, Volume 202, Issue 2, pp 219–234 | Cite as

An updated conventional- and a novel GM potato late blight R gene differential set for virulence monitoring of Phytophthora infestans

  • Suxian Zhu
  • Jack H. Vossen
  • Marjan Bergervoet
  • Maarten Nijenhuis
  • Linda Kodde
  • Geert J. T. Kessel
  • Vivianne Vleeshouwers
  • Richard G. F. Visser
  • Evert Jacobsen


Late blight is an important disease in potato that is caused by the oomycete Phytophthora infestans. In the past, Solanum demissum late blight resistance (R) genes were introgressed into cultivated potato (Solanum tuberosum). Eleven of these resistant plants were selected to characterize the virulence spectrum of individual P. infestans isolates and to monitor the dynamics of virulence in P. infestans populations. These plants are referred to as the Mastenbroek and Black differential sets. It has long been assumed that each differential plant contained one single R gene. In the current study and previous studies, however, most Mastenbroek differential plants were shown to harbor multiple R gene(s), which blurs virulence typing of late blight isolates. In order to acquire more accurate virulence profiles, we extended the Mastenbroek differential set with Solanum spp. plants harboring reduced R gene complexity and with plants containing recently identified R genes from related but different Solanum species. In addition, a differential set of ten Genetically Modified (GM) plants harboring single late blight R genes in the same genetic background (Desiree). By analyzing the virulence spectra of recently collected isolates using both newly described differential sets, we found that the GM Desiree differential set was more accurate for isolate virulence typing than the conventional (extended) differential set. Besides, the GM Desiree differential set was shown to be useful as trap plants to isolate novel P. infestans strains and to monitor virulence towards particular R genes in P. infestans populations `on site´. Legislative restrictions are, however, limiting the use of the GM Desiree differential set.


Potato Late blight Phytophthora infestans Differential set Resistance gene Virulence Genetic modification 

Supplementary material

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Supplementary material 1 (DOCX 12 kb)


  1. Armstrong MR, Whisson SC, Pritchard L, Bos JIB, Venter E, Avrova AO, Rehmany AP, Bohme U, Brooks K, Cherevach I, Hamlin N, White B, Frasers A, Lord A, Quail MA, Churcher C, Hall N, Berriman M, Huang S, Kamoun S, Beynon JL, Birch PRJ (2005) An ancestral oomycete locus contains late blight avirulence gene Avr3a, encoding a protein that is recognized in the host cytoplasm. Proc Natl Acad Sci USA 102:7766–7771CrossRefPubMedCentralPubMedGoogle Scholar
  2. Ballvora A, Ercolano MR, Weiss J, Meksem K, Bormann CA, Oberhagemann P, Salamini F, Gebhardt C (2002) The R1 gene for potato resistance to late blight (Phytophthora infestans) belongs to the leucine zipper/NBS/LRR class of plant resistance genes. Plant J 30:361–371CrossRefPubMedGoogle Scholar
  3. Black W, Mastenbroek C, Mills WR, Peterson LC (1953) A proposal for an international nomenclature of races of Phytophthora infestans and of genes controlling immunity in Solanum demissum derivates. Euphytica 2:173–179CrossRefGoogle Scholar
  4. Bus VGM, Rikkerink EHA, Caffier V, Durel CE, Plummers KM (2011) Revision of nomenclature of the differential host-pathogen interactions of Venturia inaequalis and Malus. Annu Rev Phytopathol 49:391–413CrossRefPubMedGoogle Scholar
  5. Colon LT, Jansen RC, Budding DJ (1995) Partial resistance to late blight (Phytophthora-Infestans) in hybrid progenies of 4 South-American Solanum species crossed with diploid Solanum-tuberosum. Theor Appl Genet 90:691–698CrossRefPubMedGoogle Scholar
  6. Cooke DEL, Young V, Birch PRJ, Toth R, Gourlay F, Day JP, Carnegie SF, Duncan JM (2003) Phenotypic and genotypic diversity of Phytophthora infestans populations in Scotland (1995–1997). Plant Pathol 52:181–192CrossRefGoogle Scholar
  7. Cooke DEL, Cano LM, Raffaele S, Bain RA, Cooke LR, Etherington GJ, Deahl KL, Farrer RA, Gilroy EM, Goss EM, Grünwald NJ, Hein I, MacLean D, McNicol JW, Randall E, Oliva RF, Pel MA, Shaw DS, Squires JN, Taylor MC, Vleeshouwers VGAA, Birch PRJ, Lees AK, Kamoun S (2012) Genome analyses of an aggressive and invasive lineage of the Irish potato famine pathogen. PLoS Pathog 8:e1002940CrossRefPubMedCentralPubMedGoogle Scholar
  8. DFID (2013). Accessed 19 Mar 2013
  9. Drenth A, Tas ICQ, Govers F (1994) DNA-fingerprinting uncovers a new sexually reproducing population of Phytophthora infestans in the Netherlands. Eur J Plant Pathol 100:97–107CrossRefGoogle Scholar
  10. Flor HH (1942) Inheritance of pathogenicity in a cross between physiologic races 22 and 24 of Melampsora lini. Phytopathology 32:653–669Google Scholar
  11. Förch M, Van den Bosch T, Van Bekkum P, Evenhuis B, Vossen J, Kessel G (2010) Monitoring the Dutch Phytophthora infestans population for virulence against new R-genes. Twelfth EuroBlight workshop Arras (France) 3–6 MayGoogle Scholar
  12. Foster SJ, Park TH, Pel MA, Brigneti G, Sliwka J, Jagger L, Van der Vossen EAG, Jones JDG (2009) Rpi-vnt1.1, a Tm-22 homolog from Solanum venturii confers resistance to potato late blight. Mol Plant Microbe Interact 22:589–600Google Scholar
  13. Goyeau H, Berder J, Czerepak C, Gautier A, Lanen C, Lannou C (2012) Low diversity and fast evolution in the population of Puccinia triticina causing durum wheat leaf rust in France from 1999 to 2009, as revealed by an adapted differential set. Plant Pathol 61:761–772CrossRefGoogle Scholar
  14. Guo J (2008). Phytophthora infestans avirulence genes; mapping, cloning and diversity in field isolates. Dissertation, Wageningen UniversityGoogle Scholar
  15. Haas BJ et al (2009) Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans. Nature 461:393–398CrossRefPubMedGoogle Scholar
  16. Haverkort AJ, Boonekamp PM, Hutten R, Jacobsen E, Lots LAP, Kessel GJT, Visser RGF, van der Vossen EAG (2008) Societal costs of late blight in potato and prospects of durable resistance through cisgenic modification. Potato Res 51:47–57CrossRefGoogle Scholar
  17. Hu CH, Perez FG, Donahoo R, Myers K, Ivors K, Secor G, Roberts PD, Deahl KL, Fry WE, Ristaino JB (2012) Recent Genotypes of Phytophthora infestans in the Eastern United States reveal clonal populations and reappearance of mefenoxam sensitivity. Plant Dis 96:1323–1330CrossRefGoogle Scholar
  18. Huang SW, Van der Vossen EAG, Kuang HH, Vleeshouwers VGAA, Zhang NW, Borm TJA, Van Eck HJ, Baker B, Jacobsen E, Visser RGF (2005) Comparative genomics enabled the isolation of the R3a late blight resistance gene in potato. Plant J 42:251–261Google Scholar
  19. Hwang YT, Wijekoon C, Kalischuk M, Johnson D, Howard R, Prüfer D, Kawchuk L (2014) Evolution and Management of the Irish Potato Famine Pathogen Phytophthora Infestans in Canada and the United States. Am J Potato Res. doi:10.1007/s12230-014-9401-0
  20. International Seed Federation (2013). Accessed 20 Feb 2013
  21. Irish BM, Correll JC, Koike ST, Schafer J, Morelock TE (2003) Identification and cultivar reaction to three new races of the spinach downy mildew pathogen from the United States and Europe. Plant Dis 87:567–572CrossRefGoogle Scholar
  22. Jo KR (2013) Unveiling and deploying durability of late blight resistance in potato: from natural stacking to cisgenic stacking. Dissertation, Wageningen UniversityGoogle Scholar
  23. Jo KR, Arens M, Kim TY, Jongsma MA, Visser RGF, Jacobsen E, Vossen JH (2011) Mapping of the S. demissum late blight resistance gene R8 to a new locus on chromosome IX. Theor Appl Genet 123:1331–1340CrossRefPubMedCentralPubMedGoogle Scholar
  24. Kim HJ, Lee HR, Jo KR, Mortazavian SM, Huigen DJ, Evenhuis B, Kessel G, Visser RG, Jacobsen E, Vossen JH (2012) Broad spectrum late blight resistance in potato differential set plants MaR8 and MaR9 is conferred by multiple stacked R genes. Theor Appl Genet 124:923–935CrossRefPubMedCentralPubMedGoogle Scholar
  25. Li GC, Huang SW, Guo X, Li Y, Yang Y, Guo Z, Kuang HH, Rietman H, Bergervoet M, Vleeshouwers VGGA, Van der Vossen EAG, Qu DY, Visser RGF, Jacobsen E, Vossen JH (2011) Cloning and characterization of R3b; members of the R3 superfamily of late blight resistance genes show sequence and functional divergence. Mol Plant Microbe Interact 24:1132–1142CrossRefPubMedGoogle Scholar
  26. Li Y, Van der Lee T, Zhu JH, Jin GH, Lan CZ, Zhu SX, Zhang RF, Liu BW, Zhao ZJ, Kessel G, Huang SW, Jacobsen E (2013) Population structure of Phytophthora infestans in China–geographic clusters and presence of the EU genotype Blue_13. Plant Pathol 62:932–942CrossRefGoogle Scholar
  27. Lindhout P, Meijer D, Schotte T, Hutten RCB, Visser RGF, van Eck HJ (2011) Towards F1 Hybrid Seed Potato Breeding. Potato Res 54:301–312CrossRefGoogle Scholar
  28. Lokkousou AA, Park TH, Van Arkel G, Arens M, Ruyter-Spira C, Morales J, Whisson SC, Borh PRJ, Visser RGF, Jacobsen E, Van der Vossen EAG (2009) Exploiting knowledge of R/Avr genes to rapidly clone a new LZ-NBS-LRR family of late blight resistance genes from potato linkage group IV. Mol Plant Microbe Interact 22:630–641CrossRefGoogle Scholar
  29. Lowe I, Cantu D, Dubcovsky J (2011) Durable resistance to the wheat rusts: integrating systems biology and traditional phenotype-based research methods to guide the deployment of resistance genes. Euphytica 179:69–79CrossRefGoogle Scholar
  30. Malcolmson JF, Black W (1966) New R genes in Solnum demissum Lindl. and their complementary races of Phytophthora infestans (Mont.) de Bary. Euphytica 15:199–203CrossRefGoogle Scholar
  31. McDonald BA, Linde C (2002) Pathogen population genetics, evolutionary potential, and durable resistance. Annu Rev Phytopathol 40:349–379CrossRefPubMedGoogle Scholar
  32. Oh SK, Young C, Lee M, Oliva R, Bozkurt TO, Cano LM, Win J, Bos JIB, Liu HY, Van Damme M, Morgan W, Choi D, Van der Vossen EAG, Vleeshouwers VGAA, Kamoun S (2009) In planta expression screens of Phytophthora infestans RXLR effectors reveal diverse phenotypes, including activation of the Solanum bulbocastanum disease resistance protein Rpi-blb2. Plant Cell 21:2928–2947CrossRefPubMedCentralPubMedGoogle Scholar
  33. Pel MA (2010) Mapping, isolation and characterization of genes responsible for late blight resistance in potato. Dissertation, Wageningen UniversityGoogle Scholar
  34. Pel MA, Foster SJ, Park TH, Rietman H, Van Arkel G, Jones JD, Van Eck HJ, Jacobsen E, Visser RG, Van der Vossen EA (2009) Mapping and cloning of late blight resistance genes from Solanum venturii using an interspecific candidate gene approach. Mol Plant Microbe Interact 22:601–615CrossRefPubMedGoogle Scholar
  35. Peters RD, Al-Mughrabi KI, Kalischuk ML, Dobinson KF, Conn KL, Alkher H, Islam MR, Daayf F, Lynn J, Bizimungu B, de Koeyer D, Lévesque CA, Kawchuk LM (2014) Characterization of Phytophthora infestans population diversity in Canada reveals increased migration and genotype recombination. Can J Plant Pathol 36:73–82CrossRefGoogle Scholar
  36. Raffaele S, Farrer RA, Cano LM, Studholme DJ, Maclean D, Thines M, Jiang RHY, Zody MC, Kunjeti SG, Donofrio NM, Meyers BC, Nusbaum C, Kamoun S (2010) Genome evolution following host jumps in the Irish potato famine pathogen lineage. Science 330:1540–1543CrossRefPubMedGoogle Scholar
  37. Rietman H (2011) Putting the Phytophthora infestans genome sequence at work; multiple novel avirulence and potato resistance gene candidates revealed. Dissertation, Wageningen UniversityGoogle Scholar
  38. Rietman H, Bijsterbosch G, Cano LM, Lee HR, Vossen JH, Jacobsen E, Visser RGF, Kamoun S, Vleeshouwers VGAA (2012) Qualitative and quantitative late blight resistance in the potato cultivar Sarpo Mira is determined by the perception of five distinct RXLR effectors. Mol Plant Microbe Interact 25:910–919CrossRefPubMedGoogle Scholar
  39. Sandlin C, Webb KM (2012) Guidelines for the identification of races of Fusarium oxysporum f. sp. melonis using differential Melon lines. Accessed 21 Feb 2013
  40. Saunders DGO, Breen S, Win J, Sschornack S, Hein I, Bozkurt TO, Champouret N, Vleeshouwers VGAA, Birch PRJ, Gilroy EM, Kamoun S (2012) Host protein BSL1 associates with Phytophthora infestans RXLR effector AVR2 and the Solanum demissum immune receptor R2 to mediate disease resistance. Plant Cell 24:3420–3434CrossRefPubMedCentralPubMedGoogle Scholar
  41. Swiezynski KM, Domanski L, Zarzycka H, Zimnoch-Guzowska E (2000) The reaction of potato differentials to Phytophthora infestans isolates collected in nature. Plant Breeding 119:119–126CrossRefGoogle Scholar
  42. Trognitz BR, Trognitz FC (2007) Occurrence of the R1 allele conferring resistance to late blight in potato R-gene differentials and commercial cultivars. Plant Pathol 56:150–155CrossRefGoogle Scholar
  43. Van der Vossen E, Sikkema A, Hekkert BTL, Gros J, Stevens P, Muskens M, Wouters D, Pereira A, Stiekema W, Allefs S (2003) An ancient R gene from the wild potato species Solanum bulbocastanum confers broad-spectrum resistance to Phytophthora infestans in cultivated potato and tomato. Plant J 36:867–882CrossRefPubMedGoogle Scholar
  44. Van der Vossen EAG, Gros J, Sikkema A, Muskens M, Wouters D, Wolters P, Pereira A, Allefs S (2005) The Rpi-blb2 gene from Solanum bulbocastanum is an Mi-1 gene homolog conferring broad-spectrum late blight resistance in potato. Plant J 44:208–222CrossRefPubMedGoogle Scholar
  45. Van Poppel PMJA, Guo J, De Vondervoort PJIV, Jung MWM, Birch PRJ, Whisson SC, Govers F (2008) The Phytophthora infestans avirulence gene Avr4 encodes an RXLR- dEER effector. Mol Plant Microbe Interact 21:1460–1470CrossRefPubMedGoogle Scholar
  46. Van Poppel PMJA, Huigen DJ, Govers F (2009) Differential recognition of Phytophthora infestans races in potato R4 breeding lines. Phytopathology 99:1150–1155CrossRefPubMedGoogle Scholar
  47. Vleeshouwers VGAA, Van Dooijeweert W, Keizer LCP, Sijpkes L, Govers F, Colon LT (1999) A laboratory assay for Phytophthora infestans resistance in various Solanum species reflects the field situation. Eur J Plant Pathol 105:241–250CrossRefGoogle Scholar
  48. Vleeshouwers VGAA, Rietman H, Krenek P, Champouret N, Young C, Oh SK, Wang M, Bouwmeester K, Vosman B, Visser RGF, Jacobsen E, Govers F, Kamoun S, Van der Vossen EA (2008) Effector genomics accelerates discovery and functional profiling of potato disease resistance and Phytophthora infestans avirulence genes. PLoS ONE 3:e2875CrossRefPubMedCentralPubMedGoogle Scholar
  49. Vleeshouwers VGAA, Raffaele S, Vossen JH, Champouret N, Oliva R, Segretin ME, Rietman H, Cano LM, Lokkousou A, Kessel G, Pel MA, Kamoun S (2011) Understanding and exploiting late blight resistance in the age of effectors. Annu Rev Phytopathol 49:507–531CrossRefPubMedGoogle Scholar
  50. Vossen JH, Nijenhuis M, van der Vossen EAG, Jacobsen E, Visser RGF (2009) Cloning and exploitation of a functional R-gene from Solanum chacoense. Patent application WO2011034433 A1. Published by the world intellectual property organization 18 September 2009Google Scholar
  51. Whitaker VM, Debener T, Roberts AV, Hokanson SC (2010) A standard set of host differentials and unified nomenclature for an international collection of Diplocarpon rosae races. Plant Pathol 59:745–752CrossRefGoogle Scholar
  52. Zhu S, Zhu J, Li Y, Nijenhuis M, Bergervoet M, Rietman H, Jacobsen E (2010) Broad spectrum resistance from Rpi-blb1 homologous R-genes has been broken by Phytophthora infestans isolates collected from Solanum stoloniferum. Acta Hortic Sinica 37(2):241–246Google Scholar
  53. Zhu S, Li Y, Vossen JH, Visser RGF, Jacobsen E (2012) Functional stacking of three resistance genes against Phytophthora infestans in potato. Transgenic Res 21:89–99CrossRefPubMedCentralPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2014

Authors and Affiliations

  • Suxian Zhu
    • 1
  • Jack H. Vossen
    • 1
  • Marjan Bergervoet
    • 1
  • Maarten Nijenhuis
    • 1
  • Linda Kodde
    • 1
  • Geert J. T. Kessel
    • 2
  • Vivianne Vleeshouwers
    • 1
  • Richard G. F. Visser
    • 1
  • Evert Jacobsen
    • 1
  1. 1.Wageningen UR Plant BreedingWageningen University and Research CenterWageningenThe Netherlands
  2. 2.Plant Research International, Biointeractions and Plant HealthWageningen University and Research CenterWageningenThe Netherlands

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