Outcome of sexual reproduction in the Phytophthora infestans population in Estonian potato fields

  • Riinu Kiiker
  • Merili Hansen
  • Ingrid H. Williams
  • David E. L. Cooke
  • Eve Runno-Paurson
Article
First Online:
Accepted:
  • 8 Downloads

Abstract

In this study, the Estonian population of Phytophthora infestans was characterized with mating type, sensitivity to metalaxyl, virulence on 11 potato R-gene differentials and 12 SSR markers to show the outcome of potential sexual reproduction in the population. During the three years 2010–2012, 141 P. infestans isolates, collected from 23 potato fields, showed quite a high and stable frequency of the A2 mating type, 48% of the total population. In 87% of all sampled potato fields, both mating types were recorded, suggesting continuous sexual reproduction of P. infestans and possible oospore production. Metalaxyl-sensitive isolates prevailed in all three years (68 out of 99 isolates). Amongst the 95 isolates tested, 51 virulence races were found. The race structure was diverse, and most pathotypes were unique, appearing only once; the two most common pathotypes, 1.2.3.4.6.7.10.11 and 1.2.3.4.7.10.11, comprised 35% of the population. The P. infestans population was genetically highly diverse and most of the multilocus genotypes (MLGs) appeared only once. Furthermore, all of the MLGs appeared in only one of the three sampling years. Our results confirm that the high diversity in the Estonian P. infestans population is most likely the result of frequent sexual reproduction, which benefits the survival, adaptability and diversity of the pathogen in the climate of North-Eastern Europe.

Keywords

SSR markers Genetic diversity Mating type Virulence Metalaxyl resistance Late blight 
This is a preview of subscription content, log in to check access

Notes

Acknowledgments

Alice Aav, Gerit Dreyersdorff, Kätlin Jõgi, Liis Laane, Helina Nassar, Terje Tähtjärv and Grete Zahkna are thanked for technical support. We are grateful to Asko Hannukkala from the Natural Resources Institute Finland (Luke) for supplying tester isolates for mating type determination. Many thanks too to Dr. Eva Randall at the James Hutton Institute for technical assistance.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

10658_2018_1483_MOESM1_ESM.pdf (117 kb)
Online Resource 1 (PDF 117 kb)
10658_2018_1483_MOESM2_ESM.pdf (88 kb)
Online Resource 2 (PDF 87 kb)
10658_2018_1483_MOESM3_ESM.pdf (123 kb)
Online Resource 3 (PDF 122 kb)

References

  1. Aav, A., Skrabule, I., Bimšteine, G., Kaart, T., Williams, I. H., & Runno-Paurson, E. (2015). The structure of mating type, metalaxyl resistance and virulence of Phytophthora infestans isolates collected from Latvia. Zemdirbyste-Agriculture, 102, 335–342.CrossRefGoogle Scholar
  2. Agapow, P.-M., & Burt, A. (2001). Indices of multilocus linkage disequilibrium. Molecular Ecology Notes, 1, 101–102.CrossRefGoogle Scholar
  3. Balloux, F., Lehmann, L., & De Meeus, T. (2003). The population genetics of clonal and partially clonal diploids. Genetics, 164, 1635–1644.Google Scholar
  4. 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, 323–330.CrossRefPubMedGoogle Scholar
  5. Brurberg, M. B., Hannukkala, A., & Hermansen, A. (1999). Genetic variability of Phytophthora infestans in Norway and Finland as revealed by mating type and fingerprint probe RG57. Mycological Research, 103, 1609–1615.CrossRefGoogle Scholar
  6. Brurberg, M. B., Elameen, A., Le, V. H., Naerstad, R., Hermansen, A., Lehtinen, A., et al. (2011). Genetic analysis of Phytophthora infestans populations in the Nordic European countries reveals high genetic variability. Fungal Biology, 115, 335–342.CrossRefPubMedGoogle Scholar
  7. Bruvo, R., Michiels, N. K., D’Souza, T. G., & Schulenburg, H. (2004). A simple method for the calculation of microsatellite genotype distances irrespective of ploidy level. Molecular Ecology, 13, 2101–2106.CrossRefPubMedGoogle Scholar
  8. Brylinska, M., Sobkowiak, S., Stefanczyk, E., & Sliwka, J. (2016). Potato cultivation system affects population structure of Phytophthora infestans. Fungal Ecology, 20, 132–143.CrossRefGoogle Scholar
  9. Chmielarz, M., Sobkowiak, S., Dębski, K., Cooke, D. E. L., Brurberg, M. B., & Śliwka, J. (2014). Diversity of Phytophthora infestans from Poland. Plant Pathology, 63, 203–211.CrossRefGoogle Scholar
  10. Chowdappa, P., Nirmal Kumar, B. J., Madhura, S., Mohan Kumar, 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, 191–199.CrossRefGoogle Scholar
  11. Cooke, D. E. L., & Lees, A. K. (2004). Markers, old and new, for examining Phytophthora infestans diversity. Plant Pathology, 53, 692–704.CrossRefGoogle Scholar
  12. 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, e1002940.CrossRefPubMedPubMedCentralGoogle Scholar
  13. 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, 183–222.CrossRefGoogle Scholar
  14. Drenth, A., Janssen, E. M., & Govers, F. (1995). Formation and survival of oospores of Phytophthora infestans under natural conditions. Plant Pathology, 44, 86–94.CrossRefGoogle Scholar
  15. Estonian Weather Service (2016). Climate normals. http://www.ilmateenistus.ee/kliima/kliimanormid/ohutemperatuur/?lang=en. Accessed 16 July 2016.
  16. EuroBlight (2017). A potato late blight network for Europe. euroblight.net. Accessed 1 March 2017.
  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, 562–572.CrossRefGoogle Scholar
  18. Fry, W. E., Goodwin, S. B., Dyer, A. T., Matuszak, J. M., Drenth, A., Tooley, P. W., et al. (1993). Historical and recent migrations of Phytophthora infestans: Chronology, pathways, and implications. Plant Disease, 77, 653–661.CrossRefGoogle Scholar
  19. Fry, W. E., McGrath, M. T., Seaman, A., Zitter, T. A., McLeod, A., Danies, G., Small, I. M., Myers, K., Everts, K., Gevens, A. J., Gugino, B. K., Johnson, S. B., Judelson, H., Ristaino, J., Roberts, P., Secor, G., Seebold Jr., K., Snover-Clift, K., Wyenandt, A., Grünwald, N. J., & Smart, C. D. (2013). The 2009 late blight pandemic in the eastern United States – causes and results. Plant Disease, 97, 296–306.CrossRefGoogle Scholar
  20. Gisi, U., & Cohen, Y. (1996). Resistance to phenylamide fungicides: A case study with Phytophthora infestans involving mating type and race structure. Annual Review of Phytopathology, 34, 549–572.CrossRefPubMedGoogle Scholar
  21. Gisi, U., Walder, F., Resheat-Eini, Z., Edel, D., & Sierotzki, H. (2011). Changes of genotype, sensitivity and aggressiveness in Phytophthora infestans isolates collected in European countries in 1997, 2006 and 2007. Journal of Phytopathology, 159, 223–232.CrossRefGoogle Scholar
  22. Goodwin, S. B., Cohen, B. A., & Fry, W. E. (1994). Panglobal distribution of a single clonal lineage of the Irish potato famine fungus. Proceedings of the National Academy of Science of the USA, 91, 11591–11595.CrossRefGoogle Scholar
  23. Grönberg, L., Andersson, B., & Yuen, J. (2012). Can weed hosts increase aggressiveness of Phytophthora infestans on potato? Phytopathology, 102, 429–433.CrossRefPubMedGoogle Scholar
  24. Hannukkala, A. O. (2012). History and consequences of migrations, changes in epidemiology and population structure of potato late blight, Phytophthora infestans, in Finland from 1845 to 2011. Doctoral Dissertation. MTT Science 18. MTT Agrifood Research Finland, Jokioinen, 136 p. Available at http://www.mtt.fi/mtttiede/pdf/mtttiede18.pdf.
  25. Hannukkala, A. O., Kaukoranta, T., Lehtinen, A., & Rahkonen, A. (2007). Late-blight epidemics on potato in Finland, 1933-2002; increased and earlier occurrence of epidemics associated with climate change and lack of rotation. Plant Pathology, 56, 167–176.CrossRefGoogle Scholar
  26. Hermansen, A., Hannukkala, A., Hafskjold Nærstad, R., & Brurberg, M. B. (2000). Variation in populations of Phytophthora infestans in Finland and Norway: Mating type, metalaxyl resistance and virulence phenotype. Plant Pathology, 49, 11–22.CrossRefGoogle Scholar
  27. Hu, C.-H., Perez, F. G., Donahoo, R., McLeod, A., Myers, K., Ivors, K., et al. (2012). Recent genotypes of Phytophthora infestans in the eastern United States reveal clonal populations and reappearance of mefenoxam sensitivity. Plant Disease, 96, 1323–1330.CrossRefGoogle Scholar
  28. Kamvar, Z. N., Tabima, J. F., & Grünwald, N. J. (2014). poppr: an R package for genetic analysis of populations with mixed (clonal/sexual) reproduction. Peer J, 2, e281.CrossRefPubMedPubMedCentralGoogle Scholar
  29. Knapova, G., & Gisi, U. (2002). Phenotypic and genotypic structure of Phytophthora infestans populations on potato and tomato in France and Switzerland. Plant Pathology, 51, 641–653.CrossRefGoogle Scholar
  30. 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, 311–319.CrossRefGoogle Scholar
  31. Lehtinen, A., & Hannukkala, A. (2004). Oospores of Phytophthora infestans in soil provide an important new source of primary inoculum in Finland. Agricultural and Food Science, 13, 399–410.CrossRefGoogle Scholar
  32. Lehtinen, A., Hannukkala, A., Andersson, B., Hermansen, A., Le, V. H., Naerstad, R., et al. (2008). Phenotypic variation in Nordic populations of Phytophtora infestans in 2003. Plant Pathology, 57, 227–234.CrossRefGoogle Scholar
  33. Li, Y., van der Lee, T. A. J., Evenhuis, A., van den Bosch, G. B. M., van Bekkum, P. J., Förch, M. G., 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, 1529–1540.PubMedPubMedCentralGoogle Scholar
  34. 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, 316–322.CrossRefPubMedGoogle Scholar
  35. 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, 932–942.CrossRefGoogle Scholar
  36. 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, 199–203.CrossRefGoogle Scholar
  37. Mazakova, J., Taborsky, V., Zouhar, M., Ryšanek, P., Hausvater, E., & Doležal, P. (2006). Occurrence and distribution of mating types A1 and A2 of Phytophthora infestans (Mont.) de Bary in the Czech Republic. Plant Protection Science, 42, 41–48.CrossRefGoogle Scholar
  38. Mayton, H., Smart, C. D., Moravec, B. C., Mizubuti, E. S. G., Muldoon, A. E., & Fry, W. E. (2000). Oospore survival and pathogenicity of single oospore recombinant progeny from 23 a cross involving US-17 and US-8 genotypes of Phytophthora infestans. Plant Disease, 84, 1190–1196.CrossRefGoogle Scholar
  39. Michalska, A. M., Sobkowiak, S., Flis, B., & Zimnoch-Guzowska, E. (2016). Virulence and aggressiveness of Phytophthora infestans isolates collected in Poland from potato and tomato plants identified no strong specificity. European Journal of Plant Pathology, 144, 325–336.CrossRefGoogle Scholar
  40. Montarry, J., Andrivon, D., Glais, I., Corbiere, R., Mialdea, G., & Delmotte, F. (2010). Microsatellite markers reveal two admixed genetic groups and an ongoing displacement within the French population of the invasive plant pathogen Phytophthora infestans. Molecular Ecology, 19, 1965–1977.CrossRefPubMedGoogle Scholar
  41. 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, 744–753.CrossRefGoogle Scholar
  42. Nei, M. (1978). Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics, 89, 583–590.PubMedPubMedCentralGoogle Scholar
  43. Peakall, R., & Smouse, P. E. (2006). GENALEX 6: Genetic analysis in excel. Population genetic software for teaching and research. Molecular Ecology Notes, 6, 288–295.CrossRefGoogle Scholar
  44. Peakall, R., & Smouse, P. E. (2012). GenAlEx 6.5: Genetic analysis in excel. Population genetic software for teaching and research-an update. Bioinformatics, 28, 2537–2539.CrossRefPubMedPubMedCentralGoogle Scholar
  45. Pobedinskaya, M. A., Elansky, S. N., Statsyuk, N. V., & Plyakhnevich, M. P. (2011). Fungicide resistance of Russian Phytophthora infestans strains. PPO – Special Report, 15, 243–248.Google Scholar
  46. Runno-Paurson, E., Fry, W. E., Myers, K. L., Koppel, M., & Mänd, M. (2009). Characterisation of Phytophthora infestans isolates collected from potato in Estonia during 2002-2003. European Journal of Plant Pathology, 124, 565–575.CrossRefGoogle Scholar
  47. Runno-Paurson, E., Fry, W. E., Remmel, T., Mänd, M., & Myers, K. L. (2010). Phenotypic and genotypic characterisation of Estonian isolates of Phytophthora infestans in 2004-2007. Journal of Plant Pathology, 92, 375–384.Google Scholar
  48. Runno-Paurson, E., Hannukkala, A., Williams, I., Koppel, M., & Mänd, M. (2012). The structure of mating type, virulence, metalaxyl resistance of Phytophthora infestans in a long-term phenotypic study in distinct location in eastern Estonia. Journal of Plant Diseases and Protection, 119, 45–52.CrossRefGoogle Scholar
  49. Runno-Paurson, E., Williams, I. H., Metspalu, L., Kaart, T., & Mänd, M. (2013a). Current potato varieties are too susceptible to late blight to be grown without chemical control under north-east European conditions. Acta Agriculturae Scandinavica, Section B – Soil & Plant Science, 63, 80–88.Google Scholar
  50. Runno-Paurson, E., Hannukkala, A., Williams, I., Koppel, M., & Mänd, M. (2013b). Impact of phytosanitary quality of seed potato and temporal epidemic progress on the phenotypic diversity of Phytophthora infestans populations. American Journal of Potato Research, 90, 245–254.CrossRefGoogle Scholar
  51. Runno-Paurson, E., Hannukkala, A., Kotkas, K., Koppel, M., Williams, I. H., & Mänd, M. (2014). Population changes and phenotypic diversity of Phytophthora infestans isolates from Estonia and Finland. Journal of Plant Pathology, 96, 85–95.Google Scholar
  52. Runno-Paurson, E., Ronis, A., Hansen, M., Aav, A., & Williams, I. H. (2015). Lithuanian populations of Phytophthora infestans revealed a high phenotypic diversity. Journal of Plant Diseases and Protection, 122, 57–65.CrossRefGoogle Scholar
  53. Runno-Paurson, E., Kiiker, R., Joutsjoki, T., & Hannukkala, A. (2016). High genotypic diversity found among population of Phytophthora infestans collected in Estonia. Fungal Biology, 120, 385–392.CrossRefPubMedGoogle Scholar
  54. Shattock, R. C., Janssen, B. D., Whitbread, R., & Shaw, D. S. (1977). An interpretation of the frequencies of host specific genotypes of Phytophthora infestans in North Wales. Annals of Applied Biology, 86, 249–260.CrossRefGoogle Scholar
  55. Sheldon, A. L. (1969). Equitability indices: Dependence on the species count. Ecology, 50, 466–467.CrossRefGoogle Scholar
  56. Sjöholm, L., Andersson, B., Högberg, N., Widmark, A.-K., & Yuen, J. (2013). Genotypic diversity and migration patterns of Phytophthora infestans in the Nordic countries. Fungal Biology, 117, 722–730.CrossRefPubMedGoogle Scholar
  57. Śliwka, J., Sobkowiak, S., Lebecka, R., Avendańo Córcoles, J., & Zimnoch-Guzowska, E. (2006). Mating type, virulence, aggressiveness and metalaxyl resistance of isolates of Phytophthora infestans in Poland. Potato Research, 49, 155–166.Google Scholar
  58. Spielman, L. J., Drenth, A., Davidse, L. C., Sujkowski, L. J., Gu, W., Tooley, P. W., & Fry, W. E. (1991). A second world-wide migration and population displacement of Phtyophthora infestans. Plant Pathology, 40, 422–430.CrossRefGoogle Scholar
  59. Statsyuk, N. V., Kozlovskaya, I. N., Koslovsky, B. E., Ulanova, T. I., Morozova, E. V., & Kuznetsova, M. (2013). Changes in phenotypic characteristics of the Moscow Phytophthora infestans population in the period of 2000–2011. Proceedings of the 4th International Symposium “Agrosym 2013” (pp. 607–613). Istočno Sarajevo: Jahorina.Google Scholar
  60. Statsyuk, N. V., Semina, Y. V., Perez, F. G. M., Larsen, M. M., Kuznetsova, M. A., Kozlovskaya, I. N., et al. (2014). Characterization of Russian Phytophthora infestans populations: DNA fingerprinting and SSR analysis. PPO – Special report, 16, 255–266.Google Scholar
  61. Turkensteen, L. J., Flier, W. G., Wanningen, R., & Mulder, A. (2000). Production, survival and infectivity of oospores of Phytophthora infestans. Plant Pathology, 49, 688–696.CrossRefGoogle Scholar
  62. USAblight (2017). A national project on tomato & potato late blight in the United States. https://usablight.org/. Accessed 1 March 2017.
  63. Vorobyeva, Y. V., Gridnev, V. V., Bashaeva, E. G., Pospelova, L. A., Kvasnyuk, N. Y., Kuznetsova, L. N., et al. (1991). On the occurrence of the A2 mating type isolates of Phytophthora infestans (Mont.) de Bary in the USSR. Mikologija i fitopatologija, 62–67.Google Scholar
  64. Widmark, A.-K., Andersson, B., Cassel-Lundhagen, A., Sandström, M., & Yuen, J. E. (2007). Phytophthora infestans in a single field in Southwest Sweden early in spring: Symptoms, spatial distribution and genotypic variation. Plant Pathology, 56, 573–579.CrossRefGoogle Scholar
  65. Yuen, J. E., & Andersson, B. (2013). What is the evidence for sexual reproduction of Phytophthora infestans in Europe? Plant Pathology, 62, 485–491.CrossRefGoogle Scholar

Copyright information

© Koninklijke Nederlandse Planteziektenkundige Vereniging 2018

Authors and Affiliations

  • Riinu Kiiker
    • 1
  • Merili Hansen
    • 1
  • Ingrid H. Williams
    • 1
  • David E. L. Cooke
    • 2
  • Eve Runno-Paurson
    • 1
  1. 1.Institute of Agricultural and Environmental SciencesEstonian University of Life SciencesTartuEstonia
  2. 2.The James Hutton InstituteDundeeUK

Personalised recommendations