Abstract
Succinate dehydrogenase inhibitors (SDHIs) are an important group of fungicides (FRAC Group 7) for the control of Venturia inaequalis. Mechanisms which lead to reduced SDHI sensitivity in fungi are based on mutations in the SDH-subunits B, C, or D of the target gene. Monitoring studies have shown that most of the European population is still sensitive to SDHIs. Single cases of SDHI resistance have been detected shortly after market introduction although mainly at trial sites. The underlying resistance mechanisms have been identified as target site mutations (B-T258I, C-N85S and C-H151R). However, these were single findings which did not increase in frequency or even disappeared when the same field was analyzed one or more seasons later. This is in contrast to findings on other resistance cases which are stable over several seasons even without selection pressure, such as QoI and benzimidazole resistance. High frequencies of target site mutations for QoIs and benzimidazoles (G143A and E198A, respectively) have been detected in a 2022 survey, whereas no SDHI target site mutation exceeded the detection limit of our molecular detection assay in any sample.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
Bowen, J. K., Mesarich, C. H., Bus, V. G., Beresford, R. M., Plummer, K. M., & Templeton, M. D. (2011). Venturia inaequalis: The causal agent of apple scab. Molecular Plant Pathology, 12, 105–122. https://doi.org/10.1111/j.1364-3703.2010.00656.x
Carisse, O., & Bernier, J. (2002). Effect of environmental factors on growth, pycnidial production and spore germination of Microsphaeropsis isolates with biocontrol potential against apple scab. Mycological Research, 106, 1455–1462. https://doi.org/10.1017/s0953756202006858
Chapman, K. S., Sundin, G. W., & Beckerman, J. L. (2011). Identification of resistance to multiple fungicides in field populations of Venturia inaequalis. Plant Disease, 95, 921–926. https://doi.org/10.1094/PDIS-12-10-0899
Chatzidimopoulos, M., Lioliopoulou, F., Sotiropoulos, T., & Vellios, E. (2020). Efficient control of apple scab with targeted spray applications. Agronomy, 10, 1–9. https://doi.org/10.3390/agronomy10020217
Dooley, H., Shaw, M. W., Mehenni-Ciz, J., Spink, J., & Kildea, S. (2016). Detection of Zymoseptoria tritici SDHI-insensitive field isolates carrying the SdhC-H152R and SdhD-R47W substitutions. Pest Management Science, 72, 2203–2207. https://doi.org/10.1002/ps.4269
EPPO. (2015). Efficacy evaluation of plant protection products. Resistance risk analysis PP 1/213 (4). Bulletin OEPP/EPPO, 45, 371–387.
Farber, R. B., Chin, K. M., & Leadbitter, N. (2002). Sensitivity of Venturia inaequalis to trifloxystrobin. Pest Management Science, 58, 261–267. https://doi.org/10.1002/ps.443
FRAC. (2013). Protocol of the discussions and use recommendations of the SDHI Working Group of the Fungicide Resistance Action Committee (FRAC). https://www.frac.info/docs/default-source/working-groups/sdhi-meeting-minutes/minutes-of-the-2013-sdhi-meeting-recommendations-for-2014.pdf?sfvrsn=c934459a_2. Accessed 4 May 2023.
FRAC. (2015). Protocol of the discussions and use recommendations of the SDHI Working Group of the Fungicide Resistance Action Committee (FRAC). https://www.frac.info/docs/default-source/working-groups/sdhi-meeting-minutes/minutes-of-the-2015-sdhi-meeting-recommendations-for-2016.pdf?sfvrsn=47d4a9a_2. Accessed 4 May 2023.
FRAC. (2019). Pathogen Risk List. https://www.frac.info/docs/default-source/publications/pathogen-risk/frac-pathogen-list-2019.pdf?sfvrsn=caf3489a_2. Accessed 4 May 2023
FRAC. (2023). Protocol of the discussions and use recommendations of the SDHI Working Group of the Fungicide Resistance Action Committee (FRAC). https://www.frac.info/docs/default-source/working-groups/sdhi-fungicides/sdhi-meeting-minutes/minutes-of-the-2023-sdhi-meeting-with-recommendations-for-2023-from-17-18th-jan-2023.pdf?sfvrsn=d74c4e9a_2. Accessed 7 May 2023.
Germer, S., Holland, M. J., & Higuchi, R. (2000). High-throughput SNP allele-frequency determination in pooled DNA samples by kinetic PCR. Genome Research, 10, 258–266. https://doi.org/10.1101/gr.10.2.258
Grasso, V., Palermo, S., Sierotzki, H., Garibaldi, A., & Gisi, U. (2006). Cytochrome b gene structure and consequences for resistance to Qo inhibitor fungicides in plant pathogens. Pest Management Science, 62, 465–472. https://doi.org/10.1002/ps.1236
Hoffmeister, M., Martens, G., Yarnell, L., Blain, N., Wieja, B., Riediger, N., & Stammler, G. (2021b). Method for QoI sensitivity monitoring in Colletotrichum lentis by a species-specific pyrosequencing assay. Canadian Journal of Plant Pathology, 44, 128–135. https://doi.org/10.1080/07060661.2021.1958010
Hoffmeister, M., Zito, R., Böhm, J., & Stammler, G. (2021a). Mutations in Cyp51 of Venturia inaequalis and their effects on DMI sensitivity. Journal of Plant Diseases and Protection, 128, 1467–1478. https://doi.org/10.1007/s41348-021-00516-0
Huf, A. (2016). Untersuchungen zur Sensitivität von Venturia inaequalis gegenüber Succinat-Dehydrogenase Inhibitoren. Universität Hohenheim.
Huf, A., Rehfuß, A., Teichmann, M., Gold, R., Stammler, G. (2017). Sensitivity of Venturia inaequalis to Fungicides In Deising HB, Fraaije B, Mehl A, Oerke EC, Sierotzki H, Stammler G (Eds), Modern Fungicides and Antifungal Compounds VIII DPG, pp 197–198.
Kiebacher, H., & Hoffmann, G. M. (1976). Resistance against benzimidazole fungicides in Venturia inaequalis. Journal of Plant Diseases and Protection, 83, 352–358.
Koch, A., Felsenstein, F., & Stammler, G. (2015). No evidence of QoI resistance in apple powdery mildew (Podosphaera leucotricha). Journal of Phytopathology, 163, 178–184. https://doi.org/10.1111/jph.12302
Koenraadt, H., Somerville, S. C., & Jones, A. L. (1992). Characterization of mutations in the beta-tubulin gene of benomyl-resistant field strains of Venturia inaequalis and other plant pathogenic fungi. Phytopathology, 82, 1348–1354.
Mondino, P., Casanova, L., Celio, A., Bentancur, O., Leoni, C., & Alaniz, S. (2015). Sensitivity of Venturia inaequalis to trifloxystrobin and difenoconazole in Uruguay. Journal of Phytopathology, 163, 1–10. https://doi.org/10.1111/jph.12274
Passey, T. A. J., Robinson, J. D., Shaw, M. W., & Xu, X. M. (2017). The relative importance of conidia and ascospores as primary inoculum of Venturia inaequalis in a southeast England orchard. Plant Pathology, 66, 1445–1451. https://doi.org/10.1111/ppa.12686
Rehfus, A., Matusinsky, P., Strobel, D., Bryson, R., & Stammler, G. (2019). Mutations in target genes of succinate dehydrogenase inhibitors and demethylation inhibitors in Ramularia collo-cygni in Europe. Journal of Plant Diseases and Protection, 126, 447–459. https://doi.org/10.1007/s41348-019-00246-4
Rehfus, A., Miessner, S., Achenbach, J., Strobel, D., Bryson, R., & Stammler, G. (2016). Emergence of succinate dehydrogenase inhibitor resistance of Pyrenophora teres in Europe. Pest Management Science, 72, 1977–1988. https://doi.org/10.1002/ps.4244
Rehfus, A., Strobel, D., Bryson, R., & Stammler, G. (2017). Mutations in sdh genes in field isolates of Zymoseptoria tritici and impact on the sensitivity to various succinate dehydrogenase inhibitors. Plant Pathology, 67, 175–180. https://doi.org/10.1111/ppa.12715
Schmitz, H., Mehl, A., Kerz-Möhlendick, F. Punktmutationen (2014) Am Zielgen der SDHI Fungizide – Relevanz für den Getreidebau? In Kühn-Institut J (Ed) 59. Deutsche Pflanzenschutztagung, Albert-Ludwigs-Universität Freiburg, Julius Kühn-Archiv, p 185.
Schmitz, H., Mehl, A., Kleemann, J. (2015). Relevance of point mutations in the target gene of SDHI fungicides for growing cereals. In: Feldmann F, Heinrichs EAS (Eds) XVIII International Plant Protection Congress.
Sierotzki, H., & Stammler, G. (2019). Chapter 8: Resistance of plant pathogens to QoI fungicides (FRAC Code 11). In K. L. Stevenson, M. T. McGrath, & C. A. Wyenandt (Eds.), Fungicide resistance in North America (pp. 97–113). APS Press.
Simões, K., Hawlik, A., Rehfus, A., Gava, F., & Stammler, G. (2017). First detection of a SDH variant with reduced SDHI sensitivity in Phakopsora pachyrhizi. Journal of Plant Diseases and Protection, 125, 21–26. https://doi.org/10.1007/s41348-017-0117-5
Welle, M. (2017). Fitness of Venturia inaequalis and Zymoseptoria tritici strains with reduced sensitivity to succinate dehydrogenase inhibitor fungicides. Masterthesis: Ruprecht-Karls-Universität Heidelberg.
Acknowledgements
The authors thank Gabriele Berthold from BASF SE for excellent technical assistance, and EpiLogic GmbH for the sensitivity evaluation and providing isolates for further investigations.
Funding
Not applicable.
Author information
Authors and Affiliations
Contributions
All authors contributed in a comparable extend to the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
Authors are employees of BASF SE, the manufacturer of fluxapyroxad.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Hoffmeister, M., Scheu, P., Glaab, A. et al. Sensitivity evolution in Venturia inaequalis towards SDHIs in comparison to other modes of action. Eur J Plant Pathol 168, 763–773 (2024). https://doi.org/10.1007/s10658-023-02798-6
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10658-023-02798-6