Fitness of Venturia inaequalis isolates with resistance to multiple chemical classes of fungicides in vitro
Abstract
Background. The development of fungicide resistance in the apple scab pathogen suggests the development of measures to manage the development of resistance that can functionally delay the emergence of resistant populations of the pathogen. Knowledge of the pathogen's fitness is essential to applying this approach and assessing how successful it will be, since resistance may come with a fitness cost.
Purpose. To evaluate the fitness of sensitive Venturia inaequalis isolates and isolates with multiple fungicide resistances to osmotic and oxidative stress in vitro.
Methods. The size of isolates from four groups (a group with baseline sensitivity and three groups with different multiple resistances to fungicides) was evaluated on potato-glucose agar with the addition of various concentrations of NaCl (2, 3, 4, and 6%) and H2O2 (2, 5, and 10 mM).
Results. The inhibition of mycelium growth in variants with the addition of NaCl relative to the control occurred on average by about 10% with an increase in concentration of 1%. In all variants of the experiment, the average size of isolates in the initial group was smaller than in the pathogen groups with resistance to fungicides. Oxidative stress has the following effect on the average size of the isolates: in the control, it was 12.2 mm; at a concentration of H2O2, it was 2 mM–6.7 mm; and at 5 mM–1.3 mm. There was a tendency for the isolates to have a higher average size in the group with simultaneous resistance to two fungicides, compared with other groups at concentrations of H2O2 of 2 mM and 5 mM.
Conclusion. The absence of significant lower values of the average size of isolates in groups with multiple resistances to fungicides in comparison with the baseline group under in vitro stress conditions shows the absence of fitness cost.
Sponsorship information. The research was carried out with the financial support of the Kuban Science Foundation within the framework of the scientific project № MFI-20.1/98.
EDN: KAIYAV
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References
Ivanova, E. V., Nikishina, M. B., Tretyakova, A. V., Mukhtorov, L. G., Perelomov, L. V., & Atroschenko, Yu. M. (2021). Study of the fungicidal activity of new derivatives of 7-R-1,5-dinitro-3,7-diazabicyclo [3.3.1] nonane-2-one. Siberian Journal of Life Sciences & Agriculture, 13(5), 307-320. https://doi.org/10.12731/2658-6649-2021-13-5-307-320 EDN: https://elibrary.ru/xwvffk
Nasonov, A. I. (2019). A new method for obtaining Venturia inaequalis culture from ascospores. Mycology and Phytopathology, 53(1), 46-48. https://doi.org/10.1134/S0026364819010094 EDN: https://elibrary.ru/ytixyt
Nasonov, A. I., & Bardak, M. V. (2023). Morphotype composition and sensitivity to difenoconazole of populations of the apple scab pathogen differing in fungicide application history. Siberian Journal of Life Sciences and Agriculture, 15(3), 219-238. https://doi.org/10.12731/2658-6649-2023-15-3-219-238 EDN: https://elibrary.ru/qppsxf
Nasonov, A. I., Yakuba, G. V., & Astapchuk, I. L. (2021). Sensitivity of the Krasnodar population of Venturia inaequalis to difenoconazole, a sterol demethylation inhibitor. Mycology and Phytopathology, 55(4), 297-308. https://doi.org/10.31857/S0026364821040103 EDN: https://elibrary.ru/jahfjc
Nasonov, A. I., Yakuba, G. V., Astapchuk, I. L., & Marchenko, N. A. (2024). Sensitivity of initial and orchard populations of Venturia inaequalis to succinate dehydrogenase inhibitors (SDHI) fungicides. Siberian Journal of Life Sciences and Agriculture, 16(1), 189-210. https://doi.org/10.12731/2658-6649-2024-16-1-707 EDN: https://elibrary.ru/notwnf
Nasonov, A. I., Yakuba, G. V., Bardak, M. V., Astapchuk, I. L., & Marchenko, N. A. (2024). Characterization of the adaptability of Venturia inaequalis isolates resistant and sensitive to fungicides in vitro. Scientific Notes of Kazan University. Series: Natural Sciences, 166(1), 23-37. https://doi.org/10.26907/2542-064X.2024.1.23-37 EDN: https://elibrary.ru/djqcyr
Nasonov, A. I., Yakuba, G. V., & Lobodina, E. V. (2022). Long-term persistence of carbendazim resistance in Venturia inaequalis in the Krasnodar Territory (Russia). Mycology and Phytopathology, 56(5), 374-378. https://doi.org/10.31857/S0026364822050087 EDN: https://elibrary.ru/cmvduj
Pozhilova, E. V., Novikov, V. E., & Levchenkova, O. S. (2015). Reactive oxygen species in cell physiology and pathology. Bulletin of Smolensk State Medical Academy, 14(2), 13-22. EDN: https://elibrary.ru/uhovfr
Antonovics, J., Alexander, H. M. (1989). The concept of fitness in plant-fungal pathogen systems. Plant Disease Epidemiology, 2, 185-214.
Bardas, G. A., Myresiotis, C. K., Karaoglanidis, G. S. (2008). Stability and fitness of anilinopyrimidine-resistant strains of Botrytis cinerea. Phytopathology, 98(4), 443-450. https://doi.org/10.1094/PHYTO-98-4-0443
Bauske, M. J., Mallik, I., Yellareddygari, S. K. R., Gudmestad, N. C. (2018). Spatial and temporal distribution of mutations conferring QoI and SDHI resistance in Alternaria solani across the United States. Plant Disease, 102(2), 349-358. https://doi.org/10.1094/PDIS-06-17-0852-RE
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(8), 921-926. https://doi.org/10.1094/PDIS-12-10-0899
Dorigan, A. F., Moreira, S. I., Ceresini, P. C., Pozza, E. A., Belan, L. L., da Silveira, P. R., Alves, E. (2022). Higher fitness and competitive advantage of Pyricularia oryzae Triticum lineage resistant to QoI fungicides. Pest Management Science, 78(12), 5251-5258. https://doi.org/10.1002/ps.7144 EDN: https://elibrary.ru/bwmtoi
Dowling, M., Gelain, J., May De Mio, L. L., Schnabel, G. (2021). Characterization of high fludioxonil resistance in Botrytis cinerea isolates from Calibrachoa flowers. Phytopathology, 111(3), 478-484. https://doi.org/10.1094/phyto-07-20-0268-r EDN: https://elibrary.ru/idsdym
Fan, Z., Yang, J. H., Fan, F., Luo, C. X., Schnabel, G. (2015). Fitness and competitive ability of Alternaria alternata field isolates with resistance to SDHI, QoI and MBC fungicides. Plant Disease, 99(12), 1744-1750. https://doi.org/10.1094/PDIS-03-15-0354-RE
Fernández-Ortuño, D., Grabke, A., Bryson, P. K., Amiri, A., Peres, N. A., & Schnabel, G. (2014). Fungicide resistance profiles in Botrytis cinerea from strawberry fields of seven southern U.S. states. Plant Disease, 98(6), 825-833. https://doi.org/10.1094/PDIS-09-13-0970-RE
Fiaccadori, R. (2018). Persistence of Venturia inaequalis populations resistant to strobilurins in the field and in the glasshouse. American Journal of Plant Sciences, 9(4), 552-560. https://doi.org/10.4236/ajps.2018.94042
Frederick, Z. A., Villani, S. M., Cooley, D. R., Biggs, A. R., Raes, J. J., & Cox, K. D. (2014). Prevalence and stability of qualitative QoI resistance in populations of Venturia inaequalis in the Northeastern United States. Plant Disease, 98(8), 1122-1130. https://doi.org/10.1094/PDIS-10-13-1042-RE
Hammer, Ø., & Harper, D. A. (2001). Past: paleontological statistics software package for education and data analysis. Palaeontologia Electronica, 4(1), 1-9.
Karaoglanidis, G. S., Luo, Y., & Michailides, T. J. (2011). Competitive ability and fitness of Alternaria alternata isolates resistant to QoI fungicides. Plant Disease, 95(2), 178-182. https://doi.org/10.1094/PDIS-07-10-0510
Kim, Y. K., & Xiao, C. L. (2011). Stability and fitness of pyraclostrobin- and boscalid-resistant phenotypes in field isolates of Botrytis cinerea from apple. Phytopathology, 101(11), 1385-1391. https://doi.org/10.1094/PHYTO-04-11-0123
Lesniak, K. E., Proffer, T. J., Beckerman, J. L., & Sundin, G. W. (2011). Occurrence of QoI resistance and detection of the G143A mutation in Michigan populations of Venturia inaequalis. Plant Disease, 95(8), 927-934. https://doi.org/10.1094/PDIS-12-10-0898
Malandrakis, A. A., Vattis, K. N., Doukas, E. G., & Markoglou, A. N. (2013). Effect of phenylpyrrole-resistance on fitness parameters and ochratoxin production in Aspergillus carbonarius. International Journal of Food Microbiology, 165(3), 287-294. https://doi.org/10.1016/j.ijfoodmicro.2013.05.019
Mikaberidze, A., McDonald, B. A., & Bonhoeffer, S. (2014). Can high-risk fungicides be used in mixtures without selecting for fungicide resistance? Phytopathology, 104(4), 324-331. https://doi.org/10.1094/PHYTO-07-13-0204-R
Quello, K. L., Chapman, K. S., & Beckerman, J. L. (2010). In situ detection of benzimidazole resistance in field isolates of Venturia inaequalis in Indiana. Plant Disease, 94(6), 744-750. https://doi.org/10.1094/PDIS-94-6-0744
Ren, W., Shao, W., Han, X., Zho, M., & Chen, C. (2016). Molecular and biochemical characterization of laboratory and field mutants of Botrytis cinerea resistant to fludioxonil. Plant Disease, 100(7), 1414-1423. https://doi.org/10.1094/PDIS-11-15-1290-RE
Standish, J. R., Brenneman, T. B., Brewer, M. T., & Stevenson, K. L. (2019). Assessing fitness costs and phenotypic instability of fentin hydroxide and tebuconazole resistance in Venturia effuse. Plant Disease, 103(9), 2271-2276. https://doi.org/10.1094/PDIS-12-18-2292-RE
Wen, Z., Zhang, Y., Chen, Y., Zhao, Y., Shao, W., & Ma, Z. (2024). Characterization of the fludioxonil and phenamacril dual resistant mutants of Fusarium graminearum. Pesticide Biochemistry and Physiology, 200, 105815. https://doi.org/10.1016/j.pestbp.2024.105815 EDN: https://elibrary.ru/mjbhui
Yakuba, G. V., Astapchuk, I. L., Mazyrin, E. S., Nasonov, A. I., & Milovanov, A. V. (2022). The first report on the mycoparasite Trichothecium roseum (Pers. 1809) on Venturia inaequalis (Cooke) G. Winter in Russia. Siberian Journal of Life Sciences & Agriculture, 14(3), 11-23. https://doi.org/10.12731/2658-6649-2022-14-3-11-23 EDN: https://elibrary.ru/bqxkrn
Zhao, W., Sun, C., Wei, L., Chen, W., Wang, B., Li, F., & Xiang, Z. (2021). Detection and fitness of dicarboximide-resistant isolates of Alternaria alternata from Dendrobium officinale, a Chinese indigenous medicinal herb. Plant Disease, 105(8), 2222-2230. https://doi.org/10.1094/PDIS-06-20-1246-RE EDN: https://elibrary.ru/lbhzhd
Список литературы
Иванова, Е. В., Никишина, М. Б., Третьякова, А. В., Мухторов, Л. Г., Переломов, Л. В., Атрощенко, Ю. М. (2021). Изучение фунгицидной активности новых производных 7-R-1,5-динитро-3,7-диазабицикло [3.3.1] нонан-2-она. Siberian Journal of Life Sciences & Agriculture, 13(5), 307-320. https://doi.org/10.12731/2658-6649-2021-13-5-307-320 EDN: https://elibrary.ru/xwvffk
Насонов, А. И. (2019). Новый способ получения культуры Venturia inaequalis из аскоспор. Микология и фитопатология, 53(1), 46-48. https://doi.org/10.1134/S0026364819010094 EDN: https://elibrary.ru/ytixyt
Насонов, А. И., Бардак, М. В. (2023). Морфотипический состав и чувствительность к дифеноконазолу популяций возбудителя парши яблони, различающихся историей применения фунгицида. Siberian Journal of Life Sciences and Agriculture, 15(3), 219-238. https://doi.org/10.12731/2658-6649-2023-15-3-219-238 EDN: https://elibrary.ru/qppsxf
Насонов, А. И., Якуба, Г. В., Астапчук, И. Л. (2021). Чувствительность краснодарской популяции Venturia inaequalis к дифеноконазолу, ингибитору деметилирования стеринов. Микология и фитопатология, 55(4), 297-308. https://doi.org/10.31857/S0026364821040103 EDN: https://elibrary.ru/jahfjc
Насонов, А. И., Якуба, Г. В., Астапчук, И. Л., Марченко, Н. А. (2024). Чувствительность исходной и садовых популяций Venturia inaequalis к фунгицидам класса ингибиторов сукцинатдегидрогеназы (SDHI). Siberian Journal of Life Sciences and Agriculture, 16(1), 189-210. https://doi.org/10.12731/2658-6649-2024-16-1-707 EDN: https://elibrary.ru/notwnf
Насонов, А. И., Якуба, Г. В., Бардак, М. В., Астапчук, И. Л., Марченко, Н. А. (2024). Характеристика приспособленности устойчивых и чувствительных к фунгицидам изолятов Venturia inaequalis in vitro. Ученые записки Казанского университета. Серия: Естественные науки, 166(1), 23-37. https://doi.org/10.26907/2542-064X.2024.1.23-37 EDN: https://elibrary.ru/djqcyr
Насонов, А. И., Якуба, Г. В., Лободина, Е. В. (2022). Длительное сохранение резистентности к карбендазиму у Venturia inaequalis в Краснодарском крае (Россия). Микология и фитопатология, 56(5), 374-378. https://doi.org/10.31857/S0026364822050087 EDN: https://elibrary.ru/cmvduj
Пожилова, Е. В., Новиков, В. Е., Левченкова, О. С. (2015). Активные формы кислорода в физиологии и патологии клетки. Вестник Смоленской государственной медицинской академии, 14(2), 13-22. EDN: https://elibrary.ru/uhovfr
Antonovics, J., Alexander, H. M. (1989). The concept of fitness in plant-fungal pathogen systems. Plant Disease Epidemiology, 2, 185-214.
Bardas, G. A., Myresiotis, C. K., Karaoglanidis, G. S. (2008). Stability and fitness of anilinopyrimidine-resistant strains of Botrytis cinerea. Phytopathology, 98(4), 443-450. https://doi.org/10.1094/PHYTO-98-4-0443
Bauske, M. J., Mallik, I., Yellareddygari, S. K. R., Gudmestad, N. C. (2018). Spatial and temporal distribution of mutations conferring QoI and SDHI resistance in Alternaria solani across the United States. Plant Disease, 102(2), 349-358. https://doi.org/10.1094/PDIS-06-17-0852-RE
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(8), 921-926. https://doi.org/10.1094/PDIS-12-10-0899
Dorigan, A. F., Moreira, S. I., Ceresini, P. C., Pozza, E. A., Belan, L. L., da Silveira, P. R., Alves, E. (2022). Higher fitness and competitive advantage of Pyricularia oryzae Triticum lineage resistant to QoI fungicides. Pest Management Science, 78(12), 5251-5258. https://doi.org/10.1002/ps.7144 EDN: https://elibrary.ru/bwmtoi
Dowling, M., Gelain, J., May De Mio, L. L., Schnabel, G. (2021). Characterization of high fludioxonil resistance in Botrytis cinerea isolates from Calibrachoa flowers. Phytopathology, 111(3), 478-484. https://doi.org/10.1094/phyto-07-20-0268-r EDN: https://elibrary.ru/idsdym
Fan, Z., Yang, J. H., Fan, F., Luo, C. X., Schnabel, G. (2015). Fitness and competitive ability of Alternaria alternata field isolates with resistance to SDHI, QoI and MBC fungicides. Plant Disease, 99(12), 1744-1750. https://doi.org/10.1094/PDIS-03-15-0354-RE
Fernández-Ortuño, D., Grabke, A., Bryson, P. K., Amiri, A., Peres, N. A., & Schnabel, G. (2014). Fungicide resistance profiles in Botrytis cinerea from strawberry fields of seven southern U.S. states. Plant Disease, 98(6), 825-833. https://doi.org/10.1094/PDIS-09-13-0970-RE
Fiaccadori, R. (2018). Persistence of Venturia inaequalis populations resistant to strobilurins in the field and in the glasshouse. American Journal of Plant Sciences, 9(4), 552-560. https://doi.org/10.4236/ajps.2018.94042
Frederick, Z. A., Villani, S. M., Cooley, D. R., Biggs, A. R., Raes, J. J., & Cox, K. D. (2014). Prevalence and stability of qualitative QoI resistance in populations of Venturia inaequalis in the Northeastern United States. Plant Disease, 98(8), 1122-1130. https://doi.org/10.1094/PDIS-10-13-1042-RE
Hammer, Ø., & Harper, D. A. (2001). Past: paleontological statistics software package for education and data analysis. Palaeontologia Electronica, 4(1), 1-9.
Karaoglanidis, G. S., Luo, Y., & Michailides, T. J. (2011). Competitive ability and fitness of Alternaria alternata isolates resistant to QoI fungicides. Plant Disease, 95(2), 178-182. https://doi.org/10.1094/PDIS-07-10-0510
Kim, Y. K., & Xiao, C. L. (2011). Stability and fitness of pyraclostrobin- and boscalid-resistant phenotypes in field isolates of Botrytis cinerea from apple. Phytopathology, 101(11), 1385-1391. https://doi.org/10.1094/PHYTO-04-11-0123
Lesniak, K. E., Proffer, T. J., Beckerman, J. L., & Sundin, G. W. (2011). Occurrence of QoI resistance and detection of the G143A mutation in Michigan populations of Venturia inaequalis. Plant Disease, 95(8), 927-934. https://doi.org/10.1094/PDIS-12-10-0898
Malandrakis, A. A., Vattis, K. N., Doukas, E. G., & Markoglou, A. N. (2013). Effect of phenylpyrrole-resistance on fitness parameters and ochratoxin production in Aspergillus carbonarius. International Journal of Food Microbiology, 165(3), 287-294. https://doi.org/10.1016/j.ijfoodmicro.2013.05.019
Mikaberidze, A., McDonald, B. A., & Bonhoeffer, S. (2014). Can high-risk fungicides be used in mixtures without selecting for fungicide resistance? Phytopathology, 104(4), 324-331. https://doi.org/10.1094/PHYTO-07-13-0204-R
Quello, K. L., Chapman, K. S., & Beckerman, J. L. (2010). In situ detection of benzimidazole resistance in field isolates of Venturia inaequalis in Indiana. Plant Disease, 94(6), 744-750. https://doi.org/10.1094/PDIS-94-6-0744
Ren, W., Shao, W., Han, X., Zho, M., & Chen, C. (2016). Molecular and biochemical characterization of laboratory and field mutants of Botrytis cinerea resistant to fludioxonil. Plant Disease, 100(7), 1414-1423. https://doi.org/10.1094/PDIS-11-15-1290-RE
Standish, J. R., Brenneman, T. B., Brewer, M. T., & Stevenson, K. L. (2019). Assessing fitness costs and phenotypic instability of fentin hydroxide and tebuconazole resistance in Venturia effuse. Plant Disease, 103(9), 2271-2276. https://doi.org/10.1094/PDIS-12-18-2292-RE
Wen, Z., Zhang, Y., Chen, Y., Zhao, Y., Shao, W., & Ma, Z. (2024). Characterization of the fludioxonil and phenamacril dual resistant mutants of Fusarium graminearum. Pesticide Biochemistry and Physiology, 200, 105815. https://doi.org/10.1016/j.pestbp.2024.105815 EDN: https://elibrary.ru/mjbhui
Yakuba, G. V., Astapchuk, I. L., Mazyrin, E. S., Nasonov, A. I., & Milovanov, A. V. (2022). The first report on the mycoparasite Trichothecium roseum (Pers. 1809) on Venturia inaequalis (Cooke) G. Winter in Russia. Siberian Journal of Life Sciences & Agriculture, 14(3), 11-23. https://doi.org/10.12731/2658-6649-2022-14-3-11-23 EDN: https://elibrary.ru/bqxkrn
Zhao, W., Sun, C., Wei, L., Chen, W., Wang, B., Li, F., & Xiang, Z. (2021). Detection and fitness of dicarboximide-resistant isolates of Alternaria alternata from Dendrobium officinale, a Chinese indigenous medicinal herb. Plant Disease, 105(8), 2222-2230. https://doi.org/10.1094/PDIS-06-20-1246-RE EDN: https://elibrary.ru/lbhzhd
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