Identification of putative SDHI target site mutations in the SDHB, SDHC, and SDHD subunits of the grape powdery mildew pathogen Erysiphe necator

Authors: STERGIOPOULOS, IOANNIS - University Of California, Davis; AOUN, N - University Of California, Davis; HUYNH, QUE VAN - University Of California, Davis; Neill, Tara; LOWDER, SARAH - Oregon State University; NEWBOLD, CHELSEA - Oregon State University; COOPER, MONICA - University Of California; DING, SHUNPING - California Polytechnic State University; MOYER, MICHELLE - Washington State University; MILES, TIM - Michigan State University; OLIVER, CHARLOTTE - Washington State University; URBEZ-TORRES, JOSE RAMON - Agriculture And Agri-Food Canada; Mahaffee, Walter - Walt

Submitted to: Plant Disease
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/26/2022
Publication Date: 8/3/2022
Citation: Stergiopoulos, I., Aoun, N., Huynh, Q., Neill, T.M., Lowder, S., Newbold, C., Cooper, M.L., Ding, S., Moyer, M., Miles, T.D., Oliver, C.L., Urbez-Torres, J., Mahaffee, W.F. 2022. Identification of putative SDHI target site mutations in the SDHB, SDHC, and SDHD subunits of the grape powdery mildew pathogen Erysiphe necator. Molecular Plant Pathology. 106(9):2310-2320. https://doi.org/10.1094/PDIS-09-21-1993-RE.
DOI: https://doi.org/10.1094/PDIS-09-21-1993-RE

Interpretive Summary: Grape powdery mildew (GPM) management has been threatened by the development of fungicide resistance to DMI (dimethylesterase inhibitors) and strobilurin (QoI) fungicides, which has caused growers to use more SDHI (Succinate dehydrogenase inhibitors). In order to prevent the severe crop loss that appeared when GPM populations resistant to both DMI and QoI emerged, this work present results of work to develop genetic markers for monitoring the emergence of SDHI resistance and initial results from surveying GPM population for SDHI resistance in California, Oregon, Washington and Michigan, and the Canadian province of British Columbia. Results indicate that several genetic markers are likely associated with resistance in addition to unknown mechanisms. They also indicate the SDHI resistance is emerging and needs to monitored.

Technical Abstract: Succinate dehydrogenase inhibitors (SDHIs) are fungicides used in control of numerous fungal plant pathogens, including Erysiphe necator, the causal agent of grapevine powdery mildew (GPM). In this study, the sdhb, sdhc, and sdhd genes of E. necator were screened for mutations that may associate with SDHI resistance. GPM samples were collected from 2017 to 2020 from the U.S. states of California, Oregon, Washington and Michigan, and the Canadian province of British Columbia. Forty-five polymorphisms were identified in the three sdh genes, 17 of which affected missense mutations. Of these, the SDHC-p.H242R and SDHC-p.I244V substitutions are shown to reduce sensitivity of E. necator towards boscalid, and boscaclid and fluopyram, respectively, whereas the equivalents of the SDHB-p.H242L, SDHC-p.A83V, and SDHD-p.I71F substitutions are associated with increased SDHI tolerance in other fungi. In contrast, the SDHC-p.G25R substitution is shown not to affect SDHI sensitivity. Generally, only a single amino acid substitution was present in the SDHB, SDHC, or SDHD subunit of E. necator isolates, and only a few isolates had substitutions in more than one subunit. Most novel mutations appeared only sporadically in single years or sampling areas, but mutations linked to SDHI resistance were widely distributed in the sampled areas and increased in frequency from 2017 to 2020. Several isolates were also identified with increased tolerance towards boscalid or fluopyram but with no or only the SDHC-p.G25R amino acid substitution present in SDHB, SDHC, and SDHD subunits, suggesting that target-site mutations is not the only mechanism conferring resistance to SDHIs in E. necator.