Abstract

Nematodes have evolved the ability to parasitize plants on at least four independent occasions, with plant parasites present in Clades 1, 2, 10 and 12 of the phylum. In the case of Clades 10 and 12, horizontal gene transfer of plant cell wall degrading enzymes from bacteria and fungi has been implicated in the evolution of plant parasitism. We have used ribonucleic acid sequencing (RNAseq) to generate reference transcriptomes for two economically important nematode species, Xiphinema index and Longidorus elongatus, representative of two genera within the early-branching Clade 2 of the phylum Nematoda. We used a transcriptome-wide analysis to identify putative horizontal gene transfer events. This represents the first in-depth transcriptome analysis from any plant-parasitic nematode of this clade. For each species, we assembled ~30 million Illumina reads into a reference transcriptome. We identified 62 and 104 transcripts, from X. index and L. elongatus, respectively, that were putatively acquired via horizontal gene transfer. By cross-referencing horizontal gene transfer prediction with a phylum-wide analysis of Pfam domains, we identified Clade 2-specific events. Of these, a GH12 cellulase from X. index was analysed phylogenetically and biochemically, revealing a likely bacterial origin and canonical enzymatic function. Horizontal gene transfer was previously shown to be a phenomenon that has contributed to the evolution of plant parasitism among nematodes. Our findings underline the importance and the extensiveness of this phenomenon in the evolution of plant-parasitic life styles in this speciose and widespread animal phylum.

Highlights

  • Plant-parasitic nematodes (PPN) cause damage to crops across the world and are a major threat to global food security

  • PPN, we report the deep sequencing of transcriptomes of X. index and L. elongatus and an analysis of genes potentially acquired via horizontal gene transfer (HGT) in these species

  • We demonstrate the presence of a biochemically active Glycoside Hydrolase Family 12 (GH12) cellulase of likely bacterial origin in X. index, confirming that independent HGT has occurred in this group and may have played a role in the evolution of plant parasitism

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Summary

Introduction

Plant-parasitic nematodes (PPN) cause damage to crops across the world and are a major threat to global food security. 12 (Tylenchida), and include migratory endoparasitic species as well as the biotrophic, sedentary endoparasitic root-knot and cyst nematodes. These nematodes, and the Clade 10 plant parasite. Bursaphelenchus xylophilus, have been intensively studied and extensive genome and transcriptome resources are available for these nematodes. These resources include full genome sequences for several root-knot and cyst nematodes (e.g., [3,4,5,6]) and B. xylophilus [7] as well as extensive transcriptome analysis for a wide range of other species in these clades (reviewed in [8]). The molecular process by which Clades 1 and 2 ectoparasitic nematodes infect plants is poorly known

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