Oomycete Fungicides: Phenylamides, Quinone Outside Inhibitors, and Carboxylic Acid Amides

Abstract

Oomycetes are “fungal-like” protista that are phylogenetically distinct from fungi, they are diploid, and cell walls contain cellulose. Oomycetes comprise major plant pathogens within the orders Saprolegniales, Pythiales, Peronosporales (“downy mildews” including species of Plasmopara, Phytophthora, Peronospora, Pseudoperonospora, Bremia), and Sclerosporales. Control of oomycete diseases relies mainly on chemical measures using products within 16 different chemical groups, among which the phenylamides (PAs), quinone outside inhibitors (QoIs), carboxylic acid amides (CAAs), and multisite inhibitors are most widely used. However, resistance evolved against most single-site inhibitors in many oomycete pathogen species. Resistance against PAs (inhibitors of RNA polymerase I) was detected in most oomycete pathogen species; the molecular mechanism was associated recently with the presence of the Y382F mutation in the RNApolI gene. QoIs inhibit electron transport in complex III of the respiration chain; two major mutations, G143A (in Plasmopara viticola) and F129L (in Pythium spp.), have been identified in the cytochrome b, cyt b gene coding for resistance. However, no resistant isolates were observed in Phytophthora species. CAAs inhibit cellulose synthase; several mutations, G1105S/V (in P. viticola) and G1105V/W (in Pseudoperonospora cubensis), were detected in the cellulose synthase, CesA3 gene of CAA-resistant field isolates. In Phytophthora infestans and P. capsici, no CAA-resistant field isolates were discovered, whereas in artificial mutants, the mutations G1105A/V and V1109L/M were found. The L1109 and M1109 amino acid configurations are responsible for the intrinsic insensitivity to CAAs of the entire genus Pythium and all oomycetes outside Peronosporales. Resistance is inherited by one recessive nuclear gene (CesA3) for CAAs, one maternal mitochondrial gene (cytb) for QoIs, and mainly one semidominant nuclear gene for PAs. The consequences of the molecular mechanisms for evolution and stability of resistance are discussed in the light of oomycete pathogen biology.