Resistance to Site-Specific Succinate Dehydrogenase Inhibitor Fungicides Is Pervasive in Populations of Black and Yellow Sigatoka Pathogens in Banana Plantations from Southeastern Brazil

Author:

Silva Tatiane C.12,Moreira Silvino I.13ORCID,de Souza Daniel M.1ORCID,Christiano Felix S.1,Gasparoto Maria C. G.4ORCID,Fraaije Bart A.5ORCID,Goldman Gustavo H.26,Ceresini Paulo C.1ORCID

Affiliation:

1. Department of Crop Protection, Agricultural Engineering and Soil, Faculty of Engineering, São Paulo State University—UNESP, Ilha Solteira 15385-000, Brazil

2. Faculty of Pharmaceutical Sciences of Ribeirão Preto (FCFRP), University of São Paulo, São Paulo 14040-900, Brazil

3. Department of Plant Pathology, Federal University of Lavras—UFLA, Lavras 37200-000, Brazil

4. Faculty of Agricultural Sciences from Ribeira Valley, São Paulo State University—UNESP, Registro 11900-000, Brazil

5. Business Unit Biointeractions & Plant Health, Wageningen University & Research, 6700 AA Wageningen, The Netherlands

6. National Institute of Science and Technology in Human Pathogenic Fungi, São Paulo 14040-900, Brazil

Abstract

The Sigatoka disease complex (SDC), caused by Mycosphaerella fijiensis (Mf) and M. musicola (Mm), comprises the most destructive fungal leaf streak and spot diseases of commercial banana crops worldwide. In Brazil, the site-specific succinate dehydrogenase inhibitor (SDHI) fungicides labeled for SDC management since 2014 present a high risk for the emergence of resistance if deployed intensively and solo. Our study determined the levels of sensitivity to boscalid and fluxapyroxad in four populations of the SDC pathogens sampled in 2020 from three distinct geographical regions under contrasting fungicide programs. Resistance, defined as EC50 values exceeding 20 µg mL−1, was prevalent at 59.7% for fluxapyroxad and 94.0% for boscalid. Only 1.5% of isolates exhibited sensitivity to both fungicides. We also assessed the changes in the corresponding fungicide target protein-encoding genes (SdhB, C, and D). None of the target site alterations detected were associated with reduced sensitivity. A second SdhC paralog was also analyzed, but target alterations were not found. However, MDR (multidrug resistance) was detected in a selection of isolates. Further monitoring for Sdh target mutations will be important, but an important role for other resistance mechanisms such as the presence of additional Sdh paralogs and MDR cannot be ruled out. These results highlight the importance of implementing sound anti-resistance management strategies when SDHI fungicides are deployed for the management of SDC.

Funder

São Paulo Research Foundation

Brazilian National Council for Scientific and Technological Development

Newton Fund/BBSRC

Coordination for the Improvement of Higher Level Personnel

São Paulo State University’s Vice-Presidency for Research

Joint Canada-Israel Health Research Program

Publisher

MDPI AG

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