Horizontal acquisition of transposable elements and viral sequences: patterns and consequences

Abstract

It is becoming clear that most eukaryotic transposable elements (TEs) owe their evolutionary success in part to horizontal transfer events, which enable them to invade new species. Recent large-scale studies are beginning to unravel the mechanisms and ecological factors underlying this mode of transmission. Viruses are increasingly recognized as vectors in the process but also as a direct source of genetic material horizontally acquired by eukaryotic organisms. Because TEs and endogenous viruses are major catalysts of variation and innovation in genomes, we argue that horizontal inheritance has had a more profound impact in eukaryotic evolution than is commonly appreciated. To support this proposal, we compile a list of examples, including some previously unrecognized, whereby new host functions and phenotypes can be directly attributed to horizontally acquired TE or viral sequences. We predict that the number of examples will rapidly grow in the future as the prevalence of horizontal transfer in the life cycle of TEs becomes even more apparent, firmly establishing this form of non-Mendelian inheritance as a consequential facet of eukaryotic evolution.

Figure 1.. Numbers of horizontal transfers of transposable elements and vertebrate endogenous retroviruses

The barplots show the numbers of HTT events per TE superfamily (A) and per TE class (B) as taken from HTT-db in October 2017 (Dotto et al. 2015). The barplot in C) shows the number of clusters of related ERV sequences for each ERV family unearthed from 65 vertebrate genomes by Hayward et al. (2015). The presence of >3000 ERV lineages in vertebrates, each inferred to descend from a discrete endogenisation event [96], suggests that this form of HTT has been pervasive during vertebrate evolution.

Figure 2.. Phenotypic consequences of the horizontal introduction of transposable elements in plants.

TEs are depicted as black boxes, host genes as white boxes. A. The LTR retrotransposon Tcs2 provided an alternative start site in Jingxian blood orange, inducing cold-dependent overexpression of the Ruby gene, which encodes a MYB transcription factor controlling anthocyanin biosynthesis. This results in the production of orange fruits with more deeply pigmented flesh [72,88]. We found that Tcs2 has been horizontally transferred, either directly or indirectly via intermediate species between orange and asparagus (Table 1). The recent introduction of the Tcs2 element in the orange genome is supported by the fact that it is currently actively transposing [72,88]. B. The LTR retrotransposon Rider triggered the apparition of at least two traits in tomato (yellow flesh and elongated shape) that have been selected by breeders. One copy of Rider is responsible for a duplication of the SUN locus, which leads to increased SUN expression and results in the production of elongated fruits characteristic of the ‘Roma’ variety of tomato [71]. Another copy of Rider disrupts the phytoene synthase (PSY1) gene. The resulting lack of carotenoid leads to the production of yellow tomato flesh [70]. We found that Rider has been horizontally transferred, either directly or indirectly via intermediate species between tomato and spinach (Table 1). The recent introduction of the Rider element in the tomato genome is supported by its absence from the potato (Solanum tuberosum) genome, which diverged only 8 Mya from tomato [85]. Importantly, Cheng et al. (2009) also reported that Rider was horizontally transferred between tomato and the Arabidopsis lineage [85].