The Origin And Evolution Of Pseudo-retroviruses

Pararetroviruses are double-stranded DNA viruses,whose replication requires reverse transcription,including plant pararetroviruses(Caulimoviridae)and animal pararetroviruses(Hepadnaviridae).Pararetroviruses can occasionally integrate into host genomes,forming endogenous viral elements.Endogenous viral elements document past viral infections,providing “molecular fossils” for studying the deep history and macroevolution of viruses.Here we use a large-scale phylogenomic approach to systematically mine endogenous pararetroviruses(EPRVs)within eukaryotic genomes.Plant pararetroviruses were thought to exclusively infect angiosperms.Here we systematically mine EPRVs within the genomes of 20 plants outside angiosperms and report the identification of EPRVs in the genomes of gymnosperms and ferns,suggesting Caulimoviridae widely infects euphyllophytes.We find that the copy numbers of EPRVs are generally high,implying that EPRVs represent important components of the euphyllophyte genomes.Phylogenetic analyses show that the known angiosperm viruses constitute only a minor part of the Caulimoviridae diversity and independently originated through multiple cross-species transmissions.Orthologous integration events and proliferation dynamics of EPRVs within the host genomes suggest the EPRV integration events occurred at least 100 million years ago.The incongrence between Caulimoviridae and host phylogenies reveals frequent cross-species transmissions of Caulimoviridae.Animal pararetroviruses infect a varity of vertebrates.Both hepadnaviruses and retrotransposons encode reverse transcriptase and RNase H,but all the known retrotransposons are only distantly related to hepadnaviruses.The origin of hepadnaviruses remains mysterious.Here we report the discovery of two novel lineages of retroelements,which we designate hepadnavirus-like retroelement(HEART1 and HEART2),within the 4 insect genomes through screening 1,095 eukaryotic genomes.Conserved domain analyses and paralogous/orthologous empty sites of HEART insertions suggest transposable nature of HEART elements.Phylogenetic analyses show that the HEART retroelements represent the closest relatives of hepadnaviruses.The discovery of HEART elements narrows down the evolutionary gap between hepadnaviruses and retrotransposons,and further supports the escaped retrotransposon hypothesis of hepadnavirus origin.This study has important implications in our understandings of the diversity and macroevolution of plant and animal pararetroviruses and provides novel insights into the origin and evolution of pararetroviruses.