Search Menu
DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information
Search Scholarly Publications

Title: Horizontal gene transfer and gene dosage drives adaptation to wood colonization in a tree pathogen

Abstract

Some of the most damaging tree diseases are caused by pathogens that induce cankers, a stem deformation often lethal. To investigate the cause of this adaptation, we sequenced the genomes of poplar pathogens that do and do not cause cankers. We found a unique cluster of genes that produce secondary metabolites and are co-activated when the canker pathogen is grown on poplar wood and leaves. The gene genealogy is discordant with the species phylogeny, showing a signature of horizontal transfer from fungi associated with wood decay. Furthermore, genes encoding hemicellulose-degrading enzymes are up-regulated on poplar wood chips, with some having been acquired horizontally. In conclusion, we propose that adaptation to colonize poplar woody stems is the result of acquisition of these genes.

Authors:
 [1];  [1];  [2];  [1];  [3];  [2];  [4];  [1];  [5];  [1];  [2];  [6];  [2];  [7];  [2];  [2];  [1];  [1];  [1];  [7] more »;  [2];  [8];  [4];  [9] « less
+ Show Author Affiliations
  1. The Univ. of British Columbia, Vancouver, BC (Canada)
  2. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  3. Univ. Laval, QC (Canada)
  4. Natural Resources Canada, QC (Canada)
  5. Aix-Marseille Univ., Marseille (France); King Abdulaziz Univ., Jeddah (Saudi Arabia)
  6. Aix-Marseille Univ., Marseille (France)
  7. Fungal Physiology, Centraalbureau voor Schimmelcultures-Royal Netherlands Academy of Arts and Sciences Fungal Biodiversity Centre (CBS-KNAW), Utrecht (The Netherlands); Utrecht Univ., Utrecht (The Netherlands)
  8. Purdue Univ., West Lafayette, IN (United States)
  9. The Univ. of British Columbia, Vancouver, BC (Canada); Natural Resources Canada, QC (Canada)
Publication Date:
Research Org.:
USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC); The Netherlands Organization for Scientific Research; The Netherlands Genomics Initiative
OSTI Identifier:
1347689
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Volume: 112; Journal Issue: 11; Journal ID: ISSN 0027-8424
Publisher:
National Academy of Sciences, Washington, DC (United States)
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Septoria canker; fungal genomics; tree disease; poplar pathogen

Citation Formats

Dhillon, Braham, Feau, Nicolas, Aerts, Andrea L., Beauseigle, Stéphanie, Bernier, Louis, Copeland, Alex, Foster, Adam, Gill, Navdeep, Henrissat, Bernard, Herath, Padmini, LaButti, Kurt M., Levasseur, Anthony, Lindquist, Erika A., Majoor, Eline, Ohm, Robin A., Pangilinan, Jasmyn L., Pribowo, Amadeus, Saddler, John N., Sakalidis, Monique L., de Vries, Ronald P., Grigoriev, Igor V., Goodwin, Stephen B., Tanguay, Philippe, and Hamelin, Richard C. Horizontal gene transfer and gene dosage drives adaptation to wood colonization in a tree pathogen. United States: N. p., 2015. Web. doi:10.1073/pnas.1424293112.
Copy to clipboard
Dhillon, Braham, Feau, Nicolas, Aerts, Andrea L., Beauseigle, Stéphanie, Bernier, Louis, Copeland, Alex, Foster, Adam, Gill, Navdeep, Henrissat, Bernard, Herath, Padmini, LaButti, Kurt M., Levasseur, Anthony, Lindquist, Erika A., Majoor, Eline, Ohm, Robin A., Pangilinan, Jasmyn L., Pribowo, Amadeus, Saddler, John N., Sakalidis, Monique L., de Vries, Ronald P., Grigoriev, Igor V., Goodwin, Stephen B., Tanguay, Philippe, & Hamelin, Richard C. Horizontal gene transfer and gene dosage drives adaptation to wood colonization in a tree pathogen. United States. https://doi.org/10.1073/pnas.1424293112
Copy to clipboard
Dhillon, Braham, Feau, Nicolas, Aerts, Andrea L., Beauseigle, Stéphanie, Bernier, Louis, Copeland, Alex, Foster, Adam, Gill, Navdeep, Henrissat, Bernard, Herath, Padmini, LaButti, Kurt M., Levasseur, Anthony, Lindquist, Erika A., Majoor, Eline, Ohm, Robin A., Pangilinan, Jasmyn L., Pribowo, Amadeus, Saddler, John N., Sakalidis, Monique L., de Vries, Ronald P., Grigoriev, Igor V., Goodwin, Stephen B., Tanguay, Philippe, and Hamelin, Richard C. Mon . "Horizontal gene transfer and gene dosage drives adaptation to wood colonization in a tree pathogen". United States. https://doi.org/10.1073/pnas.1424293112. https://www.osti.gov/servlets/purl/1347689.
Copy to clipboard
@article{osti_1347689,
title = {Horizontal gene transfer and gene dosage drives adaptation to wood colonization in a tree pathogen},
author = {Dhillon, Braham and Feau, Nicolas and Aerts, Andrea L. and Beauseigle, Stéphanie and Bernier, Louis and Copeland, Alex and Foster, Adam and Gill, Navdeep and Henrissat, Bernard and Herath, Padmini and LaButti, Kurt M. and Levasseur, Anthony and Lindquist, Erika A. and Majoor, Eline and Ohm, Robin A. and Pangilinan, Jasmyn L. and Pribowo, Amadeus and Saddler, John N. and Sakalidis, Monique L. and de Vries, Ronald P. and Grigoriev, Igor V. and Goodwin, Stephen B. and Tanguay, Philippe and Hamelin, Richard C.},
abstractNote = {Some of the most damaging tree diseases are caused by pathogens that induce cankers, a stem deformation often lethal. To investigate the cause of this adaptation, we sequenced the genomes of poplar pathogens that do and do not cause cankers. We found a unique cluster of genes that produce secondary metabolites and are co-activated when the canker pathogen is grown on poplar wood and leaves. The gene genealogy is discordant with the species phylogeny, showing a signature of horizontal transfer from fungi associated with wood decay. Furthermore, genes encoding hemicellulose-degrading enzymes are up-regulated on poplar wood chips, with some having been acquired horizontally. In conclusion, we propose that adaptation to colonize poplar woody stems is the result of acquisition of these genes.},
doi = {10.1073/pnas.1424293112},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 11,
volume = 112,
place = {United States},
year = {Mon Mar 02 00:00:00 EST 2015},
month = {Mon Mar 02 00:00:00 EST 2015}
}
Copy to clipboard
Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1073/pnas.1424293112
Copyright Statement
Other availability
Search WorldCat Search WorldCat to find libraries that may hold this journal
Citation Metrics:
Cited by: 50 works
Citation information provided by
Web of Science
Save / Share:
Export Metadata
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.

Works referenced in this record:

Obligate biotrophy features unraveled by the genomic analysis of rust fungi
journal, May 2011

  • Duplessis, S.; Cuomo, C. A.; Lin, Y. -C.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 22
  • DOI: 10.1073/pnas.1019315108

Assessing the impact of transcriptomics, proteomics and metabolomics on fungal phytopathology
journal, September 2009

Acetylesterase-Mediated Deacetylation of Pectin Impairs Cell Elongation, Pollen Germination, and Plant Reproduction
journal, January 2012

Phytotoxic chaetoglobosins are produced by the plant pathogen Calonectria morganii(anamorph Cylindrocladium scoparium).
journal, January 2001

  • Wallbrunn, Christian von; Luftmann, Heinrich; Bergander, Klaus
  • The Journal of General and Applied Microbiology, Vol. 47, Issue 1
  • DOI: 10.2323/jgam.47.33

Genome Expansion and Gene Loss in Powdery Mildew Fungi Reveal Tradeoffs in Extreme Parasitism
journal, December 2010

Gene transfer into the fungi
journal, July 2011

  • Richards, Thomas A.; Leonard, Guy; Soanes, Darren M.
  • Fungal Biology Reviews, Vol. 25, Issue 2
  • DOI: 10.1016/j.fbr.2011.04.003

The Histology of Hybrid Poplar Clones Inoculated with Septoria musiva
journal, December 2007

Chlorination and Cleavage of Lignin Structures by Fungal Chloroperoxidases
journal, August 2003

Surface α-1,3-Glucan Facilitates Fungal Stealth Infection by Interfering with Innate Immunity in Plants
journal, August 2012

Characterization of SNP1, a Cell Wall-Degrading Trypsin, Produced During Infection by Stagonospora nodorum
journal, May 2000

  • Carlile, A. J.; Bindschedler, L. V.; Bailey, A. M.
  • Molecular Plant-Microbe Interactions, Vol. 13, Issue 5
  • DOI: 10.1094/MPMI.2000.13.5.538

Attributes and congruence of three molecular data sets: Inferring phylogenies among Septoria-related species from woody perennial plants
journal, September 2006

  • Feau, Nicolas; Hamelin, Richard C.; Bernier, Louis
  • Molecular Phylogenetics and Evolution, Vol. 40, Issue 3
  • DOI: 10.1016/j.ympev.2006.03.029

antiSMASH 2.0—a versatile platform for genome mining of secondary metabolite producers
journal, May 2013

  • Blin, Kai; Medema, Marnix H.; Kazempour, Daniyal
  • Nucleic Acids Research, Vol. 41, Issue W1
  • DOI: 10.1093/nar/gkt449

Molecular Basis of Cytochalasan Biosynthesis in Fungi:  Gene Cluster Analysis and Evidence for the Involvement of a PKS-NRPS Hybrid Synthase by RNA Silencing
journal, August 2007

  • Schümann, Julia; Hertweck, Christian
  • Journal of the American Chemical Society, Vol. 129, Issue 31
  • DOI: 10.1021/ja072884t

Recent advances related to poplar leaf spot and canker caused by Septoria musiva : Minireview/Minisynthèse
journal, June 2010

  • Feau, Nicolas; Mottet, Marie-Josée; Périnet, Pierre
  • Canadian Journal of Plant Pathology, Vol. 32, Issue 2
  • DOI: 10.1080/07060661003740009

Poplar as a feedstock for biofuels: A review of compositional characteristics
journal, March 2010

  • Sannigrahi, Poulomi; Ragauskas, Arthur J.; Tuskan, Gerald A.
  • Biofuels, Bioproducts and Biorefining, Vol. 4, Issue 2
  • DOI: 10.1002/bbb.206

The Infection Biology of Sphaerulina musiva: Clues to Understanding a Forest Pathogen
journal, July 2014

Bioactive metabolites produced by Chaetomium globosum, an endophytic fungus isolated from Ginkgo biloba
journal, March 2009

  • Qin, Jian-Chun; Zhang, Ya-Mei; Gao, Jin-Ming
  • Bioorganic & Medicinal Chemistry Letters, Vol. 19, Issue 6
  • DOI: 10.1016/j.bmcl.2009.02.025

Carbon and nitrogen allocation in trees
journal, January 1989

Oxidative Cleavage of Cellulose by Fungal Copper-Dependent Polysaccharide Monooxygenases
journal, December 2011

  • Beeson, William T.; Phillips, Christopher M.; Cate, Jamie H. D.
  • Journal of the American Chemical Society, Vol. 134, Issue 2
  • DOI: 10.1021/ja210657t

Molecular Characterization of a Subtilase from the Vascular Wilt Fungus Fusarium oxysporum
journal, May 2001

  • Pietro, Antonio Di; Huertas-González, M. Dolores; Gutierrez-Corona, J. Felix
  • Molecular Plant-Microbe Interactions, Vol. 14, Issue 5
  • DOI: 10.1094/MPMI.2001.14.5.653

Horizontal Gene Transfer of Glycosyl Hydrolases of the Rumen Fungi
journal, March 2000

Assessing the gene space in draft genomes
journal, November 2008

  • Parra, Genis; Bradnam, Keith; Ning, Zemin
  • Nucleic Acids Research, Vol. 37, Issue 1
  • DOI: 10.1093/nar/gkn916

Acquisition of prokaryotic genes by fungal genomes
journal, January 2010

An ?-(1,4)-amylase is essential for ?-(1,3)-glucan production and virulence in Histoplasma capsulatum
journal, November 2006

The complexity of nitrogen metabolism and nitrogen-regulated gene expression in plant pathogenic fungi
journal, July 2008

  • Bolton, Melvin D.; Thomma, Bart P. H. J.
  • Physiological and Molecular Plant Pathology, Vol. 72, Issue 4-6
  • DOI: 10.1016/j.pmpp.2008.07.001

The nutrient supply of pathogenic fungi; a fertile field for study
journal, May 2003

Biotechnology and the domestication of forest trees
journal, April 2005

Primeiro relato da ocorrência de Septoria musiva em álamo no Brasil
journal, January 2010

Diverse Lifestyles and Strategies of Plant Pathogenesis Encoded in the Genomes of Eighteen Dothideomycetes Fungi
journal, December 2012

Allozyme divergence and evolutionary relationships among Populus deltoides , P . nigra , and P . maximowiczii
journal, February 1990

  • Rajora, Om P.; Zsuffa, Louis
  • Genome, Vol. 33, Issue 1
  • DOI: 10.1139/g90-008

Prediction of Long-Term Canker Disease Damage from the Responses of Juvenile Poplar Clones to Inoculation with Septoria musiva
journal, December 2003

Penicillium expansum :  Consistent Production of Patulin, Chaetoglobosins, and Other Secondary Metabolites in Culture and Their Natural Occurrence in Fruit Products
journal, April 2004

  • Andersen, Birgitte; Smedsgaard, Jørn; Frisvad, Jens C.
  • Journal of Agricultural and Food Chemistry, Vol. 52, Issue 8
  • DOI: 10.1021/jf035406k

Expansion of the enzymatic repertoire of the CAZy database to integrate auxiliary redox enzymes
journal, January 2013

  • Levasseur, Anthony; Drula, Elodie; Lombard, Vincent
  • Biotechnology for Biofuels, Vol. 6, Issue 1, Article No. 41
  • DOI: 10.1186/1754-6834-6-41

Purification and Characterization of a Secreted Laccase of Gaeumannomyces graminis var.tritici
journal, July 1999

Genome expansion and gene loss in powdery mildew fungi reveal tradeoffs in extreme parasitism
text, January 2010

  • Spanu, P. D.; Abbott, J. C.; Amselem, J.
  • American Association for the Advancement of Science (AAAS)
  • DOI: 10.5167/uzh-43503
    Sort by:
    [ × clear filter / sort ]

    Works referencing / citing this record:

    Anthropogenic signature in the incidence and distribution of an emerging pathogen of poplars
    journal, February 2016

    • Herath, Padmini; Beauseigle, Stephanie; Dhillon, Braham
    • Biological Invasions, Vol. 18, Issue 4
    • DOI: 10.1007/s10530-015-1051-8

    Ecology of invasive forest pathogens
    journal, June 2017

    An evolutionary ecology perspective to address forest pathology challenges of today and tomorrow
    journal, March 2016

    • Desprez-Loustau, Marie-Laure; Aguayo, Jaime; Dutech, Cyril
    • Annals of Forest Science, Vol. 73, Issue 1
    • DOI: 10.1007/s13595-015-0487-4

    Molecular Genetic Approaches Toward Understanding Forest-Associated Fungi and Their Interactive Roles Within Forest Ecosystems
    journal, May 2018

    • Stewart, Jane E.; Kim, Mee-Sook; Klopfenstein, Ned B.
    • Current Forestry Reports, Vol. 4, Issue 2
    • DOI: 10.1007/s40725-018-0076-5

    Fungal canker pathogens trigger carbon starvation by inhibiting carbon metabolism in poplar stems
    journal, July 2019

    Biosynthetic gene clusters and the evolution of fungal chemodiversity
    journal, January 2020

    • Rokas, Antonis; Mead, Matthew E.; Steenwyk, Jacob L.
    • Natural Product Reports, Vol. 37, Issue 7
    • DOI: 10.1039/c9np00045c

    OcculterCut: A Comprehensive Survey of AT-Rich Regions in Fungal Genomes
    journal, June 2016

    • Testa, Alison C.; Oliver, Richard P.; Hane, James K.
    • Genome Biology and Evolution, Vol. 8, Issue 6
    • DOI: 10.1093/gbe/evw121

    Genomic biosurveillance of forest invasive alien enemies: A story written in code
    journal, June 2019

    • Hamelin, Richard C.; Roe, Amanda D.
    • Evolutionary Applications, Vol. 13, Issue 1
    • DOI: 10.1111/eva.12853

    Fungal phytopathogens encode functional homologues of plant rapid alkalinization factor (RALF) peptides: Fungal phytopathogens encode functional homologues
    journal, September 2016

    • Thynne, Elisha; Saur, Isabel M. L.; Simbaqueba, Jaime
    • Molecular Plant Pathology, Vol. 18, Issue 6
    • DOI: 10.1111/mpp.12444

    Global population genomics of the forest pathogen Dothistroma septosporum reveal chromosome duplications in high dothistromin‐producing strains
    journal, April 2019

    • Bradshaw, Rosie E.; Sim, Andre D.; Chettri, Pranav
    • Molecular Plant Pathology, Vol. 20, Issue 6
    • DOI: 10.1111/mpp.12791

    Secondary metabolite gene clusters in the entomopathogen fungus Metarhizium anisopliae: genome identification and patterns of expression in a cuticle infection model
    journal, October 2016

    • Sbaraini, Nicolau; Guedes, Rafael Lucas Muniz; Andreis, Fábio Carrer
    • BMC Genomics, Vol. 17, Issue S8
    • DOI: 10.1186/s12864-016-3067-6

    Genome-Enhanced Detection and Identification (GEDI) of plant pathogens
    journal, January 2018

    • Feau, Nicolas; Beauseigle, Stéphanie; Bergeron, Marie-Josée
    • PeerJ, Vol. 6
    • DOI: 10.7717/peerj.4392

    The Architecture of Metabolism Maximizes Biosynthetic Diversity in the Largest Class of Fungi
    journal, May 2020

    • Gluck-Thaler, Emile; Haridas, Sajeet; Binder, Manfred
    • Molecular Biology and Evolution, Vol. 37, Issue 10
    • DOI: 10.1093/molbev/msaa122

    An evolutionary ecology perspective to address forest pathology challenges of today and tomorrow
    journal, March 2016

    • Desprez-Loustau, Marie-Laure; Aguayo, Jaime; Dutech, Cyril
    • Annals of Forest Science, Vol. 73, Issue 1
    • DOI: 10.1007/s13595-015-0487-4

    Fungal canker pathogens trigger carbon starvation by inhibiting carbon metabolism in poplar stems
    journal, July 2019

    OcculterCut: A Comprehensive Survey of AT-Rich Regions in Fungal Genomes
    journal, June 2016

    • Testa, Alison C.; Oliver, Richard P.; Hane, James K.
    • Genome Biology and Evolution, Vol. 8, Issue 6
    • DOI: 10.1093/gbe/evw121

    Genomic biosurveillance of forest invasive alien enemies: A story written in code
    journal, June 2019

    • Hamelin, Richard C.; Roe, Amanda D.
    • Evolutionary Applications, Vol. 13, Issue 1
    • DOI: 10.1111/eva.12853

    Secondary metabolite gene clusters in the entomopathogen fungus Metarhizium anisopliae: genome identification and patterns of expression in a cuticle infection model
    journal, October 2016

    • Sbaraini, Nicolau; Guedes, Rafael Lucas Muniz; Andreis, Fábio Carrer
    • BMC Genomics, Vol. 17, Issue S8
    • DOI: 10.1186/s12864-016-3067-6

    The MSDIN family in amanitin-producing mushrooms and evolution of the prolyl oligopeptidase genes
    journal, December 2018

      Sort by:
      [ × clear filter / sort ]

      Similar Records in DOE PAGES and OSTI.GOV collections: