Horizontal gene transfer is more frequent with increased heterotrophy and contributes to parasite adaptation

Abstract

Horizontal gene transfer (HGT) is the transfer of genetic material across species boundaries and has been a driving force in prokaryotic evolution. HGT involving eukaryotes appears to be much less frequent, and the functional implications of HGT in eukaryotes are poorly understood. We test the hypothesis that parasitic plants, because of their intimate feeding contacts with host plant tissues, are especially prone to horizontal gene acquisition. We sought evidence of HGTs in transcriptomes of three parasitic members of Orobanchaceae, a plant family containing species spanning the full spectrum of parasitic capabilities, plus the free-living Lindenbergia. Following initial phylogenetic detection and an extensive validation procedure, 52 highconfidence horizontal transfer events were detected, often from lineages of known host plants and with an increasing number of HGT events in species with the greatest parasitic dependence. Analyses of intron sequences in putative donor and recipient lineages provide evidence for integration of genomic fragments far more often than retro-processed RNA sequences. Purifying selection predominates in functionally transferred sequences, with a small fraction of adaptively evolving sites. HGT-acquired genes are preferentially expressed in the haustorium-the organ of parasitic plants-and are strongly biased in predicted gene functions, suggesting that expression products of horizontally acquired genes are contributing to the unique adaptive feeding structure of parasitic plants.

On the evolutionary significance of horizontal gene transfers in plants

“…Much of the modern research regarding HGT in plants has focused on several lineages of parasitic plants, including Cuscuta (Vogel et al, 2018), Orobanchaceae (Yang et al, 2016;Kado & Innan, 2018), Striga (Yoshida et al, 2010), Rafflesia (Xi et al, 2012) and Santalales (Davis et al, 2005). The prevalence of HGT in heterotrophic plants is perhaps unsurprising given their close physical association with their hosts.…”

“…Several studies have found evidence of the movement of mRNA transcripts from host plants in Orobanchaceae (David-Schwartz et al, 2008), implying that such mobile mRNA could act as an intermediate for the horizontal transfer of genes (Yoshida et al, 2010). However, subsequent research in Orobanchaceae and Cuscuta, in particular, has shown that the vast majority of transfers seem to be derived from genomic fragments of DNA rather than an mRNA intermediate (Yang et al, 2016;Kado & Innan, 2018).…”

“…There are several lines of evidence suggesting that the parasites may have repurposed the host-derived genes for a heterotrophic lifestyle. Studies in Orobanchaceae, Cuscuta and Rafflesia have found that many horizontally transferred genes are being expressed (Xi et al, 2012;Yang et al, 2016;Vogel et al, 2018;Yang et al, 2019), and in many cases preferentially in haustorial tissues. Furthermore, of the identified HGT cases in Cuscuta and Orobanchaceae, 18 of them came from the same gene families .…”

RNA-seq highlights parallel and contrasting patterns in the evolution of the nuclear genome of holo-mycoheterotrophic plants

“…On an evolutionary scale, a large number of horizontal gene transfer (HGT) events from hosts to parasites have been found in the organellar and nuclear genomes of parasitic plants (Bellot et al, 2016;. A recent large-scale survey of HGT in Orobanchaceae showed that the number of these events correlates positively with the degree of heterotrophy (Yang et al, 2016). The second aspect is the evolution of organellar (mainly plastid) genomes.…”

Mitochondrial genome of non-photosynthetic mycoheterotrophic plant Hypopitys monotropa,its structure, gene expression and RNA editing

“…HGT is a phenomenon very common in parasitic plants (Yang et al, 2016). HGT from host plants into the mitochondrial genome was shown for Rafflesiaceae (Xi et al, 2013), Orobanchaceae (Yang et al, 2016), Cynomorium (Cynomoriaceae) (Bellot et al, 2016), Lophophytum mirabile (Balanophoraceae). In the latter case horizontally transferred homologs replaced almost all native mitochondrial genes (Sanchez-Puerta et al, 2017).…”