Abstract
Pydiflumetofen is a new succinate dehydrogenase inhibitor fungicide, registered in China in 2021 for the control of tomato gray mold. In order to characterize and decipher the sensitivity of tomato B. cinerea to pydiflumetofen, the sensitivity to pydiflumetofen was determined in 103 B. cinerea isolates collected from diseased tomato fruits and leaves from greenhouses in eight districts of Liaoning province in China during 2020–2022. The results indicated that for the 76 tested isolates, the EC50 values of pydiflumetofen conformed to a normal distribution. The mean EC50 value was determined to be 1.0641 ± 0.5820 (SD) μg/mL and was considered as the baseline sensitivity. Thirty-two resistant isolates were detected, corresponding to a resistance frequency of 31.07%. Differences were observed in mycelium growth rate and dry weight, spore production, and spore germination rate among isolates, which were not associated with resistance to pydiflumetofen. However, the resistant isolates had lower pathogenicity compared to the sensitive isolates. No cross-resistance was observed between pydiflumetofen and fludioxonil, pyrimethanil procymidone, and iprodione. Some resistant isolates had mutations in the SdhB subunit gene (N230I, H272R). These results indicated a moderate to high risk of pydiflumetofen resistance development in B. cinerea. Therefore, pydiflumetofen should be used in an alternating or mixed application with fungicides with no cross-resistance and not more than twice per season to delay resistance development.
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11 June 2024
A Correction to this paper has been published: https://doi.org/10.1007/s10658-024-02899-w
References
Amiri, A., Heath, S. M., & Peres, N. A. (2013). Phenotypic characterization of multi-fungicide resistance in Botrytis cinerea isolates from strawberry fields in Florida. Plant Disease, 97(3), 393–401. https://doi.org/10.1094/pdis-08-12-0748-re
Amiri, A., Heath, S. M., & Peres, N. A. (2014). Resistance to fluopyram, fluxapyroxad, and penthiopyrad in Botrytis cinerea from strawberry. Plant Disease, 98(4), 532–539. https://doi.org/10.1094/pdis-07-13-0753-re
Bi, Q. Y., Lu, F., Yang, K., Wu, J., Zhang, S. Q., Han, X. Y., Wang, W. Q., & Zhao, J. J. (2022). Baseline sensitivity and resistance of Botrytis cinerea to penthiopyrad in Hebei Province, China. Horticulturae, 8(8), 686. https://doi.org/10.3390/horticulturae8080686
Breunig, M., & Chilvers, M. I. (2021). Baseline sensitivity of Fusarium graminearum from wheat, corn, dry bean and soybean to pydiflumetofen in Michigan, USA. Crop Protection, 140, 105419. https://doi.org/10.1016/j.cropro.2020.105419
De Miccolis Angelini, R. M., Rotolo, C., Masiello, M., Gerin, D., Pollastro, S., & F-aretra, F. (2014). Occurrence of fungicide resistance in populations of Botryotinia fuckeliana (Botrytis cinerea) on table grape and strawberry in southern Italy. Pest Management Science, 70(12), 1785–1796. https://doi.org/10.1002/ps.3711
Fan, F., Hamada, M. S., Li, N., Li, G. Q., & Luo, C. X. (2017). Multiple fungicide resistance in Botrytis cinerea from greenhouse strawberries in Hubei province, China. Plant Disease, 101(4), 601–606.
Fernández-Ortuño, D., Chen, F., & Schnabel, G. (2012). Resistance to pyraclostrobin and boscalid in Botrytis cinerea isolates from strawberry fields in the Carolinas. Plant Disease, 96(8), 1198–1203.
Fernández-Ortuño, D., Pérez-García, A., Chamorro, M., de la Peña, E., de Vicente, A., & Torés, J. A. (2017). Resistance to the SDHI fungicides boscalid, fluopyram, fluxapyroxad, and penthiopyrad in Botrytis cinerea from commercial strawberry fields in Spain. Plant Disease, 101(7), 1306–1313.
Fraaije, B. A., Bayon, C., Atkins, S., Cools, H. J., Lucas, J. A., & Fraaije, M. W. (2012). Risk assessment studies on succinate dehydrogenase inhibitors, the new weapons in the battle to control Septoria leaf blotch in wheat. Molecular Plant Pathology, 13(3), 263–275. https://doi.org/10.1111/j.1364-3703.2011.00746.x
Gao, P., Zeng, R., Gao, S., Xu, L., Song, Z., & Dai, F. (2023). Resistance Profiles of Botrytis cinerea to Fluxapyroxad from Strawberry Fields in Shanghai, China. Plant Disease, 107(9), 2724–2728. https://doi.org/10.1094/pdis-10-22-2416-re
Hagerhall, C. (1997). Succinate: quinone oxidoreductases. Variations on a conserved t-heme. Biochimica et Biophysica Acta, 1320, 107–141. https://doi.org/10.1016/S0005-2728(97)00019-4
Hauschildt, M., Steinkellner, S., & Weber, R. W. S. (2020). Grey mold populations in northern German sweet cherry and plum orchards: selection of fungicide-resistant Botrytis cinerea strains over sensitive B. pseudocinerea by fungicide treatments. European Journal of Plant Pathology, 157(3), 615–623. https://doi.org/10.1007/s10658-020-02026-5
He, L., Cui, K., Song, Y., Li, T., Liu, N., Mu, W., & Liu, F. (2020). Activity of the novel succinate dehydrogenase inhibitor fungicide pydiflumetofen against SDHI-sensitive and resistant isolates of Botrytis cinerea and efficacy against gray mold. Plant Disease, 104(8), 2168–2173. https://doi.org/10.1094/pdis-12-19-2564-re
Horsefield, R., Yankovskaya, V., Sexton, G., Whittingham, W., Shiomi, K., Ōmura, S., Byrne, B., Cecchini, G., & Iwata, S. (2006). Structural and computational analysis of the quinone-binding site of complex II (succinate-ubiquinone oxidoreductase): a mechanism of electron transfer and proton conduction during ubiquinone reduction. Journal of Biological Chemistry, 281, 7309–7316. https://doi.org/10.1074/jbc.m508173200
Hou, Y.-P., Mao, X.-W., Wang, J.-X., Zhan, S.-W., & Zhou, M.-G. (2017). Sensitivity of Fusarium asiaticum to a novel succinate dehydrogenase inhibitor fungicide pydiflumetofen. Crop Protection, 96, 237–244. https://doi.org/10.1016/j.cropro.2017.02.011
Hu, M. J., Fernández-Ortuño, D., & Schnabel, G. (2016). Monitoring resistance to S-DHI fungicides in Botrytis cinerea from strawberry fields. Plant Disease, 100(5), 959–965. https://doi.org/10.1094/pdis-10-15-1210-re
Hu, W. Q. (2020). Research progresses in resistance of plant pathogenic fungi to suc-cinate dehydrogenase inhibitors. World Pesticide, 42(12), 1–5. https://doi.org/10.16201/j.cnki.cn10-1660/tq.2020.12.01. (In Chinese).
Konstantinou, S., Veloukas, T., Leroch, M., Menexes, G., Hahn, M., & Karaoglanidis, G. (2015). Population structure, fungicide resistance profile, and sdhB mutation freq-uency of Botrytis cinerea from strawberry and greenhouse-grown tomato in Greece. P-lant Disease, 99(2), 240–248. https://doi.org/10.1094/pdis-04-14-0373-re
Lalève, A., Gamet, S., Walker, A. S., Debieu, D., Toquin, V., & Fillinger, S. (2014). Site-directed mutagenesis of the P225, N230 and H272 residues of succinate dehydrogenase subunit B from Botrytis cinerea highlights different roles in enzyme activity an-d inhibitor binding. Environmental Microbiology, 16(7), 2253–2266. https://doi.org/10.1111/1462-2920.12282
Leroux, P., Gredt, M., Leroch, M., & Walker, A. S. (2010). Exploring mechanisms of resistance to respiratory inhibitors in field strains of Botrytis cinerea, the causal agen-t of gray mold. Applied and Environmental Microbiology, 76(19), 6615–6630. https://doi.org/10.1128/aem.00931-10
Liu, S. M., Che, Z. P., & Chen, G. Q. (2016). Multiple-fungicide resistance to carbe-ndazim, diethofencarb, procymidone, and pyrimethanil in field isolates of Botrytis cin-erea from tomato in Henan Province. China. Crop Protection, 84(06), 56–61. https://doi.org/10.1016/j.cropro.2016.02.012
Liu, S., Fu, L., Tan, H., Jiang, J., Che, Z., Tian, Y., & Chen, G. (2021). Resistance to boscalid in Botrytis cinerea from greenhouse grown tomato. Plant Disease, 105(3), 628–635. https://doi.org/10.1094/pdis-06-20-1191-re
Mercier, A., Carpentier, F., Duplaix, C., Auger, A., Pradier, J. M., Viaud, M., Gladieux, P., & Walker, A. S. (2019). The polyphagous plant pathogenic fungus Botrytis cinerea encompasses host-specialized and generalist populations. Environmental Microbiology, 21(12), 4808–4821. https://doi.org/10.1111/1462-2920.14829
Nielsen, B. J., Jensen, N. L., Hartvig, P., Hjelmroth, L., & Weber, R. W. S. (2021). Fungicide resistance in Botrytis in Danish strawberry production. Erwerbs-Obstbau, 63(1), 1–6. https://doi.org/10.1007/s10341-021-00541-1
Oyedotun, K. S., & Lemire, B. D. (2004). The quaternary structure of the Saccharomyces cerevisiae succinate dehydrogenase-homology modeling, cofactor docking and molecular dynamics simulation studies. Journal of Biological Chemistry, 279, 9424–9431. https://doi.org/10.1074/jbc.M311876200
Rathi, S., McFeeters, H., McFeeters, R. L., & Davis, M. R. (2012). Purification and phytotoxic analysis of Botrytis cinerea virulence factors: new avenues for crop protection. Agriculture, 2(3), 154–164. https://doi.org/10.3390/agriculture2030154
Rodríguez, A., Acosta, A., & Rodríguez, C. (2014). Fungicide resistance of Botrytis cinerea in tomato greenhouses in the Canary Islands and effectiveness of non-chemical treatments against gray mold. World Journal of Microbiology & Biotechnology, 30(9), 2397–2406. https://doi.org/10.1007/s11274-014-1665-5
Rupp, S., Weber, R. W., Rieger, D., Detzel, P., & Hahn, M. (2016). Spread of Botrytis cinerea strains with multiple fungicide resistance in German horticulture. Frontiers in Microbiology, 7, 2075. https://doi.org/10.3389/fmicb.2016.02075
Sierotzki, H., & Scalliet, G. (2013). A review of current knowledge of resistance aspects for the next-generation succinate dehydrogenase inhibitor fungicide. Phytopathology, 103(9), 880–887. https://doi.org/10.1094/phyto-01-13-0009-rvw
Song, Y. F. (2019). Detection of the sensitivity of Botrytis cinerea to six succinate dehydrogenase inhibitors fungicides and study of resistance mechanism to boscalid in Shandong Province. MA thesis. Shandong Agricultural University. https://doi.org/10.27277/d.cnki.gsdnu.2019.000085(In Chinese).
Song, Y., Zhang, Z., Chen, L., He, L., Lu, H., Ren, Y., Mu, W., & Liu, F. (2016). B-aseline sensitivity of Botrytis cinerea to the succinate dehydrogenase inhibitor isopyrazam and efficacy of this fungicide. Plant Disease, 100, 1314–1320. https://doi.org/10.1094/pdis-10-15-1220-re
Thomas, A., Langston, D. B., Jr., & Stevenson, K. L. (2012). Baseline Sensitivity and Cross-Resistance to Succinate-Dehydrogenase-Inhibiting and Demethylation-Inhibiting Fungicides in Didymella bryoniae. Plant Disease, 96, 979–984. https://doi.org/10.1094/pdis-09-11-0744-re
Veloukas, T., Kalogeropoulou, P., Markoglou, A. N., & Karaoglanidis, G. S. (2014). Fitness and competitive ability of Botrytis cinerea field isolates with dual resistance to SDHI and QoI fungicides, associated with several sdhB and the cytb G143A mutations. Phytopathology, 104(4), 347–356. https://doi.org/10.1094/phyto-07-13-0208-r
Veloukas, T., Leroch, M., Hahn, M., & Karaoglanidis, G. S. (2011). Detection and molecular characterization of boscalid-resistant Botrytis cinerea isolates from Strawberry. Plant Disease, 95(10), 1302–1307. https://doi.org/10.1094/pdis-04-11-0317
Veloukas, T., Markoglou, A. N., & Karaoglanidis, G. S. (2013). Differential effect of sdhB gene mutations on the sensitivity to SDHI fungicides in Botrytis cinerea. Plant Disease, 97(1), 118–122. https://doi.org/10.1094/pdis-03-12-0322-re
Wang, Y., Wang, M. M., Xu, L. T., Sun, Y., & Feng, J. T. (2020). Baseline sensitivity and toxic action of the sterol demethylation inhibitor flusilazole against Botrytis cin-erea. Plant Disease, 104, 2986–2993. https://doi.org/10.1094/pdis-11-19-2478-re
Weber, R. W. S., Entrop, A.-P., Goertz, A., & Mehl, A. (2015). Status of sensitivity of Northern German Botrytis populations to the new SDHI fungicide fluopyram prior to its release as a commercial fungicide. Journal of Plant Diseases and Protection, 122(2), 81–90. https://doi.org/10.1007/BF03356535
Williamson, B., Tudzynski, B., Tudzynski, P., & van Kan, J. A. (2007). Botrytis cine-rea: The cause of grey mold disease. Molecular Plant Pathology, 8(5), 561–580. https://doi.org/10.1111/j.1364-3703.2007.00417.x
Wu, L. T., Liu, J. N., Wang, K., Pan, S., & Qi, Z. Q. (2023). Baseline sensitivity and resistance analysis of fluopyram against Botrytis cinerea from tomato in Liaoning Province, China. Journal of Phytopathology, 171(9), 421–429. https://doi.org/10.1111/JPH.13199
Yang, K. X., Bi, Q. Y., Wu, J., Lu, F., Wang, W. Q., Han, X. Y., & Zhao, J. J. (2022). Characterization of Botrytis cinerea isolates with different sensitivity types to py-diflumetofen. Chinese Journal of Pesticide Science, 24(04), 743–751. https://doi.org/10.16801/j.issn.1008-7303.2022.0053. (In Chinese).
Zhao, J., Lu, F., Wu, J., Ma, Z., Han, X., & Wang, W. (2018). Sensitivity of Botrytis cinerea from greenhouses in Hebei Province to boscalid and fludioxonil. Acta Phytopathologica Sinica, 48(06), 817–821. https://doi.org/10.13926/j.cnki.apps.000135. (In Chinese).
Zhao, J., Wu, J., Lu, F., Bi, Q., Yang, K., Han, X., & Wang, W. (2022). Baselinesen-sitivity of Botrytis cinerea to pydiflumetofen and its efficacy on tomato gray mold in Hebei Province, China. Crop Protection, 158, 105989. https://doi.org/10.1016/j.cropro.2022.105989
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Thanks to the Project of Liaoning Provincial Department of Education (LJKMZ20221045) for supporting this work.
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Shiqing Chen, Zhiqiu Qi, Liting Wu and Zian Zhao wrote the manuscript. Shiqing Chen and Yi Li conducted experiments and performed the data analysis and interpretation of the results. Zhiqiu Qi designed the project.
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Chen, S., Wu, L., Li, Y. et al. Baseline sensitivity and resistance analysis of Botrytis cinerea to pydiflumetofen in Liaoning Province, China. Eur J Plant Pathol (2024). https://doi.org/10.1007/s10658-024-02880-7
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DOI: https://doi.org/10.1007/s10658-024-02880-7