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

Richard J O'Connell (1) , Michael R Thon (2) , Stéphane Hacquard (1) , Stefan G Amyotte (3) , Jochem Kleeman (4) , Maria F Torres (3) , Ulrike Damm (5) , Ester A Buiate (6) , Lynn Epstein (7) , Noam Alkan (8) , Janine Altmüller (9) , Lucia Alvarado-Balderrama (10) , Christopher A. Bauser (11) , Christian Becker (12) , Bruce W. Birren (10) , Zehua Chen (10) , Jaeyoung Choi (13) , Jo Aann Crouch (14) , Jonathan P. Duvick (15) , Mark A. Farman (3) , Pamela Gan (16) , David Heiman (10) , Bernard Henrissat (17) , Richard J Howard (15) , Mehdi Kabbage (18) , Christian Koch (19) , Barbara Kracher (1) , Yasuyuki Kubo (20) , Audrey D Law (3) , Marc-Henri Lebrun (21) , Yong-Hwan Lee (13) , Itay Miyara (22) , Neil Moore (23) , Ulla Neumann (24) , Karl Nordström (25) , Daniel G Panaccione (26) , Ralph Panstruga (1, 27) , Michael Place (28) , Robert H Proctor (29) , Dov Prusky (22) , Gabriel Rech (30) , Richard Reinhardt (31) , Jeffrey A Rollings (32) , Steve Rounsley (10) , Christopher L Schardl (3) , David C Schwartz (28) , Narmada Shenoy (10) , Ken Shirasu (16) , Usha R Sikhakolli (33) , Kurt Stüber (31) , Serenella A Sukno (30) , James A Sweigard (34) , Yoshitaka Takano (35) , Hiroyuki Takahara (1) , Frances Trail (33) , Charlotte H van Der Does (1) , Lars M Voll (36) , Isa Will (1) , Sarah Young (10) , Qiandong Zeng (10) , Jingze Zhang (10) , Shiguo Zhou (28) , Martin B Dickman (37) , Paul Schulze-Lefert (1) , Emiel Ver Loren van Themaat (1) , Li-Jun Ma (10) , Lisa J Vaillancourt (3)

1 Department of Plant Microbe Interactions
2 Centro Hispano-Luso de Investigaciones Agrarias, Departamento de Microbiología y Genétic
3 Department of Plant Pathology
4 1. Department of Plant Microbe Interactions
5 Fungal Biodiversity Centre
6 3. Department of Plant Pathology
7 Department of Plant Pathology
8 6. Department of Postharvest Science of Fresh Produce, Agricultural Research Organizati
9 Cologne Center for Genomics
10 Broad Institute [Cambridge]
11 GATC Biotech AG [Konstanz]
12 Center for Genomics
13 10. Department of Agricultural Biotechnology, Center for Fungal Genetic Resources
14 Systematic Mycology and Microbiology Laboratory
15 DuPont Agricultural Biotechnology
16 Plant Immunity Research Group
17 AFMB - Architecture et fonction des macromolécules biologiques
18 15. Department of Plant Pathology and Microbiology, Institute for Plant Genomics and Biotechnology, Borlaug Genomics and Bioinformatics Center, Texas
19 Department of Biology, Division of Biochemistry, Friedrich-Alexander
20 Laboratory of Plant Pathology, Graduate School of Life and Environmental Sciences
21 BIOGER - BIOlogie et GEstion des Risques en agriculture
22 6. Department of Postharvest Science of Fresh Produce, Agricultural Research Organization
23 Department of Computer Science
24 Central Microscopy
25 Department of Plant Developmental Biology
26 Division of Plant and Soil Sciences
27 Institute for Biology I, Unit of Plant Molecular Cell Biology, Rheinisch-Westfälische Technische Hochschule
28 Laboratory for Molecular and Computational Genomics
29 Agriculture Research Service, National Center for Agricultural Utilization Research
30 2. Centro Hispano-Luso de Investigaciones Agrarias, Departamento de Microbiología y Genética
31 MP-GC - Max Planck-Genome-centre Cologne
32 Department of Plant Pathology
33 Department of Plant Biology
34 DuPont Agricultural Biotechnology,
35 Laboratory of Plant Pathology, Graduate School of Agriculture
36 Department of Biology, Division of Biochemistry
37 Department of Plant Pathology and Microbiology, Institute for Plant Genomics and Biotechnology

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.

Mots clés: basal resistance; effectors; host status; nonhost; operative targe; specificity

Domaines: Sciences du Vivant [q-bio]

Richard J O'Connell, Michael R Thon, Stéphane Hacquard, Stefan G Amyotte, Jochem Kleeman, et al.. Lifestyle transitions in plant pathogenic Colletotrichum fungi deciphered by genome and transcriptome analyses. Nature Genetics, 2012, 44 (09), pp.1060-1065. ⟨10.1038/ng.2372⟩. ⟨hal-01191183⟩