Lifestyle transitions in plant pathogenic Colletotrichum fungi deciphered by genome and transcriptome analyses
Open accessAbstract
Richard O'Connell and colleagues report the genomes and transcriptomes of two Colletotrichum plant fungal pathogens. C. higginsianum infects Arabidopsis thaliana, and C. graminicola infects maize (Zea mays); comparative genomics in both species lead to molecular insights into the transition from biotrophic to necrotrophic life stages. 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.
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Colletotrichum species adopt either intracellular hemibiotrophy or subcuticular, intramural necrotrophy.
“Colletotrichum species adopt either intracellular hemibiotrophy or subcuticular, intramural necrotrophy (Wharton & Diéguez-Uribeondo 2004, Münch et al. 2008, O'Connell et al. 2012, de Silva et al. 2017).”
From Colletotrichum: lifestyles, biology, morpho-species, species complexes and accepted species (2021) · cites this paper as O'Connell et al. 2012
The Main section describes intracellular biotrophic hyphae in Colletotrichum that later switch to necrotrophy, supporting the intracellular hemibiotrophy part. It does not describe subcuticular, intramural necrotrophy as an alternative infection strategy; the necrotrophy it discusses follows intracellular biotrophy. (LLM, conf=0.86)
Experimental — accuracy not yet measuredComparative analyses of Colletotrichum genomes have revealed that species may tailor their plant cell wall degrading enzymes and proteinases according to their lifestyle.
“Comparative analyses of these genomes have revealed that Colletotrichum species may tailor their plant cell wall degrading enzymes and proteinases according to their lifestyle (O'Connell et al. 2012, Baroncelli et al. 2016, Hacquard et al. 2016).”
From Colletotrichum: lifestyles, biology, morpho-species, species complexes and accepted species (2021) · cites this paper as O'Connell et al. 2012
Species of Colletotrichum undergo major transformations in cell morphology and infection mode when switching lifestyles.
“Species of Colletotrichum undergo major transformations in cell morphology and infection mode when switching lifestyles (O'Connell et al. 2012).”
From Colletotrichum: lifestyles, biology, morpho-species, species complexes and accepted species (2021) · cites this paper as O'Connell et al. 2012
Colletotrichum has different lifestyles that vary between groups of species, and many species can switch between lifestyles.
“Being a complex genus, Colletotrichum has different lifestyles that vary between groups of species, many of which can switch between lifestyles (Promputtha et al. 2007, O'Connell et al. 2012).”
From Colletotrichum: lifestyles, biology, morpho-species, species complexes and accepted species (2021) · cites this paper as O'Connell et al. 2012
Most species of Colletotrichum develop a necrotrophic stage in their life cycles.
“Most of the species of Colletotrichum develop a necrotrophic stage in their life cycles (Cannon et al. 2012, O'Connell et al. 2012, de Silva et al. 2017).”
From Colletotrichum: lifestyles, biology, morpho-species, species complexes and accepted species (2021) · cites this paper as O'Connell et al. 2012
The destructivum species complex is monophyletic and distinct from other Colletotrichum species complexes.
“O'Connell et al. (2012) showed that the destructivum species complex is monophyletic and distinct from other Colletotrichum species complexes.”
From Colletotrichum: lifestyles, biology, morpho-species, species complexes and accepted species (2021) · cites this paper as O'Connell et al. 2012
The Main section describes C. graminicola and C. higginsianum as belonging to sister clades, and the Methods section describes a Colletotrichum phylogeny. Searches for the destructivum species complex and its monophyly found no passage in our copy establishing that it is monophyletic or distinct from other species complexes. No page numbers are available for these passages. (LLM, conf=0.75)
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- Authors
- O'Connell, R. J., Thon, M. R., Hacquard, S., Amyotte, S. G., Kleemann, J., Torres, M. F., Damm, U., Buiate, E. A., Epstein, L., Alkan, N., Altmüller, J., Alvarado-Balderrama, L., Bauser, C. A., Becker, C., Birren, B. W., Chen, Z., Choi, J., Crouch, J. A., Duvick, J. P., Farman, M. A., Gan, P., Heiman, D., Henrissat, B., Howard, R. J., Kabbage, M., Koch, C., Kracher, B., Kubo, Y., Law, A. D., Lebrun, M.-H., Lee, Y.-H., Miyara, I., Moore, N., Neumann, U., Nordström, K., Panaccione, D. G., Panstruga, R., Place, M., Proctor, R. H., Prusky, D., Rech, G., Reinhardt, R., Rollins, J. A., Rounsley, S., Schardl, C. L., Schwartz, D. C., Shenoy, N., Shirasu, K., Sikhakolli, U. R., Stüber, K., Sukno, S. A., Sweigard, J. A., Takano, Y., Takahara, H., Trail, F., van der Does, H. C., Voll, L. M., Will, I., Young, S., Zeng, Q., Zhang, J., Zhou, S., Dickman, M. B., Schulze-Lefert, P., Ver Loren van Themaat, E., Ma, L.-J., & Vaillancourt, L. J.
- Affiliations
- Universidad de Salamanca (ES)
- Max Planck Institute for Plant Breeding Research (DE)
- University of Kentucky (US)
- Royal Netherlands Academy of Arts and Sciences (NL)
- University of California, Davis (US)
- Agricultural Research Organization (IL)
- University of Cologne (DE)
- Broad Institute (US)
- GATC Biotech (Germany) (DE)
- Seoul National University (KR)
- Agricultural Research Service (US)
- DuPont (United States) (US)
- RIKEN (JP)
- Centre National de la Recherche Scientifique (FR)
- Texas A&M University (US)
- Friedrich-Alexander-Universität Erlangen-Nürnberg (DE)
- Kyoto Prefectural University (JP)
- Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement (FR)
- West Virginia University (US)
- University of Wisconsin–Madison (US)
- Max Planck Society (DE)
- University of Florida (US)
- Michigan State University (US)
- Kyoto University (JP)
- Corresponding author
- Vaillancourt, Lisa J
- ORCID
- Thon, Michael R
- Hacquard, Stéphane
- Damm, Ulrike
- Epstein, Lynn
- Alkan, Noam
- Altmüller, Janine
- Bauser, Christopher A
- Becker, Christian
- Birren, Bruce W
- Chen, Zehua
- Choi, Jaeyoung
- Crouch, Jo Anne
- Gan, Pamela
- Heiman, David
- Henrissat, Bernard
- Howard, Richard J
- Kabbage, Mehdi
- Kracher, Barbara
- Kubo, Yasuyuki
- Lebrun, Marc-Henri
- Lee, Yong-Hwan
- Moore, Neil
- Neumann, Ulla
- Nordström, Karl
- Panaccione, Daniel G
- Panstruga, Ralph
- Place, Michael
- Proctor, Robert H
- Prusky, Dov
- Rech, Gabriel
- Reinhardt, Richard
- Rollins, Jeffrey A
- Rounsley, Steve
- Schardl, Christopher L
- Schwartz, David C
- Shirasu, Ken
- Sukno, Serenella A
- Takano, Yoshitaka
- Takahara, Hiroyuki
- Trail, Frances
- Voll, Lars M
- Young, Sarah
- Zeng, Qiandong
- Zhang, Jingze
- Zhou, Shiguo
- Dickman, Martin B
- Ma, Li-Jun
- Vaillancourt, Lisa J
- Venue
- Nature Genetics
- Published
- 2012-08-12
- Volume
- 44
- Issue
- 9
- Pages
- 1060-1065
- ISSN
- 1061-4036 (ISSN-L)
- 1546-1718
- PMC
- PMC9754331
- OpenAlex
- W2003266704
- Cited by
- 1,047
- References
- 63
- Citations by year
- 2026: 61 · 2025: 79 · 2024: 77 · 2023: 85 · 2022: 97 · 2021: 107 · 2020: 67 · 2019: 65 · 2018: 77 · 2017: 73 · 2016: 82 · 2015: 67 · 2014: 61 · 2013: 43 · 2012: 6
- FWCI
- 26.83
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Nature Genetics (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion, cc-by-nc-sa)
- PubMed (publishedVersion)
- MDC Repository (Max-Delbrueck-Center for Molecular Medicine) (acceptedVersion)
- HAL AMU (submittedVersion, other-oa)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- RWTH Publications (RWTH Aachen) (submittedVersion)
- KNAW Research Portal (The Royal Netherlands Academy of Arts and Sciences) (submittedVersion)
- MPG.PuRe (Max Planck Society) (submittedVersion)
- Funders
- U.S. Department of Agriculture
- University of Kentucky
- Deutsche Forschungsgemeinschaft (SPP1212)
- Max-Planck-Gesellschaft
- Ministerio de Ciencia e Innovación
- Cooperative State Research, Education, and Extension Service (20093445720125, 2007-35600-17829)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Plant Pathogens and Fungal Diseases
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Disease Resistance and Genetics
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant-Microbe Interactions and Immunity
- Keywords
- Colletotrichum higginsianum, Colletotrichum graminicola, plant pathogenic fungi, secreted effectors, pectin-degrading enzymes, hydrolytic enzymes, gene expression profiling, host-pathogen interaction, Arabidopsis thaliana, maize, comparative genomics
- MeSH terms
- Mitosporic Fungi, Models, Biological, Phylogeny, Plant Diseases, Gene Expression Regulation, Fungal, Cluster Analysis, Genome, Fungal, Arabidopsis, Sequence Analysis, DNA, Gene Expression Regulation, Developmental, Colletotrichum, Gene Expression Profiling, Host-Pathogen Interactions, Transcriptome
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