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

• Published in: PLoS genetics Vol. 16; no. 12; p. e1009291
• Main Authors: Miller, Marisa E, Nazareno, Eric S, Rottschaefer, Susan M, Riddle, Jakob, Dos Santos Pereira, Danilo, Li, Feng, Nguyen-Phuc, Hoa, Henningsen, Eva C, Persoons, Antoine, Saunders, Diane G O, Stukenbrock, Eva, Dodds, Peter N, Kianian, Shahryar F, Figueroa, Melania
• Format: Journal Article
• Language: English
• Published: United States Public Library of Science 28-12-2020; Public Library of Science (PLoS)
• Subjects: Asexuality; Avena - microbiology; Biology and Life Sciences; Diseases and pests; Epidemics; Evolution; Fungi; Gene Frequency; Genes; Genes, Fungal; Genetic aspects; Genetic diversity; Genomes; Hybridization; Infections; Leucine; Medicine and Health Sciences; Mutation; Oats; Pathogens; Physiological aspects; Plant diseases; Plant population genetics; Polymorphism, Genetic; Population; Population genetics; Principal components analysis; Puccinia - genetics; Puccinia - pathogenicity; Puccinia coronata avenae; Pucciniales; Recombination; Rust diseases; Rust fungi; Selection, Genetic; Virulence; Virulence (Microbiology); Virulence - genetics; United Kingdom; United States > US; North America
• ISSN: 1553-7404; 1553-7390; 1553-7404
• DOI: 10.1371/journal.pgen.1009291

Pathogen populations are expected to evolve virulence traits in response to resistance deployed in agricultural settings. However, few temporal datasets have been available to characterize this process at the population level. Here, we examined two temporally separated populations of Puccinia coronata f. sp. avenae (Pca), which causes crown rust disease in oat (Avena sativa) sampled from 1990 to 2015. We show that a substantial increase in virulence occurred from 1990 to 2015 and this was associated with a genetic differentiation between populations detected by genome-wide sequencing. We found strong evidence for genetic recombination in these populations, showing the importance of the alternate host in generating genotypic variation through sexual reproduction. However, asexual expansion of some clonal lineages was also observed within years. Genome-wide association analysis identified seven Avr loci associated with virulence towards fifteen Pc resistance genes in oat and suggests that some groups of Pc genes recognize the same pathogen effectors. The temporal shift in virulence patterns in the Pca populations between 1990 and 2015 is associated with changes in allele frequency in these genomic regions. Nucleotide diversity patterns at a single Avr locus corresponding to Pc38, Pc39, Pc55, Pc63, Pc70, and Pc71 showed evidence of a selective sweep associated with the shift to virulence towards these resistance genes in all 2015 collected isolates.