Fusarium head blight (FHB) is a global significant threat to crop production in small grains such as wheat. Till recently, we still lack empirical data on the selective effects of wheat quantitative resistance on aggressiveness changes in diverse FHB pathogens which may lead to potential resistance erosion because of the difficulty of conducting such studies under field conditions. Four FHB causative agents were used to study the evolution of aggressiveness using in vitro serial passage assays on susceptible «S» and moderately resistant «MR» wheat cultivars. These pathogens were previously tested and were found to be highly aggressive in vitro. Differences due to the selective impact of a cultivar among non-selected and selected isolates were measured for traits contributing to parasitic (latent period (LP) and area under disease progress curve (AUDPC)) and saprophytic (growth rate) fitness. The pathogen populations evolved faster on «MR» cultivars than «S» cultivars. Selected isolates were significantly more aggressive than non-selected isolates for LP and AUDPC, while no increase in aggressiveness was found on potato dextrose agar, indicating that the evolution of aggressiveness in FHB agents is associated with the presence of wheat plants with contrasted resistance levels. Selected isolates from «MR» cultivars were more aggressive than selected isolates from «S» cultivars, as they had a shorter LP (48.8 %) and a higher level of AUDPC (18.4 %). These results provide the first direct evidence that FHB pathogens adapt to wheat by increasing aggressiveness, suggesting a risk of directional selection and possible erosion of FHB resistance, an essential element for the development of durable management strategies for resistant wheat cultivars to FHB infection.
Keywords: area under disease progress curve, erosion, FHB pathogens, latent period, selection pressure
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Abang, M.M., Baum, M., Ceccarelli, S., et al., Differential selection on Rhynchosporium secalis during parasitic and saprophytic phases in the barley scald disease cycle, Phytopathology, 2006, vol. 96, no. 11, pp. 1214–1222. https://doi.org/10.1094/PHYTO-96-1214
Ahmed, H.U., Mundt, C.C., Hoffer, M.E., et al., Selective influence of wheat cultivars on pathogenicity of Mycosphaerella graminicola (anamorph Septoria tritici), Phytopathology, 1996, vol. 86, no. 5, pp. 454–458. https://doi.org/10.1094/Phyto-86-454
Akinsanmi, O.A., Chakraborty, S., Backhouse, D., et al., Passage through alternative hosts changes the fitness of Fusarium graminearum and Fusarium pseudograminearum, Environ. Microbiol., 2007, vol. 9, no. 2, pp. 512–520. https://doi.org/10.1111/j.1462-2920.2006.01168.x
Bottalico, A. and Perrone, G., Toxigenic Fusarium species and mycotoxins associated with head blight in small-grain cereals in Europe, Eur. J. Plant Pathol., vol. 108, no. 7, pp. 611–624. https://doi.org/10.1023/A:1020635214971
Browne, R.A., Investigation into components of partial disease resistance, determined in vitro, and the concept of types of resistance to Fusarium head blight (FHB) in wheat, Eur. J. Plant Pathol., 2009, vol. 123, no. 2, pp. 229–234. https://doi.org/10.1007/s10658-008-9353-7
Burdon, J.J., and Silk, J., Sources and patterns of diversity in plantpathogenic fungi, Phytopathology, 1997, vol. 87, no. 7, pp. 664–669. https://doi.org/10.1094/PHYTO.1997.87.7.664
Caten, C.E., Intra racial variation in Phytophthora infestans and adaptation to field resistance for potato late blight, Ann. Appl. Biol., 1974, vol. 77, no. 3, pp. 259–270. https://doi.org/10.1111/j.1744-7348.1974.tb01402.x
Chen, Y., Wang, W.X., Zhang, A.F., et al., Activity of the fungicide JS399-19 against Fusarium head blight of wheat and the risk of resistance, Agric. Sci. China, 2011, vol. 10, no. 12, pp. 1906–1913. https://doi.org/10.1016/S1671-2927(11)60191-0
Cowger, C. and Mundt, C.C., Aggressiveness of Mycosphaerella graminicola isolates from susceptible and partially resistant wheat cultivars, Phytopathology, 2002, vol. 92, no. 6, pp. 624–630. https://doi.org/10.1094/PHYTO.2002.92.6.624
Delmas, C.E.L., Fabre, F., and Jolivet, J., Adaptation of a plant pathogen to partial host resistance: selection for greater aggressiveness in grapevine downy mildew, Evol. Appl., 2016, vol. 9, no. 5, pp 709–725. https://doi.org/10.1111/eva.12368
Dweba, C.C., Figlan, S., Shimelis, H.A., et al., Fusarium head blight of wheat: Pathogenesis and control strategies, Crop Prot., 2017, vol. 91, pp. 114–122. https://doi.org/10.1016/j.cropro.2016.10.002
Fedak, G., Cao, W., Wolfe D., et al., Molecular characterization of Fusarium resistance from Elymus repens introgressed into bread wheat, Cytol. Genet., 2017, vol. 51, no. 130–133. https://doi.org/10.3103/S0095452717020025
Karelov, A.V., Borzykh, O.I., Kozub, N.O., et al., Current approaches to identification of Fusarium fungi infecting wheat, Cytol. Genet., 2021, vol. 55, no. 5, pp. 433–446. https://doi.org/10.3103/S0095452721050030
Kimura, M., Some models of neutral evolution, compensatory evolution, and the shifting balance process, Theor. Popul. Biol., 1990, vol. 37, no. 1, pp. 150–158. https://doi.org/10.1016/0040-5809(90)90032-Q
Krenz, J.E., Sackett, K.E., and Mundt, C.C., Specificity of incomplete resistance to Mycosphaerella graminicola in wheat, Phytopathology, 2008, vol. 98, no. 5, pp. 555–561. https://doi.org/10.1094/PHYTO-98-5-0555
Laurent, B., Moinard, M., Spataro, C., et al., QTL mapping for aggressiveness variation in F. graminearum revealed one causal mutation in FgVe1 velvet protein, bioRxiv, 2020, vol. 2020. https://doi.org/10.1101/2020.06.19.161349
Leach, J., Cruz, C., Bai, J., et al., Pathogen fitness penalty as a predictor of durability of disease resistance genes, Annu. Rev. Phytopathol., 2001, vol. 39, pp. 187–224. https://doi.org/10.1146/annurev.phyto.39.1.187
Lehman, J.S. and Shaner, G., Selection of populations of Puccinia recondita f. sp. tritici for shortened latent period on a partially resistant wheat cultivar, Phytopathology, 1997, vol. 87, no. 2, pp. 170–176. https://doi.org/10.1094/PHYTO.1997.87.2.170
McDonald, B. and Linde, C., Pathogen population genetics, evolutionary potential, and durable resistance, Phytopathology, 2002, vol. 40, pp. 349–379. https://doi.org/10.1146/annurev.phyto.40.120501.101443
Mundt, C.C., Durable resistance: A key to sustainable management of pathogens and pests, Infect., Genet. Evol., 2014, vol. 27, pp. 446–455. https://doi.org/10.1016/j.meegid.2014.01.011
Mundt, C., Cowger, C., and Garrett, K., Relevance of integrated disease management to resistance durability, Euphytica, 2002, vol. 124, no. 2, pp. 245–252. https://doi.org/10.1023/A:1015642819151
Pariaud, B., Ravigne, V., Halkett, F., et al., Aggressiveness and its role in the adaptation of plant pathogens, Plant Pathol., 2009, vol. 58, pp. 409–424. https://doi.org/10.1111/j.1365-3059.2009.02039.x
Parlevliet, J.E., Durability of resistance against fungal, bacterial and viral pathogens; present situation, Euphytica, 2002, vol. 124, pp. 147–156. https://doi.org/10.1023/A:1015642819151
Parry, D.W., Jekinson, P., and McLeod, L., Fusarium ear blight (scab) in small grain cereals—a review, Plant Pathol., 1995, vol. 44, no. 2, pp. 207–238. https://doi.org/10.1111/j.1365-3059.1995.tb02773.x
Purahong, W., Alkadri, D., Nipoti, P., et al., Validation of a modified Petri-dish test to quantify aggressiveness of Fusarium graminearum in durum wheat, Eur. J. Plant Pathol., 2012, vol. 132, no. 3, pp. 381–391. https://doi.org/10.1007/s10658-011-9883-2
Puri, K.D. and Zhong S., The 3ADON population of Fusarium graminearum found in North Dakota is more aggressive and produces a higher level of DON than the prevalent 15ADON population in spring wheat, Phytopathology, 2010, vol. 100, no. 10, pp. 1007–1014. https://doi.org/10.1094/PHYTO-12-09-0332
Sakr, N., Aggressiveness of fusarium head blight species towards two modern Syrian wheat cultivars in an in vitro Petri-dish, Cereal Res. Commun., 2018a, vol. 46, no. 3, pp. 480–489. https://doi.org/10.1556/0806.46.2018.031
Sakr, N., Interaction between Triticum aestivum plants and four Fusarium head blight species on the level of pathogenicity: Detected in an in vitro Petri-dish assay, Acta Phytopathol. Entomol. Hung., 2018b, vol. 53, no. 2, pp. 171–179. https://doi.org/10.1556/038.53.2018.010
Sakr, N., Intra- and inter-species variability of the aggressiveness in four Fusarium head blight species on durum wheat plants detected in an in vitro Petri-dish assay, Arch. Phytopathol. Plant Prot., 2018c, vol. 51, nos. 15–16, pp. 814–823. https://doi.org/10.1080/03235408.2018.1495390
Sakr, N., In vitro quantitative resistance components in wheat plants to Fusarium head blight, Open Agric. J., 2019a, vol. 13, no. 9–18. https://doi.org/10.2174/1874331501913010009
Sakr, N., Long term storage for five important cereal phytopathogenic species, Pak. J. Phytopathol., 2019b, vol. 31, no. 2, pp. 155–162. https://doi.org/10.33866/phytopathol.031.02.0503
Sakr, N., Pathogenicity and quantitative resistance in Mediterranean durum and bread wheat cultivars of Syrian origin towards Fusarium head blight agents under controlled conditions, J. Plant Protect. Res., 2019c, vol. 59, no. 4, pp. 451–464. https://doi.org/10.24425/jppr.2019.131261
Sakr, N., Aggressiveness of Fusarium species causing head blight on wheat plants determined in detached leaf and seedling in vitro assays, Indian Phytopathol., 2020a, vol. 73, no. 3, pp. 483–491. https://doi.org/10.1007/s42360-020-00234-x
Sakr, N., In vitro analysis of Fusarium head blight resistance in ancient Syrian wheat cultivars (Triticum sp.), Indian J. Agric. Sci., 2020b, vol. 90, no. 2, pp. 283–286.
Sakr, N. and Shoaib, A., Pathogenic and molecular variation of Fusarium species causing head blight on barley landraces, Acta Phytopathol. Entomol. Hung., vol. 56, no. 1, pp. 5–23. https://doi.org/10.1556/038.2021.00006
Steele, K.A., Humphreys, E., Wellings, C.R., et al., Support for a stepwise mutation model for pathogen evolution in Australasian Puccinia striiiformis f. sp. tritici by use of molecular markers, Plant Pathol., 2001, vol. 50, no. 2, pp. 174–180. https://doi.org/10.1046/j.1365-3059.2001.00558.x
Tunali, B., Obanor, F., Erginbas, G., et al., Fitness of three Fusarium pathogens of wheat, FEMS Microbiol. Ecol., 2012, vol. 81, no. 3, pp. 596–609. https://doi.org/10.1111/j.1574-6941.2012.01388.x
Van der Plank, J.E., Disease Resistance in Plants, New York: Academic Press, 1968.
Wang, B., et al., Evolution of virulence in Fusarium oxysporum f. sp. vasinfectum using serial passage assays through susceptible cotton, Phytopathology, 2008, vol. 98, no. 3, pp. 296–303. https://doi.org/10.1094/PHYTO-98-3-0296
Xu, X. and Nicholson, P., Community ecology of fungal pathogens causing wheat head blight. Annu. Rev. Phytopathol., vol. 47, pp. 83–103. https://doi.org/10.1146/annurev-phyto-080508-081737
Xue, A.G., Armstrong, K.C., Voldeng, H.D., et al., Comparative aggressiveness of isolates of Fusarium species causing head blight on wheat in Canada, Can. J. Plant Pathol., 2004, vol. 26, no. 1, pp. 81–88. https://doi.org/10.1080/07060660409507117