Population genomics provide insights into the global genetic structure of Colletotrichum graminicola, the causal agent of maize anthracnose

Authors: ROGÉRIO, FLÁVIA - University Of Salamanca; BARONCELLI, RICCARDO - University Of Salamanca; CUEVAS-FERNÁNDEZ, FRANCISCO - University Of Salamanca; BECERRA, SIOLY - University Of Salamanca; Crouch, Jo Anne; BETTIOL, WAGNER - Embrapa; AZCÁRATE-PERIL, M. ANDREA - University Of North Carolina; MALAPI-WIGHT, MARTHA - Animal And Plant Health Inspection Service (APHIS); ORTEGA, VERONIQUE - Syngenta Seeds, Inc; BETRAN, JAVIER - Bayer Cropscience; TENUTA, ALBERT - University Of Guelph; DAMBOLENA, JOSE - Universidad De Cordoba; ESKER, PAUL - Pennsylvania State University; REVILLA, PEDRO - Spanish National Research Council; JACKSON-ZIEMS, TAMARA - University Of Nebraska; HILTBRUNNER, JURG - Agroscope; MUNKVOLD, GARY, - Iowa State University; VICENTE-VILLARDÓN, JOSÉ - University Of Salamanca; SUKNO, SERENELLA - University Of Salamanca; THON, MICHAEL - University Of Salamanca

Submitted to: bioRxiv
Publication Type: Other
Publication Acceptance Date: 5/7/2022
Publication Date: 5/10/2022
Citation: Rogério, F., Baroncelli, R., Cuevas-Fernández, F., Becerra, S., Crouch, J., Bettiol, W., Azcárate-Peril, M., Malapi-Wight, M., Ortega, V., Betran, J., Tenuta, A., Dambolena, J.S., Esker, P.D., Revilla, P., Jackson-Ziems, T., Hiltbrunner, J., Munkvold, G., Vicente-Villardón, J., Sukno, S., Thon, M. 2022. Population genomics provide insights into the global genetic structure of Colletotrichum graminicola, the causal agent of maize anthracnose. bioRxiv. https://doi.org/10.1101/2022.05.07.490914.
DOI: https://doi.org/10.1101/2022.05.07.490914

Interpretive Summary: Anthracnose disease can have a profoundly negative impact on corn production worldwide. Although corn anthracnose first emerged as a problem in the 1970s, the origins of the disease in the U.S. and globally remains unknown. Therefore, the genome sequences of 108 samples of the corn anthracnose pathogen collected from 14 countries were sequenced and compared. The research showed that geographic origin strongly impacts pathogen genetic type. Three unique genetic groups were each present on a single continent: North America, South America, or Europe. North American populations showed more than twice as much genetic diversity and a separate evolutionary history from populations on other continents. European populations showed little genetic diversity, consistent with the introduction of a single genetic type that spread by making clones of itself. The presence of European genotypes in Argentina suggests long distance migration of the pathogen, possibly through the movement of corn germplasm through breeding programs. Virulence was not correlated with genetic profiles, and a wide range of virulence was characterized worldwide. Since the effectiveness of genetic resistance depends on knowledge of the genetic structure of pathogens, the findings from this research supports efforts to breed anthracnose-resistant corn. This research is also important because it shows how spread of the corn anthracnose fungus has occurred and suggests how it will continue to move globally and in the U.S.

Technical Abstract: Colletotrichum graminicola, the causal agent of maize anthracnose, is an important crop disease worldwide. Understanding the genetic diversity and mechanisms underlying genetic variation in pathogen populations is crucial to the development of effective control strategies. The genus Colletotrichum is largely recognized as asexual, but several species have been reported to have a sexual cycle. Here, we employed a population genomics approach to investigate the genetic diversity and reproductive biology of C. graminicola isolates infecting maize. We sequenced 108 isolates of C. graminicola collected in 14 countries using restriction site-associated DNA sequencing (RAD-Seq) and whole-genome sequencing (WGS). Results: Clustering analyses based on single-nucleotide polymorphisms showed populational differentiation at a global scale, with three genetic groups delimited by continental origin, compatible with short-dispersal of the pathogen, and geographic subdivision. Distinct levels of genetic diversity were observed between these clades, suggesting different evolutionary histories. Intra and inter-continental migration was predicted between Europe and South America, likely associated with the movement of contaminated germplasm. Low clonality and evidence of genetic recombination were detected 51 from the analysis of linkage disequilibrium and the pairwise homoplasy index (PHI) test for clonality. We show evidence that even if rare (possibly due to losses of sex and meiosis-associated genes) C. graminicola can undergo sexual recombination based on lab assays and genomic analyses. Conclusions: Our results support hypotheses of intra and intercontinental pathogen migration and genetic recombination with great impact on C. graminicola population structure.