Genome evolution and transcriptome plasticity is associated with adaptation to monocot and dicot plants in Colletotrichum fungi

Author:

Baroncelli Riccardo12ORCID,Cobo-Díaz José F3ORCID,Benocci Tiziano4ORCID,Peng Mao5ORCID,Battaglia Evy5,Haridas Sajeet6ORCID,Andreopoulos William6ORCID,LaButti Kurt6ORCID,Pangilinan Jasmyn6ORCID,Lipzen Anna6ORCID,Koriabine Maxim6,Bauer Diane6ORCID,Le Floch Gaetan7ORCID,Mäkelä Miia R8ORCID,Drula Elodie910ORCID,Henrissat Bernard91011ORCID,Grigoriev Igor V612ORCID,Crouch Jo Anne13ORCID,de Vries Ronald P5ORCID,Sukno Serenella A2ORCID,Thon Michael R2ORCID

Affiliation:

1. Department of Agricultural and Food Sciences (DISTAL) , University of Bologna, Viale Fanin 40-50, 40127 Bologna , Italy

2. Department of Microbiology and Genetics, Institute for Agribiotechnology Research (CIALE) , University of Salamanca, Calle del Duero, 37185 Villamayor, Salamanca , Spain

3. Department of Food Hygiene and Technology and Institute of Food Science and Technology , University of León, Campus Vegazana, 24007 León , Spain

4. Center for Health and Bioresources , Austrian Institute of Technology (AIT), Konrad-Lorenz-Straße 24, 3430 Tulln an der Donau , Austria

5. Westerdijk Fungal Biodiversity Institute & Fungal Molecular Physiology , Fungal Physiology, Utrecht University, Uppsalalaan 8, 3584 CT Utrecht , The Netherlands

6. Joint Genome Institute, Lawrence Berkeley National Laboratory , United States Department of Energy, McMillan rd, CA 94720 Berkeley , USA

7. Laboratory of Biodiversity and Microbial Ecology (LUBEM) , IBSAM, ESIAB, EA 3882, University of Brest, Technopôle Brest-Iroise, Parv. Blaise Pascal, 29280 Plouzané , France

8. Department of Microbiology, Faculty of Agriculture and Forestry , University of Helsinki, Siltavuorenpenger 5, 00170 Helsinki , Finland

9. UMR 7257, Architecture et Fonction des Macromolécules Biologiques, The French National Centre for Scientific Research (CNRS) , University of Aix-Marseille (AMU), 163 Avenue de Luminy, Parc Scientifique et Technologique de Luminy, 13288 Marseille , France

10. The French National Institute for Agricultural Research (INRA) , USC 1408 AFMB, 163 Avenue de Luminy, Parc Scientifique et Technologique de Luminy, 13288 Marseille , France

11. Department of Biological Sciences , King Abdulaziz University, 23453 Jeddah , Saudi Arabia

12. Department of Plant and Microbial Biology , University of California Berkeley, Berkeley, CA , USA

13. Mycology and Nematology Genetic Diversity and Biology Laboratory , Agricultural Research Service, United States Department of Agriculture, 10300 Baltimore Ave, MD 20705, Beltsville , USA

Abstract

Abstract Background Colletotrichum fungi infect a wide diversity of monocot and dicot hosts, causing diseases on almost all economically important plants worldwide. Colletotrichum is also a suitable model for studying gene family evolution on a fine scale to uncover events in the genome associated with biological changes. Results Here we present the genome sequences of 30 Colletotrichum species covering the diversity within the genus. Evolutionary analyses revealed that the Colletotrichum ancestor diverged in the late Cretaceous in parallel with the diversification of flowering plants. We provide evidence of independent host jumps from dicots to monocots during the evolution of Colletotrichum, coinciding with a progressive shrinking of the plant cell wall degradative arsenal and expansions in lineage-specific gene families. Comparative transcriptomics of 4 species adapted to different hosts revealed similarity in gene content but high diversity in the modulation of their transcription profiles on different plant substrates. Combining genomics and transcriptomics, we identified a set of core genes such as specific transcription factors, putatively involved in plant cell wall degradation. Conclusions These results indicate that the ancestral Colletotrichum were associated with dicot plants and certain branches progressively adapted to different monocot hosts, reshaping the gene content and its regulation.

Publisher

Oxford University Press (OUP)

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