Horizontal Gene Transfer in Five Parasite Plant Species in Orobanchaceae.

Tomoyuki Kado,Hideki Innan,Tal Dagan

doi:10.1093/gbe/evy219

Abstract

We sequenced genomes of five parasite species in family Orobanchaceae to explore the evolutionary role of horizontal gene transfer in plants. Orobanche minor and Aeginetia indica are obligate parasites with no photosynthetic activity, whereas the other three (Pedicularis keiskei, Phtheirospermum japonicum, and Melampyrum roseum) are facultative parasites. By using reference genome sequences and/or transcriptomes of 14 species from Fabaceae and Poaceae, their major host families, we detected 106 horizontally transferred genes (HGT genes), only in the genomes of the two obligate parasites (22 and 84 for Oro. minor and Ae. indica, respectively), whereas none in the three facultative parasites. The HGT genes, respectively, account for roughly 0.1% and 0.2% of the coding genes in the two species. We found that almost all HGT genes retained introns at the same locations as their homologs in potential host species, indicating a crucial role of DNA-mediated gene transfer, rather than mRNA mediated retro transfer. Furthermore, some of the HGT genes might have transferred simultaneously because they located very closely in the host reference genome, indicating that the length of transferred DNA could exceed 100 kb. We confirmed that almost all introns are spliced in the current genome of the parasite species, and that about half HGT genes do not have any missense mutations or frameshift-causing indels, suggesting that some HGT genes may be still functional. Evolutionary analyses revealed that the nonsynonymous–synonymous substitution ratio is on average elevated on the lineage leading to HGT genes, due to either relaxation of selection or positive selection.

Highlights

Horizontal gene transfer (HGT) between plant species has been extensively investigated
We focused on HGTs to the five parasite species from their potential hosts, this strategy works for identifying HGTs in the opposite direction because they results in a gene tree that is inconsistent with the species tree
If there was no horizontal event involved, the HGT gene identified in the parasite species should locate close to the Orobanchaceae cluster that belong to the order Lamiales

Summary

Introduction

Horizontal gene transfer (HGT) between plant species has been extensively investigated (reviewed by Richardson and Palmer 2007; Bock 2010; Davis and Xi 2015; Soucy et al 2015). Most nuclear HGT genes identified far are in parasite plants, most likely transferred from their host plants (Yoshida et al 2010; Xi et al 2012; Zhang et al 2013, 2014; Yang et al 2016). The authors found that a poly-A-like sequence at the 30 end of the gene, suggesting that this transfer might have occurred through a reverse transcribed mRNA. This makes sense because parasitic plants form an invasive organ called a haustorium, which interconnects their vasculature with that of their hosts, thereby allowing transfer of nutrients, water, and even mRNAs.

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Conclusion