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 Farman, Pamela 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

doi:10.1038/ng.2372

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.

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

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