Carboxylesterase and Cytochrome P450 Confer Metabolic Resistance Simultaneously to Azoxystrobin and Some Other Fungicides in Botrytis cinerea

J Agric Food Chem. 2024 May 1;72(17):9680-9690. doi: 10.1021/acs.jafc.4c02409. Epub 2024 Apr 18.

Abstract

Plant pathogens have frequently shown multidrug resistance (MDR) in the field, often linked to efflux and sometimes metabolism of fungicides. To investigate the potential role of metabolic resistance in B. cinerea strains showing MDR, the azoxystrobin-sensitive strain B05.10 and -resistant strain Bc242 were treated with azoxystrobin. The degradation half-life of azoxystrobin in Bc242 (9.63 days) was shorter than that in B05.10 (28.88 days). Azoxystrobin acid, identified as a metabolite, exhibited significantly lower inhibition rates on colony and conidia (9.34 and 11.98%, respectively) than azoxystrobin. Bc242 exhibited higher expression levels of 34 cytochrome P450s (P450s) and 11 carboxylesterase genes (CarEs) compared to B05.10 according to RNA-seq analysis. The expression of P450 genes Bcin_02g01260 and Bcin_12g06380, along with the CarEs Bcin_12g06360 in Saccharomyces cerevisiae, resulted in reduced sensitivity to various fungicides, including azoxystrobin, kresoxim-methyl, pyraclostrobin, trifloxystrobin, iprodione, and carbendazim. Thus, the mechanism of B. cinerea MDR is linked to metabolism mediated by the CarE and P450 genes.

Keywords: RNA sequence analysis; gene expression; metabolomic detoxification; multidrug resistance.

MeSH terms

  • Botrytis* / drug effects
  • Botrytis* / genetics
  • Carboxylesterase* / genetics
  • Carboxylesterase* / metabolism
  • Cytochrome P-450 Enzyme System* / genetics
  • Cytochrome P-450 Enzyme System* / metabolism
  • Drug Resistance, Fungal* / genetics
  • Fungal Proteins* / genetics
  • Fungal Proteins* / metabolism
  • Fungicides, Industrial* / metabolism
  • Fungicides, Industrial* / pharmacology
  • Methacrylates / metabolism
  • Methacrylates / pharmacology
  • Plant Diseases / microbiology
  • Pyrimidines* / metabolism
  • Pyrimidines* / pharmacology
  • Strobilurins* / chemistry
  • Strobilurins* / metabolism
  • Strobilurins* / pharmacology

Substances

  • Fungicides, Industrial
  • Strobilurins
  • Pyrimidines
  • Cytochrome P-450 Enzyme System
  • azoxystrobin
  • Fungal Proteins
  • Carboxylesterase
  • Methacrylates

Supplementary concepts

  • Botrytis cinerea