Genomic insights into the origin of parasitism in the emerging plant pathogen bursaphelenchus xylophilus

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Kikuchi, Taisei and Cotton, James A. and Dalzell, Jonathan J. and Hasegawa, Koichi and Kanzaki, Natsumi and McVeigh, Paul and Takanashi, Takuma and Tsai, Isheng J. and Assefa, Samuel A. and Cock, Peter J.A. and Da Otto, Thomasn and Hunt, Martin and Reid, Adam J. and Sanchez-Flores, Alejandro and Tsuchihara, Kazuko and Yokoi, Toshiro and Larsson, Mattias C. and Miwa, Johji and Maule, Aaron G. and Sahashi, Norio and Jones, John T. and Berriman, Matthew (2011) Genomic insights into the origin of parasitism in the emerging plant pathogen bursaphelenchus xylophilus. PLOS Pathogens, 7 (9). e1002219. ISSN 1553-7366 (https://doi.org/10.1371/journal.ppat.1002219)

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Abstract

Bursaphelenchus xylophilus is the nematode responsible for a devastating epidemic of pine wilt disease in Asia and Europe, and represents a recent, independent origin of plant parasitism in nematodes, ecologically and taxonomically distinct from other nematodes for which genomic data is available. As well as being an important pathogen, the B. xylophilus genome thus provides a unique opportunity to study the evolution and mechanism of plant parasitism. Here, we present a high-quality draft genome sequence from an inbred line of B. xylophilus, and use this to investigate the biological basis of its complex ecology which combines fungal feeding, plant parasitic and insect-associated stages. We focus particularly on putative parasitism genes as well as those linked to other key biological processes and demonstrate that B. xylophilus is well endowed with RNA interference effectors, peptidergic neurotransmitters (including the first description of ins genes in a parasite) stress response and developmental genes and has a contracted set of chemosensory receptors. B. xylophilus has the largest number of digestive proteases known for any nematode and displays expanded families of lysosome pathway genes, ABC transporters and cytochrome P450 pathway genes. This expansion in digestive and detoxification proteins may reflect the unusual diversity in foods it exploits and environments it encounters during its life cycle. In addition, B. xylophilus possesses a unique complement of plant cell wall modifying proteins acquired by horizontal gene transfer, underscoring the impact of this process on the evolution of plant parasitism by nematodes. Together with the lack of proteins homologous to effectors from other plant parasitic nematodes, this confirms the distinctive molecular basis of plant parasitism in the Bursaphelenchus lineage. The genome sequence of B. xylophilus adds to the diversity of genomic data for nematodes, and will be an important resource in understanding the biology of this unusual parasite.

ORCID iDs

Kikuchi, Taisei, Cotton, James A., Dalzell, Jonathan J., Hasegawa, Koichi, Kanzaki, Natsumi, McVeigh, Paul, Takanashi, Takuma, Tsai, Isheng J., Assefa, Samuel A., Cock, Peter J.A. ORCID logoORCID: https://orcid.org/0000-0001-9513-9993, Da Otto, Thomasn, Hunt, Martin, Reid, Adam J., Sanchez-Flores, Alejandro, Tsuchihara, Kazuko, Yokoi, Toshiro, Larsson, Mattias C., Miwa, Johji, Maule, Aaron G., Sahashi, Norio, Jones, John T. and Berriman, Matthew;
  • Item type:Article
    ID code:90571
    Dates:
    Date
    Event
    1 September 2011
    Published
    Notes:This work was partially supported by Grants-in-Aid for Scientific Research (KAKENHI 23248024 and 23380092) (http://www.jsps.go.jp/) and research grant #200704 of FFPRI (http://www.ffpri.affrc.go.jp/). TK was supported by JSPS Postdoctoral Fellowships for Research Abroad (http://www.jsps.go.jp/). JAC, IJT, SAS, AJR, AS-F, and MB are supported by the Wellcome Trust [grant WT 085775/Z/08/Z] (http://www.wellcome.ac.uk/). TDO is supported by European Union’s Seventh Framework Programme (FP7/2007-2013) under grant agreement nu242095: EVIMalaR - Towards the establishment of a permanent European Virtual Institute dedicated to Malaria Research (EVIMalaR) (http://cordis.europa.eu/fp7/). JH Institute receives funding from the Scottish Government. This work benefited from links funded though COST Action 872 (http://www.cost.esf.org/) and through ERASMUS MUNDUS project 2008-102 (EUMAINE) (http://www.eumaine.ugent. be). Swedish University of Agricultural Sciences was supported by Swedish Science Council, Carl Trygger Foundation (http://www.carltryggersstiftelse.se/), the Linnaeus initiative ‘‘Insect Chemical Ecology, Ethology and Evolution’’ (ICE3).
    Subjects:Science > Natural history > Biology
    Science > Natural history > Genetics
    Department:Faculty of Science > Strathclyde Institute of Pharmacy and Biomedical Sciences
    Depositing user: Pure Administrator
    Date deposited:16 Sep 2024 11:26
    Last modified:15 Dec 2024 09:43
    Related URLs:
    URI:https://strathprints.strath.ac.uk/id/eprint/90571
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