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Front. Microbiol. | doi: 10.3389/fmicb.2018.00276

Genome-Wide Analysis of Corynespora cassiicola Leaf Fall Disease Putative Effectors

David Lopez1, Sébastien Ribeiro2, 3, Philippe Label1, Boris Fumanal1,  Jean-Stéphane Venisse1,  Annegret Kohler4, Ricardo R. de Oliveira5, Kurt Labutti6, Anna Lipzen6, Kathleen Lail6, Diane Bauer6, Robin A. Ohm6, Kerry W. Barry6,  Joseph Spatafora7,  Igor V. Grigoriev8, 9,  Francis M. Martin4 and  Valérie Pujade-Renaud2, 10, 11*
  • 1INRA Physique et physiologie Intégratives de l'Arbre fruitier et Forestier, France
  • 2Université Clermont Auvergne, France
  • 3Université de Montpellier, France
  • 4INRA UMR1136 Interactions Arbres-Microorganismes, France
  • 5Departemento de Agronomia, Universidade Estadual de Maringà, Brazil
  • 6United States Department of Energy, Joint Genome Institute (DOE), United States
  • 7Department of Botany and Plant Pathology, Oregon State University, United States
  • 8Department of Plant and Microbial Biology, University of California Berkeley, United States
  • 9United States Department of Energy, Joint Genome Institute (DOE), United States
  • 10INRA UMR Amélioration génétique et adaptation des plantes méditerranéennes et tropicales, France
  • 11UMR AGAP, Centre de coopération internationale en recherche agronomique pour le développement (CIRAD), France

Corynespora cassiicola is an Ascomycetes fungus with a broad host range and diverse life styles. Mostly known as a necrotrophic plant pathogen, it has also been associated with rare cases of human infection. In the rubber tree, this fungus causes the Corynespora leaf fall (CLF) disease, which increasingly affects natural rubber production in Asia and Africa. It has also been found as an endophyte in South American rubber plantations where no CLF outbreak has yet occurred. The C. cassiicola species is genetically highly diverse, but no clear relationship has been evidenced between phylogenetic lineage and pathogenicity. Cassiicolin, a small glycosylated secreted protein effector, is thought to be involved in the necrotrophic interaction with the rubber tree but some virulent C. cassiicola isolates do not have a cassiicolin gene. This study set out to identify other putative effectors involved in CLF. The genome of a highly virulent C. cassiicola isolate from the rubber tree (CCP) was sequenced and assembled. In silico prediction revealed 2870 putative effectors, comprising CAZymes, lipases, peptidases, secreted proteins and enzymes associated with secondary metabolism. Comparison with the genomes of 44 other fungal species, focusing on effector content, revealed a striking proximity with phylogenetically unrelated species (Colletotrichum acutatum, Colletotrichum gloesporioides, Fusarium oxysporum, nectria hematococca and Botrosphaeria dothidea) sharing life style plasticity and broad host range. Candidate effectors involved in the compatible interaction with the rubber tree were identified by transcriptomic analysis. Differentially expressed genes included 92 putative effectors, among which cassiicolin and two other secreted singleton proteins. Finally, the genomes of 35 C. cassiicola isolates representing the genetic diversity of the species were sequenced and assembled, and putative effectors identified. At the intraspecific level, effector-based classification was found to be highly consistent with the phylogenomic trees. Identification of lineage-specific effectors is a key step toward understanding C. cassiicola virulence and host specialization mechanisms.

Keywords: Corynespora cassiicola, Hevea brasiliensis, Plant-pathogens interaction, Effectors, Cassiicolin, Genomics, Gene Expression

Received: 28 Jul 2017; Accepted: 07 Feb 2018.

Edited by:

Gail Preston, University of Oxford, United Kingdom

Reviewed by:

Guus Bakkeren, Agriculture and Agri-Food Canada (AAFC), Canada
Bryan Bailey, United States Department of Agriculture, United States  

Copyright: © 2018 Lopez, Ribeiro, Label, Fumanal, Venisse, Kohler, de Oliveira, Labutti, Lipzen, Lail, Bauer, Ohm, Barry, Spatafora, Grigoriev, Martin and Pujade-Renaud. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

* Correspondence: Dr. Valérie Pujade-Renaud, Université Clermont Auvergne, Clermont-Ferrand, France, valerie.pujade-renaud@cirad.fr