Population Genomics Provide Insights into the Global Genetic Structure of Colletotrichum graminicola, the Causal Agent of Maize Anthracnose
Flávia Rogério,
Riccardo Baroncelli,
Francisco Borja Cuevas-Fernández,
Sioly Becerra,
JoAnne Crouch,
Wagner Bettiol,
M. Andrea Azcárate-Peril,
Martha Malapi-Wight,
Veronique Ortega,
Javier Betran,
Albert Tenuta,
José S. Dambolena,
Paul D. Esker,
Pedro Revilla,
Tamra A. Jackson-Ziems,
Jürg Hiltbrunner,
Gary Munkvold,
Ivica Buhiniček,
José L. Vicente-Villardón,
Serenella A. Sukno,
Michael R. Thon
Affiliations
Flávia Rogério
Instituto de Investigación en Agrobiotecnología (CIALE), Departamento de Microbiología y Genética, Universidad de Salamanca, Salamanca, Spain
Riccardo Baroncelli
Instituto de Investigación en Agrobiotecnología (CIALE), Departamento de Microbiología y Genética, Universidad de Salamanca, Salamanca, Spain
Francisco Borja Cuevas-Fernández
Instituto de Investigación en Agrobiotecnología (CIALE), Departamento de Microbiología y Genética, Universidad de Salamanca, Salamanca, Spain
Sioly Becerra
Instituto de Investigación en Agrobiotecnología (CIALE), Departamento de Microbiología y Genética, Universidad de Salamanca, Salamanca, Spain
JoAnne Crouch
Foreign Disease and Weed Science Unit, United States Department of Agriculture, Fort Detrick, Maryland, USA
Wagner Bettiol
Embrapa Environment, Jaguariúna, São Paulo, Brazil
M. Andrea Azcárate-Peril
Center for Gastrointestinal Biology and Disease, Department of Medicine, School of Medicine, University of North Carolina, Chapel Hill, North Carolina, USA
Martha Malapi-Wight
USDA Animal and Plant Health Inspection Services, Biotechnology Regulatory Services, Riverdale, Maryland, USA
Veronique Ortega
Syngenta Seeds La Grangette, Lombez, France
Javier Betran
Bayer Crop Science/Monsanto SAS, Monbequi, France
Albert Tenuta
Ontario Ministry of Agriculture, Food, and Rural Affairs, University of Guelph-Ridgetown, Ridgetown, Ontario, Canada
José S. Dambolena
Facultad de Ciencias Exactas Físicas y Naturales, Universidad Nacional de Córdoba, IMBIV-CONICET-ICTA, Córdoba, Argentina
Paul D. Esker
Department of Plant Pathology and Environmental Microbiology, The Pennsylvania State University, State College, Pennsylvania, USA
Pedro Revilla
Misión Biológica de Galicia, Spanish National Research Council (CSIC), Pontevedra, Spain
Tamra A. Jackson-Ziems
Department of Plant Pathology, University of Nebraska-Lincoln, Nebraska, USA
Jürg Hiltbrunner
Federal Department of Economic Affairs, Zurich, Switzerland
Gary Munkvold
Department of Plant Pathology and Microbiology, Iowa State University, Ames, Iowa, USA
Ivica Buhiniček
BC Institute for Breeding and Production of Field Crops, Dugo Selo, Croatia
José L. Vicente-Villardón
Statistics Department, University of Salamanca, Salamanca, Spain
Serenella A. Sukno
Instituto de Investigación en Agrobiotecnología (CIALE), Departamento de Microbiología y Genética, Universidad de Salamanca, Salamanca, Spain
Michael R. Thon
Instituto de Investigación en Agrobiotecnología (CIALE), Departamento de Microbiología y Genética, Universidad de Salamanca, Salamanca, Spain
ABSTRACT Understanding the genetic diversity and mechanisms underlying genetic variation in pathogen populations is crucial to the development of effective control strategies. We investigated the genetic diversity and reproductive biology of Colletotrichum graminicola isolates which infect maize by sequencing the genomes of 108 isolates collected from 14 countries using restriction site-associated DNA sequencing (RAD-seq) and whole-genome sequencing (WGS). Clustering analyses based on single-nucleotide polymorphisms revealed three genetic groups delimited by continental origin, compatible with short-dispersal of the pathogen and geographic subdivision. Intra- and intercontinental migration was observed between Europe and South America, likely associated with the movement of contaminated germplasm. Low clonality, evidence of genetic recombination, and high phenotypic diversity were detected. We show evidence that, although it is rare (possibly due to losses of sexual reproduction- and meiosis-associated genes) C. graminicola can undergo sexual recombination. Our results support the hypotheses that intra- and intercontinental pathogen migration and genetic recombination have great impacts on the C. graminicola population structure. IMPORTANCE Plant pathogens cause significant reductions in yield and crop quality and cause enormous economic losses worldwide. Reducing these losses provides an obvious strategy to increase food production without further degrading natural ecosystems; however, this requires knowledge of the biology and evolution of the pathogens in agroecosystems. We employed a population genomics approach to investigate the genetic diversity and reproductive biology of the maize anthracnose pathogen (Colletotrichum graminicola) in 14 countries. We found that the populations are correlated with their geographical origin and that migration between countries is ongoing, possibly caused by the movement of infected plant material. This result has direct implications for disease management because migration can cause the movement of more virulent and/or fungicide-resistant genotypes. We conclude that genetic recombination is frequent (in contrast to the traditional view of C. graminicola being mainly asexual), which strongly impacts control measures and breeding programs aimed at controlling this disease.
