Abstract
Integration into the nuclear genome of germ line cells can lead to vertical inheritance of retroviral genes as host alleles. For other viruses, germ line integration has only rarely been documented. Nonetheless, we identified endogenous viral elements (EVEs) derived from ten non-retroviral families by systematic in silico screening of animal genomes, including the first endogenous representatives of double-stranded RNA, reverse-transcribing DNA, and segmented RNA viruses, and the first endogenous DNA viruses in mammalian genomes. Phylogenetic and genomic analysis of EVEs across multiple host species revealed novel information about the origin and evolution of diverse virus groups. Furthermore, several of the elements identified here encode intact open reading frames or are expressed as mRNA. For one element in the primate lineage, we provide statistically robust evidence for exaptation. Our findings establish that genetic material derived from all known viral genome types and replication strategies can enter the animal germ line, greatly broadening the scope of paleovirological studies and indicating a more significant evolutionary role for gene flow from virus to animal genomes than has previously been recognized.
Highlights
Viral infection of germ line cells can lead to viral genes or genomes becoming integrated into chromosomes and inherited as host alleles [1,2]
For endogenous viral elements (EVEs) that were found to encode uninterrupted open reading frames (ORFs), putative protein sequences were used with the tBLASTn program to search expressed sequence tag (EST) databases for the corresponding mRNA
In addition to numerous EVEs derived from bornavirus NP genes (some of which have previously been reported as endogenous Borna-like N (EBLN) elements [11]), we identified EVEs derived from bornavirus Lpolymerase, matrix (M) and glycoprotein (GP) genes (Figure 2a)
Summary
Viral infection of germ line cells (i.e. gametes, or cells of the early embryo) can lead to viral genes or genomes becoming integrated into chromosomes and inherited as host alleles [1,2]. These insertions, which we refer to here as endogenous viral elements (EVEs), are usually eliminated from the host gene pool within a small number of generations. Retroviruses are the only animal viruses that integrate into the genome of the host cell as an obligate step in their replication strategy, and are predisposed to enter the host germ line (Figure 1). Genomic integration of non-retroviral viruses may be mediated by non-homologous recombination with chromosomal DNA [16,17,18] or by interactions with retroelements in the host cell [11,19,20,21,22] (Figure 1)
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