Theoretical and Applied Genetics

, Volume 112, Issue 4, pp 674–687 | Cite as

Characterization and mapping of R Pi-ber , a novel potato late blight resistance gene from Solanum berthaultii

  • G. M. Rauscher
  • C. D. Smart
  • I. Simko
  • M. Bonierbale
  • H. Mayton
  • A. Greenland
  • W. E. Fry
Original Paper

Abstract

Phytophthora infestans, the causal agent of late blight, threatens potato production worldwide. An important tool in the management of the disease is the use of resistant varieties. Eleven major resistance genes have been identified and introgressed from Solanum demissum. However, new sources of resistance are continually sought. Here, we report the characterization and refined genetic localization of a resistance gene previously identified as Rber in a backcross progeny of Solanum tuberosum and Solanum berthaultii. In order to further characterize Rber, we developed a set of P. infestans isolates capable of identifying each of the 11 R-genes known to confer resistance to late blight in potato. Our results indicate that Rber is a new resistance gene, different from those recognized in S. demissum, and therefore, it has been named R Pi-ber according to the current system of nomenclature. In order to add new molecular markers around R Pi-ber , we used a PCR-based mapping technique, named MASP-map, which located R Pi-ber in a 3.9 cM interval between markers CT240 and TG63 on potato chromosome X. The location of R Pi-ber coincides with an area involved in resistance to different pathogens of potato and tomato.

Abbreviations

AUDPC

Area under the disease progress curve

BCT

Backcross to S. tuberosum progeny

BSA

Bulk segregant analysis

CAPS

Cleaved amplified polymorphic sequences

MASP-map

Multiplex allele-specific PCR mapping

R-gene

Resistance gene

chr

Chromosome

RFLP

Restriction fragment length polymorphisms

Notes

Acknowledgements

The present study was supported by Syngenta. We are grateful to Jason Rauscher, for critical reading and helpful suggestions on the manuscript, and to Kevin Myers and Barbara Esposito for their skilled technical assistance. RFLP markers were kindly provided by S. Tanksley.

References

  1. Abu-El Samen FM, Secor GA, Gudmestad NC (2003) Variability in virulence among asexual progenies of Phytophthora infestans. Phytopathology 93:293–304CrossRefGoogle Scholar
  2. Ballvora A, Ercolano MR, WeiB 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 30:361–371PubMedCrossRefGoogle Scholar
  3. Black W, Mastenbroek C, Mills WR, Peterson LC (1953) A proposal for an international nomenclature of races of Phytophthora infestans and genes controlling immunity in Solanum demissum derivatives. Euphytica 2:173–179CrossRefGoogle Scholar
  4. Bonierbale MW, Plaisted RL, Pineda O, Tanksley SD (1994) QTL analysis of trichome-mediated insect resistance in potato. Theor Appl Genet 87:973–987CrossRefGoogle Scholar
  5. Bonierbale MW, Plaisted RL, Tanksley SD (1988a) Construction of a genetic map of potato based on molecular markers from tomato. Am J Potato Res.65:471–472Google Scholar
  6. Bonierbale MW, Plaisted RL, Tanksley SD (1988b) RFLP maps based on a common set of clones reveal modes of chromosomal evolution in potato and tomato. Genetics 120:1095–1103Google Scholar
  7. Bormann CA, Rickert AM, Castillo Ruiz RA, Paal J, Lübeck J, Strahwald J, Buhr K, Gebhardt C (2004) Tagging quantitative trait loci for maturity-corrected late blight resistance in tetraploid potato with PCR-based candidate gene markers. Mol Plant-Microbe Interact 17:1126–1139PubMedCrossRefGoogle Scholar
  8. Caten CE, Jinks. JL (1968) Spontaneous variability of single isolates of Phytophthora infestans. I. Cultural variation. Can J Bot 46:329–348CrossRefGoogle Scholar
  9. Cha RS, Zarbl H, Keohavong P, G.Thilly W (1992) Mismatch amplification mutation assay (MAMA): application to the c-H-ras gene. PCR Methods Appl 2:14–20PubMedGoogle Scholar
  10. Chen XM, Line RF, Leung H (1998) Genome scanning for resistance-gene analogs in rice, barley and wheat by high resolution electrophoresis. Theor Appl Genet 97:345–355CrossRefGoogle Scholar
  11. Chunwongse J, Chunwongse C, Black L, Hanson P (2002) Molecular mapping of the Ph-3 gene for late blight resistance in tomato. J Horticult Sci Biotechnol 77:281–286Google Scholar
  12. Clewley JP, Arnold C (1997) MEGALIGN. The multiple alignment module of LASERGENE. Methods Mol Biol 70:119–129PubMedGoogle Scholar
  13. Deahl KL, Inglis DA, Demuth SP (1993) Testing for resistance to metalaxyl in Phytophthora infestans isolates from northwestern Washington. Am J Potato Res 70:779–795Google Scholar
  14. Dorrance AE, Inglis DA (1997) Assessment of greenhouse and laboratory screening methods for evaluating potato foliage for resistance to late blight. Plant Dis 81:1206–1213CrossRefGoogle Scholar
  15. Doyle JJ, Doyle JL (1990) Isolation of plant DNA from fresh tissue. Focus 12:13–15Google Scholar
  16. El-Kharbotly A, Palomino-Sanchez C, Salamini F, Jacobsen E, Gebhardt C (1996) R6 and R7 alleles of potato conferring race-specific resistance to Phytophthora infestans (Mont.) de Bary identified genetic loci clustering with the R3 locus on chromosome XI. Theor Appl Genet 92:880–884CrossRefGoogle Scholar
  17. Ewing EE, Simko I, Smart CD, Bonierbale MW, Mizubuti ESG, May GD, Fry WE (2000) Genetic mapping of qualitative and quantitative field resistance to Phytophthora infestans in a population derived from Solanum tuberosum and Solanum berthaultii. Mol Breed 6:25–36CrossRefGoogle Scholar
  18. Fry WE, Goodwin SB (1997) Resurgence of the Irish potato famine fungus. BioScience 47:363–371CrossRefGoogle Scholar
  19. Ganal MW, Czihal R, Hannapel U, Kloos D, Polley A, Ling H-Q (1998) Sequencing cDNA clones from the genetic map of tomato (Lycopersicon esculentum). Genome Res 8:842–847PubMedGoogle Scholar
  20. Gebhardt C, Ritter E, Barone A, Debener T, Walkemeier B, Schachtschabel U, Kaufmann H, Thompson RD, Bonierbale MW, Ganal MW, Tanksley SD, Salamini F (1991) RFLP maps of potato and their alignment with the homoeologus tomato genome. Theor Appl Genet 83:49–57CrossRefGoogle Scholar
  21. Gebhardt C, Valkonen JPT (2001) Organization of genes controlling disease resistance in the potato genome. Annu Rev Phytopathol 39:79–102PubMedCrossRefGoogle Scholar
  22. GILB (2004) Global initiative on late blight, http://www.cipotato.org/gilb/
  23. Goodwin SB, Sujkowski LS, Fry WE (1996) Widespread distribution and probable origin of resistance to metalaxyl in clonal genotypes of Phytophthora infestans in the United States and Western Canada. Phytopathology 86:793–800CrossRefGoogle Scholar
  24. Grube RC, Radwanski ER, Jahn M (2000) Comparative genetics of disease resistance within the Solanaceae. Genetics 155:873–887PubMedGoogle Scholar
  25. Grunwald NJ, Flier WG, Sturbaum AK, Garay-Serrano E, van den Bosch TBM, Smart CD, Matuszak JM, Lozoya-Saldana H, Turkensteen LJ, Fry WE (2001) Population structure of Phytophthora infestans in the Toluca valley region of central Mexico. Phytopathology 91:882–890CrossRefPubMedGoogle Scholar
  26. Helgeson JP, Pohlman JD, Austin S, Haberlach GT, Wielgus SM, Ronis D, Zambolim L, Tooley P, McGrath JM, James RV, Stevenson WR (1998) Somatic hybrids between Solanum bulbocastanum and potato: a new source of resistance to late blight. Theor Appl Genet 96:738–742CrossRefGoogle Scholar
  27. Huang S (2005) High allelic diversity of the potato R3 complex locus suggests a novel strategy for late blight control. Ph. D Thesis. Wageningen University, The NetherlandsGoogle Scholar
  28. Huang S, van der Vossen EAG, Kuang H, Vleeshouwers VGAA, Zhang N, Borm THA, van Eck H, Baker BJ, Jacobsen E, Visser RGF (2005) Comparative genomics enabled the isolation of the R3a late blight resistance gene in potato. Plant J (in press)Google Scholar
  29. Huang SW, Vleeshouwers V, Werij JS, Hutten RCB, van Eck HJ, Visser RGF, Jacobsen E (2004) The R3 resistance to Phytophthora infestans in potato is conferred by two closely linked R genes with distinct specificities. Mol Plant-Microbe Interact 17:428–435PubMedCrossRefGoogle Scholar
  30. Kanazin V, Marek LF, Shoemaker RC (1996) Resistance gene analogs are conserved and clustered in soybean. Proc Natl Acad Sci USA 93:11746–11750PubMedCrossRefGoogle Scholar
  31. Konieczny A, Ausubel FM (1993) A procedure for mapping Arabidopsis mutations using codominant ecotype-specific PCR-based markers. Plant J 4:403–410PubMedCrossRefGoogle Scholar
  32. Kuhl JC, Hanneman RE, Havey MJ (2001) Characterization and mapping of Rpi1, a late blight resistance locus from diploid (1EBN) Mexican Solanum pinnatisectum. Mol Genet Genom 265:977–985CrossRefGoogle Scholar
  33. Leister D, Ballvora A, Salamini F, Gebhardt C (1996) A PCR-based approach for isolating pathogen resistance genes from potato with potential for wide application in plants. Nat Genet 14:421–429PubMedCrossRefGoogle Scholar
  34. Leister D, Berger A, Thelen H, Lehmann W, Salamini F, Gebhardt C (1997) Construction of potato YAC library and identification of clones linked to the disease resistance loci R1 and Gro1. Theor Appl Genet 95:954–960CrossRefGoogle Scholar
  35. Leonards-Schippers C, Gieffers W, Salamini F, Gebhardt C (1992) The R1 gene conferring race-specific resistance to Phytophthora infestans in potato is located on potato chromosome V. Mol Gen Genet 233:278–283PubMedCrossRefGoogle Scholar
  36. Leonards-Schippers C, Gieffers W, Schafer-Pregl R, Ritter E, Knapp S, Salamini F, Gebhardt C (1994) Quantitative resistance to Phytophthora infestans in potato: a case study for QTL mapping in an allogamous plant species. Genetics 137:67–77PubMedGoogle Scholar
  37. Li X, van Eck HJ, Rouppe van der Voort JNAM, Huigen DJ, Stam P, Jacobsen E (1998) Autotetraploids and genetic mapping using common AFLP markers: the R2 allele conferring resistance to Phytophthora infestans mapped on potato chromosome 4. Theor Appl Genet 96:1121–1128CrossRefGoogle Scholar
  38. Malcomson JF, Black W (1966) New R-genes in Solanum demissum Lindl. and their complementary races of Phytophthora infestans (Mont) de Bary. Euphytica 15:199–203CrossRefGoogle Scholar
  39. Manly KF, Cudmore JRH, Meer JM (2001) Map manager QTX, cross platform software for genetic mapping. Mamm Genome 12:930–932PubMedCrossRefGoogle Scholar
  40. Mastenbroek C (1952) Investigations into the inheritance of the immunity from Phytophthora infestans De B. of Solanum demissum Lindl. Euphytica 1:187–198CrossRefGoogle Scholar
  41. Meksem K, Leister D, Peleman J, Zabeau M, Salamini F, Gebhardt C (1995) A high resolution map of the vicinity of the R1 locus on chromosome V of potato based on RFLP and AFLP markers. Mol Gen Genet 249:74–81PubMedCrossRefGoogle Scholar
  42. Michelmore RW, Paran I, Kesseli RV (1991) Identification of markers linked to disease-resistance genes by bulk segregant analysis: a rapid method to detect markers in specific genomic regions by using segregating populations. Proc Natl Acad Sci USA 88:9828–9832PubMedCrossRefGoogle Scholar
  43. Milbourne D, Meyer RC, Collins AJ, Ramsay LD, Gebhardt C, Waugh R (1998) Isolation, characterization and mapping of simple sequence repeat loci in potato. Mol Gen Genet 259:233–245PubMedCrossRefGoogle Scholar
  44. Moreau P, Thoquet P, Olivier J, Laterrot H, Grimsley N (1998) Genetic mapping of Ph-2, a single locus controlling partial resistance to Phytophthora infestans in tomato. Mol Plant-Microbe Interact 11:259–269CrossRefGoogle Scholar
  45. Naess SK, Bardeen JM, Wielgus SM, Haberlach GT, McGrath JM, Hegelson JP (2000) Resistance to late blight in Solanum bulbocastanum is mapped to chromosome 8. Theor Appl Genet 295:1–8Google Scholar
  46. Okimoto R, Dogson JB (1996) Improved PCR amplification of multiple specific alleles (PAMSA) using internally mismatched primers. Biotechniques 21:20–26PubMedGoogle Scholar
  47. Paterson AH (1996) Making genetic maps. In: Paterson AH (eds) Genome mapping in plants. Academic, Austin pp 22–39Google Scholar
  48. Rivera-Peña A (1990) Wild tuber-bearing species of Solanum and incidence of Phythophthora infestans (Mont.) de Bary on the western slopes of the volcano Nevado de Toluca. 5. Type of resistance to P. infestans. Potato Res 33:479–486CrossRefGoogle Scholar
  49. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, PlainviewGoogle Scholar
  50. Schick R, Schick E, Haussdorfer M (1958) Ein beitrag zur physiologischen spezialisierung von Phytophthora infestans. Phytopath Z 31:225–236Google Scholar
  51. Shaner G, Finney RE (1977) The effect of nitrogen fertilization on the expression of slow-mildewing resistance in Knowx wheat. Phytopathology 67:1051–1056Google Scholar
  52. Simko I (2002) Comparative analysis of quantitative trait loci for foliage resistance to Phytophthora infestans in tuber-bearing Solanum species. Am J Potato Res 79:125–132Google Scholar
  53. Solomon-Blackburn RM, Barker H (2001) A review of host major-gene resistance to potato viruses X, Y, A and V in potato: genes, genetics and mapped locations. Heredity 86:8–16PubMedCrossRefGoogle Scholar
  54. Song J, Bradeen JM, Naess SK, Raasch JA, Wielgus SM, Haberlach GT, Liu J, Kuang H, Austin-Phillips S, Buell CR, Helgeson JP, Jiang J (2003) Gene RB cloned from Solanum bulbocastanum confers broad spectrum resistance to potato late blight. Proc Natl Acad Sci USA 100:9128–9133PubMedCrossRefGoogle Scholar
  55. Spielman LJ, McMaster BJ, Fry WE (1989) Dominance and recessiveness at loci for virulence against potato and tomato in Phytophthora infestans. Theor Appl Genet 77:832–838CrossRefGoogle Scholar
  56. Stewart HE, Bradshaw JE, Pande B (2003) The effect of the presence of R-genes for resistance to late blight (Phytophthora infestans) of potato (Solanum tuberosum) on the underlying level of field resistance. Plant Pathol 52:193–198CrossRefGoogle Scholar
  57. Tanksley SD, Ganal MW, Prince JP, Vicente MCd, Bonierbale MW, Broun P, Fulton TM, Giovanoni JJ, Grandillo S, Martin GB, Messenger R, Miller JC, Miller L, Paterson AH, Pineda O, Roder MS, Wing RA, Wu W, Young ND (1992) High density molecular linkage maps of the tomato and potato genomes. Genetics 132:1141–1160PubMedGoogle Scholar
  58. Tooley PW, Sweigard JA, Fry WE (1986) Fitness and virulence of Phytophthora infestans isolates from sexual and asexual populations. Phytopathology 76:1209–1212Google Scholar
  59. Umaerus V, Umaerus M (1994) Inheritance of resistance to late blight. In: Bradshaw JE, Mackay GR (eds) Potato genetics. CAB International, Oxon pp 365–401Google Scholar
  60. USDA and ARS (1999) National genetic resources program. Germplasm Resources information network (GRIN). On-line database National Germplasm Resources Laboratory, Beltsville, Maryland. Available http://www.ars-grin.gov/npgs/searchgrin.html
  61. Van der Plank JE (1963) Plant diseases: epidemics and control. New YorkGoogle Scholar
  62. Wastie RL (1991) Breeding for resistance. Adv Plant Pathol. 7:193–223Google Scholar
  63. Ye S, Dhillon S, Ke X, Collins AR, Day INM (2001) An efficient procedure for genotyping single nucleotide polymorphisms. Nucl Acids Res 29:e88PubMedCrossRefGoogle Scholar
  64. Yu YG, Buss GR, Maroof MAS (1996) Isolation of a superfamily of candidate disease-resistance genes in soybean based on a conserved nucleotide binding site. Proc Natl Acad Sci USA 93:11751–11756PubMedCrossRefGoogle Scholar
  65. Zhang LP, Khan AA, Niño-Liu D, Foolad MR (2002) A molecular linkage map of tomato displaying chromosomal locations of resistance gene analogs based on a Lycopersicon esculentum × Lycopersicon hirsutum cross. Genome 45:133–146PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  • G. M. Rauscher
    • 1
  • C. D. Smart
    • 1
    • 6
  • I. Simko
    • 2
    • 5
  • M. Bonierbale
    • 3
  • H. Mayton
    • 1
  • A. Greenland
    • 4
    • 7
  • W. E. Fry
    • 1
  1. 1.Department of Plant PathologyCornell UniversityIthacaUSA
  2. 2.Department of HorticultureCornell UniversityIthacaUSA
  3. 3.Centro Internacional de la PapaLimaPeru
  4. 4.Syngenta Jealott’s HillBracknellUK
  5. 5.USDA-ARSBeltsvilleUSA
  6. 6.Department of Plant PathologyCornell UniversityGenevaUSA
  7. 7.National Institute for Agricultural BotanyCambridgeUK

Personalised recommendations