Skip to main content
Log in

Potato late blight as a model of pathogen-host plant coevolution

  • Lectures
  • Published:
Russian Journal of Plant Physiology Aims and scope Submit manuscript

Abstract

A striking progress in molecular genetic studies of Phytophthora infestans and the genes for resistance to this pathogen in cultivated and wild Solanum species made potato late blight an instructive experimental model of “arms race” — rapid coevolution of the pathogen, oomycete P. infestans, and Solanum host plants. Mechanisms of this coevolution are discussed in the context of new information on the origin of past and present forms of P. infestans and cultivated potato. The focus of the lecture is on the functional organization of the genes for pathogen virulence and the race-specific genes for plant resistance as well as on the molecular interactions of the products of these genes: pathogen RxLR effectors and plant CC-NB-LRR receptor kinases. New knowledge on the molecular mechanisms of interaction between P. infestans and potato will promote breeding for durable resistance to late blight, especially with new technologies of effectoromics introduced to detect promising resistance genes in Solanum genetic collections, to characterize these genes and to promote their deployment in breeding process.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

AVR:

avirulence factor, effector

Avr gene:

avirulence gene

CC-NB-LRR kinase:

receptor kinase comprising coiled coil domain, nucleotide-binding domain and leucine-rich repeat domain

ETI:

effector-triggered immunity

ipi/IPI:

in-planta induced gene/effector

PAMP:

pathogen-associated molecular pattern

PTI:

PAMP-triggered immunity

PR proteins:

pathogenesis-related proteins

QTL:

quantitative trait locus

R genes:

resistance genes

Rpi genes:

genes for resistance to Phytophthora infestans

RxLR:

pathogen effector comprising amino acid sequence: arginine-any amino acid residue-leucine-arginine

References

  1. Fry W., Phytophthora infestans: the plant (and R gene) destroyer, Mol. Plant Pathol., 2008, vol. 9, pp. 385–402.

    Article  PubMed  Google Scholar 

  2. Haverkort A.J., Boonekamp P.M., Hutten R.C.B., Jacobsen E., Lotz L.A.P., Kessel G.J.T., Visser R.G.F., and van der Vossen E.A.G., Societal costs of late blight in potato and prospects of durable resistance through cisgenic modification, Potato Res., 2008, vol. 51, pp. 47–57.

    Article  Google Scholar 

  3. 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., Birch P.R., Lees A.K., and Kamoun S., Genome analyses of an aggressive and invasive lineage of the Irish Potato Famine pathogen, PLoS Pathol., 2012, vol. 8: e1002940.

    Article  Google Scholar 

  4. Lees A.K., Stewart J.A., Lynott J.S., Carnegie S.F., Campbell H., and Roberts A.M.I., The effect of a dominant Phytophthora infestans genotype (13_A2) in Great Britain on host resistance to foliar late blight in commercial potato cultivars, Potato Res., 2012, vol. 55, pp. 125–134.

    Article  Google Scholar 

  5. Haas B.J., Kamoun S., Zody M.C., Jiang R.H.Y., Handsaker R.E., Cano L.M., Grabherr M., Kodira C.D., Raffaele S., Torto-Alalibo T., Bozkurt T.O., Ah-Fong A.M., Alvarado L., Anderson V.L., Armstrong M.R., Avrova A., Baxter L., Beynon J., Boevink P.C., Bollmann S.R., Bos J.I., Bulone V., Cai G., Cakir C., Carrington J.C., Chawner M., Conti L., Costanzo S., Ewan R., Fahlgren N., Fischbach M.A., Fugelstad J., Gilroy E.M., Gnerre S., Green P.J., Grenville-Briggs L.J., Griffith J., Grünwald N.J., Horn K., Horner N.R., Hu C.H., Huitema E., Jeong D.H., Jones A.M., Jones J.D., Jones R.W., Karlsson E.K., Kunjeti S.G., Lamour K., Liu Z., Ma L., MacLean D., Chibucos M.C., McDonald H., McWalters J., Meijer H.J., Morgan W., Morris P.F., Munro C.A., O’Neill K., Ospina-Giraldo M., Pinzón A., Pritchard L., Ramsahoye B., Ren Q., Restrepo S., Roy S., Sadanandom A., Savidor A., Schornack S., Schwartz D.C., Schumann U.D., Schwessinger B., Seyer L., Sharpe T., Silvar C., Song J., Studholme D.J., Sykes S., Thines M., van de Vondervoort P.J., Phuntumart V., Wawra S., Weide R., Win J., Young C., Zhou S., Fry W., Meyers B.C., and van West P., Genome sequence and analysis of the Irish Potato Famine pathogen Phytophthora infestans, Nature, 2009, vol. 461, pp. 393–398.

    Article  CAS  PubMed  Google Scholar 

  6. Potato Genome Sequencing Consortium. Genome sequence and analysis of the tuber crop potato, Nature, 2011, vol. 475, pp. 189–195.

    Article  Google Scholar 

  7. Vleeshouwers V.G.A.A., Raffaele S., Vossen J., Champouret N., Oliva R., Segretin M.E., Rietman H., Cano L.M., Lokossou A., Kessel G., Pel M.A., and Kamoun S., Understanding and exploiting late blight resistance in the age of effectors, Annu. Rev. Phytopathol., 2011, vol. 49, pp. 507–531.

    Article  CAS  PubMed  Google Scholar 

  8. Pais M., Win J., Yoshida K., Etherington G.J., Cano L.M., Raffaele S., Banfield M.J., Jones A., Kamoun S., and Saunders D.G., From pathogen genomes to host plant processes: the power of plant parasitic oomycetes, Genome Biol., 2013, vol. 14: 211, http://genomebiology.com/2013/14/6/211

    Article  PubMed Central  PubMed  Google Scholar 

  9. Rodewald, J. and Trognitz B., Solanum resistance genes against Phytophthora infestans and their corresponding avirulence genes, Mol. Plant Pathol., 2013, vol. 14, pp. 740–757.

    Article  CAS  PubMed  Google Scholar 

  10. Vleeshouwers, V.G.A.A. and Oliver R.P., Effectors as tools in disease resistance breeding against biotrophic, hemibiotrophic, and necrotrophic plant pathogens, Mol. Plant–Microbe Interact., 2014, vol. 27, pp. 196–206.

    Article  CAS  PubMed  Google Scholar 

  11. Simko I., Jansky S.H., Stephenson S., and Spooner D.M., Genetics of resistance to pests and disease, Potato Biology and Biotechnology: Advances and Perspectives, Vreugdenhil D., Bradshaw J., Gebhardt C., and Govers F., Mackerron D.K.L., Taylor M.A., Ross H.A., Eds., Amsterdam: Elsevier, 2007, pp. 117–155.

    Chapter  Google Scholar 

  12. Poland J.A., Balint-Kurti P.J., Wisser R.J., Pratt R.C., and Nelson R.J., Shades of gray: the world of quantitative disease resistance, Trends Plant Sci., 2009, vol. 14, pp. 21–29.

    Article  CAS  PubMed  Google Scholar 

  13. Flor H.H., Current status of the gene-for-gene concept, Annu. Rev. Phytopathol., 1971, vol. 9, pp. 275–296.

    Article  Google Scholar 

  14. Du J., Elicitin-triggered apoplastic immunity against late blight in potato, PhD thesis, Wageningen, the Netherlands: Wageningen University, 2014.

    Google Scholar 

  15. Jones, J.D. and Dangl J.L., The plant immune system, Nature, 2006, vol. 444, pp. 323–329.

    Article  CAS  PubMed  Google Scholar 

  16. Hein I., Gilroy E.M., Armstrong M.R., and Birch P.R., The zig-zag-zig in oomycete–plant interactions, Mol. Plant Pathol., 2009, vol. 10, pp. 547–562.

    Article  CAS  PubMed  Google Scholar 

  17. Dodds, P.N. and Rathjen J.P., Plant immunity: towards an integrated view of plant–pathogen interactions, Nat. Rev. Genet., 2010, vol. 11, pp. 539–548.

    Article  CAS  PubMed  Google Scholar 

  18. Pritchard, L. and Birch P.R.J., The zigzag model of plant–microbe interactions: is it time to move on? Mol. Plant Pathol., 2014, vol. 15, pp. 865–870.

    Article  PubMed  Google Scholar 

  19. Thomma B.P.H.J., Nürnberger T., and Joosten M.H.A.J., Of PAMPs and effectors: the blurred PTI-ETI dichotomy, Plant Cell, 2011, vol. 23, pp. 4–15.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  20. Danan S., Veyrieras, J.-B., and Lefebvre V., Construction of a potato consensus map and QTL metaanalysis offer new insights into the genetic architecture of late blight resistance and plant maturity traits, BMC Plant Biol., 2011, vol. 11: 16, http://www.biomedcentral.com/1471-2229/11/16

    Article  PubMed Central  PubMed  Google Scholar 

  21. Jupe F., Pritchard L., Etherignton G.J., Mackenzie K., Cock P.J., Wright F., Sharma S.K., Bolser D., Bryan G.J., Jones J.D., and Hein I., Identification and localization of the NB-LRR gene family within the potato genome, BMC Genomics, 2012, vol. 13: 75, http://www.biomedcentral.com/1471-2164/13/75

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  22. Draffehn A.M., Li L., Krezdorn N., Ding J., Lübeck J., Strahwald J., Muktar M.S., Walkemeier B., Rotter B., and Gebhardt C., Comparative transcript profiling by SuperSAGE identifies novel candidate genes for controlling potato quantitative resistance to late blight not compromised by late maturity, Front. Plant Sci., 2013, vol. 4: 423, doi 10.3389/fpls.2013.00423

    Google Scholar 

  23. Ali A., Sandin M., Resjö S., Lenman M., Hedley P., Levander F., and Andreasson E., Quantitative proteomics and transcriptomics of potato in response to Phytophthora infestans in compatible and incompatible interactions, BMC Genomics, 2014, vol. 15: 497, http://www.biomedcentral.com/1471-2164/15/497

    Article  PubMed Central  PubMed  Google Scholar 

  24. Pajerowska-Mukhtar K., Stich B., Achenbach U., Ballvora A., Lübeck J., Strahwald J., Tacke E., Hofferbert H.R., Ilarionova E., Bellin D., Walkemeier B., Basekow R., Kersten B., and Gebhardt C., Single nucleotide polymorphisms in the allene oxide synthase 2 gene are associated with field resistance to late blight in populations of tetraploid potato cultivars, Genetics, 2009, vol. 181, pp. 1115–1127.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  25. Du J., Tian Z., Liu J., Vleeshouwers V.G., Shi X., and Xie C., Functional analysis of potato genes involved in quantitative resistance to Phytophthora infestans, Mol. Biol. Rep., 2013, vol. 40, pp. 957–967.

    Article  CAS  PubMed  Google Scholar 

  26. Bengtsson T., Weighill D., Proux-Wéra E., Levander F., Resjö S., Burra D.D., Moushib L.I., Hedley P.E., Liljeroth E., Jacobson D., Alexandersson E., and Andreasson E., Proteomics and transcriptomics of the BABA-induced resistance response in potato using a novel functional annotation approach, BMC Genomics, 2014, vol. 15: 315, http://www.biomedcentral.com/1471-2164/15/315

    Article  PubMed Central  PubMed  Google Scholar 

  27. Ovchinnikova A., Krylova E., Gavrilenko T., Smekalova T., Zhuk M., Knapp S., and Spooner D.M., Taxonomy of cultivated potatoes (Solanum section Petota: Solanaceae), Bot. J. Linn. Soc., 2011, vol. 165, pp. 107–155.

    Article  Google Scholar 

  28. Grünwald, N.J. and Flier W.G., The biology of Phytophthora infestans at its center of origin, Annu. Rev. Phytopathol., 2005, vol. 43, pp. 171–190.

    Article  PubMed  Google Scholar 

  29. Fry W.E., Grünwald N.J., Cooke D.E.L., McLeod A., Forbes G.A., and Cao K., Population genetics and population diversity of Phytophthora infestans, Oomycete Genetics and Genomics: Diversity, Interactions, and Research Tools, Lamour K., Kamoun S., Eds., Oxford, UK: Wiley-Blackwell, 2009, pp. 139–164.

    Chapter  Google Scholar 

  30. Martin M.D., Cappellini E., Samaniego J.A., Zepeda M.L., Campos P.F., Seguin-Orlando A., Ho S.Y.W., Dietrich F.S., Mieczkowski P.A., Heitman J., Willerslev E., Krogh A., Ristaino J.B., and Gilbert M.T.P., Reconstructing genome evolution in historic samples of the Irish Potato Famine pathogen, Nat. Commun., 2013, vol. 4: 2172, doi 10.1038/ncomms3172

    PubMed Central  PubMed  Google Scholar 

  31. Yoshida K., Burbano H.A., Krause J., Thines M., Weigel D., and Kamoun S., Mining herbaria for plant pathogen genomes: back to the future, PLoS Pathog., 2014, vol. 10: e1004028.

    Article  Google Scholar 

  32. Goss E.M., Tabima J.F., Cooke D.E.L., Restrepo S., Fry W.E., Forbes G.A., Fieland V.J., Cardenas M., and Grünwald N.J., The Irish Potato Famine pathogen Phytophthora infestans originated in central Mexico rather than the Andes, Proc. Natl. Acad. Sci. USA, 2014, vol. 111, pp. 8791–8796.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  33. Rogozina E.V., Molecular genetic interactions in the system “pathogen–host” with potato late blight and modern breeding strategies, S.-Kh. Biol., 2011, vol. 5, pp. 17–30.

    Google Scholar 

  34. Oliva R.F., Chacon M.G., Cooke D.E.L., Lees A.K., and Forbes G.A., Is Phytophthora infestans a good taxonomist? Host recognition and co-evolution in the Phytophthora/Solanum interaction, Acta Hort., 2007, vol. 745, pp. 465–470.

    CAS  Google Scholar 

  35. Montarry J., Andrivon D., Glais I., Corbiere R., Mialdea G., and Delmotte F., Microsatellite markers reveal two admixed genetic groups and an ongoing displacement within the French population of the invasive plant pathogen Phytophthora infestans, Mol. Ecol., 2010, vol. 19, pp. 1965–1977.

    Article  CAS  PubMed  Google Scholar 

  36. Young G.K., Cooke L.R., Kirk W.W., Tumbalam P., Perez F.M., and Deahl K.L., Influence of competition and host plant resistance on selection in Phytophthora infestans populations in, Michigan, USA and in Northern Ireland, Plant Pathol., 2009, vol. 58, pp. 703–714.

    Google Scholar 

  37. Montarry J., Corbiere R., Lesueur S., Glais I., and Andrivon D., Does selection by resistant hosts trigger local adaptation in plant–pathogen systems? J. Evol. Biol., 2006, vol. 19, pp. 522–531.

    Article  CAS  PubMed  Google Scholar 

  38. Chowdappa P., Nirmal Kumar B.J., Madhura S., Mohan Kumar S.P., Myers K.L., Fry W.E., and Cooke D.E.L., Severe outbreaks of late blight on potato and tomato in South India caused by recent changes in the Phytophthora infestans population, Plant Pathol., 2014, doi 10.1111/ppa.12228

    Google Scholar 

  39. Mariette N., Montarry J., Boulard F., Mabon R., Corbière R., and Andrivon D., Aggressiveness and genetic structure of French populations of Phytophthora infestans from 2001 to 2008, Proc. 19th Triennual Conference EAPR2014 (6–11 July, 2014, Brussels), http://www.eapr.net/eapr-19th-triennial-conference-brussels-belgium-july-2014

    Google Scholar 

  40. Saunders D.G.O., Breen S., Win J., Schornack S., Hein I., Bozkurt T.O., Champouret N., Vleeshouwers V.G.A.A., Birch P.R.J., Gilroy E.M., and Kamoun S., Host protein BSL1 associates with Phytophthora infestans RXLR effector AVR2 and the Solanum demissum immune receptor R2 to mediate disease resistance, Plant Cell, 2012, vol. 24, pp. 3420–3434.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  41. Clement J.A.J., Magalon H., Glais I., Jacquot E., and Andrivon D., To be or not to be solitary: Phytophthora infestans’ dilemma for optimizing its reproductive fitness in multiple infections, PLoS ONE, 2012, vol. 7: e37838.

    Article  Google Scholar 

  42. Raffaele, S. and Kamoun S., Genome evolution in filamentous plant pathogens: why bigger can be better, Nat. Rev. Microbiol., 2012, vol. 10, pp. 417–430.

    CAS  PubMed  Google Scholar 

  43. Dong S., Stam R., Cano L.M., Song J., Sklenar J., Yoshida K., Bozkurt T.O., Oliva R., Liu Z., Tian M., Win J., Banfield M.J., Jones A.M.E., van der Hoorn R.A.L., and Kamoun S., Effector specialization in a lineage of the Irish Potato Famine pathogen, Science, 2014, vol. 343, pp. 552–555.

    Article  CAS  PubMed  Google Scholar 

  44. D’yakov, Yu.T. and Elanskii S.N., Population genetics of Phytophthora infestans, Mikologiya segodnya (Mycology Today), D’yakov, Yu.T. and Sergeev, Yu.V., Eds., Moscow: Natsional’naya Akademiya Mikologii, 2007, vol. 1, pp. 107–139.

    Google Scholar 

  45. Birch P.R., Boevink P.C., Gilroy E.M., Hein I., Pritchard L., and Whisson S.C., Oomycete RXLR effectors: delivery, functional redundancy and durable disease resistance, Curr. Opin. Plant Biol., 2008, vol. 11, pp. 373–379.

    Article  CAS  PubMed  Google Scholar 

  46. Bouwmeester K., Meijer H.J.G., and Govers F., At the frontier: RXLR effectors crossing the Phytophthora–host interface, Front. Plant Sci., 2011, vol. 2: 75, doi 10.3389/fpls.2011.00075

    Google Scholar 

  47. Kale S.D., Oomycete and fungal effector entry, a microbial Trojan horse, New Phytol., 2012, vol. 193, pp. 874–881.

    Article  CAS  PubMed  Google Scholar 

  48. Martens, C. and van de Peer Y., The hidden duplication past of the plant pathogen Phytophthora and its consequences for infection, BMC Genomics, 2010, vol. 11: 353, http://www.biomedcentral.com/1471-2164/11/353

    Article  PubMed Central  PubMed  Google Scholar 

  49. Vetukuri R.R., Åsman, A.K., Jahan S.N., Avrova A.O., Whisson S.C., and Dixelius C., Phenotypic diversification by gene silencing in Phytophthora plant pathogens, Commun. Integr. Biol., 2013, vol. 6: e25890.

    Article  Google Scholar 

  50. Birch P.R., Armstrong M., Bos J., Boevink P., Gilroy E.M., Taylor R.M., Wawra S., Pritchard L., Conti L., Ewan R., Whisson S.C., van West P., Sadanandom A., and Kamoun S., Towards understanding the virulence functions of RXLR effectors of the oomycete plant pathogen Phytophthora infestans, J. Exp. Bot., 2009, vol. 60, pp. 1133–1140.

    Article  CAS  PubMed  Google Scholar 

  51. Rietman H., Putting the Phytophthora infestans genome sequence at work; multiple novel avirulence and potato resistance gene candidates revealed: PhD thesis, Wageningen, The Netherlands: Wageningen University, 2011.

    Google Scholar 

  52. Bouwmeester K., Poppel P.M.J.A., and Govers F., Genome biology cracks enigmas of oomycete plant pathogens, Molecular Aspects of Plant Disease Resistance, Parker J.E., Ed., Oxford, UK: Wiley-Blackwell, 2009, pp. 102–134.

    Google Scholar 

  53. Wawra S., Agacan M., Boddey J.A., Davidson I., Gachon C.M., Zanda M., Grouffaud S., Whisson S.C., Birch P.R., Porter A.J., and van West P., Avirulence protein 3a (AVR3a) from the potato pathogen Phytophthora infestans forms homodimers through its predicted translocation region and does not specifically bind phospholipids, J. Biol. Chem., 2012, vol. 287, pp. 38 101–38 109.

    Article  CAS  Google Scholar 

  54. Bos J.I.B., Armstrong M.R., Gilroy E.M., Boevink P.C., Hein I., Taylor R.M., Zhendong T., Engelhardt S., Vetukuri R.R., Harrower B., Dixelius C., Bryan G., Sadanandom A., Whisson S.C., Kamoun S., and Birch P.R.J., Phytophthora infestans effector AVR3a is essential for virulence and manipulates plant immunity by stabilizing host E3 ligase CMPG1, Proc. Natl. Acad. Sci. USA, 2010, vol. 107, pp. 9909–9914.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  55. Halterman D.A., Chen Y., Sopee J., Berduo-Sandoval J., and Sánchez-Pérez A., Competition between Phytophthora infestans effectors leads to increased aggressiveness on plants containing broad-spectrum late blight resistance, PLoS ONE, 2010, vol. 5: e10536.

    Article  Google Scholar 

  56. Whisson S.C., Avrova A.O., Boevink P.C., Armstrong M.R., Seman Z.A., Hein I., and Birch P.R.J., Exploiting knowledge of pathogen effectors to enhance late blight resistance in potato, Potato Res., 2011, vol. 54, pp. 325–340.

    Article  Google Scholar 

  57. Chen Y., Liu Z., and Halterman D.A., Molecular determinants of resistance activation and suppression by Phytophthora infestans effector IPI-O, PLoS Pathol., 2012, vol. 8: e1002595.

    Article  Google Scholar 

  58. Segretin M.E., Pais M., Franceschetti M., ChaparroGarcia A., Bos J.I., Banfield M.J., and Kamoun S., Single amino acid mutations in the potato immune receptor R3a expand response to Phytophthora effectors, Mol. Plant–Microbe Interact., 2014, vol. 27, pp. 624–637.

    Article  CAS  PubMed  Google Scholar 

  59. Hein I., Birch P.R.J., Danan S., Lefebvre V., Odeny D.A., Gebhardt C., Trognitz F., and Bryan G.J., Progress in mapping and cloning qualitative and quantitative resistance against Phytophthora infestans in potato and its wild relatives, Potato Res., 2009, vol. 52, pp. 215–227.

    Article  Google Scholar 

  60. Wang M., Allefs S., Berg R.G., Vleeshouwers V.G.A.A., van der Vossen E.A., and Vosman B., Allele mining in Solanum: conserved homologues of Rpi-blb1 are identified in Solanum stoloniferum, Theor. Appl. Genet., 2008, vol. 116, pp. 933–943.

    Article  CAS  PubMed  Google Scholar 

  61. Park T.H., Vleeshouwers V.G.A.A., Jacobsen E., Visser R.G.F., and van der Vossen E.A.G., Molecular breeding for resistance to Phytophthora infestans in potato, Plant Breed., 2009, vol. 128, pp. 109–117.

    Article  CAS  Google Scholar 

  62. Tiwari J.K., Siddappa S., Singh B.P., Kaushik S.K., Chakrabarti S.K., Bhardwaj V., and Chandel P., Molecular markers for late blight resistance breeding of potato: an update, Plant Breed., 2013, vol. 132, pp. 237–245.

    Article  CAS  Google Scholar 

  63. Kuang H., Woo, S.-S., Meyers B.C., Nevo E., and Michelmore R.W., Multiple genetic processes result in heterogeneous rates of evolution within the major cluster disease resistance genes in lettuce, Plant Cell, 2004, vol. 16, pp. 2870–2894.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  64. Kuang H., Wei F., Marano M.R., Wirtz U., Wang X., Liu J., Shum W.P., Zaborsky J., Tallon L.J., Rensink W., Lobst S., Zhang P., Tornqvist C.E., Tek A., Bamberg J., Helgeson J., Fry W., You F., Luo M.C., Jiang J., Buell C.R., and Baker B., The R1 resistance gene cluster contains three groups of independently evolving, type I R1 homologues and shows substantial structural variation among haplotypes of Solanum demissum, Plant J., 2005, vol. 44, pp. 37–51.

    Article  CAS  PubMed  Google Scholar 

  65. Liu, Z. and Halterman D., Identification and characterization of RB-orthologous genes from the late blight resistant wild potato species Solanum verrucosum, Physiol. Mol. Plant Pathol., 2006, vol. 69, pp. 230–239.

    Article  CAS  Google Scholar 

  66. Jo K.R., Unveiling and deploying durability of late blight resistance in potato: from natural stacking to cisgenic stacking: PhD thesis, Wageningen, The Netherlands: Wageningen University, 2013.

    Google Scholar 

  67. Rietman H., Bijsterbosch G., Cano L.M., Lee H.R., Vossen J.H., Jacobsen E., Visser R.G., Kamoun S., and Vleeshouwers V.G., 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., 2012, vol. 25, pp. 910–919.

    Article  CAS  PubMed  Google Scholar 

  68. Tomczynska I., Stefanczyk E., Chmielarz M., Karasiewicz B., Kaminski P., Jones J.D.G., Lees A.K., and Sliwka J., A locus conferring effective late blight resistance in potato cultivar Sárpo Mira maps to chromosome XI, Theor. Appl. Genet., 2014, vol. 127, pp. 647–657.

    Article  PubMed Central  PubMed  Google Scholar 

  69. Bradeen J.M., Iorizzo M., Mollov D.S., Raasch J., Kramer L.C., Millett B.P., Austin-Phillips S., Jiang J., and Carputo D., Higher copy numbers of the potato RB transgene correspond to enhanced transcript and late blight resistance levels, Mol. Plant–Microbe Interact., 2009, vol. 22, pp. 437–446.

    Article  CAS  PubMed  Google Scholar 

  70. Li Y., van der Lee T.A., Evenhuis A., van den Bosch G.B., van Bekkum P.J., Förch M.G., van Gent-Pelzer M.P., van Raaij H.M., Jacobsen E., Huang S.W., Govers F., Vleeshouwers V.G., and Kessel G.J., Population dynamics of Phytophthora infestans in the Netherlands reveals expansion and spread of dominant clonal lineages and virulence in sexual offspring, G3 (Bethesda), 2012, vol. 2, pp. 1529–1540.

    Article  PubMed Central  CAS  Google Scholar 

  71. Gebhardt C., Bridging the gap between genome analysis and precision breeding in potato, Trends Genet., 2013, vol. 29, pp. 248–256.

    Article  CAS  PubMed  Google Scholar 

  72. Haverkort A.J., Struik P.C., Visser R.G.F., and Jacobsen E., Applied biotechnology to combat late blight in potato caused by Phytophthora infestans, Potato Res., 2009, vol. 52, pp. 249–264.

    Article  Google Scholar 

  73. Michelmore R.W., Christopoulou M., and Caldwell K.S., Impacts of resistance gene genetics, function, and evolution on a durable future, Annu. Rev. Phytopathol., 2013, vol. 51, pp. 291–319.

    Article  CAS  PubMed  Google Scholar 

  74. Chapman S., Stevens L.J., Boevink P.C., Engelhardt S., Alexander C.J., Harrower B., Champouret N., McGeachy K., van Weymers P.S.M., Chen X., Birch P.R.J., and Hein I., Detection of the virulent form of AVR3a from Phytophthora infestans following artificial evolution of potato resistance gene R3a, PLoS ONE, 2014, vol. 9: e110158.

    Article  Google Scholar 

  75. Bradshaw J.E., Potato breeding at the Scottish Plant Breeding Station and the Scottish Crop Research Institute: 1920–2008, Potato Res., 2009, vol. 52, pp. 141–172.

    Article  Google Scholar 

  76. Jo K.R., Kim C.J., Kim S.J., Kim T.Y., Bergervoet M., Jongsma M.A., Visser R.G., Jacobsen E., and Vossen J.H., Development of late blight resistant potatoes by cisgene stacking, BMC Biotechnol., 2014, vol. 14: 50, http://www.biomedcentral.com/1472-6750/14/50

    Article  PubMed Central  PubMed  Google Scholar 

  77. Jones J.D.G., Witek K., Verweij W., Jupe F., Cooke D., Dorling S., Tomlinson L., Smoker M., Perkins S., and Foster S., Elevating crop disease resistance with cloned genes, Philos. Trans. R. Soc. London, Ser. B., 2014, vol. 369, no. 1639, doi 10.1098/rstb.2013.0087

    Article  Google Scholar 

  78. Kim H.J., Lee H.R., Jo K.R., Mortazavian S.M., Huigen D.J., Evenhuis B., Kessel G., Visser R.G., Jacobsen E., and Vossen J.H., Broad spectrum late blight resistance in potato differential set plants MaR8 and MaR9 is conferred by multiple stacked R genes, Theor. Appl. Genet., 2012, vol. 124, pp. 923–935.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  79. Zhu S., Vossen J.H., Bergervoet M., Nijenhuis M., Kodde L., Kessel G.J.T., Vleeshouwers V., Visser R.G.F., and Jacobsen E., An updated conventionaland a novel GM potato late blight R gene differential set for virulence monitoring of Phytophthora infestans, Euphytica, 2014, doi 10.1007/s10681-014-1276-0

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to E. E. Khavkin.

Additional information

Published in the author’s version.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Khavkin, E.E. Potato late blight as a model of pathogen-host plant coevolution. Russ J Plant Physiol 62, 408–419 (2015). https://doi.org/10.1134/S1021443715030103

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1021443715030103

Keywords

Navigation