Broken, silent, and in hiding: tamed endogenous pararetroviruses escape elimination from the genome of sugar beet (Beta vulgaris)

Endogenous pararetroviruses (EPRVs) are widespread components of plant genomes that originated from episomal DNA viruses of the Caulimoviridae family. Due to fragmentation and rearrangements, most EPRVs have lost their ability to replicate through reverse transcription and to initiate viral infection. Similar to the closely related retrotransposons, extant EPRVs were retained and often amplified in plant genomes for several million years. Here, we characterize the complete genomic EPRV fraction of the crop sugar beet (Beta vulgaris, Amaranthaceae) to understand how they shaped the beet genome and to suggest explanations for their absent virulence.

Endogenous pararetroviruses (EPRVs) are widespread components of plant genomes that originated from episomal DNA viruses of the Caulimoviridae family. Due to fragmentation and rearrangements, most EPRVs have lost their ability to replicate through reverse transcription and to initiate viral infection. Similar to the closely related retrotransposons, extant EPRVs were retained and often amplified in plant genomes for several million years. Here, we characterize the complete genomic EPRV fraction of the crop sugar beet (Beta vulgaris, Amaranthaceae) to understand how they shaped the beet genome and to suggest explanations for their absent virulence.

Our study in beet illustrates the variability of EPRV structure and sequence in a single host genome. Evidence of sequence fragmentation and epigenetic silencing implies possible plant strategies to cope with long-term persistence of EPRVs, including amplification, fixation in the heterochromatin, and containment of EPRV virulence.

Using next- and third-generation sequencing data and genome assembly, we reconstructed full-length in silico representatives for the three host-specific EPRVs (beetEPRVs) in the B. vulgaris genome. Focusing on the endogenous caulimovirid beetEPRV3, we investigated its chromosomal localization, abundance and distribution by fluorescent in situ and Southern hybridization. Key

Full-length beetEPRVs range between 7.5 and 10.7 kb in size, are heterogeneous in structure and sequence, and occupy about 0.3 % of the beet genome. Although all three beetEPRVs were assigned to the florendoviruses, they showed variably arranged protein-coding domains, different fragmentation, and preferences for diverse sequence contexts. We observed small RNAs that specifically target the individual beetEPRVs, indicating stringent epigenetic suppression. BeetEPRV3 sequences occur along all sugar beet chromosomes, preferentially in the vicinity of each other and are associated with heterochromatic, centromeric and intercalary satellite DNAs. BeetEPRV3 members also exist in genomes of related wild species, indicating an initial beetEPRV3 integration 13.4-7.2 million years ago. Conclusions: Our study in beet illustrates the variability of EPRV structure and sequence in a single host genome. Evidence of sequence fragmentation and epigenetic silencing implies possible plant strategies to cope with long-term persistence of EPRVs, including amplification, fixation in the heterochromatin, and containment of EPRV virulence.