Increased virulence of Puccinia coronata f. sp.avenae populations through allele frequency changes at multiple putative Avr loci

Authors: MILLER, MARISA - University Of Minnesota; NAZARENO, ERIC - University Of Minnesota; ROTTSCHAEFER, SUSAN - University Of Minnesota; Riddle, Jakob; DOS SANTOS PEREIRA, DANILO - Brazilian Agricultural Research Corporation (EMBRAPA); LI, FENG - University Of Minnesota; NGUYEN-PHUC, HOA - University Of Minnesota; HENNINGSEN, EVA - University Of Minnesota; PERSOONS, ANTOINE - Institut National De La Recherche Agronomique (INRA); SAUNDERS, DIANE - John Innes Center; STUKENBROCK, EVA - Max Planck Institute Of Molecular Plant Physiology; DODDS, PETER - Commonwealth Scientific And Industrial Research Organisation (CSIRO); Kianian, Shahryar; FIGUEROA, MELANIA - Commonwealth Scientific And Industrial Research Organisation (CSIRO)

Submitted to: PLoS Genetics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/4/2020
Publication Date: 12/28/2020
Citation: Miller, M.E., Nazareno, E.S., Rottschaefer, S.M., Riddle, J.M., Dos Santos Pereira, D.A., Li, F., Nguyen-Phuc, H., Henningsen, E., Persoons, A., Saunders, D.G., Stukenbrock, E., Dodds, P., Kianian, S.F., Figueroa, M. 2020. Increased virulence of Puccinia coronata f. sp.avenae populations through allele frequency changes at multiple putative Avr loci. PLoS Genetics. 16(12). Article e1009291. https://doi.org/10.1371/journal.pgen.1009291.
DOI: https://doi.org/10.1371/journal.pgen.1009291

Interpretive Summary: Oat crown rust, caused by Puccinia coronata f. sp. avenae (Pca), is a major disease of cultivate oat and has global impact on grain production. Disease management strategies for oat crown rust rely heavily on breeding for race-specific resistance. However, Pca rapidly evolves virulence to new resistance genes and field populations are highly polymorphic with high numbers of races (pathotypes), which limits the efficacy of this approach. This has coincided with a dramatic decline in U.S. oat production. Here, we apply a population genomic approach to dissect important aspects of the evolutionary trajectory of Pca in the U.S. Pca populations from 1990 and 2015 showed a drastic shift to broader virulence and whole-genome sequencing demonstrated extensive genetic differentiation between these populations likely as a result of in situ evolution. An analysis identified seven Avr loci associated with virulence phenotypes on fifteen Pc resistance genes in oat and provided evidence that some groups of Pc genes recognize the same pathogen effectors. The outcomes of this study underscore the value of population genomic-based approaches to characterize the population structure, determine the demographic factors that contribute to the pathogen evolution in the field and identify key virulence loci.

Technical Abstract: Puccinia coronata f. sp. avenae (Pca) is the causal agent of crown rust disease in cultivated oat (Avena sativa) and has a global impact on grain production. In recent decades, the management of crown rust has become more challenging as populations of this pathogen now display virulence to the vast majority of previously resistant oat cultivars. This has coincided with a dramatic decline in U.S. oat production. Here, we apply a population genomic approach to dissect important aspects of the evolutionary trajectory of Pca in the U.S. Pca populations from 1990 and 2015 showed a drastic shift to broader virulence and whole-genome sequencing demonstrated extensive genetic differentiation between these populations likely as a result of in situ evolution. Substantial genetic variation and linkage disequilibrium decay indicated a strong influence of sexual reproduction in these populations, but we also observed evidence of long-distance migration within the U.S. and the expansion of some clonal lineages within a season. A GWAS analysis identified seven Avr loci associated with virulence phenotypes on fifteen Pc resistance genes in oat and provided evidence that some groups of Pc genes recognize the same pathogen effectors. A selective sweep at a single Avr locus corresponding to Pc38, Pc39, Pc55, Pc63, Pc70, Pc71 is associated with a shift to virulence on these resistance genes in the 2015 population. The outcomes of this study underscore the value of population genomic-based approaches to characterize the population structure, determine the demographic factors that contribute to the pathogen evolution in the field and identify key virulence loci.