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

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 corona...

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Main Authors: Marisa E Miller, Eric S Nazareno, Susan M Rottschaefer, Jakob Riddle, Danilo Dos Santos Pereira, Feng Li, Hoa Nguyen-Phuc, Eva C Henningsen, Antoine Persoons, Diane G O Saunders, Eva Stukenbrock, Peter N Dodds, Shahryar F Kianian, Melania Figueroa
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2020-12-01
Series:PLoS Genetics
Online Access:https://doi.org/10.1371/journal.pgen.1009291
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spelling doaj-3667cf86ce814d169463213d836792972021-04-21T14:34:20ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042020-12-011612e100929110.1371/journal.pgen.1009291Increased virulence of Puccinia coronata f. sp.avenae populations through allele frequency changes at multiple putative Avr loci.Marisa E MillerEric S NazarenoSusan M RottschaeferJakob RiddleDanilo Dos Santos PereiraFeng LiHoa Nguyen-PhucEva C HenningsenAntoine PersoonsDiane G O SaundersEva StukenbrockPeter N DoddsShahryar F KianianMelania FigueroaPathogen 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.https://doi.org/10.1371/journal.pgen.1009291
collection DOAJ
language English
format Article
sources DOAJ
author Marisa E Miller
Eric S Nazareno
Susan M Rottschaefer
Jakob Riddle
Danilo Dos Santos Pereira
Feng Li
Hoa Nguyen-Phuc
Eva C Henningsen
Antoine Persoons
Diane G O Saunders
Eva Stukenbrock
Peter N Dodds
Shahryar F Kianian
Melania Figueroa
spellingShingle Marisa E Miller
Eric S Nazareno
Susan M Rottschaefer
Jakob Riddle
Danilo Dos Santos Pereira
Feng Li
Hoa Nguyen-Phuc
Eva C Henningsen
Antoine Persoons
Diane G O Saunders
Eva Stukenbrock
Peter N Dodds
Shahryar F Kianian
Melania Figueroa
Increased virulence of Puccinia coronata f. sp.avenae populations through allele frequency changes at multiple putative Avr loci.
PLoS Genetics
author_facet Marisa E Miller
Eric S Nazareno
Susan M Rottschaefer
Jakob Riddle
Danilo Dos Santos Pereira
Feng Li
Hoa Nguyen-Phuc
Eva C Henningsen
Antoine Persoons
Diane G O Saunders
Eva Stukenbrock
Peter N Dodds
Shahryar F Kianian
Melania Figueroa
author_sort Marisa E Miller
title Increased virulence of Puccinia coronata f. sp.avenae populations through allele frequency changes at multiple putative Avr loci.
title_short Increased virulence of Puccinia coronata f. sp.avenae populations through allele frequency changes at multiple putative Avr loci.
title_full Increased virulence of Puccinia coronata f. sp.avenae populations through allele frequency changes at multiple putative Avr loci.
title_fullStr Increased virulence of Puccinia coronata f. sp.avenae populations through allele frequency changes at multiple putative Avr loci.
title_full_unstemmed Increased virulence of Puccinia coronata f. sp.avenae populations through allele frequency changes at multiple putative Avr loci.
title_sort increased virulence of puccinia coronata f. sp.avenae populations through allele frequency changes at multiple putative avr loci.
publisher Public Library of Science (PLoS)
series PLoS Genetics
issn 1553-7390
1553-7404
publishDate 2020-12-01
description 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.
url https://doi.org/10.1371/journal.pgen.1009291
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