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The transcriptomes of Xiphinema index and Longidorus elongatus suggest independent acquisition of some plant parasitism genes by horizontal gene transfer in early-branching nematodes

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Date
23/10/2017
Author
Danchin, Etienne G J
Perfus-Barbeoch, Laetitia
Rancurel, Corinne
Thorpe, Peter
Da Rocha, Martine
Bajew, Simon
Neilson, Roy
Guzeeva, Elena Sokolova
Da Silva, Corinne
Guy, Julie
Labadie, Karine
Esmenjaud, Daniel
Helder, Johannes
Jones, John T
den Akker, Sebastian Eves-van
Keywords
Glycoside hydrolase
Horizontal gene transfer
Nematodes
Plant parasitism
QH426 Genetics
Genetics
Genetics(clinical)
DAS
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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.
Citation
Danchin , E G J , Perfus-Barbeoch , L , Rancurel , C , Thorpe , P , Da Rocha , M , Bajew , S , Neilson , R , Guzeeva , E S , Da Silva , C , Guy , J , Labadie , K , Esmenjaud , D , Helder , J , Jones , J T & den Akker , S E 2017 , ' The transcriptomes of Xiphinema index and Longidorus elongatus suggest independent acquisition of some plant parasitism genes by horizontal gene transfer in early-branching nematodes ' , Genes , vol. 8 , no. 10 , 287 . https://doi.org/10.3390/genes8100287
Publication
Genes
Status
Peer reviewed
DOI
https://doi.org/10.3390/genes8100287
ISSN
2073-4425
Type
Journal article
Rights
© 2017 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Description
Work described in this article was partly funded by the Rural & Environment Science & Analytical Services Division of the Scottish Government and by two grants from the French National Research Agency (ANR) under the Genoplante program (project ANR-PCS-08-GENO-166 NEMATARGETS) and the JCJC program (project ANR-13-JSV7-0006—ASEXEVOL). This work was facilitated by interactions funded through COST action FA1208 and Royal Society International Exchange award IE130707. Sebastian Eves-van den Akker is supported by Biotechnology and Biological Sciences Research Council (BBSRC) grant BB/M014207/1.
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URL
http://www.mdpi.com/2073-4425/8/10/287#supplementary
URI
http://hdl.handle.net/10023/12352

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