Resistance to Fluopyram, Fluxapyroxad, and Penthiopyrad in Botrytis cinerea from Strawberry

Succinate dehydrogenase inhibitors (SDHIs) constitute a mainstay in management of gray mold caused by Botrytis cinerea in strawberry and several other crops. In this study, we investigated the risks of resistance development to three newer SDHIs (i.e., fluopyram, fluxapyroxad, and penthiopyrad) and their cross-resistance with the previously registered boscalid. We investigated the mutations in the SdhB subunit and evaluated their impact on microbial fitness in field populations of B. cinerea. Amino acid substitutions associated with resistance to SDHIs were detected at three codons of the SdhB subunit (B-H272R/Y/L, B-P225F, and B-N230I) in the succinate dehydrogenase gene of field isolates from Florida. The B-H272R, B-H272Y, B-H272L, B-P225F, and B-N230I mutations were detected at frequencies of 51.5, 28.0, 0.5, 2.5, and 4%, respectively. Strong cross-resistance patterns were evident between boscalid and fluxapyroxad and penthiopyrad but not with fluopyram, except in B-H272L, B-P225F, and B-N230I mutants. All five mutations conferred moderate to very high resistance to boscalid whereas the B-H272Y conferred resistance to fluxapyroxad and penthiopyrad. The B-H272L, B-N230I, and B-P225F mutations conferred high resistance to all four SDHIs tested. Resistance monitoring following the first use of penthiopyrad in strawberry fields in Florida in 2013 suggests potential for quick selection for highly resistant populations and warrants careful use of the newer SDHIs. No evidence of major fitness costs due to the mutations in the SdhB subunit was found, which indicates the potential ability of the mutants to survive and compete with wild-type isolates. Our study suggests high risks for rapid widespread occurrence of B. cinerea populations resistant to the novel SDHIs unless appropriate rotation strategies are implemented immediately upon registration.