The diversity and host range of endogenous caulimovirids illuminate the ancient origin and early evolution of the Caulimoviridae

Endogenous viral elements (EVEs) result from the integration of viral sequences into the genome of their hosts. EVEs can be considered molecular fossils of ancient or unknown viruses. Through paleovirological approaches, EVEs can help unravel the evolutionary trajectories of related viruses across extended temporal scales. In plants, most characterized EVEs belong to the family Caulimoviridae , the only family of retrotranscribed plant viruses, and are termed endogenous caulimovirids (ECVs). Previous studies of ECVs have proposed either cospeciation or host-switching as the primary mode of Caulimoviridae transmission through plant divisions, both scenarios assuming an emergence predating the euphyllophytes. However, robust assessments of ECV diversity and hosts were hindered by the underrepresentation of basal plant genome assemblies.

Taking advantage of newly available genomic resources, we analyzed a dataset of 93 plant genome sequences representing all subdivisions of embryophytes, including basal groups such as ferns and lycophytes. We identified 47,135 ECVs in 75 genomes from lycophytes, ferns, gymnosperms, and angiosperms. Based on their diversity, these ECVs were classified into 71 operational taxonomic units (OTUs), 35 of which were previously undescribed. Our work revealed an unexpected diversity of Caulimoviridae in tracheophytes and identified a new clade restricted to gymnosperms. By comparing the phylogenetic relationships of Caulimoviridae with host plant taxonomy, we propose a new macroevolutionary scenario in which cospeciation with the tracheophytes is the main driver of Caulimoviridae diversification.