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Research Article

Genome and transcriptome analyses of the mountain pine beetle-fungal symbiont Grosmannia clavigera, a lodgepole pine pathogen

Scott DiGuistini, Ye Wang, Nancy Y. Liao, Greg Taylor, Philippe Tanguay, Nicolas Feau, Bernard Henrissat, Simon K. Chan, Uljana Hesse-Orce, Sepideh Massoumi Alamouti, Clement K. M. Tsui, Roderick T. Docking, Anthony Levasseur, Sajeet Haridas, Gordon Robertson, Inanc Birol, Robert A. Holt, Marco A. Marra, Richard C. Hamelin, Martin Hirst, Steven J. M. Jones, Jörg Bohlmann, and Colette Breuil
  1. aDepartment of Wood Science,
  2. fDepartment of Forest Science, University of British Columbia, Vancouver, BC, Canada V6T 1Z4;
  3. bBritish Columbia Cancer Agency Genome Sciences Centre, Vancouver, BC, Canada V5Z 4E6;
  4. cNatural Resources Canada, Ste-Foy, QC, Canada G1V 4C7;
  5. dUnité Mixte de Recherche 1202, Institut National de la Recherche Agronomique-Université Bordeaux I, Biodiversité, Gènes et Communautés, Institut National de la Recherche Agronomique Bordeaux-Aquitaine, 33612 Cestas Cedex, France;
  6. eArchitecture et Fonction des Macromolécules Biologiques, Unité Mixte de Recherche-6098, Centre National de la Recherche Scientifique, Universités Aix-Marseille I & II, 13288 Marseille cedex 9, France;
  7. gBiotechnologie des Champignons Filamenteux, Unité Mixte de Recherche-1161, Institut National de la Recherche, Universités de Provence et de la Méditerranée, 13288 Marseille cedex 09, France; and
  8. hMichael Smith Laboratories, University of British Columbia, Vancouver, BC, Canada V6T 1Z3

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PNAS first published January 24, 2011; https://doi.org/10.1073/pnas.1011289108
Scott DiGuistini
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Ye Wang
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Nancy Y. Liao
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Greg Taylor
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Philippe Tanguay
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Nicolas Feau
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Bernard Henrissat
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Simon K. Chan
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Uljana Hesse-Orce
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Sepideh Massoumi Alamouti
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Clement K. M. Tsui
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Roderick T. Docking
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Anthony Levasseur
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Sajeet Haridas
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Gordon Robertson
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Inanc Birol
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Robert A. Holt
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Marco A. Marra
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Richard C. Hamelin
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Martin Hirst
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Steven J. M. Jones
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Jörg Bohlmann
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  • For correspondence: bohlmann@interchange.ubc.ca colette.breuil@ubc.ca
Colette Breuil
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  • For correspondence: bohlmann@interchange.ubc.ca colette.breuil@ubc.ca
  1. Edited by Rodney B. Croteau, Washington State University, Pullman, WA, and approved December 27, 2010 (received for review August 2, 2010)

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Abstract

In western North America, the current outbreak of the mountain pine beetle (MPB) and its microbial associates has destroyed wide areas of lodgepole pine forest, including more than 16 million hectares in British Columbia. Grosmannia clavigera (Gc), a critical component of the outbreak, is a symbiont of the MPB and a pathogen of pine trees. To better understand the interactions between Gc, MPB, and lodgepole pine hosts, we sequenced the ∼30-Mb Gc genome and assembled it into 18 supercontigs. We predict 8,314 protein-coding genes, and support the gene models with proteome, expressed sequence tag, and RNA-seq data. We establish that Gc is heterothallic, and report evidence for repeat-induced point mutation. We report insights, from genome and transcriptome analyses, into how Gc tolerates conifer-defense chemicals, including oleoresin terpenoids, as they colonize a host tree. RNA-seq data indicate that terpenoids induce a substantial antimicrobial stress in Gc, and suggest that the fungus may detoxify these chemicals by using them as a carbon source. Terpenoid treatment strongly activated a ∼100-kb region of the Gc genome that contains a set of genes that may be important for detoxification of these host-defense chemicals. This work is a major step toward understanding the biological interactions between the tripartite MPB/fungus/forest system.

  • next generation sequencing
  • monoterpene
  • carbohydrate active enzymes
  • ABC transporter
  • forest genomics

Footnotes

  • 1To whom correspondence may be addressed. E-mail: bohlmann{at}interchange.ubc.ca or colette.breuil{at}ubc.ca.
  • Author contributions: S.D., S.J.M.J., J.B., and C.B. designed research; S.D., Y.W., N.Y.L., G.T., P.T., S.K.C., U.H.-O., S.M.A., and R.T.D. performed research; R.A.H., M.A.M., M.H., R.C.H., and S.J.M.J. contributed new reagents/analytic tools; S.D., A.L., B.H., N.F., U.H.-O., C.K.M.T., S.H., and I.B. analyzed data; and S.D., G.R., S.J.M.J., J.B., and C.B. wrote the paper.

  • The authors declare no conflict of interest.

  • Data deposition: The sequences reported in this paper have been deposited in NCBI GenBank as assembly and annotations accession ACXQ00000000.

  • This article is a PNAS Direct Submission.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1011289108/-/DCSupplemental.

Freely available online through the PNAS open access option.

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Genome and transcriptome analyses of the mountain pine beetle-fungal symbiont Grosmannia clavigera, a lodgepole pine pathogen
Scott DiGuistini, Ye Wang, Nancy Y. Liao, Greg Taylor, Philippe Tanguay, Nicolas Feau, Bernard Henrissat, Simon K. Chan, Uljana Hesse-Orce, Sepideh Massoumi Alamouti, Clement K. M. Tsui, Roderick T. Docking, Anthony Levasseur, Sajeet Haridas, Gordon Robertson, Inanc Birol, Robert A. Holt, Marco A. Marra, Richard C. Hamelin, Martin Hirst, Steven J. M. Jones, Jörg Bohlmann, Colette Breuil
Proceedings of the National Academy of Sciences Jan 2011, 201011289; DOI: 10.1073/pnas.1011289108

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Genome and transcriptome analyses of the mountain pine beetle-fungal symbiont Grosmannia clavigera, a lodgepole pine pathogen
Scott DiGuistini, Ye Wang, Nancy Y. Liao, Greg Taylor, Philippe Tanguay, Nicolas Feau, Bernard Henrissat, Simon K. Chan, Uljana Hesse-Orce, Sepideh Massoumi Alamouti, Clement K. M. Tsui, Roderick T. Docking, Anthony Levasseur, Sajeet Haridas, Gordon Robertson, Inanc Birol, Robert A. Holt, Marco A. Marra, Richard C. Hamelin, Martin Hirst, Steven J. M. Jones, Jörg Bohlmann, Colette Breuil
Proceedings of the National Academy of Sciences Jan 2011, 201011289; DOI: 10.1073/pnas.1011289108
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