Deciphering a pathogen’s evolution: a two-decade longitudinal study reveals virulence shifts and identifies durable Pm genes against Himalayan Blumeria graminis f. sp. tritici populations

Abstract

Wheat powdery mildew, caused by the obligate biotrophic fungus Blumeria graminis f. sp. tritici (Bgt), is a devastating disease responsible for substantial global yield reductions. Host resistance offers the most sustainable management strategy, yet its durability is continually undermined by high evolutionary potential of the pathogen, driven by sexual recombination and rapid mutation. To decipher long-term virulence dynamics, we conducted a comparative analysis of Bgt populations in the Northwestern Himalayas over two decades (1994–1998 and 2015–2019). Pathotype profiling of 285 isolates on a common set of nine differential lines revealed a significant shift in virulence structure over time. While the mean virulence complexity per isolate increased in the contemporary population, indicating enhanced pathogenic capability, overall pathotype diversity decreased, suggesting a selective sweep toward fewer, more aggressive lineages. Marked changes in virulence frequency were observed with severe efficacy erosion for Pm1a (virulence increased from 6 to 63%) and Pm8, while virulence against Pm2, Pm3a, and Pm3b declined significantly. Notably, genes Pm2 and Pm4a demonstrated complete and durable effectiveness throughout the study period. Our results identify these as stable resistance donors and underscores the continuous adaptation of Bgt populations. This study provides critical insights for designing durable resistance gene pyramids and underscores the necessity of continuous virulence surveillance to sustain wheat production in the face of evolving pathogen threats.

Keywords

Triticum aestivum / Powdery mildew / Blumeria graminis f. sp. tritici / Resistance breeding / Pathotype / Virulence dynamics / Durability

References

[1] Abdelrhim A, Abd-Alla HM, El-Sayed A, Ismail ME, Cowger C. Virulence of Egyptian Blumeria graminis f. sp. tritici population and response of Egyptian wheat cultivars. Plant Dis, 2018, 102: 391-397

[2] Akhtar S, Anjum FM, Anjum MA. Micronutrient fortification of wheat flour: recent development and strategies. Food Res Int, 2011, 44: 652-659

[3] Anonymous (2014) Progress Report of All India Coordinated Wheat and Barley Improvement Project 2013–14. In: Saharan MS et al (eds) Crop Protection. Directorate of Wheat Research, Karnal, India

[4] Bahadur P, Aggarwal R (1997) Powdery mildew of wheat: A potential disease in north western India. In: Agnihotri VP et al (eds) Management of threatening plant diseases of natural importance. Malhotra Publishing House, New Delhi

[5] Basandrai AK, Basandrai D (2017) Powdery mildew of wheat and its management. In: Singh DP (ed) Management of wheat and barley diseases. Apple Academic Press, Canada, pp 133–181. https://doi.org/10.1201/9781315207537-5

[6] Basandrai AK, Mehta A, Basandrai D. Virulence structure of wheat powdery mildew pathogen, Blumeria graminis tritici: a review. Indian Phytopathol, 2023, 76: 21-45

[7] Basandrai AK, Tyagi PD, Singh A, Singh BM, Sharma BK. Pathogenic variation in conidial populations of Erysiphe graminis f. sp. tritici in Himachal Pradesh. Indian J Mycol Plant Pathol, 2003, 33: 80-83

[8] Basandrai D, Basandrai AK, Rana SK, Sharma BK, Singh A, Singh D, Tyagi PD. Resistance to powdery mildew ( Blumeria graminis f. sp. tritici E. Marchal) in bread wheat, durum, dicoccum, and triticale genotypes. Indian J Genet Plant Breed, 2016, 76: 205-208

[9] Batista ICA, Silva MPC, Junior ALS, Arrigada MPG, Camargo MP, Figueiredo A, Júnior BTH, Mizubuti ESG. A shift in pathotype diversity and complexity of Phytophthora sojae in Brazil. Plant Dis, 2023, 107(7): 1968-1972

[10] Bhardwaj SC (2011) Resistance genes and adult plant resistance of released wheat varieties of India. Regional Research Station, Directorate of Wheat Research, India

[11] Chao A, Chiu CH, Jost L. Unifying species diversity, phylogenetic diversity, functional diversity, and related similarity and differentiation measures through Hill numbers. Annu Rev Ecol Evol Syst, 2014, 45: 297-324

[12] Dreiseitl A, Dinoor A, Kosman E. Virulence and diversity of Blumeria graminis f. sp. hordei in Israel and in the Czech Republic. Plant Dis, 2006, 90: 1031-1038

[13] Kanwar N (1993) Investigations on powdery mildew (Erysiphe graminis f. sp. tritici) resistance and intensity loss relationship in wheat. Dissertation, Himachal Pradesh Krishi Vishvavidyalaya

[14] Kosman E. Measure of multilocus correlation as a new parameter for study of plant pathogen populations. Phytopathology, 2003, 93: 1464-1470

[15] Kosman E, Dinoor A, Herrmann A, Schachtel GA (2008) Virulence Analysis Tool (VAT). User manual. Available online: http://www.tau.ac.il/lifesci/departments/plant_s/members/kosman/VAT.html. Accessed 1 Dec 2021.

[16] Lalošević M, Jevtić R, Župunski V, Maširević S, Orbović B. Virulence structure of the wheat powdery mildew population in Serbia. Agronomy, 2022, 12: 45

[17] Mehta YRWheat diseases and their management, 2014ChamSpringer

[18] Mehta A, Basandrai AK, Basandrai D, Dhillon HK, Puren H. Seedling and adult plant resistance against powdery mildew and yellow rust in Indian advanced wheat breeding material and commercial genotypes. J Crop Health, 2024, 76: 1403-1431

[19] Mehta A, Basandrai D, Kaur H, Kaur J, Basandrai AK, Basu U, Singh S, Alsakkaf WAA, Ali HM. Genotype by environment interaction analysis for resistance against powdery mildew and yellow rust in some promising exotic wheats. BMC Plant Biol, 2025, 25: 786

[20] Moustafa M. El-Shamy, Hassan M. Emara, Mohamed ME (2016) Virulence analysis of wheat powdery mildew (Blumeria graminis f. sp. tritici) and effective genes in Middle Delta, Egypt. Plant Dis 100:1927–1930. https://doi.org/10.1094/pdis-01-16-0130-re

[21] Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O'Hara RB, Simpson GL, Solymos P, Stevens H, Szöcs E, Wagner HH (2020) Vegan: Community ecology package. Ordination methods, diversity analysis and other functions for community and vegetation ecologists. R Package version 2.5–7. https://CRAN.R-project.org/package=vegan

[22] Parks R, Carbone I, Murphy JP, Marshall D, Cowger C. Virulence structure of the eastern U.S. wheat powdery mildew population. Plant Dis, 2008, 92: 1074-1082

[23] Paul R, Basandrai AK, Tyagi PD. Virulence spectrum of Erysiphe graminis f. sp. tritici in Himachal Pradesh. Indian Phytopathol, 2000, 53: 415-418

[24] Pretorius ZA, Singh RP, Wagoire WW, Payne TS (2000) Detection of virulence to wheat stem rust resistance gene Sr31 in Puccinia graminis f. sp. tritici in Uganda. Plant Dis 84:203. https://doi.org/10.1094/pdis.2000.84.2.203b

[25] Rana SK, Sharma BK, Basandrai AK. Estimation of losses due to powdery mildew of wheat in Himachal Pradesh. Indian Phytopathol, 2006, 59: 112-114

[26] Samobor V, Vukobratovic M, Jost M. Effect of powdery mildew attack on quality parameters and experimental bread baking of wheat. Acta Agric Slov, 2006, 87(2): 381-391

[27] Sharma TR, Singh BM. Virulence structure of Erysiphe graminis tritici in Himachal Pradesh. Indian Phytopathol, 1990, 43: 165-169

[28] Sharma TR, Singh BJ. Physiologic races of Erysiphe graminis tritici in Himachal Pradesh. Indian Phytopathol, 1990, 43: 33-37

[29] Sharma SC, Basandrai AK, Aulakh KS. Virulence in Erysiphe graminis f. sp. tritici causing powdery mildew in wheat. Plant Dis Res, 1990, 5: 115-117

[30] Si QM, Zhang XX, Duan XY, Sheng BQ. Identification of physiologic races of Erysiphe graminis f. sp. tritici. Scientia Agric Sin, 1987, 20: 64-70

[31] Smith HC, Blair IJD. Wheat powdery mildew investigations. Ann Appl Biol, 1950, 37: 570-583

[32] Szunics L, Szunics L, Vida G, Bedő Z, Svec M (2001) Dynamics of changes in the races and virulence of wheat powdery mildew in Hungary between 1971 and 1999. Euphyt 119:145–149

[33] Wang Y, Zhang G, Wang F, Lang X, Zhao X, Zhu J, Hu C, Hu J, Zhang Y, Yao X, Liu H, Ma T, Niu Y, Wang Z, Feng J, Wangmu LR. Virulence variability and genetic diversity in Blumeria graminis f. sp. hordei in southeastern and southwestern China. Plant Dis, 2023, 107(3): 809-819

[34] Wickham Hggplot2: Elegant graphics for data analysis, 2016Springer

[35] Wu XX, Xu XF, Ma DX, Chen RZ, Li TY, Cao YY. Virulence structure and its genetic diversity analyses of Blumeria graminis f. sp. tritici isolates in China. BMC Evol Biol, 2019, 19: 183

[36] Xue AG, Lim S, Chen Y, Humphreys G, Cao W, Menzies J, Cowger C, Li H, Serajazari M. Virulence structure of Blumeria graminis f. sp. tritici, the causal agent of wheat powdery mildew, in Ontario, Canada, in 2018 and 2019. Can J Plant Pathol, 2021, 43(6): 803-811

[37] Zeng FS, Yang LJ, Gong SJ, Shi WQ, Zhang XJ, Wang H, Xiang LB, Xue MF, Yu DZ. Virulence and diversity of Blumeria graminis f. sp. tritici populations in China. J Integr Agric, 2014, 13: 2424-2437

RIGHTS & PERMISSIONS

The Author(s)