Widespread and frequent horizontal transfers of transposable elements in plants

Abstract

Vertical, transgenerational transmission of genetic material occurs through reproduction of living organisms. In addition to vertical inheritance, horizontal gene transfer between reproductively isolated species has recently been shown to be an important, if not dominant, mechanism in the evolution of prokaryotic genomes. In contrast, only a few horizontal transfer (HT) events have been characterized so far in eukaryotes and mainly concern transposable elements (TEs). Whether these are frequent and have a significant impact on genome evolution remains largely unknown. We performed a computational search for highly conserved LTR retrotransposons among 40 sequenced eukaryotic genomes representing the major plant families. We found that 26 genomes (65%) harbor at least one case of horizontal TE transfer (HTT). These transfers concern species as distantly related as palm and grapevine, tomato and bean, or poplar and peach. In total, we identified 32 cases of HTTs, which could translate into more than 2 million among the 13,551 monocot and dicot genera. Moreover, we show that these TEs have remained functional after their transfer, occasionally causing a transpositional burst. This suggests that plants can frequently exchange genetic material through horizontal transfers and that this mechanism may be important in TE-driven genome evolution.

Massive horizontal transfer of transposable elements in insects

“…This unprecedented figure is more than four times higher than the total number of HTT events reported so far in metazoans, plants, and fungi combined (10). Such a high number is still not unexpected, given that studies focusing on one or a few TEs often found one or more HTT events between multiple, distantly related taxa (11,(14)(15)(16)22).…”

“…HT of TEs (HTT) may allow these elements to enter naive genomes, which they invade by making copies of themselves, and then escape before they become fully silenced by anti-TE defenses (13). A growing number of studies have identified such HTT (11,(14)(15)(16). However, a common drawback of these studies has been the inclusion of a limited set of TEs (11) or organisms (16), which hampers our understanding of the breadth of HTT, its contribution to genome evolution, and of the factors and barriers shaping these transfers in eukaryotes (13).…”

“…In fact, most of the genetic material that is horizontally transferred in animals and plants consists of transposable elements (TEs) (9)(10)(11), which are pieces of DNA able to move from a chromosomal locus to another (12). The greater ability of TEs to move between organisms certainly relates to their intrinsic ability to transpose within genomes, which genes cannot do.…”

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.…”

Multiple horizontal transfers of nuclear ribosomal genes between phylogenetically distinct grass lineages

“…Most of the established horizontal transfer events involving a plant genome result from interactions between a plant and a pathogen or parasite (7)(8)(9)(10)(11). Plant to plant transfers outside of the fertilization process are thought to be rare (12)(13)(14)(15)(16)(17), presumably because they require a vector to move the DNA from one plant to the other.…”