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

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. A...

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Autores principales: Taisei Kikuchi, James A Cotton, Jonathan J Dalzell, Koichi Hasegawa, Natsumi Kanzaki, Paul McVeigh, Takuma Takanashi, Isheng J Tsai, Samuel A Assefa, Peter J A Cock, Thomas Dan Otto, Martin Hunt, Adam J Reid, Alejandro Sanchez-Flores, Kazuko Tsuchihara, Toshiro Yokoi, Mattias C Larsson, Johji Miwa, Aaron G Maule, Norio Sahashi, John T Jones, Matthew Berriman
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Publicado: Public Library of Science (PLoS) 2011
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spelling oai:doaj.org-article:5b9b7d20f180440c9f667bb7948adcf32021-11-18T06:03:01ZGenomic insights into the origin of parasitism in the emerging plant pathogen Bursaphelenchus xylophilus.1553-73661553-737410.1371/journal.ppat.1002219https://doaj.org/article/5b9b7d20f180440c9f667bb7948adcf32011-09-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/21909270/?tool=EBIhttps://doaj.org/toc/1553-7366https://doaj.org/toc/1553-7374Bursaphelenchus 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.Taisei KikuchiJames A CottonJonathan J DalzellKoichi HasegawaNatsumi KanzakiPaul McVeighTakuma TakanashiIsheng J TsaiSamuel A AssefaPeter J A CockThomas Dan OttoMartin HuntAdam J ReidAlejandro Sanchez-FloresKazuko TsuchiharaToshiro YokoiMattias C LarssonJohji MiwaAaron G MauleNorio SahashiJohn T JonesMatthew BerrimanPublic Library of Science (PLoS)articleImmunologic diseases. AllergyRC581-607Biology (General)QH301-705.5ENPLoS Pathogens, Vol 7, Iss 9, p e1002219 (2011)
institution DOAJ
collection DOAJ
language EN
topic Immunologic diseases. Allergy
RC581-607
Biology (General)
QH301-705.5
spellingShingle Immunologic diseases. Allergy
RC581-607
Biology (General)
QH301-705.5
Taisei Kikuchi
James A Cotton
Jonathan J Dalzell
Koichi Hasegawa
Natsumi Kanzaki
Paul McVeigh
Takuma Takanashi
Isheng J Tsai
Samuel A Assefa
Peter J A Cock
Thomas Dan Otto
Martin Hunt
Adam J Reid
Alejandro Sanchez-Flores
Kazuko Tsuchihara
Toshiro Yokoi
Mattias C Larsson
Johji Miwa
Aaron G Maule
Norio Sahashi
John T Jones
Matthew Berriman
Genomic insights into the origin of parasitism in the emerging plant pathogen Bursaphelenchus xylophilus.
description 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.
format article
author Taisei Kikuchi
James A Cotton
Jonathan J Dalzell
Koichi Hasegawa
Natsumi Kanzaki
Paul McVeigh
Takuma Takanashi
Isheng J Tsai
Samuel A Assefa
Peter J A Cock
Thomas Dan Otto
Martin Hunt
Adam J Reid
Alejandro Sanchez-Flores
Kazuko Tsuchihara
Toshiro Yokoi
Mattias C Larsson
Johji Miwa
Aaron G Maule
Norio Sahashi
John T Jones
Matthew Berriman
author_facet Taisei Kikuchi
James A Cotton
Jonathan J Dalzell
Koichi Hasegawa
Natsumi Kanzaki
Paul McVeigh
Takuma Takanashi
Isheng J Tsai
Samuel A Assefa
Peter J A Cock
Thomas Dan Otto
Martin Hunt
Adam J Reid
Alejandro Sanchez-Flores
Kazuko Tsuchihara
Toshiro Yokoi
Mattias C Larsson
Johji Miwa
Aaron G Maule
Norio Sahashi
John T Jones
Matthew Berriman
author_sort Taisei Kikuchi
title Genomic insights into the origin of parasitism in the emerging plant pathogen Bursaphelenchus xylophilus.
title_short Genomic insights into the origin of parasitism in the emerging plant pathogen Bursaphelenchus xylophilus.
title_full Genomic insights into the origin of parasitism in the emerging plant pathogen Bursaphelenchus xylophilus.
title_fullStr Genomic insights into the origin of parasitism in the emerging plant pathogen Bursaphelenchus xylophilus.
title_full_unstemmed Genomic insights into the origin of parasitism in the emerging plant pathogen Bursaphelenchus xylophilus.
title_sort genomic insights into the origin of parasitism in the emerging plant pathogen bursaphelenchus xylophilus.
publisher Public Library of Science (PLoS)
publishDate 2011
url https://doaj.org/article/5b9b7d20f180440c9f667bb7948adcf3
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