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Endogenous viral elements (paleoviruses) provide “molecular fossils” for studying the deep history and macroevolution of viruses. Endogenous plant pararetroviruses (EPRVs) are widespread in 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 within the genomes of gymnosperms and ferns. The known angiosperm viruses constitute only a minor part of theCaulimoviridae diversity. By characterizing the distribution of EPRVs, we show that no major euphyllophyte lineages escape the activity ofCaulimoviridae , raising the possibility that many exogenousCaulimoviridae remain to be discovered in euphyllophytes. We find that the copy numbers of EPRVs are generally high, suggesting that EPRVs might define a unique group of repetitive elements and represent important components of euphyllophyte genomes. Evolutionary analyses suggest an ancient origin ofCaulimoviridae and at least three independent origins ofCaulimoviridae in angiosperms. Our findings reveal the remarkable diversity ofCaulimoviridae and have important implications for understanding the origin and macroevolution of plant pararetroviruses.IMPORTANCE Few viruses have been documented in plants outside angiosperms. Viruses can occasionally integrate into host genomes, forming endogenous viral elements (EVEs). Endogenous plant pararetroviruses (EPRVs) are widespread in angiosperms. In this study, we performed comprehensive comparative and phylogenetic analyses of EPRVs and found that EPRVs are present in the genomes of gymnosperms and ferns. We identified numerous EPRVs in gymnosperm and fern genomes, revealing an unprecedented depth in the diversity of plant pararetroviruses. Plant pararetroviruses mainly underwent cross-species transmission, and angiosperm pararetroviruses arose at least three times. Our study provides novel insights into the diversity and macroevolution of plant pararetroviruses.

Euphyllophyte Paleoviruses Illuminate Hidden Diversity and Macroevolutionary Mode of Caulimoviridae