Insights into Land Plant Evolution Garnered from the Marchantia polymorpha Genome

Abstract

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.

Sticking to it: phytopathogen effector molecules may converge on evolutionarily conserved host targets in green plants

“…The lack of experimental knowledge on effector–target relationships in non-flowering plants therefore limits comparative analyses with angiosperms, however as a first step we can assess whether known proteins and processes targeted by effectors are present across land plants. Recent phylogenetic analyses demonstrate that the general immune regulators SGT1, RAR1, and HSP90, which form a complex to regulate immune protein stability in angiosperms [28], are conserved across diverse land plant lineages that include early divergent bryophytes ( Marchantia polymorpha, Physcomitrella patens ), a vascular non-flowering lycophyte ( Selaginella moellendorffii ), a gymnosperm seed plant ( Picea abies ), and an early divergent angiosperm ( Amborella trichopoda ) [29 •• ]. Given that several unrelated phytopathogen effectors ( U. maydis SEE1, X. campestris AvrBsT, P. syringae AvrB, Phytophthora sojae CRN108) have been shown to modulate this complex [23, 24, 25,30], it is plausible that adapted or broad-host pathogens may employ effectors that target the conserved SGT1–RAR1–HSP90 complex in non-flowering plants.…”

“…The exocyst complex, and vesicular trafficking in general, is targeted by several unrelated phytopathogen effectors in angiosperms ( Phytophthora infestans AVR1, Magnaportha oryzae AVR-Pii, P. syringae HopM1) [31, 32, 33] and is broadly conserved in the green plant lineage [34]. MAP kinases regulating innate plant immunity are similarly conserved across land plants [7 • ,29 •• ] and appear to be recurring targets of effectors during pathogen–angiosperm interactions ( P. syringae AvrB, HopAI1, HopF2, HopZ3; P. infestans PexRD2, Pi17316) [35, 36, 37, 38, 39, 40, 41]. The plant-specific TCP transcription factor family is also present across the green plant lineage [29 •• ] and, as described above, is likely targeted by unrelated pathogen effectors.…”

“…MAP kinases regulating innate plant immunity are similarly conserved across land plants [7 • ,29 •• ] and appear to be recurring targets of effectors during pathogen–angiosperm interactions ( P. syringae AvrB, HopAI1, HopF2, HopZ3; P. infestans PexRD2, Pi17316) [35, 36, 37, 38, 39, 40, 41]. The plant-specific TCP transcription factor family is also present across the green plant lineage [29 •• ] and, as described above, is likely targeted by unrelated pathogen effectors. Lastly, the defense hormone salicylic acid (SA), which is commonly manipulated by various effectors in angiosperms (via enzymatic degradation or inhibition of signalling pathways; reviewed in [11,42]), has been detected in early divergent land plants that encode homologs of core SA synthesis and signalling genes [29 •• ,43, 44, 45].…”

“…The plant-specific TCP transcription factor family is also present across the green plant lineage [29 •• ] and, as described above, is likely targeted by unrelated pathogen effectors. Lastly, the defense hormone salicylic acid (SA), which is commonly manipulated by various effectors in angiosperms (via enzymatic degradation or inhibition of signalling pathways; reviewed in [11,42]), has been detected in early divergent land plants that encode homologs of core SA synthesis and signalling genes [29 •• ,43, 44, 45]. Collectively, the accumulated evidence suggests that homologs of core immune, cell biology, and hormonal pathways are at the very least present across divergent land plant lineages, which is a prerequisite for the potential convergence of effectors onto these hubs/processes.…”

“…Previous studies have reasoned that the diverse array of integrated domains in otherwise structurally similar R proteins (also called NLRs: nucleotide-binding domain, leucine rich repeats) likely represent former stand-alone targets of phytopathogen effectors [51 • ,52]. Intriguingly, candidate integrated domain-containing R proteins are present in early divergent land plants [29 •• ,51 • ], which suggests that this strategy is broadly employed across the green plant lineage, although only a few early divergent plant genomes have been sequenced thus far. This brings forth interesting questions as to how and when effector targets were integrated into R proteins (Figure 1).…”