Two hAT transposon genes were transferred from Brassicaceae to broomrapes and are actively expressed in some recipients

Abstract

A growing body of evidence is pointing to an important role of horizontal gene transfer (HGT) in the evolution of higher plants. However, reports of HGTs of transposable elements (TEs) in plants are still scarce, and only one case is known of a class II transposon horizontally transferred between grasses. To investigate possible TE transfers in dicots, we performed transcriptome screening in the obligate root parasite Phelipanche aegyptiaca (Orobanchaceae), data-mining in the draft genome assemblies of four other Orobanchaceae, gene cloning, gene annotation in species with genomic information, and a molecular phylogenetic analysis. We discovered that the broomrape genera Phelipanche and Orobanche acquired two related nuclear genes (christened BO transposase genes), a new group of the hAT superfamily of class II transposons, from Asian Sisymbrieae or a closely related tribe of Brassicaceae, by HGT. The collinearity of the flanking genes, lack of a classic border structure, and low expression levels suggest that BO transposase genes cannot transpose in Brassicaceae, whereas they are highly expressed in P. aegyptiaca.

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

“…Four TE-related sequences encode ORFs with abundant transcripts in haustorial tissues (orthogroup 1021, 5002, 14230, and 15149), suggesting a potentially active role in the parasites, a scenario similar to the recently identified Brassicaceaederived hobo-Ac-Tam3 transposon (hAT) in P. aegyptiaca (29). We also provided multiple lines of evidence for cross-validation of HGT sequences.…”

“…In addition, it includes two of the published high-confidence HGT cases (26,28). Two other published HGTs in Orobanchaceae (27,29) were detected in the stage 4-specific assembly (28) Table S9). (D) Number of HGT orthogroups supports transfers from shared and unique parasitic genera.…”

“…A second apparent concentration of horizontally acquired sequences in plant genomes is associated with parasitic plants, where both mitochondrial (14,(17)(18)(19)(20)(21)(22)(23) and nuclear horizontal transfers (24)(25)(26)(27)(28)(29) have been identified. Repeated horizontal acquisitions of mitochondrial atpI by parasitic flowering plants occurred in four extreme parasite lineages where the parasite lives inside the host for much of its lifespan (14).…”

“…Four cases of nuclear gene HGT have been identified in this family to date (26)(27)(28)(29), but this is likely to be a small fraction of the number of events. This is due to the challenges in HGT discovery and to the lack of a well-established approach for use with complex plant genomes.…”

Sequential horizontal gene transfers from different hosts in a widespread Eurasian parasitic plant, Cynomorium coccineum

“…Mahelka et al., ). Examples of nuclear transfers include actively transcribed protein‐coding genes acquired by the parasite Rafflesia cantleyi from its obligate host Tetrastigma rafflesiae (Xi et al., ), albumin genes acquired from Fabaceae and a hAT transposon from Brassicaceae acquired by of the common ancestor of parasitic Orobanche and Phelipanche (Zhang et al., ; Sun et al., ), strictosidine synthase‐like genes from Brassicaceae acquired by Phelipanche and Cuscuta (Zhang et al., ), and a nuclear gene of unknown function acquired by the Orobanchaceae Striga hermonthica from a monocot (Yoshida et al., ).…”