Abstract
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.
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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 102:7766–7771
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 30:361–371
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 2:173–179
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 49:391–413
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 90:691–698
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 52:181–192
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:e1002940
DFID (2013). http://www.dfid.gov.uk/r4d/Project/265/Default.aspx. Accessed 19 Mar 2013
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 100:97–107
Flor HH (1942) Inheritance of pathogenicity in a cross between physiologic races 22 and 24 of Melampsora lini. Phytopathology 32:653–669
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 May
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 22:589–600
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 61:761–772
Guo J (2008). Phytophthora infestans avirulence genes; mapping, cloning and diversity in field isolates. Dissertation, Wageningen University
Haas BJ et al (2009) Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans. Nature 461:393–398
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 51:47–57
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 96:1323–1330
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 42:251–261
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
International Seed Federation (2013). http://www.worldseed.org/isf/differential_hosts.html. Accessed 20 Feb 2013
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 87:567–572
Jo KR (2013) Unveiling and deploying durability of late blight resistance in potato: from natural stacking to cisgenic stacking. Dissertation, Wageningen University
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 123:1331–1340
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 124:923–935
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 24:1132–1142
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 62:932–942
Lindhout P, Meijer D, Schotte T, Hutten RCB, Visser RGF, van Eck HJ (2011) Towards F1 Hybrid Seed Potato Breeding. Potato Res 54:301–312
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 22:630–641
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 179:69–79
Malcolmson JF, Black W (1966) New R genes in Solnum demissum Lindl. and their complementary races of Phytophthora infestans (Mont.) de Bary. Euphytica 15:199–203
McDonald BA, Linde C (2002) Pathogen population genetics, evolutionary potential, and durable resistance. Annu Rev Phytopathol 40:349–379
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 21:2928–2947
Pel MA (2010) Mapping, isolation and characterization of genes responsible for late blight resistance in potato. Dissertation, Wageningen University
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 22:601–615
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 36:73–82
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 330:1540–1543
Rietman H (2011) Putting the Phytophthora infestans genome sequence at work; multiple novel avirulence and potato resistance gene candidates revealed. Dissertation, Wageningen University
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 25:910–919
Sandlin C, Webb KM (2012) Guidelines for the identification of races of Fusarium oxysporum f. sp. melonis using differential Melon lines. http://www.worldseed.org/cms/medias/file/TradeIssues/DiseasesResistance/StrainIdentification/Fusarium_wilt_melon_Differentials_Dec2012.pdf. Accessed 21 Feb 2013
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 24:3420–3434
Swiezynski KM, Domanski L, Zarzycka H, Zimnoch-Guzowska E (2000) The reaction of potato differentials to Phytophthora infestans isolates collected in nature. Plant Breeding 119:119–126
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 56:150–155
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 36:867–882
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 44:208–222
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 21:1460–1470
Van Poppel PMJA, Huigen DJ, Govers F (2009) Differential recognition of Phytophthora infestans races in potato R4 breeding lines. Phytopathology 99:1150–1155
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 105:241–250
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:e2875
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 49:507–531
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 2009
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 59:745–752
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):241–246
Zhu S, Li Y, Vossen JH, Visser RGF, Jacobsen E (2012) Functional stacking of three resistance genes against Phytophthora infestans in potato. Transgenic Res 21:89–99
Acknowledgments
The authors thank Dirk Jan Huigen and Henk Smid for their technical support. Wageningen UR Plant Breeding is acknowledged for financial support to Suxian Zhu. Geert Kessel, Jack Vossen, Marjan Bergervoet, Linda Kodde and Maarten Nijenhuis were supported by the DuRPh program, granted by the Ministry of Economic Affairs, formerly the Ministry of Agriculture and Fisheries, of the Netherlands.
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Zhu, S., Vossen, J.H., Bergervoet, M. et al. An updated conventional- and a novel GM potato late blight R gene differential set for virulence monitoring of Phytophthora infestans . Euphytica 202, 219–234 (2015). https://doi.org/10.1007/s10681-014-1276-0
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DOI: https://doi.org/10.1007/s10681-014-1276-0