Evolutionary force of AT‐rich repeats to trap genomic and episomal DNAs into the rice genome: lessons from endogenous pararetrovirus

Abstract

SUMMARYIn plant genomes, the incorporation of DNA segments is not a common method of artificial gene transfer. Nevertheless, various segments of pararetroviruses have been found in plant genomes in recent decades. The rice genome contains a number of segments of endogenous rice tungro bacilliform virus-like sequences (ERTBVs), many of which are present between AT dinucleotide repeats (ATrs). Comparison of genomic sequences between two closely related rice subspecies, japonica and indica, allowed us to verify the preferential insertion of ERTBVs into ATrs. In addition to ERTBVs, the comparative analyses showed that ATrs occasionally incorporate repeat sequences including transposable elements, and a wide range of other sequences. Besides the known genomic sequences, the insertion sequences also represented DNAs of unclear origins together with ERTBVs, suggesting that ATrs have integrated episomal DNAs that would have been suspended in the nucleus. Such insertion DNAs might be trapped by ATrs in the genome in a host-dependent manner. Conversely, other simple mono-and dinucleotide sequence repeats (SSR) were less frequently involved in insertion events relative to ATrs. Therefore, ATrs could be regarded as hot spots of double-strand breaks that induce non-homologous end joining. The insertions within ATrs occasionally generated new generelated sequences or involved structural modifications of existing genes. Likewise, in a comparison between Arabidopsis thaliana and Arabidopsis lyrata, the insertions preferred ATrs to other SSRs. Therefore ATrs in plant genomes could be considered as genomic dumping sites that have trapped various DNA molecules and may have exerted a powerful evolutionary force.

Rice genomes recorded ancient pararetrovirus activities: Virus genealogy and multiple origins of endogenization during rice speciation

“…Each of the japonica, indica, and O. rufipogon genomes harbored about 100 copies of the eRTBVL-A, -B, -C, and -D families (this study, and Liu et al, 2012), but in different proportions. We examined the endogenization patterns of the eRTBVLs in each of the three genomes by comparing their relative abundances in the eRTBVL-A, -B, and -C families (Fig.…”

“…The disease is caused primarily by infection with rice tungro bacilliform virus (Caulimoviridae, Tungrovirus; RTBV), the known extant rice pararetrovirus (Hay et al, 1991;Qu et al, 1991). EPRV sequences, which share similarity with RTBV sequences, have been found in the genomes of cultivated rice, and these EPRV sequences have been referred to as endogenous RTBV-like (eRTBVL) sequences (Kunii et al, 2004;Liu et al, 2012). Intact virus genome sequences were assembled successfully from eRTBVL fragments collected from the Nipponbare genome database (Kunii et al, 2004).…”

“…However, with the increasing decryption of plant genomes, a growing number of endogenous pararetrovirus (EPRV) sequences have been discovered as ancient integrated analogs of most members of the Caulimoviridae family (Hohn et al, 2008;Staginnus et al, 2009;Staginnus and Richert-Pöggeler, 2006). This incidental integration of pararetroviruses was thought to involve illegitimate recombination or double-strand break repair via non-homologous end joining between the pararetrovirus and host genomes (Bill and Summers, 2004;Liu et al, 2012;Staginnus and Richert-Pöggeler, 2006). When such integrations occurred in host germline cells, the pararetroviral sequences could be inherited as part of the genetic makeup of the host species across generations in a Mendelian fashion; this process is called endogenization (Feschotte and Gilbert, 2012).…”

Bringing New Plant Varieties to Market: Plant Breeding and Selection Practices Advance Beneficial Characteristics while Minimizing Unintended Changes

“…Horizontal gene transfer across phylogenetic boundaries is another natural process that results in genetic variation in plants (Bock, 2010;Soucy et al, 2015), including transfer of DNA from bacteria, viruses, and unrelated plants (Bergthorsson et al, 2003;Staginnus et al, 2007;Liu et al, 2012;El Baidouri et al, 2014;Geering et al, 2014;Kyndt et al, 2015). One recent example was a study demonstrating that a wide selection of sweet potato [Ipomoea batatas (L.) Lam.…”

A novel grapevine badnavirus is associated with the Roditis leaf discoloration disease

“…Nevertheless, a number of studies have revealed integrated sequences from members of most of the family Caulimoviridae genera, including badnaviruses, in plant genomes (Geering et al, 2001;Laney et al, 2012;Ndowora et al, 1999;Seal et al, 2014). These are known as endogenous pararetroviruses (EPRVs) (Geering et al, 2010) and probably arose from recombination between the viral and the host genome during repair of plant DNA breaks (Liu et al, 2012). The presence of an EPRV does not generally translate into an active (episomal) infection since such sequences are generally incomplete or rearranged and merely represent genetic fossils.…”