European Journal of Plant Pathology

, Volume 152, Issue 2, pp 309–326 | Cite as

Virulence variation of cucurbit powdery mildews in the Czech Republic – population approach

  • Aleš LebedaEmail author
  • Eva Křístková
  • Božena Sedláková
  • James D. McCreight
  • Evsey Kosman


Kosman diversity models were applied to analyses of virulence (disease reaction patterns) variation of 115 isolates of two cucurbit powdery mildew (CPM) species, Golovinomyces orontii (Go) and Podosphaera xanthii (Px), collected in the Czech Republic from 2010 through 2012. Diversity within and distances between Go and Px populations and each other in a spatio-temporal context and with regard to original host plant species were analyzed based on virulence patterns of individual isolates on a set of 21 melon (Cucumis melo L.) race differential genotypes. Significant differentiation among the Go and Px pathogen populations was revealed, and the results clearly demonstrate and confirm that the set of differential C. melo genotypes is well composed because of high differentiation capacity. Differentiation of pathogens among years was significant for both species. No significant difference between Go isolates from different host plant species was established due to high variability among Go isolates, but there was significant host-specific differentiation among Px isolates. Differentiation of pathogens among regions was not detected. These results revealed high virulence variation in isolates of Go and Px, and their spatio-temporal fluctuations. High diversity in virulence of Go isolates supports the treatment of Go as a complex of different (sub)species with distinct virulence factors. Similar relationships of selected Go isolates in a UPGMA dendrogram in a previously reported multigene phylogenetic tree support the logic and suitability of the Kosman assignment based approach to population studies of organisms with asexual or mixed modes of reproduction. The approach applied in this study provides a complex view of virulence structures of powdery mildew populations, and when combined with race determination and denomination on melon, it may serve as a base to understandvirulence variation of these CPM species from a spatio-temporal viewpoint.


Golovinomyces orontii Podosphaera xanthii Cucumis melo Differential set validation Virulence patterns Population diversity Assignment based approach Virulence analysis tool (VAT) software Asexual (clonal) reproduction 



This research was supported by the following grants: MSM 6198959215 Ministry of Education, Youths and Sports, Czech Repblic), QH 71229 (National Agency for Agricultural Research, Czech Ministry of Agriculture) and Internal Grant Agency of Palacký University in Olomouc (IGA_PrF_2017_001; IGA_PrF_2018_001).


1) MSM 6198959215 (Czech Ministry of Education); 2) QH71229 (NAZV, National Agency for Agricultural Research of the Czech Republic); 3) Internal Grant Agency of Palacký University in Olomouc (IGA_PrF_2017_001; IGA_PrF_2018_001).

Compliance with ethical standards

Conflict of interest

There are no potential conflicts (financial or non-financial) of interest.

Human and animal rights

Research did not involve Human Participants and/or Animals.


  1. Bardin, M., Carlier, J., & Nicot, P. C. (1999). Genetic differentiation in the French population of Erysiphe cichoracearum, a causal agent of powdery mildew of cucurbits. Plant Pathology, 48, 531–540.CrossRefGoogle Scholar
  2. Ben-David, R., Parks, R., Dinoor, A., Kosman, E., Wicker, T., Keller, B., & Cowger, C. (2016). Differentiation among Blumeria graminis f. sp. tritici isolates originating from wild vs. domesticated Triticum species in Israel. Phytopathology, 106, 861–870.CrossRefPubMedGoogle Scholar
  3. Bertrand, F. (1991). Les oïdiums des Cucurbitacées: Maintien en culture pure, Etude de leur variabilité et de la sensibilité chez le melon. PhD thesis, 225 pp. Orsay, France: Université Paris-Sud (in French).Google Scholar
  4. Braun, U., & Cook, R. T. A. (2012). Taxonomic manual of the Erysiphales (powdery mildews), CBS Biodiversity Series no. 11. Utrecht: CBS-KNAW Fungal Diversity Centre.Google Scholar
  5. Burdon, J. J., & Silk, J. (1997). Sources and patterns of diversity in plant-pathogenic fungi. Phytopathology, 87, 664–669.CrossRefPubMedGoogle Scholar
  6. CHMI 2017. Český hydrometeorologický ústav. Povětrnostní situace. Assessed 5 June 2017.
  7. Cohen, R., Burger, Y., & Katzir, N. (2004). Monitoring physiological races of Podosphaera xanthii (syn. Sphaerotheca fuliginea), the causal agent of powdery mildew in cucurbits: factors affecting race identification and the importance for research and commerce. Phytoparasitica, 32, 174–183.CrossRefGoogle Scholar
  8. del Pino, D., Olalla, I., Pérez-Garcia, A., Pivera, M. E., Garcia, S., Moreno, R., de Vicente, A., & Torés, J. A. (2002). Occurrence of races and pathotypes of cucurbit powdery mildew in Southeastern Spain. Phytoparasitica, 30, 459–466.CrossRefGoogle Scholar
  9. Dawit, W., Flath, K., Weber, W. E., Schumann, E., & Kosman, E. (2009). Virulence and diversity of Puccinia striiformis f. sp. tritici in Ethiopia. Canadian Journal of Plant Pathology, 31, 211–219.CrossRefGoogle Scholar
  10. Dreiseitl, A., Dinoor, A., & Kosman, E. (2006). Virulence and diversity of Blumeria graminis f. sp. hordei in Israel and in the Czech Republic. Plant Disease, 90, 1031–1038.CrossRefGoogle Scholar
  11. Dreiseitl, A., & Kosman, E. (2013). Virulence phenotypes of Blumeria graminis f. sp. hordei in South Africa. European Journal of Plant Pathology, 136, 113–121.CrossRefGoogle Scholar
  12. Gong, L., Paris, H. S., Stift, G., Pachner, M., Vollmann, J., & Lelley, T. (2013). Genetic relationships and evolution in Cucurbita as viewed with simple sequence repeat polymorphism: the centrality of C. okeechobeensis. Genetic Resources and Crop Evolution, 60, 1531–1546.CrossRefGoogle Scholar
  13. Gultyaeva, E., Dmitriev, A., & Kosman, E. (2012). Regional diversity of Russian populations of Puccinia triticina in 2007. Canadian Journal of Plant Pathology, 34, 213–223.CrossRefGoogle Scholar
  14. Gultyaeva, E. I., Shaydayuk, E. L., Goncharov, N. P., Akhmetova, A., Abdullaev, K. M., Belousova, M. H., & Kosman, E. (2016). Virulence of Puccinia triticina on Triticum and Aegilops species. Australasian Plant Pathology, 45, 155–163.CrossRefGoogle Scholar
  15. Hollomon, D. W., & Wheeler, I. E. (2002). Controlling powdery mildews with chemistry. In R. R. Bélanger, W. R. Bushnell, A. J. Dik, & T. L. W. Carver (Eds.), The powdery mildews. A comprehensive treatise (pp. 249–255). St. Paul: APS Press.Google Scholar
  16. Kosman, E. (1996). Difference and diversity of plant pathogen populations: a new approach for measuring. Phytopathology, 86, 1152–1155.Google Scholar
  17. Kosman, E. (2003). Nei’s gene diversity and the index of average differences are identical measures of diversity within populations. Plant Pathology, 52, 533–535.CrossRefGoogle Scholar
  18. Kosman, E. (2014). Measuring diversity: from individuals to populations. European Journal of Plant Pathology, 138, 467–486.CrossRefGoogle Scholar
  19. Kosman, E., Ben-Yehuda, P., & Manisterski, J. (2014). Diversity of virulence phenotypes among annual populations of wheat leaf rust in Israel from 1993 to 2008. Plant Pathology, 63, 563–571.CrossRefGoogle Scholar
  20. Kosman, E., & Leonard, K. J. (2007). Conceptual analysis of methods applied to assessment of diversity within and distance between populations with asexual or mixed mode of reproduction. New Phytologist, 174, 683–696.CrossRefPubMedGoogle Scholar
  21. Křístková, E. (1999). Biology and epidemiology of Erysiphales on the genus Cucurbita. Ph.D. thesis, 188 pp. Olomouc, Czech Republic: Palacký University in Olomouc (in Czech).Google Scholar
  22. Křístková, E., & Lebeda, A. (2000). Citrullus lanatus – a potential host of powdery mildew in the Czech Republic. Cucurbit Genetics Cooperative Report, 23, 46–48.Google Scholar
  23. Křístková, E., & Lebeda, A. (2001). Aggressiveness of powdery mildew isolates on Cucurbita maxima. Cucurbit Genetics Cooperative Report, 24, 73–76.Google Scholar
  24. Křístková, E., Lebeda, A., & Sedláková, B. (2009). Species spectra, distribution and host range of cucurbit powdery mildews in the Czech Republic and some other European and Middle Eastern countries. Phytoparasitica, 37, 337–350.CrossRefGoogle Scholar
  25. Lebeda, A. (1983). The genera and species spectrum of cucumber powdery mildew in Czechoslovakia. Phytopathologische Zeitschrift, 108, 71–77.CrossRefGoogle Scholar
  26. Lebeda, A. (1984). Screening of wild Cucumis species for resistance to cucumber powdery mildew (Erysiphe cichoracearum and Sphaerotheca fuliginea). Scientia Horticulturae, 24, 241–249.CrossRefGoogle Scholar
  27. Lebeda, A., Křístková, E., Sedláková, B., Coffey, M. D., & McCreight, J. D. (2011). Gaps and perspectives of pathotype and race determination in Golovinomyces cichoracearum and Podosphaera xanthii. Mycoscience, 52, 159–164.CrossRefGoogle Scholar
  28. Lebeda, A., Křístková, E., Sedláková, B., & McCreight, J. D. (2016a). Initiative for international cooperation of researchers and breeders related to determination and denomination of cucurbit powdery mildew races. In E. U. Kozik & H. S. Paris (Eds.), Proceedings of Cucurbitaceae 2016, the XIth EUCARPIA meeting on genetics and breeding of Cucurbitaceae (pp. 148–152). Skierniewice: Wydawnictvo SIGMA Sp. J.Google Scholar
  29. Lebeda, A., Křístková, E., Sedláková, B., McCreight, J. D., & Coffey, M. D. (2008). New concept for determination and denomination of pathotypes and races of cucurbit powdery mildew. In M. Pitrat (Ed.), Proceedings of Cucurbitaceae 2008, IXth EUCARPIA meeting on genetics and breeding of Cucurbitaceae (pp. 125–134). Avignon: INRA.Google Scholar
  30. Lebeda, A., Křístková, E., Sedláková, B., McCreight, J. D., & Coffey, M. D. (2016b). Cucurbit powdery mildews: methodology for objective determination and denomination of races. European Journal of Plant Pathology, 144, 399–410.CrossRefGoogle Scholar
  31. Lebeda, A., McGrath, M. T., & Sedláková, B. (2010). Fungicide resistance in cucurbit powdery mildew fungi; Chapter 11. In O. Carisse (Ed.), Fungicides (pp. 221–246). Rijeka: InTech Publishers.Google Scholar
  32. Lebeda, A., Pavelková, J., Sedláková, B., & Urban, J. (2013). Structure and temporal shifts in virulence of Pseudoperonospora cubensis populations in the Czech Republic. Plant Pathology, 62, 336–345.CrossRefGoogle Scholar
  33. Lebeda, A., & Sedláková, B. (2004). Disease impact and pathogenicity variation in Czech populations of cucurbit powdery mildews. In A. Lebeda & H. S. Paris (Eds.), Progress in cucurbit genetics and breeding research. Proceedings of Cucurbitaceae 2004, the 8th EUCARPIA meeting on cucurbit genetics and breeding (pp. 281–287). Palacký University in Olomouc: Olomouc.Google Scholar
  34. Lebeda, A., & Sedláková, B. (2006). Identification and survey of cucurbit powdery mildew races in Czech populations. In G. J. Holmes (Ed.), Proceedings of Cucurbitaceae 2006 (pp. 444–452). Raleigh: Universal Press.Google Scholar
  35. Lebeda, A., & Sedláková, B. (2010). Screening for resistance to cucurbit powdery mildews (Golovinomyces cichoracearum, Podosphaera xanthii), Chapter 19. In M. M. Spencer & A. Lebeda (Eds.), Mass screening techniques for selecting crops resistant to disease (pp. 295–307). Vienna: International Atomic Energy Agency (IAEA).Google Scholar
  36. Lebeda, A., Sedláková, B., & Křístková, E. (2004). Distribution, harmfulness and pathogenic variability of cucurbit powdery mildew in the Czech Republic. Acta fytotechnica et zootechnica, 7, 174–176.Google Scholar
  37. Lebeda, A., Sedláková, B., & Křístková, E. (2007a). Temporal changes in pathogenicity structure of cucurbit powdery mildew populations. Acta Horticulturae, 731, 381–388.CrossRefGoogle Scholar
  38. Lebeda, A., Sedláková, B., Křístková, E., & Vysoudil, M. (2009). Long-lasting changes in the species spectrum of cucurbit powdery mildew in the Czech Republic – influence of climate changes or random effect? Plant Protection Science, 45(Special Issue), S41–S47.CrossRefGoogle Scholar
  39. Lebeda, A., Widrlechner, M. P., Staub, J., Ezura, H., Zalapa, J., & Křístková, E. (2007b). Cucurbits (Cucurbitaceae; Cucumis spp., Cucurbita spp., Citrullus spp.) In R. J. Singh (Ed.), Genetic resources, chromosome engineering, and crop improvement, vol. 3, vegetable crops (pp. 271–376). Boca Raton: CRC Press, Taylor and Francis Group.Google Scholar
  40. Lebeda, A., & Zinkernagel, V. (2003). Evolution and distribution of virulence in the German population of Bremia lactucae. Plant Pathology, 52, 41–51.CrossRefGoogle Scholar
  41. Limpert, E., & Müller, K. (1994). Designation of pathotypes of plant pathogens. Journal of Phytopathology, 140, 346–358.CrossRefGoogle Scholar
  42. Limpert, E., Clifford, B., Dreiseitl, A., Johnson, R., Müller, K., Roelfs, A., & Wellings, C. (1994). Systems of designation of pathotypes of plant pathogens. Journal of Phytopathology, 140, 359–362.CrossRefGoogle Scholar
  43. Liu, T., Wan, A., Liu, D., & Chen, X. (2017). Changes of races and virulence genes in Puccinia striiformis f. sp. tritici, the wheat stripe rust pathogen, in the United States from 1968 to 2009. Plant Disease.
  44. Manisterski, J., Eyal, Z., Ben-Yehuda, P., & Kosman, E. (2000). Comparative analysis of indices in the study of virulence diversity between and within populations of Puccinia recondita f. sp. tritici in Israel. Phytopathology, 90, 601–607.CrossRefPubMedGoogle Scholar
  45. McCreight, J. D. (2006). Melon–powdery mildew interactions reveal variation in melon cultigens and Podosphaera xanthii races 1 and 2. Journal of the American Society for Horticultural Science, 131, 59–65.Google Scholar
  46. McGrath, M. T. (1996). Increased resistance to triadimefon and to benomyl in Sphaerotheca fuliginea populations following fungicide usage over one season. Plant Disease, 80, 633–639.CrossRefGoogle Scholar
  47. McDonald, B. A., & Linde, C. (2002). Pathogen population genetics, evolutionary potential, and durable resistance. Annual Review of Phytopathology, 40, 349–379.CrossRefPubMedGoogle Scholar
  48. Miazzi, M., Laguardia, C., & Faretza, F. (2011). Variation in Podosphaera xanthii on cucurbits in Southern Italy. Journal of Phytopathology, 159, 538–545.CrossRefGoogle Scholar
  49. Milgroom, G. M. (2015). Population biology of plant pathogens; genetics, ecology, and evolution. St. Paul: APS Press.Google Scholar
  50. Müller, K., McDermott, J. M., Wolfe, M. S., & Limpert, E. (1996). Analysis of diversity in populations of plant pathogens: the barley powdery mildew pathogen across Europe. European Journal of Plant Pathology, 102, 385–395.CrossRefGoogle Scholar
  51. Pérez-Garcia, A., Romero, D., Fernández-Ortuño, D., López-Ruiz, F., De Vicente, A., & Torés, J. A. (2009). The powdery mildew fungus Podosphaera fusca (synonym Podosphaera xanthii), a constant threat to cucurbits. Molecular Plant Pathology, 10, 153–160.CrossRefPubMedGoogle Scholar
  52. Petrželová, I., Lebeda, A., & Kosman, E. (2013). Distribution, disease level and virulence variation of Bremia lactucae on Lactuca sativa in the Czech Republic in the period 1999–2011. Journal of Phytopathology, 161, 503–514.CrossRefGoogle Scholar
  53. Pirondi, A., Pérez-Garcia, A., Battistini, G., Muzzi, E., Brunelli, A., & Collina, M. (2015a). Seasonal variations in the occurrence of Golovinomyces orontii and Podosphaera xanthii, causal agents of cucurbit powdery mildew in Northern Italy. Annals of Applied Biology, 167, 298–313.CrossRefGoogle Scholar
  54. Pirondi, A., Vela-Corcía, D., Dondini, L., Brunelli, A., Pérez-García, A., & Collina, M. (2015b). Genetic diversity analysis of the cucurbit powdery mildew fungus Podosphaera xanthii suggests a clonal population structure. Fungal Biology, 119, 791–801.CrossRefPubMedGoogle Scholar
  55. Pirondi, L., Kitner, M., Iotti, M., Sedláková, B., Lebeda, A., & Collina, M. (2016). Genetic structure and phylogeny of Italian and Czech populations of the cucurbit powdery mildew fungus Golovinomyces orontii inferred by multilocus sequence typing. Plant Pathology, 65, 959–967.CrossRefGoogle Scholar
  56. Pitrat, M., Dogimont, C., & Bardin, M. (1998). Resistance to fungal diseases of foliage in melon. In J. D. McCreight (Ed.), Cucurbitaceae '98: Evaluation and enhancement of cucurbit germplasm (pp. 167–173). Alexandria: ASHS Press.Google Scholar
  57. Schachtel, G. A., Dinoor, A., Herrmann, A., & Kosman, E. (2012). Comprehensive evaluation of virulence and resistance data: a new analysis tool. Plant Disease, 96, 1060–1063.CrossRefGoogle Scholar
  58. Sedláková, B., & Lebeda, A. (2008). Fungicide resistance in Czech populations of cucurbit powdery mildews. Phytoparasitica, 36, 272–289.CrossRefGoogle Scholar
  59. Sedláková, B., & Lebeda, A. (2010). Temporal population dynamics of cucurbit powdery mildews (Golovinomyces cichoracearum and Podosphaera xanthii) in the Czech Republic. In J. A. Thies, S. Kousik, & A. Levi (Eds.), Cucurbitaceae 2010 proceedings (pp. 244–247). Alexandria: American Society for Horticultural Science.Google Scholar
  60. Sedláková, B., Lebeda, A., Gryczová, K., & Křístková, E. (2014). Virulence structure (pathotypes, races) of cucurbit powdery mildew populations in the Czech Republic in the years 2010 – 2012. In M. Havey, Y. Weng, B. Day, & R. Grumet (Eds.), Cucurbitaceae 2014 proceedings (pp. 28–31). Alexandria: American Society for Horticultural Science.Google Scholar
  61. Sedláková, B., Rušáková, E., Křístková, E., & Lebeda, A. (2016). Long-lasting (2001-2009) variation in virulence among Czech cucurbit powdery mildew populations screened on eleven Cucumis melo differential genotypes. In E. U. Kozik & H. S. Paris (Eds.), Proceedings of Cucurbitaceae 2016, XIth EUCARPIA meeting on genetics and breeding of Cucurbitaceae (pp. 268–271). Skierniewice: Wydawnictvo SIGMA Sp. J.Google Scholar
  62. Skolotneva, E. S., Lekomtseva, S. N., & Kosman, E. (2013). The wheat stem rust pathogen in the central region of the Russian Federation. Plant Pathology, 62, 1003–1010.CrossRefGoogle Scholar
  63. Takamatsu, S., Matsuda, S., & Grigaliunaite, B. (2013). Comprehensive phylogenetic analysis of the genus Golovinomyces (Ascomycota: Erysiphales) reveals close evolutionary relationship with its host plants. Mycologia, 105, 1135–1152.CrossRefPubMedGoogle Scholar
  64. Zlochová, K. (1990). Fytopatogénne mikromycéty čeľade Erysiphaceae parazitujúce na hostiteľských rastlinách čeľade Cucurbitaceae na území Slovenska. Autoreferát dizertácie na získanie vedeckej hodnosti kandidáta biologických vied (20 p.). Bratislava, Slovak Republic: Slovenská akadémia vied. (in Slovak).Google Scholar

Copyright information

© Koninklijke Nederlandse Planteziektenkundige Vereniging 2018

Authors and Affiliations

  • Aleš Lebeda
    • 1
    Email author
  • Eva Křístková
    • 1
  • Božena Sedláková
    • 1
  • James D. McCreight
    • 2
  • Evsey Kosman
    • 3
  1. 1.Faculty of Science, Department of BotanyPalacký University in OlomoucOlomoucCzech Republic
  2. 2.U.S. Department of AgricultureAgricultural Research ServiceSalinasUSA
  3. 3.Institute for Cereal Crops Improvement, the George S. Wise Faculty of Life SciencesTel-Aviv UniversityOlomouc-HoliceIsrael

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