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Abstract
Crop protection anilinopyrimidine (AP) fungicides were introduced more than 20 years ago for the control of a range of diseases caused by ascomycete plant pathogens, and in particular for the control of gray mold caused by Botrytis cinerea. Although early mode of action studies suggested an inhibition of methionine biosynthesis, the molecular target of this class of fungicides was never fully clarified. Despite AP-specific resistance having been described in B. cinerea field isolates and in multiple other targeted species, the underlying resistance mechanisms were unknown. It was therefore expected that the genetic characterization of resistance mechanisms would permit the identification of the molecular target of these fungicides. In order to explore the widest range of possible resistance mechanisms, AP-resistant B. cinerea UV laboratory mutants were generated and the mutations conferring resistance were determined by combining whole-genome sequencing and reverse genetics. Genetic mapping from a cross between a resistant field isolate and a sensitive reference isolate was used in parallel and led to the identification of an additional molecular determinant not found from the characterized UV mutant collection. Together, these two approaches enabled the characterization of an unrivaled diversity of resistance mechanisms. In total, we report the elucidation of resistance-conferring mutations within nine individual genes, two of which are responsible for almost all instances of AP resistance in the field. All identified resistance-conferring genes encode proteins that are involved in mitochondrial processes, suggesting that APs primarily target the mitochondria. The functions of these genes and their possible interactions are discussed in the context of the potential mode of action for this important class of fungicides.
Highlights
Anilinopyrimidine (AP) fungicides were introduced into the crop protection market between 1992 and 1995
In order to facilitate the identification of anilinopyrimidine (AP) resistance-conferring mutations, UV mutants were generated in vitro using the reference B. cinerea strain B05.10, for which a well-annotated genome sequence is available (Van Kan et al, 2017)
The identification of 9 different mitochondrial proteins conferring resistance to AP fungicides very strongly supports the hypothesis of a mitochondrial target
Summary
Anilinopyrimidine (AP) fungicides were introduced into the crop protection market between 1992 and 1995. AP fungicides are currently classified as potential methionine biosynthesis inhibitors (FRAC1 target code D1). This classification emerged from early mode of action studies mainly performed on B. cinerea, which displayed partial reversal of growth inhibition when sulfur-containing amino acids, and in particular methionine or its upstream metabolite homocysteine, were added to minimal culture media containing the fungicide (Leroux, 1994; Masner et al, 1994; Leroux et al, 1995). The lack of reversal by cystathionine, a metabolite one step before homocysteine, suggested the mode of action could be methionine biosynthesis inhibition through the inhibition of cystathionine β-lyase (Masner et al, 1994; Fritz et al, 1997). Methionine and homocysteine reversal studies performed with Penicillium digitatum failed to show any reversal effect, suggesting that the metabolite-chemical interaction observed in Botrytis may be due to an indirect species-specific effect (Kanetis et al, 2008)
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