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During plant-pathogen interactions, plants use intracellular proteins with nucleotide-binding site and Leu-rich repeat (NBS-LRR) domains to detect pathogens. NBS-LRR proteins represent a major class of plant disease resistance genes ( R -genes). Whereas R -genes have been well characterized in angiosperms, little is known about their origin and early diversification. Here, we perform comprehensive evolutionary analyses of R -genes in plants and report the identification of R -genes in basal-branching streptophytes, including charophytes, liverworts, and mosses. Phylogenetic analyses suggest that plant R -genes originated in charophytes and R-proteins diversified into TIR-NBS-LRR proteins and non-TIR-NBS-LRR proteins in charophytes. Moreover, we show that plant R-proteins evolved in a modular fashion through frequent gain or loss of protein domains. Most of the R -genes in basal-branching streptophytes underwent adaptive evolution, indicating an ancient involvement of R -genes in plant-pathogen interactions. Our findings provide novel insights into the origin and evolution of R -genes and the mechanisms underlying colonization of terrestrial environments by plants.

Out of Water: The Origin and Early Diversification of Plant R-Genes