Lifestyle transitions in plant pathogenic Colletotrichum fungi deciphered by genome and transcriptome analyses

Richard J. O'Connell, Michael R. Thon, Stéphane Hacquard, Stefan G. Amyotte, Jochen Kleemann, Maria F. Torres, Ulrike Damm, Ester A. Buiate, Lynn Epstein, Noam Alkan, Janine Altmüller, Lucia Alvarado-Balderrama, Christopher A. Bauser, Christian Becker, Bruce W. Birren, Zehua Chen, Jaeyoung Choi, Jo Anne Crouch, Jonathan P. Duvick, Mark A. FarmanPamela Gan, David Heiman, Bernard Henrissat, Richard J. Howard, Mehdi Kabbage, Christian Koch, Barbara Kracher, Yasuyuki Kubo, Audrey D. Law, Marc Henri Lebrun, Yong Hwan Lee, Itay Miyara, Neil Moore, Ulla Neumann, Karl Nordström, Daniel G. Panaccione, Ralph Panstruga, Michael Place, Robert H. Proctor, Dov Prusky, Gabriel Rech, Richard Reinhardt, Jeffrey A. Rollins, Steve Rounsley, Christopher L. Schardl, David C. Schwartz, Narmada Shenoy, Ken Shirasu, Usha R. Sikhakolli, Kurt Stüber, Serenella A. Sukno, James A. Sweigard, Yoshitaka Takano, Hiroyuki Takahara, Frances Trail, H. Charlotte Van Der Does, Lars M. Voll, Isa Will, Sarah Young, Qiandong Zeng, Jingze Zhang, Shiguo Zhou, Martin B. Dickman, Paul Schulze-Lefert, Emiel Ver Loren Van Themaat, Li Jun Ma, Lisa J. Vaillancourt

Research output: Contribution to journalArticlepeer-review

606 Scopus citations

Abstract

Colletotrichum species are fungal pathogens that devastate crop plants worldwide. Host infection involves the differentiation of specialized cell types that are associated with penetration, growth inside living host cells (biotrophy) and tissue destruction (necrotrophy). We report here genome and transcriptome analyses of Colletotrichum higginsianum infecting Arabidopsis thaliana and Colletotrichum graminicola infecting maize. Comparative genomics showed that both fungi have large sets of pathogenicity-related genes, but families of genes encoding secreted effectors, pectin-degrading enzymes, secondary metabolism enzymes, transporters and peptidases are expanded in C. higginsianum. Genome-wide expression profiling revealed that these genes are transcribed in successive waves that are linked to pathogenic transitions: effectors and secondary metabolism enzymes are induced before penetration and during biotrophy, whereas most hydrolases and transporters are upregulated later, at the switch to necrotrophy. Our findings show that preinvasion perception of plant-derived signals substantially reprograms fungal gene expression and indicate previously unknown functions for particular fungal cell types.

Original languageEnglish
Pages (from-to)1060-1065
Number of pages6
JournalNature Genetics
Volume44
Issue number9
DOIs
StatePublished - Sep 2012

Bibliographical note

Funding Information:
This manuscript is dedicated to the memory of Robert Hanau. This work was primarily supported by US Department of Agriculture (USDA)–Cooperative State Research, Education and Extension Service (CSREES) grant 2007-35600-17829 (L.J.V., M.B.D., S.R. and M.R.T.), the Max Planck Society (R.J.O.) and Deutsche Forschungsgemeinschaft (SPP1212) grant OC 104/1-3 (R.J.O.). Other funding sources included USDA-CSREES grant 2009-34457-20125 (L.J.V.), the University of Kentucky College of Agriculture Research Office (L.J.V.), Ministerio de Ciencia e Innovación (MICINN) of Spain grants AGL2008-03177/AGR and AGL2011-29446/AGR (M.R.T.) and the Programme for Promotion of Basic and Applied Research for Innovations in Bio-oriented Industry (P.G. and K. Shirasu). This is manuscript number 12-12-011, published with the approval of the Director of the University of Kentucky Agricultural Experiment Station. See the Supplementary Note for a full list of acknowledgments.

ASJC Scopus subject areas

  • Genetics

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