori, K., Kamada, T., 957e963.
2010. Mutations in the Cc.rmt1 gene encoding a putative Ohm, R.A., de Jong, J.F., de Bekker, C., Wo € sten, H.A.B.,
arginine methyltransferase alter developmental programs Lugones, L.G., 2011. Transcription factor genes of Schizophyl-
in the basidiomycete Coprinopsis cinerea. Curr. Genet. 56, lum commune involved in regulation of mushroom formation.
361e367. Mol. Microbiol. 81, 1433e1445.
Nakazawa, T., Ando, Y., Kitaaki, K., Nakahori, K., Kamada, T., Ohm, R.A., Aerts, D., Wo € sten, H.A.B., Lugones, L.G., 2013. The blue
2011. Efficient gene targeting in DCc.ku70 or Cc.lig4 mutants of light receptor complex WC-1/2 of Schizophyllum commune is
the agaricomycete Coprinopsis cinerea. Fungal Genet. Biol. 48, involved in mushroom formation and protection against
939e946. phototoxicity. Env. Microbiol. 15, 943e955.
Namekawa, S.H., Iwabata, K., Sugawara, H., Hamada, F.H., Okuda, Y., Murakami, S., Honda, Y., Matsumoto, T., 2013. An
Koshiyama, A., Chiku, H., Kamada, T., Sakaguchi, K., 2005. MSH4 homolog, stpp1, from Pleurotus pulmonarius is a ‘silver
Knockdown of LIM15/DMC1 in the mushroom Coprinus cinereus bullet’ for resolving problems caused by spores in cultivated
by double-stranded RNA-mediated gene silencing. Microbiol. mushrooms. Appl. Environ. Microbiol. 79, 4520e4527.
151, 3669e3678. Pegler, D.N., 1986. Agaric Flora of Sri Lanka. Kew Bull. Add. Sci.,
Navarro-Gonza lez, M., 2008. Growth, Fruiting Body Development 12. HMSO, London, UK.
and Laccase Production of Selected Coprini. Georg-August- Pegler, D.N., 1996. Hyphal analysis of basidiomata. Mycol. Res.
University Go € ttingen, Go € ttingen, Germany. PhD thesis. 100, 129e142.
Navarro-Gonza lez, M., Domingo-Martınez, A., Navarro- Peintner, U., Bougher, N.L., Castellano, M.A., Moncalvo, J.-M.,
Gonza lez, S.S., Beutelmann, P., Ku € es, U., 2006. Monstrosities Moser, M.M., Trappe, J.M., Vilgalys, R., 2001. Multiple origins of
under the inkcap mushrooms. In: Pisabarro, A.G., Ramırez, L. sequestrate fungi related to Cortinarius (Cortinariaceae). Am. J.
(Eds.), VI Genetics and cellular biology of basidiomycetes. Bot. 88, 2168e2179.

Perkins, J.H., 1969. Morphogenesis in Schizophyllum commune. I. Reijnders, A.F.M., 2000. A morphogenetic analysis of the basic
Effect of white light. Plant Phys. 44, 1706e1711. characters of the gasteromycetes and their relation to other
Pine, E.M., Hibbett, D.S., Donoghue, M.J., 1999. Phylogenetic rela- basidiomycetes. Mycol. Res. 104, 900e910.
tionships of cantharelloid and clavaroid Homobasidiomycetes Rogers, M.A., 1973. Photoresponses of Coprinus stercocarius: basi-
based on mitochondrial and nuclear rDNA sequences. Myco- diocarp development and maturation. Mycologia 65, 907e913.
logia 91, 944e963. Rosin, I.V., Moore, D., 1985a. Origin of the hymenophore and
Pires, A.B.L., Gramacho, K.P., Silva, D.C., Go es-Neto, A., establishment of major tissue domains during fruit body
Silva, M.M., Muniz-Sobrinho, J.S., Porto, R.F., Villela- development in Coprinus cinereus. Trans. Br. Mycol. Soc. 84,
Dias, C., Brendel, M., Cascardo, J.C.M., Pereira, G.A.G., 2009. 609e619.
Early development of Moniliophthora perniciosa basidiomata Rosin, I.V., Moore, D., 1985b. Differentiation of the hymenium in
and developmentally regulated genes. BMC Microbiol. 9, Coprinus cinereus. Trans. Br. Mycol. Soc. 84, 621e628.
158. € hl, M., Ku
Ru € es, U., 2007. Mushroom production. In: Ku € es, U. (Ed.),
Plaza, D.F., Lin, C.W., Sebastiaan, N., Van der Velden, J., Aebi, M., Wood Production, Wood Technology, and Biotechnological
Ku€ nzler, M., 2014. Comparative transcriptomics of the model Impacts. Universita € tsverlag Go € ttingen, Go
€ ttingen, Germany,
mushroom Coprinopsis cinerea reveals tissue-specific armories pp. 555e586.
and a conserved circuitry for sexual development. BMC Ge- Ruiters, M.H.J., Wessels, J.G.H., 1989. In situ localization of specific
nom. 15, 492. RNAs in developing fruit bodies of the basidiomycete Schizo-
Pleszczyn ska, M., Wiater, A., Siwulski, M., Szczodrak, J., 2013. phyllum commune. Exp. Mycol. 13, 212e222.
Successful large-scale production of fruiting bodies of Laeti- Sakamoto, Y., Tamai, Y., Yajima, T., 2004. Influence of light on the
porus sulphureus (Bull.: Fr.) Murrill on an artificial substrate. morphological changes that take place during the develop-
World J. Microbiol. Biotechnol. 29, 753e758. ment of the Flammulina velutipes fruit body. Mycoscience 45,
Plunkett, B.E., 1956. The influence of factors of the aeration 333e339.
complex and light upon fruit-body form in pure cultures of an Sakamoto, Y., Ando, A., Tamai, Y., Yamiha, T., 2007. Pileus dif-
agaric and a polypore. Ann. Bot. 20, 563e586. ferentiation and pileus-specific protein expression in Flam-
Prillinger, H., Six, W., 1983. Genetische Untersuchungen zur mulina velutipes. Fungal Genet. Biol. 44, 14e24.
Fruchtko € rper- und Artbildung bei Basidiomyceten: Genetische Saksena, K.N., Marino, R., Haller, M.N., Lemke, P.A., 1976. Study
Kontrolle der Fruchtko € rperbildung bei Polyporus ciliatus. Pl. on development of Agaricus bisporus by fluorescent micro-
Syst. Evol. 141, 341e371. scopy and scanning electron microscopy. J. Bacteriol. 126,
Pringle, A., Patek, S.N., Fischer, M., Stolze, J., Money, N.P., 2005. 417e428.
The captured launch of a ballistospore. Mycologia 97, 866e871. Schubert, D., Raudaskoski, M., Knabe, N., Kothe, E., 2006. Ras
Ramel, G., Webster, J., 1995. Abnormal wood blewit basidiocarps. GTPase-activating protein Gap1 of the homobasidiomycete
Mycologist 9, 105. Schizophyllum commune regulates hyphal growth orientation
Ramel, G., McTiernan, K., Webster, J., 1998. An abnormal Laccaria and sexual development. Eukaryot. Cell. 5, 683e695.
laccata basidiocarp. Mycologist 12, 136. Schwalb, M., 1974. Effect of adenosine 30 ,50 -cyclic monophosphate
Raju, N.B., Lu, B.C., 1970. Meiosis in Coprinus. III. Timing meiotic on the morphogenesis of fruit bodies of Schizophyllum
events in C. lagopus (sensu Buller). Can. J. Bot. 48, 2183e2186. commune. Arch. Mikrobiol. 96, 17e20.
Raper, J.R., Krongelb, G.S., 1958. Genetic and environmental aspects Schwalb, M.N., 1978. Regulation of fruiting. In: Schwalb, M.N.,
of fruiting in Schizophyllum commune Fr. Mycologia 50, 707e740. Miles, P.G. (Eds.), Genetics and Morphogenesis in the Basidio-
Raudaskoski, M., Salonen, M., 1984. Interrelationships between mycetes. Academic Press, New York, NY, pp. 135e165.
vegetative development and basidiocarp initiation. In: Seelan, J.S.S., Justo, A., Nagy, L.G., 2015. Phylogenetic relationships
Jennings, D.H., Rayner, A.D.M. (Eds.), The Ecology and Physi- and morphological evolution in Lentinus, Polyporellus and Neo-
ology of the Fungal Mycelium. Cambridge University Press, favolus, emphasizing southeastern Asian taxa. Mycologia. http:
Cambridge, UK, pp. 291e322. //dx.doi.org/10.3852/14-084.
Raudaskoski, M., Vauras, R., 1982. Scanning electron microscope Seo, G.S., Shin, G.C., Otani, H., Kodama, M., Kohmoto, K., 1995a.
study of fruit body differentiation in Schizophyllum commune. Formation of atypical fruiting structures in Ganoderma lucidum
Trans. Br. Mycol. Soc. 78, 475e481. isolates on a nutrient agar medium. Mycoscience 36, 1e7.
Raudaskoski, M., Viitanen, H., 1982. Effect of aeration and light on Seo, G.S., Otani, H., Kohmoto, K., 1995b. Effect of light on the
fruit body induction in Schizophyllum commune. Trans. Br. My- formation of atypical fruiting structures in Ganoderma lucidum.
col. Soc. 78, 89e96. Mycoscience 36, 227e233.
Redhead, S.A., 1987. The Xerulaceae (Basidiomycetes), a family Shioya, T., Nakamura, H., Ishii, N., Takahashi, N., Sakamoto, Y.,
with sarcodimictic tissues. Can. J. Bot. 65, 1551e1562. Ozaki, N., Kobayashi, M., Okano, K., Kamada, T.,
Redhead, S.A., Ammirati, J.F., Walker, G.R., Norvell, L.L., Muraguchi, H., 2013. The Coprinopsis cinerea septin Cc.Cdc3 is
Puccio, M.B., 1994. Squamanita contortipes, the Rosetta Stone of involved in stipe elongation. Fungal Genet. Biol. 58e59, 80e90.
a mycoparasitic agaric genus. Can. J. Bot. 72, 1812e1824. Shirouzu, T., Hirose, D., Tokumasu, A., 2009. Taxonomic study of
Redhead, S.A., Seifert, K.A., Vilgalys, R., Moncalvo, J.M., 2000. the Japanese Dacrymycetes. Persoonia 23, 16e34.
Rhacophyllus and Zerovaemyces e teleomorphs or anamorphs? Siepmann, R., 1970. Fruchtko € rperbildung holzzersto € render Hy-
Taxon 49, 789e798. menomyceten in Reinkultur. Z. Pilzk 36, 7e17.
Reid, D.A., Manimohan, P., 1985. Auriculoscypha, a new genus Sierra, S., Cifuntes, J., 2005. A new species of Dacryopinax from
Auriculariales (Basidiomycetes) from India. Trans. Br. Mycol. Mexico. Mycotaxon 92, 243e250.
Soc. 85, 532e535. Singer, R., 1986. The Agaricales in Modern Taxonomy, fourth ed.
Reijnders, A.F.M., 1963. Les problems du de veloppement des Koeltz Scientific Books, Koenigstein, Germany.
carpophores des Agaricales et de quelques groups voisins. € kvist, E., Larsson, E., Eberhardt, U., Ryvarden, L., Larsson, K.-H.,
Sjo
N.V. Dijkstra s Drukkerij, Groningen, The Netherlands. 2012. Stipitate steroid basidiocarps have evolved multiple
Reijnders, A.F.M., 1979. Developmental anatomy of Coprinus. times. Mycologia 104, 1046e1055.
Persoonia 10, 383e424. Smith, A.H., 1966. The hyphal structure of the basidiocarp. In:
Reijnders, A.F.M., 1991. Differentiation in agaric basidiomata and Ainsworth, G.C., Sussman, A.S. (Eds.), The fungi, vol. II. Aca-
phylogenetic problems. Mycol. Res. 95, 1249e1252. demic Press, New York, NY, pp. 151e157.

34 U. Ku lez
Snetselaar, K., Mims, C.W., 1994. Light and electron microscopy of Tymon, A., Ku € es, U., Richardson, W.V.J., Casselton, L.A., 1992. A
Ustilago maydis hyphae in maize. Mycol. Res. 98, 347e355. fungal mating type protein that regulates sexual and asexual
Srivilai, P., 2006. Molecular Analysis of Genes Acting in Fruiting development contains a POU-related domain. EMBO J. 11,
Body Development in Basidiomycetes. Georg-August-Uni- 1805e1813.
versita € t Go
€ ttingen, Go € ttingen, Germany. PhD thesis. Uehling, J.K., Henkel, T.W., Aime, M.C., Vilgalys, R., Smith, M.E.,
Stahl, U., Esser, K., 1976. Genetics of fruit body production in 2012a. New species of Clavulina (Cantharellales, Basidiomy-
higher basidiomycetes. Mol. Gen. Genet. 148, 183e197. cotina) with resupinate and effused basidiomata from the
Stajich, J.E., Berbee, M.L., Blackwell, M., Hibbett, D.S., James, T.Y., Guiana shield. Mycologia 104, 547e556.
Spatafora, J.W., Taylor, J.W., 2009. The fungi. Curr. Biol. 19, Uehling, J.K., Henkel, T.W., Vilgalys, R., Smith, M.E., 2012b. Mem-
R840eR845. branomyces species are common ectomycorrhizal symbionts in
Stajich, J.E., Wilke, S.E., Ahre n, D., Au, C.H., Birren, B.W., Northern Hemisphere forests. Mycorrhiza 22, 577e581.
Borodovsky, M., Burns, C., Canba € ck, B., Casselton, L.A., Ulbrich, E., 1926. Morchelloide und tremelloide Formen von
Cheng, C.K., Deng, J.X., Dietrich, F.S., Fargo, D.C., Farman, M.L., Agaricaceen. Notitzbl. d. Kgl. Bot. Gartens u. Museums 9,
Gathman, A.C., Goldberg, J., Guigo, R., Hoegger, P.J., 998e1026.
Hooker, J.B., Huggins, A., James, T.Y., Kamada, T., Kilaru, S., Ulbrich, E., 1933a. Morchelloide und tremelloide Formen von
Kodira, C., Ku € es, U., Kupfert, D., Kwan, H.S., Lamsadze, A., Agaricaceen II. Notitzbl. d. Kgl. Bot. Gartens u. Museums 11,
Li, W.X., Lilly, W.W., Ma, L.J., Mackey, A.J., Manning, G., 904e908.
Martin, F., Muraguchi, H., Natvig, D.O., Palmerini, H., €
Ulbrich, E., 1933b. Uber eine eigenartige “Verwachsung” eines
Ramesh, M.A., Rehmeyer, C.J., Roe, B.A., Shenoy, N., ring-losen und beringten Fruchtko € rpers von Boletus luteus Fr.
Stanke, M., Ter-Hovhannisyan, V., Tunlid, A., Velagapudi, R., Notitzbl. d. Kgl. Bot. Gartens u. Museums 11, 908e911.
Vision, T.J., Zheng, Q.D., Zolan, M.E., Pukkila, P.J., 2010. Insights Umar, M.H., Van Griensven, L.J.L.D., 1997a. Morphogenetic cell
into evolution of multicellular fungi from the assembled death in developing primordia of Agaricus bisporus. Mycologia
chromosomes of the mushroom Coprinopsis cinerea (Coprinus 89, 274e277.
cinereus). Proc. Natl. Acad. Sci. U. S. A. 107, 11889e11894. Umar, M.H., Van Griensven, L.J.L.D., 1997b. Morphological studies
Stalpers, J.A., Seifert, K.A., Samson, R.A., 1991. A revision of the on the life span, developmental stages, senescence and death
genera Antromycopsis, Sclerostilbum, and Tilachlidiopsis (Hy- of fruit bodies of Agaricus bisporus. Mycol. Res. 101, 1409e1422.
phomycetes). Can. J. Bot. 69, 6e15. Umar, M.H., Van Griensen, L.J.L.D., 1998. The role of morphoge-
Stamets, P., Chilton, J.S., 1983. The Mushroom Cultivator. A netic cell death in the histogenesis of the mycelial cord of
Practical Guide to Growing Mushrooms at Home. Agarikon Agaricus bisporus and the development of macrofungi. Mycol.
Press, Olympia, WA. Res. 102, 719e735.
States, J.S., 1972. Basidiocarp development in Gloeophyllum (Len- Umar, M.H., Van Griensven, L.J.L.D., 1999. Studies on the
zites) saepiarium in the natural environment. Can. J. Bot. 50, morphogenesis of Agaricus bisporus: the dilemma of normal
1017e1024. versus abnormal fruit body development. Mycol. Res. 103,
States, J.S., 1975. Normal basidiocarp development of Gloeophyl- 1235e1244.
lum (Lenzites) saepiarium in culture. Mycologia 57, 1166e1175. van der Aa, H., 1997. Confluent basidiocarps. Mycologist 11,
Stephenson, N.A., Gooday, G.W., 1984. Nuclear numbers in stipe 80e82.
cells of C. cinerea. Trans. Br. Mycol. Soc. 82, 531e580. van der Valk, P., Marchant, R., 1978. Hyphal ultrastructure in
Stoller, B.B., 1952. Abnormal growth and fructification of the fruit-body primordia of the basidiomycetes Schizophyllum
cultivated mushroom. Science 116, 320e322. commune and Coprinus cinereus. Protoplasma 95, 57e72.
Straatsma, G., Sonnenberg, A.S.M., Van Griensven, L.J.L.D., 2013. van Leeuwen, J., Wichers, H.J., 1999. Tyrosinase activity and iso-
Development and growth of fruit bodies of the button mush- form composition in separate tissues during development of
room, Agaricus bisporus. Fungal Biol. 117, 697e707. Agaricus bisporus fruit bodies. Mycol. Res. 103, 413e418.
Sugawara, H., Iwabata, K., Koshiyama, A., Yanai, T., van Wetter, M.A., Wo € sten, H.A.B., Wessels, J.G.H., 2000. SC3 and
Daikuhara, Y., Namekawa, S.H., Hamada, F.N., Sakaguchi, K., SC4 hydrophobins have distinct roles in formation of aerial
2008. Coprinus cinereus Mer3 is required for synaptonemal structures in dikaryons of Schizophyllum commune. Mol. Mi-
complex. Chromosoma 118, 127e139. crobiol. 36, 201e210.
Swamy, S., Uno, I., Ishikawa, T., 1984. Morphogenetic effects of Velagapudi, R., 2006. Extracellular Matrix Proteins in Growth and
mutations at the A and B incompatibility factors in Coprinus Fruiting Body Development of Straw and Wood Degrading
cinereus. J. Gen. Microbiol. 130, 3219e3224. Basidiomycetes. Georg-August-University Go € ttingen,
Takemaru, T., Kamada, T., 1972. Basidiocarp development in Co- Go€ ttingen, Germany. PhD thesis.
prinus macrorhizus. I. Induction of developmental mutants. Bot. Vellinga, E.C., 2004. Genera in the family Agaricaceae: evidence
Mag. Tokyo 85, 51e57. from nrITS and nrLSU sequences. Mycol. Res. 108, 354e377.
Terashima, K., Yuki, K., Muraguchi, H., Akiyama, M., Kamada, T., Vizzini, A., 2007. Tremella versicolor, an uncommon species new to
2005. The dst1 gene involved in mushroom photomorpho- south Europe (Italy). Mycotaxon 101, 365e374.
genesis of Coprinus cinereus encodes a putative photoreceptor Volz, P.A., Niederpruem, D.J., 1969. Dikaryotic fruiting in Schizo-
for blue light. Genetics 171, 101e108. phyllum commune Fr.: morphology of the developing basidio-
Thiers, H.D., 1984. The secotioid syndrome. Mycologia 76, 1e8. carp. Arch. Mikrobiol. 68, 246e258.
Thorn, R.G., Moncalvo, J.-M., Redhead, S.A., Lodge, D.J., Volz, P.A., Niederpruem, D.J., 1970. Induced cytological aber-
Martın, M.P., 2005. A new poroid species of Resupinatus from rancies in the basidiocarp morphology of Schizophyllum
Puerto Rico, with a reassessment of the cyphelloid Stigmato- commune Fr. Arch. Mikrobiol. 72, 371e374.
lemma. Mycologia 97, 1140e1151. v. Wettstein, R., 1887. Ueber einen abnormen Fruchtko € rper von
Triratana, S., 1976. The effect of light on fruitbody production in €
Agaricus procerus Scop.. Osterr. Bot. Zeitschr. 12, 414e415.
Pholiota marginata. J. Sci. Soc. Thail. 2, 67e75. Walser, P.J., Velagapudi, R., Aebi, M., Ku € es, U., 2003. Extracellular
Tsusue , Y.M., 1969. Experimental control of fruit-body formation matrix proteins in mushroom development. Rec. Res. Dev.
in Coprinus macrorhizus. Dev. Growth Diff. 11, 164e178. Microbiol. 7, 381e415.
Turner, E.M., 1977. Development of excised sporocarps of Agaricus Walser, P.J., Ku€ es, U., Aebi, M., Ku
€ nzler, M., 2005. Ligand interac-
bisporus and its control by CO2. Trans. Br. Mycol. Soc. 69, tions of the Coprinopsis cinerea galectins. Fungal Genet. Biol. 42,
183e186. 293e305.

Watling, R., 1971. Polymorphism in Psilocybe merdaria. New Phytol. Wood, D.A., 1976. Primordium formation in axenic cultures of
70, 307e326. Agaricus bisporus (Lange) Sing. J. Gen. Microbiol. 95, 313e323.
Watling, R., 1974. Dimorphism in Entoloma abortivum. Bull. Soc. Wo€ sten, H.A.B., Wessels, J.G.H., 2006. The emergence of
Linn. Lyon 43, 449e470. fruiting bodies in basidiomycetes. In: Ku € es, U., Fischer, R.
Watling, R., Martın, M.P., 2001. A sequestrate Galerina from Scot- (Eds.), The Mycota, Growth, Differentiation and Sexuality,
land. Bot. J. Scotl. 55, 65e73. second ed., Vol. I. Springer, Berlin, Heidelberg, Germany,
Watling, R., Martın, M.P., 2003. A sequestrate Psilocybe from pp. 393e414.
Scotland. Bot. J. Scotl. 53, 245e257. Yamada, A., Ohura, T., Ohmasa, M., 2001. Cultivation of mush-
Watling, R., Moore, D., 1994. Moulding moulds into mushrooms: rooms of edible ectomycorrhizal fungi associated with Pinus
shape and form in the higher fungi. In: Ingram, D.S., densiflora by in vitro mycorrhizal synthesis. I. Primordium and
Hudson, A. (Eds.), Shape and Form in Plants and Fungi. The basidiocarp formation in open-pot culture. Mycorrhiza 11,
Linnean Society Symposium Series, no. 16. Academic Press, 59e66.
London, UK, pp. 271e290. Yamagishi, K., Kimura, T., Suzuki, M., Shinmoto, H., 2002. Sup-
Watling, R., Sweeney, J., 1971. Observations on Schizophyllum pression of fruit-body formation by constitutively active G-
commune Fries. Sabouraudia 12, 214e226. protein a-subunits ScGP-A and ScGP-C in the homobasidio-
Weiss, M., Bauer, R., Sampaio, J.P., Oberwinkler, F., 2014. Trem- mycete Schizophyllum commune. Microbiology 148, 2797e2809.
ellomycetes and related groups. In: McLaughlin, D.J., Yamagishi, K., Kimura, T., Suzuki, M., Shinmoto, H., Yamaki, K.J.,
Spatafora, J.W. (Eds.), The Mycota, Systematics and Evolution. 2004. Elevation of intracellular cAMP levels by dominant active
Part A., second ed., Vol. 7. Springer, Heidelberg, Germany, heterotrimeric G protein a subunits ScGP-A and ScGP-C in
pp. 331e355. homobasidiomycete, Schizophyllum commune. Biosci. Bio-
Wessels, J.G.H., 1965. Morphogenesis and biochemical processes technol. Biochem. 68, 1017e1026.
in Schizophyllum commune Fr. Wentia 13, 1e113. Yamanaka, K., 2005. Cultivation of new mushroom species in East
Wessels, J.G.H., 1992. Gene expression during fruiting in Schizo- Asia. Acta Edul. Fungi 12 (Suppl), 343e349.
phyllum commune. Mycol. Res. 96, 609e620. Yamanaka, T., Sagara, N., 1990. Development of basidia and ba-
Wessels, J.G.H., 1993. Fruiting in the higher fungi. Adv. Microbiol. sidiospores from slide-cultured mycelia in Lyophyllum tylicolor
Physiol. 34, 147e202. (Agaricales). Mycol. Res. 94, 847e850.
Wessels, J.G.H., 1999. Fungi in their own right. Fungal Genet. Biol. Zhou, Y., Chen, L.F., Fan, X.Z., Bian, Y.B., 2014. De novo assembly
27, 134e145. of Auricularia polytricha transcriptome using Illumina
Wessels, J.G.H., Dons, J.J.M., de Vries, O.M.H., 1985. Molecular sequencing for gene discosvery and SSR marker identification.
biology of fruit body formation in Schizophyllum commune. In: PLoS ONE 9, e91740.
Moore, D., Casselton, L.A., Wood, D.A., Frankland, J.C. (Eds.), Zmitrovich, I.V., Wasser, S.P., 2012. Phylogenetic conundrum of
Developmental biology of higher fungi. Cambridge University the mushroom-forming fungi (Agaricomycetes). In: Misra, J.K.,
Press, Cambridge, UK, pp. 485e497. Tewari, J.P., Deshmukh, S.K. (Eds.), Systematics and Evolution
Wilson, A.W., Binder, M., Hibbett, D.S., 2011. Effects of gasteroid of Fungi. CRC Press, London, UK, pp. 207e252.
fruiting body morphology on diversification rates in three in- Zolan, M.E., Tremel, C., Pukkila, P.J., 1988. Production and char-
dependent clades of fungi estimated using binary state acterization of radiation sensitive meiotic mutants of Coprinus
speciation and extinction analysis. Evol. 65, 1305e1322. cinereus. Genetics 120, 379e387.


10 1016@j FBR 2015 05 001

Uploaded by

Copyright:

Available Formats

10 1016@j FBR 2015 05 001

Uploaded by

Document Information

Original Description:

Original Title

Copyright

Available Formats

Share this document

Share or Embed Document

Sharing Options

Did you find this document useful?

Is this content inappropriate?

Copyright:

Available Formats

10 1016@j FBR 2015 05 001

Uploaded by

Copyright:

Available Formats

f u n g a l b i o l o g y r e v i e w s x x x ( 2 0 1 5 ) 1 e3 5

journal homepage: www.elsevier.com/locate/fbr

How do Agaricomycetes shape their fruiting

€ sgen-Institute, Georg-August-University G€ottingen,

article info abstract

lez, M., How do Agaricomycetes shape their fruiting bodies? 1.

1. Introduction and the Agaricomycetes (Hibbett, 2006). All three classes

lez, M., How do Agaricomycetes shape their fruiting bodies? 1.

(Fig. 1AeE). Fruiting bodies are structures in which meiotic

lez, M., How do Agaricomycetes shape their fruiting bodies? 1.

lez, M., How do Agaricomycetes shape their fruiting bodies? 1.

lez, M., How do Agaricomycetes shape their fruiting bodies? 1.

lez, M., How do Agaricomycetes shape their fruiting bodies? 1.

lez, M., How do Agaricomycetes shape their fruiting bodies? 1.

lez, M., How do Agaricomycetes shape their fruiting bodies? 1.

hymenial areas (‘cauliflower’) (Raper and Krongelb, 1958;

lez, M., How do Agaricomycetes shape their fruiting bodies? 1.

lez, M., How do Agaricomycetes shape their fruiting bodies? 1.

lez, M., How do Agaricomycetes shape their fruiting bodies? 1.

lez, M., How do Agaricomycetes shape their fruiting bodies? 1.

lez, M., How do Agaricomycetes shape their fruiting bodies? 1.

lez, M., How do Agaricomycetes shape their fruiting bodies? 1.

€ es et al., 2007; Navarro-

lez, M., How do Agaricomycetes shape their fruiting bodies? 1.

lez, M., How do Agaricomycetes shape their fruiting bodies? 1.

lez, M., How do Agaricomycetes shape their fruiting bodies? 1.

lez, M., How do Agaricomycetes shape their fruiting bodies? 1.

lez, M., How do Agaricomycetes shape their fruiting bodies? 1.

lez, M., How do Agaricomycetes shape their fruiting bodies? 1.

lez, M., How do Agaricomycetes shape their fruiting bodies? 1.

lez, M., How do Agaricomycetes shape their fruiting bodies? 1.

lez, M., How do Agaricomycetes shape their fruiting bodies? 1.

lez, M., How do Agaricomycetes shape their fruiting bodies? 1.

lez, M., How do Agaricomycetes shape their fruiting bodies? 1.

lez, M., How do Agaricomycetes shape their fruiting bodies? 1.

lez, M., How do Agaricomycetes shape their fruiting bodies? 1.

lez, M., How do Agaricomycetes shape their fruiting bodies? 1.

lez, M., How do Agaricomycetes shape their fruiting bodies? 1.

lez, M., How do Agaricomycetes shape their fruiting bodies? 1.

lez, M., How do Agaricomycetes shape their fruiting bodies? 1.

lez, M., How do Agaricomycetes shape their fruiting bodies? 1.

lez, M., How do Agaricomycetes shape their fruiting bodies? 1.

lez, M., How do Agaricomycetes shape their fruiting bodies? 1.

lez, M., How do Agaricomycetes shape their fruiting bodies? 1.

You might also like