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New Phytol. (1998), 140, 295–310

Dark septate endophytes: a review of

facultative biotrophic root-colonizing fungi

Bÿ ARI JUMPPONEN* ÿÿÿ JAMES M. TRAPPE

Department of Forest Science, Oregon State University, Corvallis,
Oregon 97331-7501, USA
(Received 4 September 1997; accepted 8 July 1998)

ÿÿÿÿÿÿÿ

Dark septate root endophytes (DSE) are conidial or sterile fungi (Deuteromycotina, Fungi Imperfecti) likely to be
ascomycetous and colonizing plant roots. They have been reported for nearly 600 plant species representing about 320
genera and 100 families. DSE fungi occur from the tropics to arctic and alpine habitats and comprise a heterogeneous
group that functionally and ecologically overlaps with soil fungi, saprotrophic rhizoplane-inhabiting fungi, obligately and
facultatively pathogenic fungi and mycorrhizal fungi. Numerous species of undescribed sterile and anamorphic taxa may
also await discovery. Although DSE are abundant in washed root and soil samples from various habitats, and are easily
isolated from surface-sterilized roots of ecto-, ectendo-, endo- and non-mycorrhizal host species, their ecological
functions are little understood. Studies of DSE thus far have yielded inconsistent results and only poorly illustrate the
role of DSE in their natural habitats. These inconsistencies are largely due to the uncertain taxonomic affinities of the
strains of DSE used. In addition, because different strains of a single anamorph taxon seem to vary greatly in function,
no clear generalizations about their ecological role have been drawn. This paper reviews the current literature on DSE
and the ecology and discusses the need for and direction of future research.

Key words: Dark septate endophytes, deuteromycetes, ecology, fungi, mycorrhizas, root endophytes.

ÿÿÿÿÿÿÿÿÿÿÿÿ
ecological role of these associations, however poorly known
they might currently be.
Fungi have a variety of symbiotic interactions with plant The objective of this paper is to review the literature of
roots, ranging from antagonism to mutualism. miscellaneous, root-associated, dark septate endophytic
Fungal colonizations that do not fit the identified categories (DSE) fungi. Despite several studies addressing various
of mutualistic or pathogenic symbiosis have been referred aspects of DSE and their associations with colonized hosts,
to in a variety of ways (Table 1). very little is known of their taxonomic affinity, host range
Some researchers (Lewis, 1973; Smith & Smith, 1990) have and ecology.
approached the problem from a more functional point of In this context, we refer to endophytic fungi in a broad
view by characterizing root–fungus interactions based on sense: they colonize living plant organs without causing any
uni- or bidirectional flow of resources (nutrients, apparent, overt negative effects (Hirsch & Braun, 1992). In
carbohydrates, etc.). a taxonomical sense, we attempt to include those conidial
Because a fungus and its hosts may have associations or sterile fungi (Deuteromycotina, Fungi Imperfecti) that
that occupy different positions on the 'mutualism–parasitism frequently colonize living plant roots and are likely to be
continuum', depending on environmental conditions ascomycetous. Because very little is known what comprises
(Johnson, Graham & Smith, 1997), the associations may Mycelium radicis atrovirens (MRA; Melin, 1922, 1923), we
not always be clearly defined. This is predictable when fungi include those MRA that seem to fulfill these requirements,
of unknown identity produce structures of unknown function all hereafter termed DSE.
when colonizing host roots. However, it is essential to
acknowledge the potentially important We recognize that an unknown number of fungal taxa
(anamorphic and or teleomorphic) are involved, and that a
considerable functional and ecological overlap might exist
between soil fungi, saprotrophic rhizoplane-inhabiting fungi,
* To whom correspondence should be addressed at (present strictly pathogenic fungi, mycorrhizal fungi and fungal
address): Department of Agricultural Research for Northern Sweden,
PO Box 4097, SE-90403 Umea, Sweden.
endophytes.
Email: Ari.Jumpponennjv.slu.se Because Richard & Fortin (1974) reviewed the

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296 A. Jumpponen and J. M. Trappe

Table 1. Terms that have been used to describe fungal of Oidium or Monilia. Within the cortical cells of the host
colonization that do not fit the identified categories of root, the hyphae aggregated into groups of thick-walled
mutualistic or pathogenic symbiosis stromal nodules (Peyronel, 1924).
Melin (1925 and references therein) reported similar
Term for structures in several members of Pinaceae referring to
fungal colonization Reference
them as 'pseudomycorrhizas'. He con-cluded that the
Casual mycorrhizal Burges (1936) 'pseudomycorrhizas' represented a parasitic rather than
Endophytic Currah et al. (1987); Stoyke & mutualistic behavior (Melin, 1924). He insisted on the
Currah (1991); Stoyke et al. term 'pseudomycorrhiza' because the colonization could
(1992); Vare et al. (1992) be observed under conditions where ectomycorrhizal
Pseudomycorrhizal Melin (1923); Thomas (1943);
associations did not develop at all.
Robertson (1954); Kowalski
(1970; 1973); Wang & Wilcox
(1985); Wilcox & Wang Melin might not have realized, however, that DSE
(1987a) coexists with mycorrhizal fungi. Endophytic and
Weakly pathogenic Wang & Wilcox (1985); Egger & Paden ectomycorrhizal fungi colonize roots concurrently (Hatch,
(1986a); Wilcox & Wang (1987a)
1934; Manka & Truszkowska, 1958; Trappe, 1962;
dark septate Haselwandter & Read (1982); Sengupta, Chakraborty & Chaudhuri, 1989; Dhillion, 1994;
Haselwandter (1987); Cazares Horton, Cazares & Bruns, 1998), as can arbuscular and
(1992); Vare et al. (1992) ectomycorrhizal fungi ( Blaschke, 1991; Cazares &
Rhizoctonia-like Peyronel (1924); Haselwandter Trappe, 1993; Dhillion, 1994; Horton et al., 1998).
& Read (1980)
Recording the endophytes may be difficult when the
Septate endophytes O'Dell et al. (1993)
ectomycorrhizas are covered by fungal mantle. Melin
(1922, 1923, 1925) reported that host roots were
literature on MRA, we only briefly cover the earlier work, intracellularly colonized and that neither Hartig net nor
and emphasize what has been published since. mantle was present. Morphological studies of colonized
roots have since revealed, however, that DSE occasionally
ÿÿÿÿÿ ÿÿÿÿÿÿÿÿÿÿÿÿ ÿÿ ÿÿÿ
develops a partial Hartig net and a thin mantle only a few
cell layers thick (O'Dell, Massicotte & Trappe, 1993;
In his initiating work, Frank (1885) referred to Fernando & Currah, 1996).
ectomycorrhizas of trees. Gallaud (1905) first reported
another type of root colonization by septate endophytes
on Allium sphaerocephalum L. and Ruscus aculeatus L.
Peyronel (1922) observed similar fungal structures on the ÿÿÿÿÿ ÿÿÿ ÿÿÿÿÿÿÿÿÿÿÿÿ ÿÿÿÿÿÿ
roots of Triticum aestivum L. He subsequently noted
another type of root colonization, later termed Richard & Fortin (1974) pointed out that DSE fungi are
'endomycorrhizas' (Peyronel, 1922, 1923). While isolating widely distributed in coniferous boreal forests.
ecto-mycorrhizal fungi and aseptically resynthesizing Morphologically similar root colonizations had also been
mycorrhizas, Melin (1922, 1923) isolated brown, or described elsewhere, eg from Australian Liliaceae (Burges,
blackish, 'pseudomycorrhizal' fungi. He called these 1936). Colonization resembling DSE has been noted in
sterile, root-associated fungi Mycelium radicis atro-virens approx. 600 plant species representing about 320 genera
(MRA) and Rhizoctonia sylvestris. Neither formed and 114 families (Table 2). These include species and
ectomycorrhizas; R. sylvestris produced sclerotia on the genera usually considered arbuscular, ericoid, orchid and
root surfaces, whereas MRA produced them intracellularly. ecto- and non-mycorrhizal. There seems to be no rule
No taxonomic affinity for these 'pseudomycorrhizal' fungi governing the species DSE colonize. They have been
was suggested at that time. MRA has since been applied observed in plant families with quite different life strategies,
to any sterile, dark and septate fungi isolated from roots suggesting little or no host specificity.
or soil.
Table 2 contains observations from habitats ranging from
South African coastal plains and lowlands to tropical,
Peyronel documented colonization by pigmented root temperate, subalpine, alpine, maritime Antarctic, and
endophytes on 135 species of angiosperms (Peyronel, arctic zones.
1924). He referred to the observed structures as Most authors (see http:www.cup.cam.ac.uk
'Rhizoctonia-like', but was convinced that more than one SPECIESTABLE.html) observed root endophytes with
fungal taxon – not necessarily Rhizoctonia spp. – was darkly pigmented, septate hyphae that, in most cases,
involved in these root colonizations (Peyronel, 1924). He formed intracellular structures similar to those termed
described the root colonization as simple, branched microsclerotia by Read & Haselwandter (1981). The sterile
hyphae that occasionally produced short, branched, dark mycelium seems ubiquitous in soil and root systems;
clavate, barrel-shaped segments similar to chlamydospores it dominated in studies of fungi from washed soil or root
samples from the

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Dark septate root endophytes 297

Table 2. Number of plant species within 144 families

Plant taxon No. of reported species
reported to be colonized by DSE
The colonized 587 species include any reports of
Ranunculaceae 18
dark, septate hyphae observed in the root systems. For
Rhizophoraceae two

list of species and references, please see http:

Rosaceae 20
www.cup.cam.ac.ukSPECIESTABLE.html. Nomenclature follows Database
Rubiaceae 4
of North American Plants
Rutaceae two

(USDA-NRCS) (available at http:www.ars-grin.gov

Salicaceae 16
npgstaxindex.html) and new provisional Global Plant
Santalaceae 1
Checklist (available at http:gbbm3.bgbm.fuberlin.de
Saxifragaceae 16
IOPIGPCquery.htm) where applicable.
Scrophulariaceae 18
Solanaceae 6
Plant taxon No. of reported species
Sterculiaceae 1
Theaceae two
ANGIOSPERMAE
Tiliaceae 1
DICOTYLEDONEAE
Ulmaceae 1
Aceraceae 1
Umbelliferae 7
Aizoaceae 4
Urticaceae 1
Anacardiaceae 1
Violaceae 6
Apocynaceae two

Vitaceae 1
Asclepiadaceae 1
Zygophyllaceae 1
Avicenniaceae 3
MONOCOTYLEDONAE
Betulaceae 5
Alliaceae 3
Bignoniaceae 3
Aloeaceae 1
Boraginaceae 4
Amaryllidaceae 1
Buddlejaceae 1
Araceae 1
Cactaceae 3
Asparagaceae 1
Campanulaceae 7
Asphodelaceae 1
Caprifoliaceae 2
Colchicaceae 1
Caryocaraceae 1
Colvallariaceae 5
Caryophyllaceae 18
Cyperaceae 15
Chenopodiaceae 2
Graminaceae 59
Cistaceae 2
Haemodoraceae 1
Compositae 37
Hyacinthaceae 1
Connaraaceae 1
Iridaceae 7
Convolvulaceae 1
Juncaceae 8
Cornaceae 1
Liliaceae 3
Crassulaceae 15
Melanthiaceae 3
Cruciferae 14
Orchidaceae 9
Empetraceae 1
Palmae two
Ericaceae 25
Ruscaceae 1
Euphorbiaceae 1
Smilacaceae 1
Fabaceae 1
Trilliaceae 1
Fagaceae 1
GYMNOSPERMAE
Geraniaceae 1
Cupressaceae 6
Gentianaceae 4
Pinaceae 25
Guttiferaceae 1
EQUISETOPSIDA
Juglandaceae 1
Equisetaceae 4
Labiatae 7
LYCOPSIDE
Lauraceae 1
Lycopodiaceae 4
Leguminosae-Caesalpiniaceae 11
Selaginellaceae two

Leguminosae-Mimosoideae 3
POLYPODIOPSIDE
Leguminosae-Papilionoideae 34
Adiantaceae two

Malpighiaceae 1
Aspleniaceae 4
Melastomataceae 1
Blechenaceae 1
Moraceae two

Cyatheaceae 1
Myrtaceae 6
Dennstaedtiaceae 1
Ochnaceae 1
Dryopteridaceae 3
Onagraceae 4
Hymenophyllaceae 3
Oleaceae 2
Marattiaceae 3
Oxalidaceae 3
Matoniaceae 1
Papaveraceae two

Pedaliaceae 1 Ophioglossaceae two

Polypodiaceae 1
Piperaceae 1
Pteridiceae 1
Plantaginaceae 3
Schizaeaceae 1
Plumbaginaceae 1
Woodsiaceae 5
Polemoniaceae two

PSYLOTOPSIDA
Polygonaceae 7
Psilotaceae 1
Portulacaceae 1
Primulaceae 8 Total – 144 587

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298 A. Jumpponen and J. M. Trappe

Table 3. Host species reported to be colonized by the five described anamorphic taxa of DSE
Reports include notations of DSE isolated from the root systems (natural) or inoculated and shown to colonize a
host plant (asepticopen pot cultures). Nomenclature follows Database of North American Plants (USDA-NRCS)
(available at http:www.arsgrin.govnpgstaxindex.html) and new provisional Global Plant Checklist (available
at http:bgbm3.bgbm.fuberlin.deIOPIGPCquery.html) where applicable.

Species of Host species Location Conditions Reference

endophyte

Chloridium Betula alleghansis — Picea Aseptic Wilcox & Wang (1987b)

paucisporum rubens Pinus —
Aseptic Wilcox & Wang (1987b)
resinosa Abies NY, USA Natural Wang & Wilcox (1985)
Leptodontidium balsamea Achillea Alberta, Canada Natural Alberta, Fernando & Currah (1996)
orchidicola sp. Canada Natural Alberta, Canada Fernando & Currah (1996)
Artemisia norvegica Natural Aseptic Alberta, Canada Fernando & Currah (1995)
—
Betula pumila Natural Fernando & Currah (1995)
Calypso bulbosa Currah et al. (1988); Currah &
Sherburne (1992); Currah
et al. (1987)
Carex sp. Alberta, Canada Natural Fernando & Currah (1995)
Castilleja sp. Alberta, Canada Natural Fernando & Currah (1996)
Coeloglossum viride Alberta, Canada Natural Currah & Sherburne (1992);
Currah et al. (1987); Fernando
& Currah (1995)
Corallorhiza maculata Alberta, Canada Natural Currah & Sherburne (1992);
Currah et al. (1987)
C. trifida Alberta, Canada Natural Currah et al. (nineteen ninety); Fernando
& Currah (1995)
—
Dryas octopetala Open pot Fernando & Currah (1996)
culture
sp. Alberta, Canada Natural Erigeron Fernando & Currah (1996)
Heracleum lanatum Alberta, Canada Natural Listera borealis Fernando & Currah (1996)
Alberta, Canada Natural Pedicularis bracteosa Alberta, Canada Currah et al. (nineteen ninety)
Natural Picea glauca Aseptic Piperia unalascensis Alberta, Fernando & Currah (1995)
—
Canada Natural Platanthera hyperborea Alberta, Canada Natural Fernando & Currah (1995)
Fernando & Currah (1995)
Currah & Sherburne (1992);
Currah et al. (1987); Fernando
& Currah (1995)
Potentilla fruticosa — AsepticOpen Fernando & Currah (1995);
pot culture Fernando & Currah (1996)
Rubus sp. Alberta, Canada Natural Fernando & Currah (1996)
—
Salix glauca AsepticOpen Fernando & Currah (1996)
pot culture
Spiranthes lacera Alberta, Canada Natural Alberta, Fernando & Currah (1995)
Trollius albiflorus Canada Natural Schwarzwald, Fernando & Currah (1996)
Phialocephala sp. Courtois (1990)
dimorphophora NaturalGermany
Picea mariana ? Natural Richard & Fortin (1973, 1974)
P. rubens —
Aseptic Wilcox & Wang (1987b)
Pinus resinosa —
Aseptic Wang & Wilcox (1985); Wilcox
& Wang (1987b)
Phialocephala Abies alba Switzerland Natural Ahlich & Sieber (1996)
fortinii Alnus rubra Canada Natural Ahlich & Sieber (1996)
Amerorchis rotundifolia Alberta, Canada Natural Currah et al. (1987)
Andromeda polifolia Alberta, Canada Natural Hambleton & Currah (1997)
Calluna vulgaris Switzerland Natural Ahlich & Sieber (1996)
Calypso bulbosa Alberta, Canada Natural Currah et al. (1988); Currah et
al. (1987)
Cassiope mertensiana Alberta, Canada Natural Currah & Tsuneda (1993);
Hambleton & Currah (1997)
C. tetragona Alberta, Canada Natural Hambleton & Currah (1997)
Chamaedaphne Alberta, Canada Natural Hambleton & Currah (1997)
calyculata
—
Dryas octopetala Open pot Fernando & Currah (1996)
culture
Empetrum nigrum Alberta, Canada Natural Hambleton & Currah (1997)
Fagus sylvatica Switzerland Natural Ahlich & Sieber (1996)
Gaultheria humifusa G. Canada Natural Hambleton & Currah (1997)
shallon Canada Natural Ahlich & Sieber (1996)

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Dark septate root endophytes 299

Table 3. (cont.)

Species of Host species Location Conditions Reference

endophyte

Kalmia microphylla British Columbia, Natural Currah & Tsuneda (1993)

Canada
K. polifolia Alberta, Canada Natural Loiseleuria procumbers Hambleton & Currah (1997)
Alberta, Canada Natural Luetkea pectinata Alberta, Canada Hambleton & Currah (1997)
Natural Lupinus latifolius Washington, Currah & Tsuneda (1993)
O'Dell et al. (1993)
NaturalUSA
Menziesia ferruginea Alberta, Canada Aseptic, Hambleton & Currah (1997);
Natural Stoyke & Currah (1993)
Picea abies Germany; Natural Ahlich & Sieber (1996);
Switzerland; Dahlberg et al. (1997)
Sweden
Pinus contorta —
AsepticGrowth Jumpponen et al. (1998); O'Dell
PouchOpen et al. (1993)
pot culture
P. resinosa —
Aseptic Wilcox & Wang (1987a)
P. sylvestris Finland; Natural Ahlich & Sieber (1996); Wang
Germany; & Wilcox (1985)
Switzerland
Potentilla fruticosa — Open pot Fernando & Currah (1996)
culture
Phyllodoce Alberta, Canada Natural Hambleton & Currah (1997)
empetriformis
P. glanduliflora Alberta, Canada Natural Hambleton & Currah (1997)
Rhododendron Alberta, Canada Natural Hambleton & Currah (1997)
albiflorum
R. brachy-carpum — R. Aseptic Currah et al. (1993)
obtusum Tottori, Japan Salix glauca Natural Currah & Tsuneda (1993)
—
AsepticOpen Fernando & Currah (1996)
pot culture
Vaccinium Alberta, Canada Natural Hambleton & Currah (1997)
membraneceum
V. myrtilloides Alberta, Canada Natural Hambleton & Currah (1997)
V. myrtillus Switzerland Natural Ahlich & Sieber (1996)
V. scoparium Alberta, Canada Natural Hambleton & Currah (1997)
V. uliginosum Alberta, Canada Natural Hambleton & Currah (1997)
V. vitis-idaea Alberta, Canada Natural Hambleton & Currah (1997)
Phialophora Betula alleghansis — Picea Aseptic Wilcox & Wang (1987a, b)
finland rubens Pinus —
Aseptic Wilcox & Wang (1987a, b)
resinosa —
Aseptic Wilcox & Wang (1987a, b)
P. sylvestris Suonenjoki, Natural Wang & Wildox (1985)
Finland

subantarctic (Heal, Bailey & Latter, 1967), boreal 3). However, these and additional reports from
coniferous forests in Canada (Summerbell, 1988, inoculation bioassays indicate wide host ranges for
1989), temperate and boreal forests in Northern and some anamorphic species. None of the known fungi
Central Europe (Holdenrieder & Sieber, 1992; endophytes appear to express any host specificity.
Ahlich & Sieber, 1996) and exotic pine plantations in For example, P. fortinii colonizes more than 20 plants
New Zealand (Chu-Chou, 1979; Chu-Chou & species in either natural or experimental conditions
Grace, 1982). Courtois (1990) reported Phialophora (Table 3).
dimorphospora and another unidentified Phialophora DSE appear to be found wherever they are sought.
sp. in addition to several sterile isolates from spruce- Their abundance in different habitats and on
roots and 'root-free' soil collected in the Black different hosts is still largely unknown. It is important
Forest region in Germany. It is currently unclear to bear in mind that the observations of
whether the isolates from soil indicate omnipresence colonized hosts have been incidental to other work
of saprotrophic dark-pigmented fungi or extra-matrical and only a few studies have attempted to identify the
mycelium of facultative biotrophic DSE endophytic taxa. No systematic surveys focusing on
extending into the soil from host roots. DSE has been conducted. Phialocephala fortinii is
Isolating and identifying the asexual fungi is the only taxon allowing inferences about its dis-
laborious. Few attempts to identify the root endo- tribution: it has been observed in eastern and
phytes from field samples have been reported (Table western North America, Europe, and Japan,

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300 A. Jumpponen and J. M. Trappe

suggesting a global distribution (Table 3). As more ÿÿÿÿÿÿÿÿÿÿ ÿÿ ÿÿÿÿÿ ÿÿÿÿÿÿÿÿÿ ÿÿ ÿÿÿ
attention is paid to other fungi in this group, their
distribution is likely to prove global as well. The profusion The pattern of DSE colonization is similar in roots of
of DSE in soil and roots of host species that belong to different plant species that are otherwise mainly
various plant families suggests not only a globally considered as arbuscular, ericoid, orchid or ecto-
ubiquitous presence and lack of host specificity, but mycorrhizal (see Peyronel, 1924; Vare, Vestberg &
also a role of importance in natural ecosystems. The Eurola, 1992; Currah, Tsuneda & Murakami, 1993;
function of DSE – when present in soil or colonizing O'Dell et al., 1993; Stoyke & Currah, 1993). Plants that
host roots – is still unknown and conclusions from the do not form mycorrhizas also have similar fungal
previous research are contradictory, as will be structures when colonized by DSE (Haselwandter &
discussed below. Read, 1982; Cazares, 1992; Vare et al., 1992). Root
Since Melin's (1922–1925) characterization of colonization by Phialocephala fortinii exemplifies DSE
'pseudomycorrhizas', studies on conifer roots have colonization and has been described in detail by several
yielded additional reports (Rayner & Levisohn, 1941; authors. Consequently, we briefly summarize the
Levisohn, 1954; Laiho, 1965; Mikola, 1965; Kowalski, general pattern of P. fortinii colonization here. Initial
1973). In most of those studies unfortunately, the fungi colonization is usually characterized by superficial
colonizing the roots remained sterile and unidentified. hyphae (Currah & Van Dyk, 1986; Figs 1, 2) that have
Consequently, it has been difficult to discern their also been called
'
potential functions and ecological roles. Mikola (1965) runner hyphae' (McKeen, 1952; Deacon, 1973).
addressed the unknown ecological role and the The individual hyphae usually grows along the
uncertain taxo-nomic affinity of root-colonizing – yet depressions between adjacent epidermal cells and can
not necessarily mycorrhizal – fungi, by suggesting the colonize the space between cortical cells along the
use of 'non-mycorrhizal roots' as a category that would main axis of the root (Currah et al., 1993). 'A loose
include roots either colonized solely intracellularly or hyphal network on the root surface' (Stoyke & Currah,
completely free of any fungal colonization. This ap- 1993) or 'loose wefts of hyphae' (O'Dell et al., 1993)
proach, however, leaves frequently observed fungal can develop during the superficial colonization. The
colonization of plant roots beyond recognition. Also, it hyphae eventually penetrate into the outer cortical cells
deprives the unknown symbiotic (sensu de Bary, 1887) (Stoyke & Currah, 1991; O'Dell et al., 1993; Stoyke &
fungi, that do not form any 'typical' mycor-rhizal Currah, 1993).
structures (see Harley & Smith, 1983), of appropriate Penetration into the root hairs has been observed and
terminology for describing their mani-festations in natural might be a way to enter the cortical layer (O'Dell et al.,
ecosystems. 1993; Fig. 3). Once into the epidermal layer, the hyphae
can grow parallel to the main axis of the host root and
Asexual reproductive structures of DSE were from cell to cell within the epidermis, usually causing no
ultimately described by Wang & Wilcox (1985), Currah, distortion of the host roots (Currah et al., 1993; O'Dell
Sigler & Hambleton (1987) and Fernando & Currah et al . , 1993; Fig. 4). The hyphae passes through
(1996), enabling identification of some of the root adjoining epidermal cell walls by narrow penetration
endophytic fungi, as well as experimental inoculations tubes (Currah et al., 1993; Fig. 4), which occasionally
for studies on the comparative morphology of roots arise from inflated, appressorium-like structures (Fig. 4).
colonized by known strains. The morphology of DSE-
colonized roots had been reported to resemble During intracellular colonization, endophytes might
ectomycorrhizas (Wilcox & Wang, 1987b; O'Dell et al. form clusters of inflated, rounded, thick-walled cells
1993), ectendo-mycorrhizas (Wilcox & Ganmore- within the cortical cells (Fig. 2) referred to as 'thick
Neumann, 1974; Wang & Wilcox, 1985; Wilcox & as pseudoparenchymatic mass' (Melin, 1923;
Wang , 1987a), and pseudomycorrhizas (Wang & Robertson, 1954), 'sclerotia' (Melin, 1923; Hatch, 1934;
Wilcox, 1985). In some cases the structures in the Stoyke & Currah, 1991; O'Dell et al., 1993; Stoyke &
colonized root suggested a pathogenic association Currah, 1993; Fernando & Currah, 1995),
(Wang & Wilcox, 1985; Wilcox & Wang, 1987a). The 'microsclerotia' (Haselwandter & Read, 1980; Read &
variety of root morphologies observed has made it Haselwandter, 1981; Haselwandter, 1987; Jumpponen,
difficult to sort out the fungal endophytes and their Mattson & Trappe, 1998) or 'sclerotial bodies' (Levisohn,
effects on hosts. 1954; Wilcox & Wang, 1987b).
Morphological structures of DSE-colonized roots do not The clusters of fungal cells within root cells have been
fall clearly into any previously described category of described as filled with 'closely packed, thick-walled
mycorrhizal, parasitic or pathogenic associations. cells' (McKeen, 1952), 'groups of swollen cells' (Deacon,
The terms consequently introduced to describe the 1973), 'intracellular sclerotia of compact, darkly
patterns of this root–fungus association were: 'dark pigmented and irregularly lobed, thick-walled
septate' (Read & Haselwandter, 1981) or 'septate' hyphae' (Stoyke & Currah, 1991), or 'thick-walled,
endophytes (O'Dell et al., 1993 ) . irregularly lobed and compacted cells'

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Dark septate root endophytes 301

Figure 1. Superficial hyphal net of Phialocephala fortinii on lateral roots of Pinus contorta. Inoculation experiment
conducted in open pot culture using strain isolated by O'Dell et al. 1993. Strain currently maintained in the USDA
Forest Service PNW Research Station (Cortallis, OR, USA). Bar, 01 mm.

Figure 2. Superficial hyphae of Phialocephala fortinii and a cell filled with microsclerotia on roots of Pinus contorta.
For details, see Fig. 1 legend. Bar, 20 µm.

Figure 3. Hyphae of Phialocephala fortinii colonizing a root hair of Pinus contorta. For details, see Fig. 1 legend.
Bar, 25 µm.

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302 A. Jumpponen and J. M. Trappe

Figure 4. Hyphae of Phialocephala fortinii penetrating through the cell wall in the root of Pinus contorta.
Note the narrow penetration tube and swollen appressorium-like structure. For details, see Fig. 1 legend.
Bar, 15 µm.
which sometimes formed sheets several cells into the cortical layer and subsequent occasional
thick' (O'Dell et al., 1993). formation of chlamydospore-like, rounded cells within
Occasionally structures resembling ectomycorrhizas the cortical cells of the host root appear common to
can also occur with ectomycorrhizal host plants. O'Dell known form-taxa of DSE fungi. Phialo-cephala fortinii,
et al. (1993) reported 'labyrinthine tissue (similar to Phialophora finlandia, Lepto-dontidium orchidicola,
Hartig net tissue)' in roots of Pinus contorta when isolates of Pezizales, as well as several unidentified
inoculated with Phialocephala fortinii. isolates, all developed structures similar to those
Similarly, Fernando & Currah (1996) reported a Hartig described above when colonizing a variety of host plants
net and a thin, patchy mantle when Salix glauca was (Wilcox & Ganmore-Neumann, 1974; Read &
inoculated with P. fortinii. In addition, occasional hyphal Haselwandter, 1981; Egger & Paden, 1986b; Wilcox &
coils (Haselwandter & Read, 1980) or peloton-like Wang, 1987a, b; Currah et al., 1993; O'Dell et al., 1993;
structures of coiled or looped, branched hyphae within Stoyke & Currah, 1993; Fernando & Currah, 1995,
root cells have been reported when DSE colonized 1996). More data are needed, however, to validate
ericaceous hosts (Currah et al., 1993 ) . Stoyke & Currah whether DSE are morphologically or phylogenetically
(1991) pointed out that none of their DSE isolates from uniform. The current evidence seems not to favor such
alpine ericaceous plants displayed dense coiling similar uni-formity, as will be discussed below. A standardized
to that frequently observed in ericoid mycor-rhizas. vocabulary, however, is necessary to describe the DSE
colonization. For this purpose, we propose the following
terms: runner hyphae' for the individual, superficial
'
Wilcox & Wang (1987a) suggest that the morphology fungal strands following the depressions between
of the colonized root is mainly controlled by the host epidermal cells; 'superficial net' for the superficial
plant. Morphology might also change with time (Wilcox colonization shown on Figure 1; 'appressorium' for the
& Ganmore-Neumann, 1974). Wilcox & Ganmore- swollen structure preceding penetration through a host
Neumann (1974) described the morphology of Pinus cell wall (Fig. 4): 'penetration tube' for the thin structure
sylvestris roots inoculated with 'a black imperfect fungus'. penetrating through the cell wall (Fig. 4); 'microsclerotia'
While observing inoculated seedlings at 2-month for the intracellular groups of rounded, thick-walled cells
intervals, they reported the structures changing from a (Fig. 2).
combination of intra-cellular and intercellular invasion
to those more typical of ectendomycorrhizas, including
a continuous or discontinuous Hartig net and a dis-
continuous, patchy mantle similar to that observed by ÿÿÿÿÿÿÿÿÿ ÿÿÿÿÿÿÿÿÿÿ ÿÿ ÿÿÿ
O'Dell et al. (1993) in an inoculation trial with
Phialocephala fortinii and Pinus contorta. Only a few taxonomic affinities of DSE have been
recognized. Most are classified within deutero-mycetes
When describing the colonization by DSE, it is and their relation to teleomorphic taxa is unknown. Some
necessary to allow adequate time for the structures to DSE are fairly easy to isolate and maintain in pure
develop. Some basic structures seem constant for DSE culture. Conidiogenesis and sporu-lation of the cultures
colonization regardless of the host species. The presence is usually necessary for identification (but see Jumpponen
of sparse superficial mycelium, penetration & Trappe, 1996;

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Dark septate root endophytes 303

Table 4. The sampled taxa and their GenBank Hambleton & Currah, 1997). Conidiogenesis
accession numbers in the neighbor-joining analyzes typically is infrequent and some strains sporulate
(Fig. 5) only after extended incubation in low temperatures
(Richard & Fortin, 1973; Wang & Wilcox, 1985;
GenBank accession Fernando & Currah, 1995; Ahlich & Sieber, 1996).
Taxon number
Usually, conidiogenesis can only be induced in a few
Pleoporales
isolates; most remain sterile and unidentifiable (see
Herpotrichia diffusa U42484 Stoyke, Egger & Currah, 1992; Ahlich & Sieber,
Herpotrichia juniperi U42483 1996).
Leptosphaeria doliolum U04205 The identity and number of fungal (anamorphic
Ophiobolus herpotrichus U43453
or teleomorphic) species included in DSE are
Pleospora herbarum U43458
Microscales uncertain. The isolates typically do not sporulate or,
Microascus trigonosporus L36987 when they do, produce only scanty conidia. The
Xylariales difficulty of identifying the root endophytes led
Xylaria hypoxylon U20378 researchers to use various names to describe similar
Pezizales
root-fungus associations. For example, Peyronel
Morchella esculenta U42642
Morchella elata U42641 (1924) called such colonization that he observed on
Bohemic verpa U42645 135 taxa of 'Rhizoctonia-like' angiosperms. Several
Dothideales researchers have referred to isolates of sterile non-
Botryosphaeria ribis U42477 Rhizoctonia fungi from orchids as 'Rhacodium spp.'
Dothidea insculpta U42474
(Harvais & Hadley, 1967; Harvais, 1974) or given
Leotiales
Confused Cudonia Z30240 them names within Rhizoctonia (eg Curtis, 1939).
Monilinia laxa Y14210 The true taxonomic affinity of these fungi is
Sclerotinia sclerotiorum L37541 obviously uncertain.
Spathularia flavida Z30239 Despite Melin's (1923) accurate description of his
Chaetothyriales
sterile isolates, it was the 1960s before any taxonomic
Capronia pilosella U42473
Elaphomycetales
identities of root or soil associated fungi in the MRA
Elaphomyces maculatus U45440 complex were suggested. Gams (1963) identified two
Eurotiales cultures of MRA isolated from soil as Phialocephala
Talaromyces bacillisporus D14409 dimorphospora Kendrick. Richard & Fortin (1973)
Onygenales were able to identify 15 of the 41 strains of MRA
Blastomyces dermatitidis M63096
Saccharomycetales
they isolated from roots of various woody plants in
Debaryomyces castellii X83819 central and northern Europe as P. dimorphospora. P.
Debaryomyces hansenii X62649 dimorphospora commonly appears to be associated
Saccharomyces rosinii X99524 with decaying wood, soil and pseudomycorrhizas or
Neolectales
ectomycorrhizas (Kendrick, 1961; Gams, 1963;
Neolecta vitellina Z27393
Taphrinales
Richard & Fortin, 1973). Richard & Fortin (1973),
Taphrina deformans U20376 however, they were somewhat uncertain of the accuracy
Mitosporic rate of their identification: ' the conidiophores of P.
alternaria alternata U05194 dimorphospora isolates were generally darker and the
Aspergillus parasiticus D63699
collarette more conspicuous'. Still, they felt that
Coccidiodes immitis M55627
Cochliobolus heterostrobus L36994 their sporulating isolates were, indeed, P. dimor-phospora.
Exophiala mansonii U20382 When studying Richard & Fortin's
Leptodontidium orchidicolaa AF056374 cultures, Wang & Wilcox (1985) pointed out a
Leptodontidium quercuum AF056375 possibility of misidentification in the previous work
Phialocephala fortinii L76626 and concluded that at least some of the P. dimor-phospora
Phialocephala fortiniib AF055885
Phialophora finland L76625 isolates might actually have been one of the
Phialophora finlandiac AF056373 later described anamorphic species, Phialocephala
Phialophora verrucosa L36999 fortinii.
Nonsporulating cultures Additional anamorphic species from the MRA
Unknown 1d AF056369
Unknown 2e AF056370
Unknown 3f AF056371
mycorrhizas, courtesy of Lynne Sigler and Randy
Unknown 4g AF056372 Currah.
d
Strain stthb, isolated from Stipa thurbeniana, courtesy
a Strain UAMH8151, isolated from Artemisia norvegica, of Marcia Wicklow.
courtesy of Lynne Sigler and Randy Currah (Fernando & and Strain WB12, isolated from Betula papyrifera, cour-tesy of
Currah, 1995). Kathleen Ann Johnson.
B f
Strain SE24, isolated from Lupinus latifolius (O'Dell Strain cc3, isolated from Carex sp., courtesy of Kurt
et al., 1993) Haselwandter (Haselwandter & Read, 1982). g
c Strain UAMH8322, isolated from Pinus strobus Strain A12b2, isolated from Alnus sp.

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304 A. Jumpponen and J. M. Trappe

Unknown 1d
67
alternaria alternata
95
50 46 Cochliobolus heterostrobus
Pleospora herbarum
50 95 Leptosphaeria doliolum
Ophiobolus herpotrichus
42 Unknown 2e
27
57 Herpotrichia diffusa
Herpotrichia juniperi
100 Microascus trigonosporus
Xylaria hypoxylon
82 Unknown 3f
19 88
Phialocephala fortinii b
26
Phialocephala fortinii
35 Leptodontidium orchidicolaa
Unknown 4g
94 Phialophora finlandiac

13 34 Phialophora finland
77 Morchella elata
68 Morchella esculenta
19
31 Bohemic verpa
62 Botryosphaeria ribis
16 Dothidea insculpta
76 Leptodontidium quercuum
85 Monilinia laxa
54
Sclerotinia sclerotiorum
98 Confused Cudonia
85
Spathularia flavida
95 Capronia pilosella
80
Phialophora verrucosa
Exophiala mansonii

38 Aspergillus parasiticus
54
45 Elaphomyces maculatus
56
Talaromyces bacillisporus
28 Blastomyces dermatitidis
Coccidiodes immitis
94 Debaryomyces hansenii
100
Debaryomyces castellii
Saccharomyces rosinii
Neolecta vitellina
Taphrina deformans

Figure 5. A 50% majority rule consensus of 1000 bootstrapped neighbor-joining trees (PAUP*, with permission from
David Swefford) based on partial sequences of small subunit of the ribosomal rRNA gene aligned at 586 positions.
Rates shown in bold colonized Pinus contorta intracellularly in aseptic synthesis.
Numbers above branches indicate bootstrap values. Accession numbers of the sampled taxa are shown in Table 4.
Footnotes as in Table 4.

complex were described: Phialocephala fortinii, Establishing connections between DSE and sexually
Phialophora finlandia, Chloridium paucisporum (Want & reproducing taxa, ie, anamorph–teleomorph relationships,
Wilcox, 1985) and Leptodontidium orchidicola (Currah would be useful for inferring the possible systematic and
et al., 1987). We decided to exclude Phialophora functional relationships between genera, species and
radicicola Cain (Cain, 1952) from this discussion. It is strains of DSE. Currently the terms MRA and DSE, as
thought to be a non-pathogenic (or parasitic) fungus employed by many investigators, represent a
that colonizes roots of grasses and cereals possessing heterogeneous mix of strains of form taxa. Many DSE
characteristics typical of the DSE colonization (see are likely ascomycetous. Our preliminary analysis of the
Deacon, 1973), but observations are sparse and usually small subunit of the nuclear ribosomal RNA gene (18S)
from agri-cultural fields. The above four species have clearly placed all the included DSE within ascomycetes
all been isolated, identified and reported from various (Fig. 5). Similarly, an analysis by Lobuglio, Berbee &
hosts and habitats (Table 3). Taylor (1996) showed clear

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Dark septate root endophytes 305

ascomycetous affinity for Phialocephala fortinii and It is not surprising that the ecology of DSE is poorly
Phialophora finlandia. Currah & Sherburne (1992) concluded understood, given that several taxa of asco-mycetes from
that Leptodontidium orchidicola has a likely ascomycetous different families and even orders are involved. As Allen &
affinity, as judged by the septal ultrastructure. Allen (1992, p. 465) explained: 'Unfortunately, few field data
exist which allow definitive statements regarding the
The placement of DSE within ascomycetes is still an open importance of different fungi on plant communities. In part
question. Their placement is poorly resolved and appears this is due to frequent inability to recognize the vegetative
polyphyletic; two of the DSE isolates that remained sterile state of fungi associated with plants in the field.' Description
were placed within Pleosporales, whereas others were placed and identification of new taxa of DSE establish a starting
close to Pezizales (operculate discomycetes) or Leotiales point for a better understanding of their interactions with hosts
(inoperculate discomycetes) (Fig. 5). The 18S data by (see Kendrick, 1961; Wang & Wilcox, 1985; Currah et al.,
Lobuglio et al. (1996) positioned Phialocephala fortinii close 1987, Fernando & Currah, 1995). Molecular and morphological
to Leotiales. Currah et al. (1993) reported small aggregations systematic studies of DSE fungi (Kendrick, 1961; Wingfield,
of apothecium-like structures on the surface of the substrate van Wyke & Wingfield, 1987; Currah & Tsuneda, 1993;
in cultures in which colonization brachycarpum was inoculated Fernando & Currah, 1995) and re-evaluation of the taxa will
with Phialocephala fortinii. Even though these ascomata open avenues for separating fungi with different ecological
remained sterile and never matured, the observed functions by accommodating morphologically or genetically
characteristics also suggest an affiliation with inoperculate distinct groups.
discomycetes. Phialophora finlandia, however, was placed
either with Leotiales or Pezizales (LoBuglio et al., 1996). In
our analysis, P. finlandia appeared more closely affiliated with
Pezizales (Fig. 5). Another line of evidence also suggests that
some of the DSE may be related to the Pezizales. Several ÿÿÿÿÿÿÿ ÿÿ ÿÿÿ ÿÿ ÿÿÿÿÿ ÿÿÿÿÿ
species within the Pezizales have been shown to colonize
roots of woody plants (Danielson, 1984; Egger & Paden, Melin (1922) first described 'pseudomycorrhizas' and MRA,
1986a, b). Some of these, such as Sphaerosporella brunnea, differentiating the structures 'harmful to seedlings and trees'
may be ecto- or ectendomycorrhizal (Danielson, 1984; Egger from 'ectotrophic mycorrhiza which is a necessary condition
& Paden, 1986b). Others, eg Geopyxis carbonaria and for their normal development'. He reported that, after forming
Trichophaea hemisphaerioides, formed patchy, discontinuous thin mycorrhizas, the MRA overgrew and killed the host plant,
mantles and extensively colonized epidermal and cortical appearing as parasites (Melin, 1923).
cells (Egger & Paden, 1986b), resembling structures
described by O'Dell et al. (1993) in the roots of Pinus contorta Robertson (1954) and Hatch & Hatch (1933) confirmed
colonized by Phialocephala fortinii. Most other species studied these results in their pure culture syntheses.
by Egger & Paden (1986a, b), however, were clearly However, because of the presence of dark mycelium on the
pathogens on their test plant, Pinus contorta. surfaces of 'healthy elongating' roots of pines in the field
samples, Robertson (1954) concluded that these fungi attack
roots only under special physiological conditions, such as
during senescence, and that they are not pathogenic 'to
healthy roots in natural soils'.

The early observations indicating that MRA strains can be

Sequencing and cladistic analyzes will doubtless be pathogenic resulted in further tests.
powerful in identifying DSE. Genetic markers and their Unidentified cultures of dark-pigmented, sterile fungi were
applications have been shown to be useful in identifying taxa inoculated on host plants: Picea abies (Schonhar, 1984),
and strains of DSE (Stoyke et al., 1992; Yan, Rogers & Wang, Pinus sylvestris (Schonhar, 1984), Chamaecyparis
1995; Jumpponen & Trappe, 1996). They can in part replace nootkatensis (Hennon, Shaw & Hansen, 1990) and Fragaria
the time-consuming morphological identification. Furthermore, vesca (Wilhelm, Nelson & Ford, 1969). Results were, not
they can be used for studying the phylogenetic relationships surprisingly, inconsistent: the strains varied from strongly
among the form taxa (eg Yan et al., 1995). For example, pathogenic (Wilhelm et al., 1969) to weakly pathogenic
RFLP data of the ribosomal RNA gene indicates that P. fortinii (Schonhar, 1984) or non-pathogenic (Hennon et al., 1990).
and similar isolates vary substantially (Stoyke et al., 1992; Haselwandter & Read (1982) inoculated two Carex species
Harney, Rogers & Wang, 1997), suggesting taxa previously with unidentified indigenous dark, septate strains from the
identified on the basis of morphological characteristics are European Alps. They reported increased biomass and
heterogeneous. Similarly, Yan et al. (1995) found disagreement phosphorus levels after inoculation and concluded that 'the
between morpho-logical and molecular identification of root–fungus association appeared to be of a mutualistic rather
Phialophora than a parasitic nature'. One of Haselwandter & Read's (1982)
isolates (unknown 3; Table 4) was

sp.

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306 A. Jumpponen and J. M. Trappe

included in the preliminary molecular phylogenetic analysis. 1965) and cellulose agar (Warcup, 1973), respectively. By
It appeared closely related to the type culture of Phialocephala contrast, O'Dell et al. (1993) used a method in which the
fortinii and some other strains identified as P. fortinii (Fig. 5). seedlings were grown in a 'growth pouch' to which nutrients,
It is essential to note that the association between a fungus but no carbohydrates, were added. Whatever the reasons for
and its host is dependent on the species of both the fungus observed inconsistencies in the host response to inoculation,
and the host, as well as the experimental conditions. it is obvious that results from any pure culture synthesis
should be viewed with some caution.
Meaningful conclusions about host–fungus relation-ships
must therefore be based on correctly identified fungi and DSE involvement in host nutrient acquisition has also been
hosts. hypothesized. Jumpponen et al. (1998) grew seedlings of P.
With the description of a few species of DSE (Kendrick, contorta in nitrogen-limited glacier soil in a fully factorial
1961; Wang & Wilcox 1985; Currah et al., 1987), interest has design with three treatments: inoculation with a strain of
increased in determining the nature of the association Phialocephala fortinii, addition of organic matter, and N. The
between the host and fungal endophyte in specific host– P. fortinii-inoculation alone did not affect growth, but
endophyte combinations. significantly increased the foliar phosphorus concentration
Wilcox & Wang (1987a) inoculated four species on Pinus regardless of the N treatment. The combination of inoculation
resinosa, Picea rubens, and Betula alleghaniensis. and N amendment resulted in a 50% larger increase in Pinus
The results were variable and host response dependent on contorta biomass than did the N amendment alone.
the host–fungus combination. They concluded that
Phialocephala dimorphospora was pathogenic, P. fortinii
pseudomycorrhizal or patho-genic, Chloridium paucisporum Haselwandter & Read (1982) grew seedlings of Carex firma
ectendomycorrhizal or pseudomycorrhizal, and Phialophora and C. sempervirens inoculated with two strains of DSE.
finlandia ectomycorrhizal or ectendomycorrhizal, depending Inoculated seedlings consistently had a significantly higher
on the host species. Their conclusions were based on the foliar P concentration, while only C. firma growth was
visual appearance of the seedlings rather than biomass stimulated. Taken together these results suggest that at least
accumulation, nutrient acquisition, or fitness. When they some strains of DSE may be involved in host nutrient
further studied the positive association between the same acquisition and therefore may indeed have a mutualistic,
hosts and P. finlandia, they concluded that the fungal mycorrhiza-like relationship with their host plants.
colonization increased growth (Wilcox & Wang, 1987b).

Additional inoculation assays with specific host– fungus

ÿÿÿÿÿÿÿ
combinations were conducted. Stoyke & Currah (1993)
inoculated Menziesia ferruginea with Phialocephala fortinii on Even if the effects of DSE on host plants vary with hosts and
cellulose agar in Petri dish cultures. P. fortinii physically growth conditions, their abundance in some natural
overgrew the seedlings in the absence of competition by environments (see Berch, Gamiet & Deom, 1988; Hennon et
other fungi under aseptic conditions. O'Dell et al. (1993), al., 1990; Cazares, 1992; Holdenrieder & Sieber, 1992 ) and
however, saw no adverse reaction or extensive degradation ubiquitous global (see http:www.cup.cam.ac.uk
of Pinus contorta tissue in response to colonization by P. presence SPECIESTABLE.html) suggests an
fortinii in an open system that received small amounts of important eco-logical role. Intercellular and intracellular
fertilizer with watering, but no additional carbohydrates. colonization, as well as the ability to colonize a wide variety
of host plants, have led researchers to propose that non-
mycorrhizal root endophytes such as Rhizoctonia sp. (Warcup,
Several possible reasons could account for the inconsistent 1985) and Phialocephala fortinii (Jumpponen & Trappe, 1996)
results of these studies. Fernando & Currah (1996) pointed can form mycelial connections between plant individuals of
out obvious strain-specific differences in the growth responses the same or even different species. These could be involved
in bioassays where P. fortinii was inoculated on several hosts in photosynthate or nutrient transport as suggested for
in aseptic and open pot cultures. The resynthesis system, as ectomycorrhizal systems (Simard et al., 1997a, b and
well as the media used in assays, can produce incongruent references therein).
results. Duddridge & Read (1984) and Duddridge (1986)
demonstrated a change in the behavior of ectomycorrhizal
fungi in the presence of exogenous carbohydrate. The Several different enzymatic activities have also been
nutritional status of the fungal endophyte might therefore be detected in DSE (see Ahlich Schlegel, 1997).
an explanation for the controversial earlier results: Wilcox & Baath & Soderstrom (1980) showed cellulolytic and proteolytic
Wang (1987a) and Stoyke & Currah (1993) used a growing activity in an unidentified darkly pigmented fungus. Ahlich
medium with readily available carbohydrates, double-strength Schlegel (1997) showed that strains of DSE possessed
MMN (Marx & Zak, laccases, lipases, amylases and polyphenol oxidases. The
activities and their relative strengths, however, varied
drastically be-

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Dark septate root endophytes 307

tween the strains. Based on a similar enzymatic activity assay exposed to frost and midsummer droughts. Resistance to
Caldwell, Trappe & Jumpponen (1996) concluded that cold and desiccation may play a significant role for the
Phialocephala fortinii and other sterile isolates of DSE similar organisms able to persist at the site from year to year.
to P. fortinii can process common detrital carbon and P
polymers. Polyphenol oxidases, which may be involved in Currah et al. (1993) hypothesized that the in-tracellular
processes such as lignin degradation, have been shown to be sclerotial bodies of Phialocephala fortinii, also heavily
produced by Leptodontidium orchidicola (Fernando & Currah, melanized, can be effective dispersal propagates. As the
1995) and P. fortinii (Currah & Tsuneda, 1993; Ahlich Schlegel, colonized roots mature, the epi-dermal cells frequently loosen
1997). Despite their enzymatic activities, it remains unclear and slough off the root.
whether DSE fungi actually decompose organic debris in their The sloughed-off cells can then disperse with the soil
natural environment. Hutchinson (1990) speculated that these movement like the spores of arbuscular mycorrhizal fungi
enzymes may be involved in fungal resistance to antifungal (Allen, 1991). Melanins would improve the persistence and
compounds rather than in decomposition. Furthermore, survival of the DSE propagales in soil. According to Currah et
penetration through host cell walls may require lignolytic and al. (1993), persistent propagules, such as the sloughed-off
cellulolytic cortical cells filled with sclerotial bodies, could explain why
DSE fungi are frequently isolated from surface-sterilized or
washed roots and mycorrhizas (Summerbell, 1989; Stoyke &
enzymes. Currah, 1991; Holdenrieder & Sieber, 1992; Stoyke et al.,
Colonization by DSE has also been observed to occur 1992; Jumpponen & Trappe, 1996).
simultaneously with arbuscular mycorrhizal (Thoen, 1987;
Sengupta et al., 1989; Horton et al., 1998) or ectomycorrhizal
fungi (Trappe, 1962; Horton et al., 1998). DSE are also The reproduction and dispersal of DSE are almost
frequently isolated from root tips colonized by ectomycorrhizal completely unknown. As described above, mycelial
fungi (Hatch, 1934; Trappe, 1962; Holdenrieder & Sieber, fragmentation is among the suggested means of dispersal
1992). Concurrent occupation by different root-associated (Currah et al., 1993). Dispersal by conidio-spores is also
fungi might indicate the dynamic nature of the root-colonizing possible. Despite the fact that to date no anamorph–
fungal community. DSE colonization appears more frequent teleomorph connections have been established, sexual
in older parts of the root system (Robertson, 1954; Livingston reproduction is possible. Currah et al. (1993) described
& Blaschke, 1984), suggesting that DSE prefers aging root immature ascomata in a pot culture synthesis. Jumpponen &
tissue or that DSE is recycling nutrients from senescent or Trappe (1996) hypothesized, based on the high genetic
dead root cells back into the active roots. On the other hand, diversity observed in a population assay, that a large number
DSE might function as mutualistic fungi taking part in nutrient of asexual individuals or frequent sexual recombination would
and water acquisition, especially in unfavorable environments be required to explain the large number of distinct phenotypes
(Sengupta et al., 1989; Jumpponen et al., 1998). The found on their small study site on a glacier forefront. However,
concurrent colonization by DSE and ectotrophic or endotrophic more data are needed to understand how the populations of
mycorrhizal fungi would thus provide a back-up system during DSE disperse and maintain themselves.
periods when mycorrhizal fungi are inhibited by the
environmental conditions.

ÿÿÿÿÿÿÿÿÿÿÿ

These hypotheses need to be tested, preferably in natural Sterile root endophytes are ubiquitous in various habitats.
environments. Harley (1950) pointed out that 'one is definitely in a position
Another interesting question is the role and presence of to state that such sterile septate mycelia are to be expected
melanins in the hyphae of DSE. in the external tissues and on the surface of roots of almost
Melanins develop in large quantities in organisms that live in any plant…'. These endophytes, DSE fungi, have been
unfavorable environments (Bell & Wheeler, 1986). They might reported from various habitats and from a wide range of hosts.
play an important role in discouraging grazing on soil micro- Hosts include species known to be arbuscular, ericoid, orchid,
organisms by other soil microfauna and enable the organisms ecto- or non-mycorrhizal. In most studies to date, all but the
to withstand desiccation and microbial lysis (Kuo & Alexander, most conventional types of root colonization have been
1967; Bell & Wheeler, 1986). Melanins might protect DSE ignored. Including root endophytes in mycorrhizal studies
hyphae from extreme temperatures and drought, and so adds laborious steps to the already time-consuming
broaden their ecological niche, as suggested for the strongly enumeration of mycorrhizas, but it would yield valuable data
melanized Cenococcum geophilum (Trappe, 1962). about the importance and frequency of other root colonizers.

Cazares (1992) and Jumpponen & Trappe (1996) isolated

several DSE from an alpine glacier foreland in northern DSE clearly comprises a heterogeneous group of known,
Washington, USA, which is frequently and possibly unknown and undescribed, taxa

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308 A. Jumpponen and J. M. Trappe

of deuteromycetes. The inconsistencies and dis-agreements Allen MF, Allen E. 1992. Mycorrhizae and plant community
development: mechanisms and patterns. In: Carroll GC, Wicklow
among results from various studies of DSE partly result from
DT, eds. The Fungal Community. New York, NY, USA: Marcel
the uncertain identities of the strains used. Phylogenetic Dekker, 455–480.
analyzes of DSE may be essential to shed light on questions Baath E, Soderstrom B. 1980. Degradation of macromolecules by
microfungi from different podzolic soil horizons. Canadian Journal
of their origin and provide further help in solving the functional
of Botany 58: 422–425.
aspects of the fungi in this group. Bell AA, Wheeler MH. 1986. Biosynthesis and functions of fungal
melanins. Annual Review in Phytopathology 24: 411–451.
Berch SM, Gamiet S, Deom E. 1988. Mycorrhizal status of some
The ecology of DSE is largely unknown and hypotheses
plants of southwestern British Columbia. Canadian Journal of
are based on sparse evidence. Root– fungus association Botany 66: 1924–1928.
might diverge from easily classifiable, morphologically Bisset J, Parkinson D. 1979. Functional relationships between soil
identifiable mycorrhizal types and yet function physiologically fungi and environment in alpine tundra. Canadian Journal of Botany
57: 1642–1659.
as mycorrhizas under natural conditions (Kope & Warcup, Blaschke H. 1991. Multiple mycorrhizal associations of individual
1986). calcicole host plants in the alpine grass-heath zone.
Thus, a primary research focus should be on the functional Mycorrhiza 1:31–34.
Burges NA. 1936. On the significance of mycorrhiza. New
aspects of the interaction between the two organisms Phytologist 35: 117–131.
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