Hidden diversity and macroevolutionary mode ofCaulimoviridaeuncovered by euphyllophyte paleoviruses

AbstractFew viruses have been documented in plants outside angiosperms. Endogenous viral elements (paleoviruses) provide ‘molecular fossils’ for studying the deep history and macroevolution of viruses. Endogenous plant pararetroviruses (EPRVs) are widespread across angiosperms, but little is known about EPRVs in earlier branching plants. Here we use a large-scale phylogenomic approach to investigate the diversity and macroevolution of plant pararetroviruses (formally known asCaulimoviridae). We uncover an unprecedented and unappreciated diversity of EPRVs in the genomes of gymnosperms and ferns. The known angiosperm viruses only constitute a minor part of theCaulimoviridaediversity. By characterizing the distribution of EPRVs, we show that no major euphyllophyte lineages escape the activity ofCaulimoviridae, raising the possibility that many exogenousCaulimoviridaeremain to be discovered in euphyllophytes. We find that the copy numbers of EPRVs are generally high, suggesting that EPRVs define a unique group of repetitive elements and represent major components of euphyllophyte genomes. Phylogenetic analyses reveal an ancient monilophyte origin ofCaulimoviridaeand at least three independent origins ofCaulimoviridaein angiosperms by cross-division transmissions. Our findings uncover the remarkable diversity ofCaulimoviridaeand have important implications in understanding the origin and macroevolution of plant pararetroviruses.