Assessment of fitness costs in Venturia inaequalis with difenoconazole resistance
- Authors: Nasonov A.I.1, Yakuba G.V.1, Bardak M.V.1, Marchenko N.A.1
-
Affiliations:
- North Caucasian Federal Scientific Center of Horticulture, Viticulture, Wine-making
- Issue: Vol 59, No 2 (2025)
- Pages: 154-168
- Section: PHYTOPATHOGENIC FUNGI
- URL: https://journal-vniispk.ru/0026-3648/article/view/288864
- DOI: https://doi.org/10.31857/S0026364825020042
- EDN: https://elibrary.ru/sqpcbi
- ID: 288864
Cite item
Abstract
Venturia inaequalis (teleomorph Fusicladium dendriticum) is the cause of apple scab, a widespread and significantly damaging disease worldwide. In an integrated management system against Venturia inaequalis, including, for example, cultural approaches and the use of scab-resistant varieties, chemical fungicides remain the key to disease management. Limitations in the use of fungicides are associated with the development of resistance in pathogens. It is assumed that the development of adaptation in the fungus to the toxic effect of a fungicide may in some cases incur physiological costs, leading to a decrease in its fitness under conditions where this fungicide is absent from the environment. This phenomenon is called the fitness cost. The presence of a fitness cost in resistant forms provides a competitive advantage for susceptible fungal isolates in the absence of fungicide treatments, for example, when rotating a fungicide from one mode of action to another. Thus, the fitness cost allows one to control the development of resistance. The aim of our study was to evaluate the effect of fitness cost based on the “predicted fitness” parameters in vitro in two pathogen populations: sensitive and resistant to difenoconazole. We evaluated the following parameters in vitro: the EC50 of difenoconazole for isolates, the growth of isolates on artificial (Leroux medium) and natural (PGA) media, the sporulation rate in liquid cultures, the spore germination rate, and the growth of isolates under osmotic stress (addition of NaCl). It was shown that the studied populations differed significantly in their average EC50 values, which were 0.0088 mg/L for the sensitive population and 2.1954 mg/L for the resistant population. No fitness cost was detected for resistant V. inaequalis isolates based on any of the studied parameters. According to the correlation analysis, there was no relationship between the sensitivity of isolates and their parameters measured in vitro.
Keywords
About the authors
A. I. Nasonov
North Caucasian Federal Scientific Center of Horticulture, Viticulture, Wine-making
Author for correspondence.
Email: nasoan@mail.ru
Russian Federation, 350901, Krasnodar
G. V. Yakuba
North Caucasian Federal Scientific Center of Horticulture, Viticulture, Wine-making
Email: galyayaku@gmail.com
Russian Federation, 350901, Krasnodar
M. V. Bardak
North Caucasian Federal Scientific Center of Horticulture, Viticulture, Wine-making
Email: maria.brd1405@mail.ru
Russian Federation, 350901, Krasnodar
N. A. Marchenko
North Caucasian Federal Scientific Center of Horticulture, Viticulture, Wine-making
Email: marchekonikita@yandex.ru
Russian Federation, 350901, Krasnodar
References
- Bardas G.A., Myresiotis C.K., Karaoglanidis G.S. Stability and fitness of anilinopyrimidine-resistant strains of Botrytis cinerea. Phytopathology. 2008. V. 98 (4). P. 443–450. https://doi.org/10.1094/phyto-98-4-0443
- Bauske M.J., Mallik I., Yellareddygari S.K.R. et al. Spatial and temporal distribution of mutations conferring QoI and SDHI resistance in Alternaria solani across the United States. Plant Dis. 2018. V. 102 (2). P. 349–358. https://doi.org/10.1094/pdis-06-17-0852-RE
- Bus V.G.M., Rikkerink E.H., Caffier V. et al. Revision of the nomenclature of the differential host-pathogen interactions of Venturia inaequalis and Malus. Ann. Rev. Phytopathol. 2011. V. 49. P. 391–413. https://doi.org/10.1146/annurev-phyto-072910-095339
- Chapman K.S., Sundin G.W., Beckerman J.L. Identification of resistance to multiple fungicides in field populations of Venturia inaequalis. Plant Dis. 2011. V. 95 (8). P. 921–926. https://doi.org/10.1094/pdis-12-10-0899
- Cox K.D. Fungicide resistance in Venturia inaequalis, the causal agent of apple scab, in the United States. In: Fungicide Resistance in Plant Pathogens. Springer, Tokyo, 2015, pp. 433–447.
- De Gracia M., Cascales M., Expert P. et al. How did host domestication modify life history traits of its pathogens? PLOS one. 2015. 10 (6). e0122909. https://doi.org/10.1371/journal.pone.0122909
- Dorigan A.F., Moreira S.I., Ceresini P.C. et al. Higher fitness and competitive advantage of Pyricularia oryzae Triticum lineage resistant to QoI fungicides. Pest Management Sci. 2022. V. 78 (12). P. 5251–5258. https://doi.org/10.1002/ps.7144
- Fernández-Ortuño D., Grabke A., Bryson P.K. et al. Fungicide resistance profiles in Botrytis cinerea from strawberry fields of seven southern U.S. states. Plant Dis. 2014. V. 98 (6). P. 825–833. https://doi.org/10.1094/pdis-09-13-0970-re
- Fiaccadori R. Researches on methodologies to verify reduced sensitivities of Venturia inaequalis in field to difenoconazole and first indications of a survey in Italy. Am.J. Plant Sciences. 2017. V. 8 (09). P. 2056–2068. https://doi.org/10.4236/ajps.2017.89138
- Gifford D., Moss E., MacLean R. Environmental variation alters the fitness effects of rifampicin resistance mutations in Pseudomonas aeruginosa. Evolution. 2016. V. 70. P. 725–730. https://doi.org/10.1111/evo.12880
- Gladieux P., Zhang X.G., Róldan‐Ruiz I.S.A.B.E.L. et al. Evolution of the population structure of Venturia inaequalis, the apple scab fungus, associated with the domestication of its host. Molec. Ecol. 2010. V. 19 (4). 658–674. https://doi.org/10.1111/j.1365-294X.2009.04498.x
- Hammer Ø., Harper D.A.T., Ryan P.D. PAST: Paleontological statistics software package for education and data analysis. Palaeontologia Electronica. 2001. V. 4 (1) Р. 9. https://palaeo-electronica.org/2001_1/past/issue1_01.htm
- Hawkins N.J., Fraaije B.A. Fitness penalties in the evolution of fungicide resistance. Annu. Rev. Phytopathol. 2018. V. 56 (1) P. 339–360. https://doi.org/10.1146/annurev-phyto-080417-050012
- Heaven T., Armitage A.D., Xu X. et al. Dose-dependent genetic resistance to Azole fungicides found in the apple scab pathogen. J. Fungi. 2023. V. 9 (12). P. 1136. https://doi.org/10.3390/jof9121136
- Henríquez Sáez J., Sarmiento O., Alarcón P. Sensitivity of Venturia inaequalis Chilean isolates to difenoconazole, fenarimol, mancozeb, and pyrimethanil. Chilean J. Agric. Res. 2011. V. 71 (1). P. 39–44. https://doi.org/10.4067/S0718-58392011000100005
- Hoffmeister M., Zito R., Boehm J. et al. Mutations in Cyp51 of Venturia inaequalis and their effects on DMI sensitivity. J. Plant Diseases and Protection. 2021. V. 128 (6). P. 1467–1478. https://doi.org/10.1007/s41348-021-00516-0
- Karaoglanidis G.S., Luo Y., Michailides T.J. Competitive ability and fitness of Alternaria alternata isolates resistant to QoI fungicides. Plant Dis. 2011. V. 95 (2). P. 178–182. https://doi.org/10.1094/pdis-07-10-0510
- Khokhryakov M.K., Dobrozrakova T.L., Stepanov K.M. et al. Identifier of plant diseases. 3rd ed., corrected. SPb., 2003. (In Russ.)
- Kim Y.K., Xiao C.L. Stability and fitness of pyraclostrobin-and boscalid-resistant phenotypes in field isolates of Botrytis cinerea from apple. Phytopathology. 2011. V. 101 (11). P. 1385–1391. https://doi.org/10.1094/phyto-04-11-0123
- Larsen N.J., Beresford R.M., Wood P.N. et al. A synthetic agar assay for determining sensitivity of Venturia inaequalis to anilinopyrimidine fungicides in New Zealand apple orchards. New Zealand Plant Prot. 2013. V. 66. P. 293–302. https://doi.org/10.30843/nzpp.2013.66.5665
- Le Van A., Durel C.E., Le Cam B. et al. The threat of wild habitat to scab resistant apple cultivars. Plant Pathol. 2011. V. 60 (4). P. 621–630. https://doi.org/10.1111/j.1365-3059.2011.02437.x
- Le Van A., Gladieux P., Lemaire C. et al. Evolution of pathogenicity traits in the apple scab fungal pathogen in response to the domestication of its host. Evolutionary Applications. 2012. V. 5 (7). P. 694–704. https://doi.org/10.1111/j.1752-4571.2012.00246.x
- Lenormand T., Harmand N., Gallet R. Cost of resistance: an unreasonably expensive concept. BioRxiv. 2018. P. 276675. https://doi.org/10.1101/276675
- Leroux P., Chapeland F., Desbrosses D. et al. Patterns of cross-resistance to fungicides in Botryotinia fuckeliana (Botrytis cinerea) isolates from French vineyards. Crop Protect. 1999. V. 18. P. 687–697. https://doi.org/10.1016/S0261-2194(99)00074-5
- Lichtemberg P.S., Michailides, T.J., Puckett R.D. et al. Fitness costs associated with G461S mutants of Monilinia fructicola could favor the management of tebuconazole resistance in Brazil. Tropical Plant Pathol. 2019. V. 44. P. 140–150. https://doi.org/10.1007/s40858-018-0254-9
- Malandrakis A.A., Vattis K.N., Doukas E.G. et al. Effect of phenylpyrrole-resistance on fitness parameters and ochratoxin production in Aspergillus carbonarius. Int. J. Food Microbiol. 2013. V. 165 (3). P. 287–294.
- Martin G., Lenormand T. The fitness effect of mutations across environments: Fisher’s geometrical model with multiple optima. Evolution. 2015. V. 69. P. 1433–1447 https://doi.org/10.1111/evo.12671
- Melnyk A.H., Wong A., Kassen R. The fitness costs of antibiotic resistance mutations. Evol. Appl. 2015. V. 8. P. 273–283. https://doi.org/10.1111/eva.12196
- Mikaberidze A., McDonald B.A., Bonhoeffer S. Can high-risk fungicides be used in mixtures without selecting for fungicide resistance? Phytopathology. 2014. V. 104 (4). Р. 324–331. https://doi.org/10.1094/phyto-07-13-0204-r
- Mondino P., Casanova L., Celio A. et al. Sensitivity of Venturia inaequalis to trifloxystrobin and difenoconazole in Uruguay. J. Phytopathol. 2015. Vol. 163 (1). P. 1–10. https://doi.org/10.1111/jph.12274
- Mubashir S.S., Bhat Z.A., Bhat M.A. et al. Baseline sensitivities of Venturia inaequalis populations to the difenaconazole, a sterol demethylation inhibitor fungicide. Frontiers Crop Improv. 2023. V. 11. P. 2965–2968.
- Nasonov A.I. New method of producing of Venturia inaequalis culture from ascospores. Mikologiya i fitopatologiya. 2019. V. 53 (1). P. 46–48. (In Russ.) https://doi.org/10.1134/S0026364819010094
- Nasonov A.I., Suprun I.I. Apple scab: peculiarities of the causal agent and the pathogenesis. Mikologiya i fitopatologiya. 2015. V. 49 (5). P. 275–285. (In Russ.)
- Nasonov A.I., Suprun I.I., Lobodina E.V. et al. Artificial scab resistance evaluation of Malus orietalis forms – a potential source of new genes for resistance to apple scab. Polythematic online electronic scientific journal of the Kuban State Agrarian University. 2017. № 131. P. 1377–1388. (In Russ.) https://doi.org/10.21515/1990-4665-131-113
- Nasonov A.I., Yakuba G.V., Astapchuk I.L. Sensitivity of the Krasnodar population of Venturia inaequalis to difenoconazole, an inhibitor of sterol demethylation. Mikologiya i fitopatologiya. 2021. V. 55 (4). P. 297–308. (In Russ.) https://doi.org/10.31857/S0026364821040103
- Nasonov A.I., Bardak M.V. Morphotypic composition and difenoconazole sensitivity of apple scab pathogen populations that differ in the history of fungicide application. Siberian journal of life sciences and agriculture. 2023. V. 15 (3). P. 219–238. (In Russ.) https://doi.org/10.12731/2658-6649-2023-15-3-219-238
- Nasonov A.I., Yakuba G.V. Apple scab: resistance to chemical fungicides. Mikologiya i fitopatologiya. 2024. V. 58. № 2. P. 91–107. (In Russ.) https://doi.org/10.31857/S0026364824020018
- Nasonov A.I., Yakuba G.V., Bardak M.V. et al. In vitro study of fitness parameters in fungicide-resistant and -sensitive Venturia inaequalis isolates. Uchenye zapiski Kazanskogo universiteta. Seriya: Estestvennye nauki. 2024. V. 166 (1). P. 23–37. (In Russ.) https://doi.org/10.26907/2542-064X.2024.1.23-37
- Nasonov A.I., Yakuba G.V., Lobodina E.V. The long-term resistance to carbendazim in Venturia inaequalis in the Krasnodar region (Russia). Mikologiya i fitopatologiya. 2022a. V. 56 (5). P. 374–378. (In Russ.) https://doi.org/10.31857/S0026364822050087
- Nasonov A.I., Yakuba G.V., Marchenko N. et al. Evaluation of sensitivity of apple scab pathogen to difenoconazole using the discriminatory dose technique. Bio Web Conf. 2022b. V. 47. P. 10002. (In Russ.) https://doi.org/10.1051/bioconf/20224710002
- Pidoplichko N.M. Fungi – parasites of cultivated plants. Identification in 3 volumes. Kiev, 1977. (In Russ.)
- Pikunova A.V., Sedov E.N. The racial composition of Venturia inaequalis in environments of the Oryol region. Mikologiya i fitopatologiya. 2019. V. 53 (5). P. 293–300. (In Russ.) https://doi.org/10.1134/S0026364819050040
- Ren W., Shao W., Han X. et al. Molecular and biochemical characterization of laboratory and field mutants of Botrytis cinerea resistant to fludioxonil. Plant Dis. 2016. V. 100 (7). P. 1414–1423. https://doi.org/10.1094/pdid-11-15-1290-re
- Sitther V., Garrido Haro P.A., Molineros J.E. et al. Genetic diversity of apple‐and crabapple‐infecting isolates of Venturia inaequalis in Pennsylvania, the United States, determined by microsatellite markers. Forest Pathol. 2018. V. 48(2). P. e12405. (In Russ.). https://doi.org/10.1111/efp.12405
- Smolyakova V.M., Yakuba G.V. Some problems of resistance to fungicides of scab and powdery mildew pathogens. In: Optimization of the phytosanitary state of orchards under weather stress. SKZNIISiV, Krasnodar, 2005, pp. 263– 268. (In Russ.)
- State catalogue of pesticides and agrochemicals, permitted for use on the territory of the Russian Federation. 2020–2024. (In Russ.)
- Villani S.M., Biggs A.R., Cooley D.R. et al. Prevalence of myclobutanil resistance and difenoconazole insensitivity in populations of Venturia inaequalis. Plant Dis. 2015. V. 99. P. 1526–1536. https://doi.org/10.1094/pdis-01-15-0002-re
- Yaegashi, H., Hirayama, K., Akahira, T. et al. Point mutation in CYP51A1 of Venturia inaequalis is associated with low sensitivity to sterol demethylation inhibitors. J. General Pl. Pathol. 2020. V. 86. 245–249. https://doi.org/10.1007/s10327-020-00924-4
- Zhao W., Sun C., Wei L. et al. Detection and fitness of dicarboximide-resistant isolates of Alternaria alternata from Dendrobium officinale, a Chinese indigenous medicinal herb. Plant Dis. 2021. V. 105 (8). P. 2222–2230. https://doi.org/10.1094/pdis-06-20-1246-re
- Zhdanov V.V., Sedov E.N. Apple breeding for resistance to scab. Tula, 1991. (In Russ.)
- Государственный каталог пестицидов и агрохимикатов, разрешенных к применению на территории Российской Федерации, 2024 г. (State catalogue) http://mcx.ru/ministry/departments/departament-rastenievodstva-mekhanizatsii-khimizatsii-izashchity-rasteniy/industry-information/info-gosudarstvennaya-usluga-po-gosudarstvennoy-registratsi ipestitsidov-i-agrokhimikatov/
- Жданов В.В., Седов Е.Н. (Zhdanov, Sedov) Селекция яблони на устойчивость к парше. Тула: Приок. кн. изд-во, 1991. 208 с.
- Насонов А.И. (Nasonov) Новый способ получения культуры Venturia inaequalis из аскоспор // Микология и фитопатология. 2019. Т. 53. № 1. С. 46–48.
- Насонов А.И., Бардак М.В. (Nasonov, Bardak) Морфотипический состав и чувствительность к дифеноконазолу популяций возбудителя парши яблони, различающихся историей применения фунгицида // Siberian journal of life sciences and agriculture. 2023. Т. 15 (3). С. 219–238.
- Насонов А.И., Супрун И.И. (Nasonov, Suprun) Парша яблони: особенности возбудителя и патогенеза // Микология и фитопатология. 2015. Т. 49. № 5. С. 275–285.
- Насонов А.И., Супрун И.И., Лободина Е.В. и др. (Nasonov et al.) Оценка на искусственном инфекционном фоне форм malusorientalis-потенциальных источников генов устойчивости к парше яблони // Политематический сетевой электронный научный журнал Кубанского государственного аграрного университета. 2017. № 131. 1377–1388.
- Насонов А.И., Якуба Г.В. (Nasonov, Yakuba) Парша яблони: устойчивость к химическим фунгицидам // Микология и фитопатология. 2024. Т. 58. № 2. С. 91–107.
- Насонов А.И., Якуба Г.В., Астапчук И.Л. (Nasonov et al.) Чувствительность краснодарской популяции Venturia inaequalis к дифеноконазолу, ингибитору деметилирования стеринов // Микология и фитопатология. 2021. Т. 55. № 4. С. 297–308.
- Насонов А.И., Якуба Г.В., Бардак М.В. и др. (Nasonov et al.) Характеристика приспособленности устойчивых и чувствительных к фунгицидам изолятов Venturia inaequalis in vitro // Ученые записки Казанского университета. Серия: Естественные науки. 2024. Т. 166. № 1. С. 23–37.
- Насонов А.И., Якуба Г.В., Лободина Е.В. (Nasonov et al.) Длительное сохранение резистентности к карбендазиму у Venturia inaequalis в Краснодарском крае (Россия) // Микология и фитопатология. 2022. Т. 56. № 5. С. 374–378.
- Пидопличко Н.М. Грибы – паразиты культурных растений. Определитель в 3-х т. Киев: Наук. Думка. 1977. 296 с.
- Пикунова А.В., Седов Е.Н. (Pikunova, Sedov) Расовый состав Venturia inaequalis в условиях Орловской области // Микология и фитопатология. 2019. Т. 53. № 5. С. 293–300.
- Смольякова В.М. Якуба Г.В. (Smolyakova, Yakuba) Некоторые проблемы резистентности к фунгицидам грибов-возбудителей парши и мучнистой росы // Оптимизация фитосанитарного состояния садов в условиях погодных стрессов. Краснодар: ГНУ СКЗНИИСиВ, 2005. С. 263–268.
- Хохряков М.К., Доброзракова Т.Л., Степанов К.М. и др. (Khokhryakov et al.) Определитель болезней растений. 3-е изд., испр. СПб.: Изд-во “Лань”, 2003. 592 с.
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