New pathways in plants and microbes

Plants and microbes have interacted through evolution in ways that shaped diversity and helped plants colonize land. Delaux and Schornack review how insights from a range of plant and algal genomes reveal sustained use through evolution of ancient gene modules as well as emergence of lineage-specific specializations. Mosses, liverworts, and hornworts have layered innovation onto existing pathways to build new microbial interactions. Such innovations may be transferrable to crop plants with an eye toward building a more sustainable agriculture.

Science, this issue p. eaba6605

Microbial interactions have shaped plant diversity in terrestrial ecosystems. By forming mutually beneficial symbioses, microbes helped plants colonize land more than 450 million years ago. In parallel, omnipresent pathogens led to the emergence of innovative defense strategies. The evolution of plant-microbe interactions encompasses ancient conserved gene modules, recurrent concepts, and the fast-paced emergence of lineage-specific innovations. Microbes form communities on the surface or inside plant tissues and organs, and most intimately, microbes live within single plant cells. Intracellular colonization is established and controlled in part by plant genes that underpin general cell processes and defense mechanisms. To benefit from microbes, plants also evolved genetic modules for symbiosis support. These modules have been maintained despite the risk of getting hijacked by pathogens.

The hundreds of land plant and algal genomes that are now available enable genome-wide comparisons of gene families associated with plant immunity and symbiosis. Reconstruction of gene phylogenies and large-scale comparative phylogenomic approaches have revealed an ancient subset of genes coevolving with the widespread arbuscular mycorrhiza symbiosis, the most ancient plant intracellular symbiosis, and with other types of more recently evolved intracellular symbioses in vascular and nonvascular plants. Intercellular symbiotic interactions formed with cyanobacteria or ectomycorrhizal fungi seem to repeatedly evolve through convergent, but not necessarily genetically conserved, mechanisms. Phylogenetic analyses revealed occurrence of candidate disease-resistance genes in green algae, as well as orthologs of flowering plant genes involved in symbiosis signaling and sensing microbial patterns. Yet, more research is needed to understand their functional conservation.

The extent to which conserved symbiosis genes also fulfill often opposing roles during pathogen-plant interactions is being explored through studies of pathogen infections in plants capable of supporting symbiotic relationships. The development of plant-microbe systems in genetically tractable species covering the diversity of land plant lineagesincluding angiosperms and bryophytes, such as the liverwort Marchantia polymorphamakes it possible to test hypotheses that emerge from phylogenetic analyses, linking genetic and functional conservation across land plants. Studies in bryophytes illustrate the range of possibilities for pathogen management: ancient genes, such as membrane receptors that perceive fungus-derived chitin; pathways with bryophyte cladespecific components, such as phenylpropanoid-derived auronidin stress metabolites; and jasmonate-like hormonal signaling for immunity.

Only a few plant-microbe interactions have been studied in depth, and those in only a few land plant lineages. Future investigations of interactions occurring across the diversity of plants may unravel new types of symbiotic or pathogenic interactions. The occurrence of microbe-sensing genes in streptophyte algae, harboring the closest algal relative to land plants, suggest the existence of overlooked and potentially ancient symbiotic associations. Genetically tractable plant-microbe model systems in diverse streptophyte algae, hornworts, liverworts, ferns, and the so far unsampled diversity of seed plants will enable dissection of the spectrum of molecular mechanisms that regulate the breadth of interactions occurring in plants. The actual function of the symbiotic genes present in bryophyte genomes also remains to be determined. Furthermore, our understanding of plant-microbe interactions will be enriched by more often combining evolutionary concepts with mechanistic studies. More efforts are needed to decipher the molecular changes that have enabled the emergence of new interactions, signaling pathways, and enzymatic specificities to support symbiosis and to protect against pathogens. Microbes manipulate plant processes, and complementary microbial studies are key to gaining a complete picture of plant-microbe evolution. Knowing the rules of engagement between distantly related plants and their microbes then helps genetic transplantation approaches into crops and the orthogonal engineering of bioprocesses aimed at achieving quantitative resistance against pathogens, improving phosphate uptake, or establishing nitrogen-fixing associations for efficient use in sustainable agriculture.

Some pathogens such as oomycetes are able to infect a wide range of extant plant lineages, including bryophytes (left), and plant pathogen interactions often evolve at a fast pace. By contrast, some symbiotic interactions that look exactly as they do today can be found in the most ancient land plant fossils, here depicted as an illustration of the Rhynie chert fossil plant Aglaophyton major (right). Still, both types of plant-microbe interactions feature evolutionarily ancient as well as rapidly evolving aspects. Extending plant-microbe studies across diverse groups of plant lineages has enriched our understanding of these processes and their evolution.

During 450 million years of diversification on land, plants and microbes have evolved together. This is reflected in todays continuum of associations, ranging from parasitism to mutualism. Through phylogenetics, cell biology, and reverse genetics extending beyond flowering plants into bryophytes, scientists have started to unravel the genetic basis and evolutionary trajectories of plant-microbe associations. Protection against pathogens and support of beneficial, symbiotic, microorganisms are sustained by a blend of conserved and clade-specific plant mechanisms evolving at different speeds. We propose that symbiosis consistently emerges from the co-option of protection mechanisms and general cell biology principles. Exploring and harnessing the diversity of molecular mechanisms used in nonflowering plant-microbe interactions may extend the possibilities for engineering symbiosis-competent and pathogen-resilient crops.

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Plant evolution driven by interactions with symbiotic and pathogenic microbes - Science Magazine