title: Fungal adaptation to contemporary fungicide applications: the case of Botrytis cinerea populations from Champagne vineyards (France).
abstract: In addition to being one of the most acute problems impeding chemical control of fungal diseases, the evolution of fungicide resistance is an emblematic case of local adaptation to spatially heterogeneous and temporally variable selection pressures. Here we dissected the adaptation of Botrytis cinerea (the causal agent of grey mould) populations on grapes to several fungicides. We carried out a 2-year survey (four collection dates) on three treated/untreated pairs of plots from vineyards in Champagne (France) and monitored the frequency of four resistant phenotypes that are unambiguously associated with four distinct genotypes. For two loci under selection by currently used fungicides (MDR1 and MDR2), the frequencies of resistant mutations at vintage were greater in treated plots compared to untreated plots, showing that the effect of selection is detectable even at the plot scale. This effect was not detectable for two other loci under selection by previously used fungicides (BenR1 and ImiR1). We also found that treatment with currently used fungicides reduced B. cinerea effective population size, leading to a significant decrease in genic diversity and allelic richness in treated vs. untreated plots. We further highlight that even under ample drift and migration, fungal populations can present an efficient response to selection. Finally, for the four studied loci, the costs of fungicide resistance were estimated by modelling the decrease in the frequency of resistant mutations in the absence of treatment. We discuss the importance of these estimates for defining strategies for limiting or counteracting the local adaptation of pests to fungicides.
authors.affiliation: UMR BIOGER, INRA, AgroParisTech, Université Paris-Saclay, Avenue Lucien Brétignières, 78850, Thiverval-Grignon, France.
authors.forename: A-S
authors.identifier: http://orcid.org/0000-0002-1246-246X
authors.initials: AS
authors.lastname: Walker
authors.affiliation: CIRAD, UMR PVBMT, 97410, Saint-Pierre, Réunion, France.|CIRAD, UMR BGPI, 34398, Montpellier, France.
authors.forename: V
authors.initials: V
authors.lastname: Ravigne
authors.affiliation: CIRAD, UMR PVBMT, 97410, Saint-Pierre, Réunion, France.|CIRAD, UMR BGPI, 34398, Montpellier, France.
authors.forename: A
authors.initials: A
authors.lastname: Rieux
authors.affiliation: UMR BGPI, INRA, CIRAD, Montpellier SupAgro, TA A 54/K, Campus international de Baillarguet, 34398, Montpellier Cedex 5, France.|Institute of Biotechnology & Genetic Engineering, The University of Agriculture, Peshawar, 25000, Pakistan.
authors.forename: S
authors.initials: S
authors.lastname: Ali
authors.affiliation: UMR BIOGER, INRA, AgroParisTech, Université Paris-Saclay, Avenue Lucien Brétignières, 78850, Thiverval-Grignon, France.
authors.forename: F
authors.initials: F
authors.lastname: Carpentier
authors.affiliation: UMR BGPI, INRA, CIRAD, Montpellier SupAgro, TA A 54/K, Campus international de Baillarguet, 34398, Montpellier Cedex 5, France.
authors.forename: E
authors.initials: E
authors.lastname: Fournier
mesh_terms: D018435:ATP Binding Cassette Transporter, Subfamily B / Q000235:genetics; D020168:ATP Binding Cassette Transporter, Subfamily B, Member 1 / Q000235:genetics; D000222:Adaptation, Physiological / Q000235:genetics*; D020171:Botrytis / Q000187:drug effects / Q000235:genetics*; D025141:Drug Resistance, Fungal / Q000235:genetics*; D005602:France; D005656:Fungal Proteins / Q000235:genetics; D005659:Fungicides, Industrial / Q000494:pharmacology*; D005787:Gene Frequency; D056426:Genetic Loci; D005838:Genotype; D010641:Phenotype; D010935:Plant Diseases / Q000382:microbiology; D062211:Spatio-Temporal Analysis; D027843:Vitis / Q000382:microbiology; D000097202:ATP-Binding Cassette Sub-Family B Member 4
chemical_list: D018435:ATP Binding Cassette Transporter, Subfamily B; D020168:ATP Binding Cassette Transporter, Subfamily B, Member 1; D005656:Fungal Proteins; D005659:Fungicides, Industrial; D000097202:ATP-Binding Cassette Sub-Family B Member 4
keywords: diversity; fungicide resistance modelling; migration; resistance cost; selection