Widespread and frequent horizontal transfers of transposable elements in plants

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.Transposable elements (TEs) are mobile genomic DNA sequences that are found in almost all living organisms (Finnegan 1985). They so densely populate the genomes of many eukaryotic species that they are often the major components, as in human (>50%) (Prak and Kazazian 2000) or bread wheat (>95%) (Bennetzen 2000). In this regard, TEs have been shown to have a major impact on both structural and functional modifications of genomes (Bennetzen 2000; Feschotte 2008). They are usually classified into two distinct types. Class I elements (retrotransposons) transpose via an RNA intermediate through a copy and paste mechanism, whereas class II elements (transposons) transpose through a cut-and-paste mechanism (Wicker et al. 2007). Both classes comprise various types (orders and superfamilies in Wicker''s classification). Although most of these types can be found in all the plant genomes sequenced so far, LTR retrotransposons represent by far the major genomic constituents in the kingdom. In this regard, LTR retrotransposons have been shown to strongly impact genome structure (Piegu et al. 2006), whereas several reports have demonstrated their putative functional impact as epigenetic mediators (Kobayashi et al. 2004).TEs achieve their transposition cycle within their host and are thus considered to be lineage specific because, like genes, they are inherited vertically from one generation to another. However, unlike genes, they do not encode any information essential for their host, and their insertion into genes can in some cases have a negative effect on fitness. This “selfish” and potentially deleterious nature has raised the question of their persistence in eukaryotic lineages, especially after it was shown that TEs are strictly controlled by several silencing pathways (Slotkin and Martienssen 2007; Rigal and Mathieu 2011) and efficiently eliminated from their host genomes through deletions (Vitte and Panaud 2005). Horizontal transfers could allow TEs to escape this process by transposing into a new “naive” host genome, therefore ensuring their long-term survival. However, although horizontal gene transfers are very common in Bacteria (Rocha 2013), evidence of HTTs in eukaryotes remains scarce, although recent reports suggest their potential impact in genome evolution (Schaack et al. 2010). Three criteria have been defined for the detection of HTTs: patchy distributions of TEs in phylogenies; identification of TEs exhibiting high sequence similarity between distantly related taxa; and phylogenetic incongruence between the host and TEs (Gilbert et al. 2010; Kuraku et al. 2012; Wallau et al. 2012; Walsh et al. 2013). An exhaustive search for HTTs that meet these three criteria in a wide taxonomic range thus requires a comprehensive set of genomic resources. Next-generation sequencing (NGS) has made available full genome sequences for many organisms, enabling genome-wide comparative surveys for a large panel of evolutionary lineages. Using such resources, we surveyed HTTs across the plant kingdom, and we show that they are very frequent and widespread among monocots and dicots.