, Volume 47, Issue 5, pp 693–709 | Cite as

Severe outbreaks of Phytophthora infestans on potato in Turkey caused by recent changes in the pathogen population structure

  • Mehmet Erhan GöreEmail author
  • Nedim Altın
  • Tolga Yaman
  • Kevin Myers
  • Abdurrahman Çağlı
  • David E. L. Cooke
  • Uğur Pırlak
  • Mehtap Alkan
  • Hüseyin Kabakçı
  • Nusret Zencirci
  • William Earl Fry
  • Göksel Özer


Potato late blight, caused by Phytophthora infestans, has been the most damaging disease in Turkey since 2010. In this study, 127 isolates of P. infestans were obtained from the main growing areas of Turkey between 2015 and 2017. Their phenotypic and genotypic features were revealed and presented with those of reference isolates. These isolates were categorized by their mating type, in vitro mefenoxam sensitivity, mtDNA haplotype, RG57 DNA fingerprinting patterns, simple sequence repeat (SSR) markers, and aggressiveness on a set of potato differential lines. All isolates were of the A2 mating type and mtDNA haplotype Ia, were resistant to mefenoxam, and had RG57 and SSR fingerprints similar to the 13_A2 clonal lineage reported in Europe. This is the first report of 13_A2 in Turkey. Virulence abilities against potato resistance (R) genes R1, R2, R3, R4, R6, R7, R10, and R11 were observed in most of the isolates. The mating type ratios and SSR marker analysis indicate that in Turkey, the sexual reproduction of P. infestans is limited. These results underline that the movement of asexual individuals and the generation of sub-clonal difference are the factors driving the population structure of P. infestans in Turkey.


Genotype Late blight Mefenoxam resistance Virulence phenotype 


Authors’ contributions

MEG and WEF designed the study. MEG, NA, GÖ, KM, AÇ, WEF, UP, TY, MA, HK, DELC, and NZ carried out the experiments. MEG, WEF, NA, GÖ, and DELC contributed to the interpretation of the results. MEG took the lead in writing the manuscript. All authors read and approved the final manuscript.

Funding information

This research was supported by TUBITAK (grant 116O329).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Bakonyi, J., Láday, M., Dula, T., & Érsek, T. (2002). Characterisation of isolates of Phytophthora infestans from Hungary. European Journal of Plant Pathology, 108(2), 139–146.Google Scholar
  2. Black, W., Mastenbroek, C., Mills, W. R., & Peterson, L. C. (1953). A proposal for an international nomenclature of races of Phytophthora infestans and of genes controlling immunity in Solanum demissum derivatives. Euphytica, 2(3), 173–179.Google Scholar
  3. Blandón-Díaz, J. U., Widmark, A. K., Hannukkala, A., Andersson, B., Högberg, N., & Yuen, J. E. (2012). Phenotypic variation within a clonal lineage of Phytophthora infestans infecting both tomato and potato in Nicaragua. Phytopathology, 102(3), 323–330.PubMedGoogle Scholar
  4. Brurberg, M. B., Elameen, A., Le, V. H., et al. (2011). Genetic analysis of Phytophthora infestans populations in the Nordic European countries reveals high genetic variability. Fungal Biology, 115(4–5), 335–342.PubMedGoogle Scholar
  5. Caten, C. E., & Jinks, J. L. (1968). Spontaneous variability of single isolates of Phytophthora infestans. I. Cultural variation. Canadian Journal of Botany, 46(4), 329–348.Google Scholar
  6. Chmielarz, M., Sobkowiak, S., Debski, K., Cooke, D. E. L., Brurberg, M. B., & Sliwka, J. (2014). Diversity of Phytophthora infestans from Poland. Plant Pathology, 63(1), 203–211.Google Scholar
  7. Chowdappa, P., Kumar, N. B. J., Madhura, S., Kumar, M. S. P., Myers, K. L., Fry, W. E., Squires, J. N., & Cooke, D. E. L. (2013). Emergence of 13_A2 blue lineage of Phytophthora infestans was responsible for severe outbreaks of late blight on tomato in south-West India. Journal of Phytopathology, 161(1), 49–58.Google Scholar
  8. Chowdappa, P., Kumar, N. B. J., Madhura, S., Kumar, M. S. P., Myers, K. L., Fry, W. E., & Cooke, D. E. L. (2015). Severe outbreaks of late blight on potato and tomato in South India caused by recent changes in the Phytophthora infestans population. Plant Pathology, 64(1), 191–199.Google Scholar
  9. Cohen, Y., Reuveni, M., & Eyal, H. (1979). The systemic antifungal activity of Ridomil against Phytophthora infestans on tomato plants. Phytopathology, 69(6), 645–649.Google Scholar
  10. Cooke, D. E. L., & Lees, A. K. (2004). Markers, old and new, for examining Phytophthora infestans diversity. Plant Pathology, 53(6), 692–704.Google Scholar
  11. Cooke, L. R., Little, G., Armstrong, C., et al. (2009). Recent changes in the Phytophthora infestans population in Northern Ireland and first results from a new all-Ireland late blight project. PPO-Special Report, 13, 183–190.Google Scholar
  12. Cooke, L. R., Schepers, H. T. A. M., Hermansen, A., Bain, R. A., Bradshaw, N. J., Ritchie, F., Shaw, D. S., Evenhuis, A., Kessel, G. J. T., Wander, J. G. N., Andersson, B., Hansen, J. G., Hannukkala, A., Nærstad, R., & Nielsen, B. J. (2011). Epidemiology and integrated control of potato late blight in Europe. Potato Research, 54(2), 183–222.Google Scholar
  13. Cooke, D. E. L., Cano, L. M., Raffaele, S., Bain, R. A., Cooke, L. R., Etherington, G. J., Deahl, K. L., Farrer, R. A., Gilroy, E. M., Goss, E. M., Grünwald, N. J., Hein, I., MacLean, D., McNicol, J. W., Randall, E., Oliva, R. F., Pel, M. A., Shaw, D. S., Squires, J. N., Taylor, M. C., Vleeshouwers, V. G. A. A., Birch, P. R. J., Lees, A. K., & Kamoun, S. (2012). Genome analyses of an aggressive and invasive lineage of the Irish potato famine pathogen. PLoS Pathogens, 8(10), 1–14.Google Scholar
  14. Danies, G., Small, I. M., Myers, K., Childers, R., & Fry, W. E. (2013). Phenotypic characterization of recent clonal lineages of Phytophthora infestans in the United States. Plant Disease, 97(7), 873–881.PubMedGoogle Scholar
  15. Deahl, K. L., Pagani, M. C., Vilaro, F. L., Perez, F. M., Moravec, B., & Cooke, L. R. (2003). Characteristics of Phytophthora infestans isolates from Uruguay. European Journal of Plant Pathology, 109(3), 277–281.Google Scholar
  16. Dey, T., Saville, A., Myers, K., Tewari, S., Cooke, D. E. L., Tripathy, S., Fry, W. E., Ristaino, J. B., & Roy, S. G. (2018). Large sub-clonal variation in Phytophthora infestans from recent severe late blight epidemics in India. Scientific Reports, 8, 4429.PubMedPubMedCentralGoogle Scholar
  17. Flier, W. G., Kroon, L. P. N. M., Hermansen, A., van Raaij, H. M. G., Speiser, B., Tamm, L., Fuchs, J. G., Lambion, J., Razzaghian, J., Andrivon, D., Wilcockson, S., & Leifert, C. (2007). Genetic structure and pathogenicity of populations of Phytophthora infestans from organic potato crops in France, Norway, Switzerland and the United Kingdom. Plant Pathology, 56(4), 562–572.Google Scholar
  18. Forbes, G. A. (2012). Using host resistance to manage potato late blight with particular reference to developing countries. Potato Research, 55(3–4), 205–216.Google Scholar
  19. Forbes, G. A., Goodwin, S. B., Drenth, A., Oyarzun, P., Ordonez, M. E., & Fry, W. E. (1998). A global marker database for Phytophthora infestans. Plant Disease, 82(7), 811–818.PubMedGoogle Scholar
  20. Fry, W. E. (2008). Phytophthora infestans: the plant (and R gene) destroyer. Molecular Plant Pathology, 9(3), 385–402.PubMedPubMedCentralGoogle Scholar
  21. Fry, W. E., Goodwin, S. B., Dyer, A. T., Matuzak, J. M., Drenth, A., Tooley, P. W., Sujkowski, L. S., Koh, Y. J., Cohen, B. A., Spielman, L. J., Deahl, K. L., Inglis, D. A., & Sandlan, K. P. (1993). Historical and recent migration of Phytophthora infestans: chronology, pathways and implication. Plant Disease, 77(7), 653–661.Google Scholar
  22. Goodwin, S. B., Drenth, A., & Fry, W. E. (1992). Cloning and genetic analyses of two highly polymorphic, moderately repetitive nuclear DNAs from Phytophthora infestans. Current Genetics, 22(2), 107–115.PubMedGoogle Scholar
  23. Goodwin, S., Schneider, R., & Fry, W. E. (1995). Use of cellulose-acetate electrophoresis for rapid identification of allozyme genotypes of Phytophthora infestans. Plant Disease, 79(11), 1181–1185.Google Scholar
  24. Griffith, G. W., & Shaw, D. S. (1998). Polymorphisms in Phytophthora infestans: four mitochondrial haplotypes are detected after PCR amplification of DNA from pure cultures or from host lesions. Applied and Environmental Microbiology, 64(10), 4007–4014.PubMedPubMedCentralGoogle Scholar
  25. Grünwald, N. J., Sturbaum, A. K., Romero Montes, G., Garray Serrano, E., Lozoya-Saldaña, H., & Fry, W. E. (2006). Selection for fungicide resistance within a growing season in field populations of Phytophthora infestans at the center of origin. Phytopathology, 96(12), 1397–1403.PubMedGoogle Scholar
  26. Gunacti, H., Ay, T., & Can, C. (2019). Genotypic and phenotypic characterization of Phytophthora infestans populations from potato in Turkey. Phytoparasitica, 47(3), 429–439.Google Scholar
  27. Guo, J., van der Lee, T., Qu, D. Y., Yao, Y. Q., Gong, X. F., Liang, D. L., Xie, K. Y., Wang, X. W., & Govers, F. (2009). Phytophthora infestans isolates from Northern China show high virulence diversity but low genotypic diversity. Plant Biology, 11(1), 57–67.PubMedGoogle Scholar
  28. Hu, C. H., Perez, F., Donohoo, R., et al. (2012). Recent genotypes of Phytophthora infestans in eastern USA reveal clonal populations and reappearance of mefenoxam sensitivity. Plant Disease, 96(9), 1323–1330.PubMedGoogle Scholar
  29. Jiang, R. H. Y., Tripathy, S., Govers, F., & Tyler, B. M. (2008). The RXLR effector reservoir in two Phytophthora species is dominated by a single rapidly evolving super-family with more than 700 members. Proceedings of the National Academy of Sciences of the United States of America, 105(2), 4874–4879.PubMedPubMedCentralGoogle Scholar
  30. Judelson, H. S. (1997). The genetics and biology of Phytophthora infestans: modern approaches to a historical challenge. Fungal Genetics and Biology, 22(2), 65–76.PubMedGoogle Scholar
  31. Kanetis, L., Pittas, L., Tsaltas, D., & Ioannou N. (2013). Population structure of P. infestans in Cyprus and a synopsis on its Mediterranean status. EuroBlight Workshop, 12-15 May, Limassol, Cyprus.Google Scholar
  32. Kiiker, R., Hansen, M., Williams, I. H., Cooke, D. E. L., & Runno-Paurson, E. (2018). Outcome of sexual reproduction in the Phytophthora infestans population in Estonian potato fields. European Journal of Plant Pathology, 152(2), 395–407.Google Scholar
  33. Knapova, G., & Gisi, U. (2002). Phenotypic and genotypic structure of Phytophthora infestans populations on potato and tomato in France and Switzerland. Plant Pathology, 51(5), 641–653.Google Scholar
  34. Kröner, A., Mabon, R., Corbiére, R., Montarry, J., & Andrivon, D. (2017). The coexistence of generalist and specialist clonal lineages in natural populations of the Irish Famine pathogen Phytophthora infestans explains local adaptation to potato and tomato. Molecular Ecology, 26(7), 1891–1901.PubMedGoogle Scholar
  35. Kumar, S., Stecher, G., Li, M., Knyaz, C., & Tamura, K. (2018). MEGA X: molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution, 35(6), 1547–1549.PubMedPubMedCentralGoogle Scholar
  36. Lees, A. K., Wattier, R., Shaw, D. S., Sullivan, L., Williams, N. A., & Cooke, D. E. L. (2006). Novel microsatellite markers for the analysis of Phytophthora infestans populations. Plant Pathology, 55(3), 311–319.Google Scholar
  37. Lehtinen, A., Hannukkala, A., Andersson, B., Hermansen, A., Le, V. H., Naerstad, R., Brurberg, M. B., Nielsen, B. J., Hansen, J. G., & Yuen, J. (2008). Phenotypic variation in Nordic populations of Phytophthora infestans in 2003. Plant Pathology, 57(2), 227–234.Google Scholar
  38. Li, Y., Govers, F., Mendes, O., Testa, A., Jacobsen, E., Huang, S. W., & van der Lee, T. A. J. (2010). A new set of highly informative SSR markers for Phytophthora infestans population analysis assembled into an efficient multiplex. Molecular Ecology Resources, 10(6), 1098–1105.PubMedGoogle Scholar
  39. Li, Y., van der Lee, T. A., Evenhuis, A., et al. (2012). Population dynamics of Phytophthora infestans in the Netherlands reveals expansion and spread of dominant clonal lineages and virulence in sexual offspring.G3. Genes Genomes Genetics, 2(12), 1529–1540.PubMedGoogle Scholar
  40. Li, Y., Cooke, D. E. L., Jacobsen, E., & van der Lee, T. (2013a). Efficient multiplex simple sequence repeat genotyping of the oomycete plant pathogen Phytophthora infestans. Journal of Microbiological Methods, 92(3), 316–322.PubMedGoogle Scholar
  41. Li, Y., van der Lee, T., Zhu, J. H., Jin, G. H., Lan, C. Z., Zhu, S. X., Zhang, R. F., Liu, B. W., Zhao, Z. J., Kessel, G., Huang, S. W., & Jacobsen, E. (2013b). Population structure of Phytophthora infestans in China - geographic clusters and presence of the EU genotype Blue_13. Plant Pathology, 62(4), 932–942.Google Scholar
  42. Malcolmson, J. F., & Black, W. (1966). New R genes in Solanum demissum Lindl. and their complementary races of Phytophthora infestans (Mont.) de Bary. Euphytica, 15(2), 199–203.Google Scholar
  43. Mariette, N., Mabon, R., Corbiere, R., Boulard, F., Glais, I., Marquer, B., Pasco, C., Montarry, J., & Andrivon, D. (2016). Phenotypic and genotypic changes in French populations of Phytophthora infestans: are invasive clones the most aggressive? Plant Pathology, 65(4), 577–586.Google Scholar
  44. Montes, M. S., Nielsen, B. J., Schmidt, S. G., Bødker, L., Kjøller, R., & Rosendahl, S. (2016). Population genetics of Phytophthora infestans in Denmark reveals dominantly clonal populations and specific alleles linked to metalaxyl-M resistance. Plant Pathology, 65(5), 744–753.Google Scholar
  45. Pérez, W. G., Gamboa, J. S., Falcon, Y. V., Coca, M., Raymundo, R. M., & Nelson, R. J. (2001). Genetic structure of Peruvian populations of Phytophthora infestans. Phytopathology, 91(10), 956–965.PubMedGoogle Scholar
  46. Rekad, F. Z., Cooke, D. E. L., Puglisi, I., Randall, E., Guenaoui, Y., Bouznad, Z., Evoli, M., Pane, A., Schena, L., Magnano di San Lio, G., & Cacciola, S. O. (2017). Characterization of Phytophthora infestans populations in northwestern Algeria during 2008-2014. Fungal Biology, 121(5), 467–477.PubMedGoogle Scholar
  47. Ristaino, J. B., Groves, C. T., & Parra, G. R. (2001). PCR amplification of the Irish potato famine pathogen from historic specimens. Nature, 411, 695–697.PubMedGoogle Scholar
  48. Runno-Paurson, E., Fry, W. E., Myers, K. L., Koppel, M., & Mand, M. (2009). Characterisation of Phytophthora infestans isolates collected from potato in Estonia during 2002-2003. European Journal of Plant Pathology, 124(4), 565–575.Google Scholar
  49. R Development Core Team. (2019). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.Google Scholar
  50. Stellingwerf, J. S., Phelan, S., Doohan, F. M., Ortiz, V., Griffin, D., Bourke, A., Hutten, R. C. B., Cooke, D. E. L., Kildea, S., & Mullins, E. (2018). Evidence for selection pressure from resistant potato genotypes but not from fungicide application within a clonal Phytophthora infestans population. Plant Pathology, 67(7), 1528–1538.Google Scholar
  51. Stroud, J. A., Shaw, D. S., Hale, M. D., & Steele, K. A. (2016). SSR assessment of Phytophthora infestans populations on tomato and potato in British gardens demonstrates high diversity but no evidence for host specialization. Plant Pathology, 65(2), 334–341.Google Scholar
  52. Tian, Y. E., Yin, J. L., Sun, J. P., Ma, Y. F., Wang, Q. H., Quan, J. L., & Shan, W. X. (2016). Population genetic analysis of Phytophthora infestans in northwestern China. Plant Pathology, 65(1), 17–25.Google Scholar
  53. Tosun, N., Yıldırım, A., Türküsay, H., & Tanyolaç, B. (2007). Genetic variation among Phytophthora infestans (tomato blight) isolates from western Turkey revealed by inter simple sequence repeat (ISSR) and random amplified polymorphic DNA (RAPD) markers. Pakistan Journal of Botany, 39(3), 897–902.Google Scholar
  54. TUIK (2018). Accessed 10 Sept 2019.

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  • Mehmet Erhan Göre
    • 1
    Email author
  • Nedim Altın
    • 2
  • Tolga Yaman
    • 1
  • Kevin Myers
    • 3
  • Abdurrahman Çağlı
    • 4
  • David E. L. Cooke
    • 5
  • Uğur Pırlak
    • 4
  • Mehtap Alkan
    • 1
  • Hüseyin Kabakçı
    • 1
  • Nusret Zencirci
    • 6
  • William Earl Fry
    • 3
  • Göksel Özer
    • 1
  1. 1.Department of Plant Protection, Faculty of Agriculture and Natural ScienceAbant Izzet Baysal UniversityBoluTurkey
  2. 2.Department of Plant Protection, Faculty of Agriculture and Natural ScienceDüzce UniversityDüzceTurkey
  3. 3.Department of Plant Pathology and Plant-Microbe BiologyCornell UniversityIthacaUSA
  4. 4.Potato Research Institute, General Directorate of Agricultural Research and PoliciesMinistry of Agriculture and ForestryNiğdeTurkey
  5. 5.James Hutton InstituteDundeeUK
  6. 6.Department of Biology, Faculty of Arts and ScienceAbant Izzet Baysal UniversityBoluTurkey

Personalised recommendations