Insights into Land Plant Evolution Garnered from the Marchantia polymorpha Genome.

The evolution of land flora transformed the terrestrial environment. Land plants evolved from an ancestral charophycean alga from which they inherited developmental, biochemical, and cell biological attributes. Additional biochemical and physiological adaptations to land, and a life cycle with an alternation between multicellular haploid and diploid generations that facilitated efficient dispersal of desiccation tolerant spores, evolved in the ancestral land plant. We analyzed the genome of the liverwort Marchantia polymorpha, a member of a basal land plant lineage. Relative to charophycean algae, land plant genomes are characterized by genes encoding novel biochemical pathways, new phytohormone signaling pathways (notably auxin), expanded repertoires of signaling pathways, and increased diversity in some transcription factor families. Compared with other sequenced land plants, M. polymorpha exhibits low genetic redundancy in most regulatory pathways, with this portion of its genome resembling that predicted for the ancestral land plant. PAPERCLIP.

The renaissance and enlightenment of Marchantia as a model system.

The liverwort Marchantia polymorpha has been utilized as a model for biological studies since the 18th century. In the past few decades, there has been a Renaissance in its utilization in genomic and genetic approaches to investigating physiological, developmental, and evolutionary aspects of land plant biology. The reasons for its adoption are similar to those of other genetic models, e.g. simple cultivation, ready access via its worldwide distribution, ease of crossing, facile genetics, and more recently, efficient transformation, genome editing, and genomic resources. The haploid gametophyte dominant life cycle of M. polymorpha is conducive to forward genetic approaches. The lack of ancient whole-genome duplications within liverworts facilitates reverse genetic approaches, and possibly related to this genomic stability, liverworts possess sex chromosomes that evolved in the ancestral liverwort. As a representative of one of the three bryophyte lineages, its phylogenetic position allows comparative approaches to provide insights into ancestral land plants. Given the karyotype and genome stability within liverworts, the resources developed for M. polymorpha have facilitated the development of related species as models for biological processes lacking in M. polymorpha.

KANADI promotes thallus differentiation and FR-induced gametangiophore formation in the liverwort Marchantia.

In angiosperms, KANADI transcription factors have roles in the sporophyte generation regulating tissue polarity, organogenesis and shade avoidance responses, but are not required during the gametophyte generation. Whether these roles are conserved in the gametophyte-dominant bryophyte lineages is unknown, which we examined by characterising the sole KANADI ortholog, MpKAN, in the liverwort Marchantia polymorpha. In contrast to angiosperm orthologs, MpKAN functions in the gametophyte generation in Marchantia, where it regulates apical branching and tissue differentiation, but does not influence tissue polarity in either generation. MpKAN can partially rescue the sporophyte polarity defects of kanadi mutants in Arabidopsis, indicating that MpKAN has conserved biochemical activity to its angiosperm counterparts. Mpkan loss-of-function plants display defects in far-red (FR) light responses. Mpkan plants have reduced FR-induced growth tropisms, have a delayed transition to sexual reproduction and fail to correctly form gametangiophores. Our results indicate that MpKAN is a modulator of FR responses, which may reflect a conserved role for KANADI across land plants. Under FR, MpKAN negatively regulates MpDELLA expression, suggesting that MpKAN and MpDELLA act in a pathway regulating FR responses, placing MpKAN in a gene regulatory network exhibiting similarities with those of angiosperms.

Evolution and co-option of developmental regulatory networks in early land plants.

Land plants evolved from an ancestral alga from which they inherited developmental and physiological characters. A key innovation of land plants is a life cycle with an alternation of generations, with both haploid gametophyte and diploid sporophyte generations having complex multicellular bodies. The origins of the developmental genetic programs patterning these bodies, whether inherited from an algal ancestor or evolved de novo, and whether programs were co-opted between generations, are largely open questions. We first provide a framework for land plant evolution and co-option of developmental regulatory pathways and then examine two cases in more detail.

Something ancient and something neofunctionalized-evolution of land plant hormone signaling pathways.

The evolution of land plants from a charophycean algal ancestor was accompanied by an increased diversity of regulatory networks, including signaling pathways mediating cellular communication within plants and between plants and the environment. Canonical land plant hormone signaling pathways were originally identified in angiosperms, and comparative studies in basal taxa show that they have been assembled from both ancient and newly evolved components, both before and during land plant evolution. In this review we present our current understanding, and highlight several uncertainties, of the evolution of hormone signaling pathways, focusing on the biosynthetic pathways generating putative ligands and the downstream perception and signaling pathways often leading to transcriptional responses.