Multilocus resistance evolution to azole fungicides in fungal plant pathogen populations

Norfarhan Mohd Assa`Ad, Bruce A. McDonald, Daniel Croll

Research output: Contribution to journalArticle

13 Citations (Scopus)

Abstract

Evolution of fungicide resistance is a major threat to food production in agricultural ecosystems. Fungal pathogens rapidly evolved resistance to all classes of fungicides applied to the field. Resistance to the commonly used azole fungicides is thought to be driven mainly by mutations in a gene (CYP51) encoding a protein of the ergosterol biosynthesis pathway. However, some fungi gained azole resistance independently of CYP51 mutations and the mechanisms leading to CYP51-independent resistance are poorly understood. We used whole-genome sequencing and genome-wide association studies (GWAS) to perform an unbiased screen of azole resistance loci in Rhynchosporium commune, the causal agent of the barley scald disease. We assayed cyproconazole resistance in 120 isolates collected from nine populations worldwide. We found that mutations in highly conserved genes encoding the vacuolar cation channel YVC1, a transcription activator, and a saccharopine dehydrogenase made significant contributions to fungicide resistance. These three genes were not previously known to confer resistance in plant pathogens. However, YVC1 is involved in a conserved stress response pathway known to respond to azoles in human pathogenic fungi. We also performed GWAS to identify genetic polymorphism linked to fungal growth rates. We found that loci conferring increased fungicide resistance were negatively impacting growth rates, suggesting that fungicide resistance evolution imposed costs. Analyses of population structure showed that resistance mutations were likely introduced into local populations through gene flow. Multilocus resistance evolution to fungicides shows how pathogen populations can evolve a complex genetic architecture for an important phenotypic trait within a short time span.

Original languageEnglish
Pages (from-to)6124-6142
Number of pages19
JournalMolecular Ecology
Volume25
Issue number24
DOIs
Publication statusPublished - 1 Dec 2016

Fingerprint

fungicide resistance
azoles
Azoles
fungicide
plant pathogens
fungicides
pathogen
mutation
Mutation
Genome-Wide Association Study
animal pathogenic fungi
Population
Saccharopine Dehydrogenases
saccharopine dehydrogenase
Rhynchosporium
Fungi
cyproconazole
scald diseases
Genes
genome

Keywords

  • agricultural ecosystem
  • genome-wide association mapping
  • plant pathogens
  • population genomics
  • Rhynchosporium commune
  • trade-offs

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics
  • Genetics

Cite this

Multilocus resistance evolution to azole fungicides in fungal plant pathogen populations. / Mohd Assa`Ad, Norfarhan; McDonald, Bruce A.; Croll, Daniel.

In: Molecular Ecology, Vol. 25, No. 24, 01.12.2016, p. 6124-6142.

Research output: Contribution to journalArticle

Mohd Assa`Ad, Norfarhan ; McDonald, Bruce A. ; Croll, Daniel. / Multilocus resistance evolution to azole fungicides in fungal plant pathogen populations. In: Molecular Ecology. 2016 ; Vol. 25, No. 24. pp. 6124-6142.
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