Editorial

Marchantia: Past, Present and Future

John L. Bowman1,2, Takashi Araki3,* and Takayuki Kohchi3
1
School of Biological Sciences, Monash University, Melbourne, Victoria 3800, Australia
2
Department of Plant Biology, University of California, Davis, Davis, CA 95616, USA
3
Graduate School of Biostudies, Kyoto University, Kyoto, 606-8501 Japan
*Corresponding author: E-mail, taraqui@lif.kyoto-u.ac.jp; Fax, +81-75-753-6470.

The evolution of a land flora was a momentous event in shap- Ordovician are plentiful in the fossil record, and are recovered

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ing our planet by altering the landscape through modulation of only from terrestrial or near offshore deposits (Wellman and
geochemical cycles and facilitating the invasion of land by other Strother 2015). Cryptospores are a non-phylogenetic assem-
taxa, such as our own ancestors. By the mid-Ordovican blage of spores distinct from trilete and monolete spores and
(450 Ma), the appearance of land plants had dramatically pollen grains, but similar to spores of land plants.
changed the terrestrial environment and they rapidly became Ultrastructural and geochemical analyses indicate that crytos-
the dominant ecological force. Between the Ordovician and pore spore walls are chemically similar to those of some extant
Devonian there was an explosion in land plant diversification, liverwort spores (Steemans et al. 2010). Thus, the presence of
with the major extant lineages of land plants (liverworts, cryptospores is likely to be indicative of the presence of land
mosses, hornworts, lycophytes, ferns and seed plants) estab- plants, and, more specifically, liverwort-like bryophytic organ-
lished by the end of the Devonian (360 Ma). isms. Liverwort macrofossils also pre-date those assigned to
Land plants form a monophyletic clade that nests within a either mosses or hornworts. Further, cladistic studies of mor-
grade of freshwater and terrestrial charophycean algae (also phology and the fossil record suggest that liverworts are the
known as streptophyte algae), implying that land plants basalmost lineage of land plants, with hornworts sister to vas-
evolved from a freshwater or terrestrial alga (Pickett-Heaps cular plants, and mosses occupying the middle position of a
and Marchant 1972, Karol et al. 2001). Their rapid rise can be bryophyte grade (Mishler and Churchill 1984, Kenrick and
attributed to a number of evolved features enabling individuals Crane 1997a).
to survive the terrestrial subaerial environment, such as pig- On the other hand, in land plant phylogenies, based on
mentation and a ‘sunscreen’ for protection from harsh UV molecular data nearly every possible permutation of bryophyte
irradiation, and the ability to withstand desiccation for relationships and their relationships to vascular plants has been
extended periods of time. Many of these physiological adapta- proposed. For example, some analyses support the idea of liver-
tions to a terrestrial environment may have evolved with the worts being the basal lineage in a grade of bryophytes (Qiu et al.
charophycean algal lineage leading to land plants (Delwiche 2006), but a recent analysis suggests that hornworts are the
and Cooper 2015). In contrast, developmental innovations, basal land plant lineage, with mosses and liverworts forming
such as the evolution of an apical cell with more than two cutting a sister clade to vascular plants (Wickett et al. 2014).
faces, enabling the development of three-dimensional growth in Reconciliation of molecular phylogenies with the fossil record
the form of complex tissue and organ morphologies including may require broader taxon sampling in the former, or reinter-
anatomical innovations for water conductance, are a synapomor- pretation of the latter.
phy of land plants. Whereas the life cycles of charophycean algae
are haplobiontic—a multicellular haploid phase with a single-
celled diploid phase consisting of a zygote that immediately Why Marchantia?
undergoes meiosis—the life cycle of land plants is defined by a
The arguments above point to the need for a model liverwort
complex multicellular diploid sporophyte generation (borne from
to investigate fundamental events in land plant evolution. The
an embryo), which, combined with the complex multicellular
gametophyte body plans of liverworts are more variable than
haploid gametophyte generation, led to an alternation of genera-
those of either mosses or hornworts—there are simple thalloid,
tions. Arguably, the evolution of the sporophyte generation was
complex thalloid and leafy forms—nearly all are dorsi-ventral
instrumental in the land plant’s ascent to terrestrial dominance.
(Watson 1964, Schuster 1992, Crandall-Stotler et al. 2009). All
liverworts share a short to non-existent protonemal phase and
a subsequent prothallus stage prior to differentiating the final
Why a Liverwort?
gametophyte body, which is produced by apical cells of differ-
Few identified macrofossils represent the early colonization of ent anatomies depending upon the body plan. All liverworts
land by plants, but cryptospores dating from the early Middle also lack stomata and have membrane-bound oil bodies

Plant Cell Physiol. 57(2): 205–209 (2016) doi:10.1093/pcp/pcw023, available online at www.pcp.oxfordjournals.org
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 and ventral unicellular rhizoids, except Haplomitrium, which (n = 8 + X in female and Y in male). The gene organization of
lacks rhizoids. While some early researchers considered the the Y chromosome provided an insight into sex chromosome
complex thalloids, such as Marchantia polymorpha, to be structure and evolution in a plant with a haploid system
highly derived, recent molecular phylogenies have indicated (Yamato et al. 2007). Thus, M. polymorpha has played a leading
the Marchantiopsida, including the complex thalloids, to be role as a model for genome analysis.
basal to most simple and leafy liverwort lineages, with the Genome information is a fundamental platform for modern
exception of the Haplomitriopsida comprised of a small biology, and functional analyses should be done by fully utilizing
number of possibly relict species (Forrest et al. 2006, He- the available sequence information. The central criteria
Nygrén et al. 2006). required for versatile model organisms include forward genet-
Marchantia polymorpha has been used as a model system ics, reverse genetics, genetic transformation and genome-wide
for investigating biological processes for nearly two centuries. studies. In the past few years, techniques have been established
Prior to its use in what we might consider modern biology in M. polymorpha that promote this species as a member of the

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following the enlightenment, Marchantia had been described model organism cohort. Forward genetics and subsequent
in ancient Greek medical texts as a plant useful to apply to functional analyses of causal genes were reported for air cham-
open wounds to prevent infection and inflammation ber (Ishizaki et al. 2013b) and rhizoid (Proust et al. 2016) devel-
(Dioscorides 1529). While speculative, the basis for this sup- opment. Reverse genetics approaches were also utilized in
position may lie in the chemicals contained in the oil bodies, studies of auxin signaling (Kato et al. 2015, Flores-Sandoval
terpenoids, that have since been shown to reduce fungal and et al. 2015), phototropin (Komatsu et al. 2014), growth phase
bacterial growth. If so, most liverworts would have sufficed, transition (Kubota et al. 2014), and so on. Other studies, such as
but due to its abundance, its widespread geographical distri- those in secondary metabolism (Takemura et al. 2014) and
bution and its colonization of man-disturbed habitats nuclear-encoded plastid sigma factors (Kanazawa et al. 2013),
(Schuster 1992), M. polymorpha was the sole liverwort have also appeared. Efficient Agrobacterium-mediated transfor-
described in the earliest floras following the Renaissance. In mation systems has been developed in M. polymorpha (Ishizaki
the late 18th century Johann Hedwig and C. Schmidel used M. et al. 2008, Kubota et al. 2013, Tsuboyama and Kodama 2014),
polymorpha as one of the model species to elucidate the life enabling reverse genetics tools including artificial microRNAs
cycle of liverworts and mosses (Hedwig 1783, Schmidel 1783). (amiRs), homologous recombination and genome editing
At the beginning of the 19th century, a major question was (Ishizaki et al. 2013a, Sugano et al. 2014, Flores-Sandoval et al.
whether the entirety of an organism was composed of cells 2016). Marchantia polymorpha was also chosen for the com-
and how new cells arose. In an attempt to address these munity sequencing program at the Joint Genome Institute,
questions, François Mirbel followed, in cellular detail, the life Department of Energy, USA. The sequences will be released
cycle of M. polymorpha. While he may not have succeeded in later this year. Thus, nearly 200 years after it was first used as
his original aim, his experiments with gemmae (vegetative a biological model, a 21st century Renaissance is reviving
propagules) of M. polymorpha were perhaps the first to inves- M. polymorpha as a superb model with a suite of established,
tigate the establishment of dorsiventrality and the body plan available experimental tools.
of a plant (Mirbel 1835). The remainder of the 19th century
was the golden age of anatomy, and M. polymorpha served as a
model for studies of motile sperm and fertilization, and cul-
In This Issue
minating in Leitgeb’s detailed studies of liverwort anatomy
and development (Leitgeb 1881). The wealth of literature pro- This Special Focus Issue (SFI) is the first of such introducing
vides a valuable resource for present and future studies of M. polymorpha to a broad plant science audience. It includes
unresolved questions concerning aspects of physiology, devel- two reviews, two mini-reviews, four technical articles and four
opment, and evolution. original research articles by researchers working with M. poly-
morpha. These papers cover several topics, including its history
as a study model, taxonomy, phylogeny, morphology and life
cycle. It also includes a community proposal for a unified
The Modern Era
system of gene nomenclature, as well as recent advances in
Kanji Ohyama (1939–2013) led the early era of plant genomics experimental techniques for cell, developmental and genome
using Marchantia as a material. Sequencing genomes of chlor- biology. The first of the two reviews provides a comprehensive
oplasts (Ohyama et al. 1986) and mitochondria (Oda et al. overview of Marchantia’s history from its early recognition to
1992) from Marchantia culture cells marked important mile- its recent rediscovery as a model plant (Bowman 2016). Topics
stones in plant biology. These early structural analyses of orga- such as the usefulness of Marchantia in discovering cryptoga-
nelle genomes indicated that no fully functional enzymes and mic sex and spermatozoids (antherozoids), chromosomal-
protein complexes are produced only by the organelle-encoded based sex determination and supporting cell theory in plants
components and that extensive co-ordination of organelle and are all described. Historic research into polarity formation—one
nuclear genomes is required in plants. Moreover, M. polymor- of the long-standing questions in developmental biology—
pha was used for sex chromosome analysis. Marchantia poly- using Marchantia gemmalings is also comprehensively
morpha has eight autosomes and a single sex chromosome described. The second review by Shimamura (2016) covers

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phylogeny, taxonomy, life cycle and morphology. It describes miRs and their targets in M. polymorpha provide insight into
the phylogenetic position of Marchantia among bryophytes the spectrum of evolutionarily conserved and more lineage-
(liverworts, mosses and hornworts) and summarizes the com- restricted miRs encoded in the M. polymorpha genome (Lin
plicated taxonomy of specific and infraspecific taxa of the genus et al. 2016, Tsuzuki et al. 2016). Both research groups identified
Marchantia. This account will undoubtedly help those who use a core set of conserved miRs, but, due to differential tissue
M. polymorpha as a model organism to understand its phylo- sampling, the overlap of non-conserved miRs was not substan-
geny and taxonomy. Equally useful are the descriptions of its life tial, implying that there is more to discover.
cycle and morphology, which include original observations that
extend earlier reports such as those described by Kny (1890)
and Durand (1908), thus serving as an updated reference work Perspectives
for those especially interested in developmental aspects of this
Over the past decade, many researchers worldwide have
plant.
become increasingly attracted to M. polymorpha due to its

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To promote consistency and to reduce confusion in the
unique phylogenetic position amongst plants and to recent
scientific literature, Bowman et al. (2016) present a community
advances in the various molecular techniques and tools,
proposal for M. polymorpha gene and transgene nomenclature.
making this species a timely and significant model organism
This nomenclature was built upon the lessons of the past to suit
of choice. Critical to this trend has been the rapid growth and
an organism in the genomic era, and we strongly encourage
spread of a research community that exchanges information,
researchers to follow these guidelines.
materials and people. The expected completion and publica-
Next, we have five papers (one mini-review and four original
tion of the genome project this year will further boost research
papers) reporting tractable methods for M. polymorpha.
into M. polymorpha, while its promotion as a model basal land
Ishizaki et al. (2016) review the current molecular tools and
plant that is as versatile as the angiosperms, Arabidopsis and
techniques developed for researchers including transformation,
rice, will add to our understanding of land plant (embryo-
overexpression, and gene targeting by homologous recombina-
phytes) evolution and eventually encourage exploration of
tion and genome editing. The haploid-dominating life cycle
sister land plant groups (charophycean algal lineages). Similar
facilitates genetic analyses, but conversely limits the ability to
to Arabidopsis thaliana, we envisage that M. polymorpha will
isolate mutants of essential genes. To circumvent this issue,
serve as a useful model organism in the broader framework of
Nishihama et al. (2016) describe a system that allows condi-
the eukaryotes, where it could readily lend itself to basic cellular
tional gene expression and deletion using the promoter of a
studies or subcellular processes compared with other model
heat shock protein gene and the Cre/loxP site-specific recom-
organisms. We expect that many ambitious studies will
bination system. Concomitantly, Flores-Sandoval et al. (2016)
appear in the coming decade and we hope that this SFI will
report that amiRs with primary miR hairpin backbones are
serve as an inspiring taster of what is yet to come.
efficient for silencing genes, and that adaptation of an estro-
gen-inducible system permits phenotypic analyses at all stages
of the life cycle. In addition to nuclear-encoded genes, chloro- Funding
plast genes are also targets for genetic studies. Boehm et al.
(2016) report the development of a fluorescent reporter This work was supported by the Australian Research Council
system expressed from the chloroplast genome. Finally, [DP130100177 to J.L.B.]; the Japan Society for the Promotion of
Tanaka et al. (2016) report a simple cryopreservation protocol Science (JSPS) [Bilateral Research Program] and the Ministry of
for in vitro grown M. polymorpha gemmae, which should allow Education, Culture, Sports, Science & Technology (MEXT)
long-term preservation of transgenic and mutant lines in M. [Grant-in-Aid for Scientific Research on Innovative Area
polymorpha. (25113005 to T.A and 25113009 to T.K.)].
The remaining four research papers featured in this SFI all
describe the comprehensive analyses of Marchantia genes:
those encoding SNAREs involved in membrane trafficking Acknowledgments
(Kanazawa et al. 2016); a transcriptome analysis of developing We thank Professor Tomoyuki Yamaya, Editor-in-Chief, Plant
antheridium (male sexual organ) (Higo et al. 2016); and miRs and Cell Physiology, for providing the opportunity for this
and their targets (Lin et al. 2016, Tsuzuki et al. 2016). The paper Special Focus Issue on Marchantia polymorpha. We wish to
by Kanazawa et al. (2016) clearly demonstrates the phyloge- acknowledge the authors and reviewers who have contributed
netic importance of M. polymorpha to allow a better under- to this issue.
standing of basic subcellular processes in land plants. It also
shows the potential of M. polymorpha not only as a model
organism for plants, but also of use for studying other organ- References
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