Skip to main content
Log in

Resistance gene analogues identified through the NBS-profiling method map close to major genes and QTL for disease resistance in apple

  • Original Paper
  • Published:
Theoretical and Applied Genetics Aims and scope Submit manuscript

Abstract

We used a new method called nucleotide-binding site (NBS) profiling to identify and map resistance gene analogues (RGAs) in apple. This method simultaneously allows the amplification and the mapping of genetic markers anchored in the conserved NBS-encoding domain of plant disease resistance genes. Ninety-four individuals belonging to an F1 progeny derived from a cross between the apple cultivars ‘Discovery’ and ‘TN10-8’ were studied. Two degenerate primers designed from the highly conserved P-loop motif within the NBS domain were used together with adapter primers. Forty-three markers generated with NBS profiling could be mapped in this progeny. After sequencing, 23 markers were identified as RGAs, based on their homologies with known resistance genes or NBS/leucine-rich-repeat-like genes. Markers were mapped on 10 of the 17 linkage groups of the apple genetic map used. Most of these markers were organized in clusters. Twenty-five markers mapped close to major genes or quantitative trait loci for resistance to scab and mildew previously identified in different apple progenies. Several markers could become efficient tools for marker-assisted selection once converted into breeder-friendly markers. This study demonstrates the efficiency of the NBS-profiling method for generating RGA markers for resistance loci in apple.

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.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Alston FH (1983) Progress in transferring mildew (Podosphaera leucotricha) resistance from Malus species to the cultivated apple. In: Integrated control of pome fruit diseases. IOBC (WPRS) Bull 8:87–95

  • Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    CAS  PubMed  Google Scholar 

  • Backes G, Madsen LH, Jaiser H, Stougaard J, Herz M, Mohler V, Jahoor A (2003) Localisation of genes for resistance against Blumeria graminis sp. hordei and Puccinia graminis in a cross between a barley cultivar and a wild barley (Hordeum vulgare ssp. spontaneum) line. Theor Appl Genet 106:353–362

    CAS  PubMed  Google Scholar 

  • Bai Y, Huang CC, Van der Hulst R, Meijer-Dekens F, Bonnema G, Lindhout P (2003) QTLs for tomato powdery mildew resistance (Oidium lycopersici) in Lycopersicon parviflorum G1.1601 co-localize with two qualitative powdery mildew resistance genes. Mol Plant-Microbe Interact 16:169–176

    Google Scholar 

  • Baldi P, Patocchi A, Zini E, Toller C, Velasco R, Komjanc M (2004) Cloning and linkage mapping of resistance gene homologues in apple. Theor Appl Genet 109:231–239

    Article  Google Scholar 

  • Belfanti E, Silfverberg-Dilworth E, Tartarini S, Patocchi A, Barbieri M, Zhu J, Vinatzer BA, Gianfranceschi L, Gessler C, Sansavini S (2004) The HcrVf2 gene from a wild apple confers scab resistance to a transgenic cultivated variety. Proc Natl Acad Sci USA101:886–890

    Article  CAS  PubMed  Google Scholar 

  • Bénaouf G, Parisi L (2000) Genetics of host-pathogen relationships between Venturia inaequalis races 6 and 7 and Malus species. Phytopathology 90:236–242

    Google Scholar 

  • Calenge F, Faure A, Drouet D, Parisi L, Brisset M-N, Paulin J-P, Van der Linden CG, Van de Weg WE, Schouten H, Lespinasse Y, Durel C-E (2003) Genomic organization of resistance factors against scab (Venturia inaequalis), powdery mildew (Podosphaera leucotricha) and fire blight (Erwinia amylovora) in apple. In: Proceedings of the XI international congress on molecular plant-microbe interactions, St. Petersburg

  • Calenge F, Faure A, Goerre M, Gebhardt C, Van de Weg WE, Parisi L, Durel C-E (2004) A QTL analysis reveals both broad-spectrum and isolate-specific QTL for scab resistance in an apple progeny challenged with eight isolates of Venturia inaequalis. Phytopathology 94:370–379

    Google Scholar 

  • Collins NC, Webb CA, Seah S, Ellis JG, Hulbert SH, Pryor A (1998) The isolation and mapping of disease resistance gene analogs in maize. Mol Plant-Microbe Interact 11:968–978

    Google Scholar 

  • Dangl J, Jones J (2001) Plant pathogens and integrated defence responses to infection. Nature 411:826–833

    Article  CAS  PubMed  Google Scholar 

  • Durel C-E, Van de Weg WE, Venisse J-S, Parisi L (2000) Localisation of a major gene for apple scab resistance on the European genetic map of the Prima × Fiesta cross. In: Integrated control of pome fruit diseases. IOBC-WPRS Bull 23:245–246

  • Durel C-E, Parisi L, Laurens F, Van de Weg E, Liebhard R, Koller B, Jourjon MF (2003) Genetic dissection of partial resistance against two monoconidial strains of the new race 6 of Venturia inaequalis in apple. Genome 46:224–234

    Article  Google Scholar 

  • Evans KM, James CM (2003) Identification of SCAR markers linked to Pl-w mildew resistance in apple. Theor Appl Genet 106:1178–1183

    Google Scholar 

  • Faris JD, Li WL, Liu DJ, Chen PD, Gill BS (1999) Candidate gene analysis of quantitative disease resistance in wheat. Theor Appl Genet 98: 219–225

    Article  CAS  Google Scholar 

  • Gebhardt C, Valkonen JPT (2001) Organization of genes controlling disease resistance in the potato genome. Annu Rev Phytopathol 39: 79–102

    Article  CAS  PubMed  Google Scholar 

  • Geffroy V, Sevignac M, De Oliveira JC, Fouilloux G, Skroch P, Thoquet P, Gepts P, Langin T, Dron M (2000) Inheritance of partial resistance against Colletotrichum lindemuthianum in Phaseolus vulgaris and co-localization of quantitative trait loci with genes involved in specific resistance. Mol Plant-Microbe Interact 13:287–96

    Google Scholar 

  • Grattapaglia D, Sederoff R (1994) Genetic linkage maps of Eucaliptus grandis and E. urophylla using a pseudo-testcross mapping strategy and RAPD markers. Genetics 137:1121–1137

    CAS  PubMed  Google Scholar 

  • Grube RC, Radwanski ER, Jahn M (2000) Comparative genetics of disease resistance within the Solanaceae. Genetics 155:873–887

    CAS  PubMed  Google Scholar 

  • Hammond-Kosack KE, Parker JE (2003) Deciphering plant–pathogen communications: free perspectives for molecular resistance breeding. Curr Opin Biotechnol 14:177–193

    Article  Google Scholar 

  • Hayes AJ, Saghai Maroof MA (2000) Targeted resistance gene mapping in soybean using modified AFLPs. Theor Appl Genet 100:1279–1283

    Article  CAS  Google Scholar 

  • Hemmat M, Brown SK (2002) Tagging and mapping scab resistance genes from R12740-7A apple. J Am Soc Hortic Sci 127:365–370

    CAS  Google Scholar 

  • Hulbert SH, Webb CA, Smith SM, Sun Q (2001) Resistance gene complexes: evolution and utilization. Annu Rev Phytopathol 39:285–312

    Article  CAS  PubMed  Google Scholar 

  • Kanazin V, Frederick Marek L, Shoemaker RC (1996) Resistance gene analogs are conserved and clustered in soybean. Proc Natl Acad Sci USA 93:11746–11750

    Article  CAS  PubMed  Google Scholar 

  • Lee S-Y, Seo J-S, Rodriguez-Lanetty M, Lee D-H (2003) Comparative analysis of superfamilies of NBS-encoding disease resistance gene analogs in cultivated and wild apple species. Mol Genet Genomics 269: 101–108

    CAS  PubMed  Google Scholar 

  • 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. Nature genetics 14:421–429

    Article  Google Scholar 

  • Lespinasse Y (1989) Breeding pome fruits with stable resistance to diseases. Genes, resistance mechanisms, present work and prospects. In: Integrated control of pome fruit diseases. IOBC-WPRS Bull 2:100–115

  • Liebhard R, Koller B, Gianfranceschi L, Gessler C (2003a) Creating a saturated reference map for the apple (Malus × domestica Borkh.) genome. Theor Appl Genet 106:1497–1508

    CAS  PubMed  Google Scholar 

  • Liebhard R, Koller B, Patocchi A, Kellerhalls M, Pfammatter W, Jermini M, Gessler C (2003b) Mapping quantitative field resistance in apple against scab. Phythopathology 93:493–501

    Google Scholar 

  • MacHardy WE, Gadoury DM, Gessler C (2001) Parasitic and biological fitness of Venturia inaequalis: relationship to disease management strategies. Plant Dis 85:1036–1051

    Google Scholar 

  • Meyers BC, Dickerman AW, Michelmore RW, Sivaramakrishnan S, Sobral BW, Young ND (1999) Plant disease resistance genes encode members of an ancient and diverse protein family within the nucleotide-binding superfamily. Plant J 20:317–332

    Article  CAS  PubMed  Google Scholar 

  • Meyers BC, AK, Griego A, Kuang H, Michelmore R (2003) Genome-wide analysis of NBS–LRR-encoding genes in Arabidopsis. Plant Cell 15:809–834

    Article  CAS  PubMed  Google Scholar 

  • Pan Q, Liu Y, Budai-Hadrian O, Sela M, Carmel-Goren L, Zamir D, Fluhr R (2000) Comparative genetics of nucleotide binding site-leucine rich repeat resistance gene homologues in the genomes of two dicotyledons: tomato and Arabidopsis. Genetics 155:309–322

    CAS  PubMed  Google Scholar 

  • Patocchi A, Bigler B, Koller B, Liebhard R, Kellerhalls M, Gessler C (2003) Mapping of Vr2, a third apple scab resistance gene of Russian seedling (R12740-7A) P450. Plant and animal genomes XI conference, San Diego

  • Pflieger S, Palloix A, Caranta C, Blattes A, Lefebvre V (2001) Defense response genes co-localize with quantitative disease resistance loci in pepper. Theor Appl Genet 103:920–929

    Article  CAS  Google Scholar 

  • Ramalingam J, Vera Cruz CM, Kukreja K, Chittoor JM, Wu JL, Lee SW, Baraoidan M, George ML, Cohen MB, Hulbert SH, Leach JE, HL (2003) Candidate defense genes from rice, barley, and maize and their association with qualitative and quantitative resistance in rice. Mol Plant-Microbe Interact 16:14–24

    Google Scholar 

  • Shen KA, Meyers BC, Islam-Faridi MN, Chin DB, Stelly DM, Michelmore RW (1998) Resistance gene candidates identified by PCR with degenerate oligonucleotide primers map to clusters of resistance genes in lettuce. Mol Plant-Microbe Interact 11:815–823

    Google Scholar 

  • Speulman E, Bouchez D, Holub EB, Beynon JL (1998) Disease resistance gene homologs correlate with disease resistance loci of Arabidopsis thaliana. Plant J 14:467–474

    Article  CAS  PubMed  Google Scholar 

  • Tartarini S, Gennari F, Pratesi D, Palazzetti C, Sansavini S, Parisi L, Fouillet A, Fouillet V, Durel C-E (2003) Characterization of a race 6 scab resistance gene from Italian germplasm. Proceedings of the Eucarpia symposium on fruit breeding and genetics, Angers

  • Trognitz F, Manosalva P, Gysin R, Niño-Liu D, Simon R, del Rosario Herrera M, Trognitz B, Ghislain M, Nelson R (2002) Plant defense genes associated with quantitative resistance to potato late blight in Solanum phureja × dihaploid S. tuberosum hybrids. Mol Plant-Microbe Interact 15:587–597

    Google Scholar 

  • Van der Linden CG, Wouters DCAE, Mihalka V, Kochieva EZ, Smulders MJM, Vosman B (2004) Efficient targeting of plant disease resistance loci using NBS profiling. Theor Appl Genet 109:384–393

    PubMed  Google Scholar 

  • Williams EB, Kuc J (1969) Resistance in Malus to Venturia inaequalis. Annu Rev Phytopathol 7:223–246

    Article  CAS  Google Scholar 

  • Young ND (2000) The genetic architecture of resistance. Curr Opin Plant Biol 3:285–290

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Carole Köning-Boucoiran and Martijn Van Kaauwen for their excellent technical assistance and Pr. Graham King for his rereading of our manuscript. This work was partly supported by the European project QLK5-CT-2002-01492 (HiDRAS: high-quality disease resistant apples for a sustainable agriculture).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to C.-E. Durel.

Additional information

Communicated by C. Möllers

Rights and permissions

Reprints and permissions

About this article

Cite this article

Calenge, F., Van der Linden, C.G., Van de Weg, E. et al. Resistance gene analogues identified through the NBS-profiling method map close to major genes and QTL for disease resistance in apple. Theor Appl Genet 110, 660–668 (2005). https://doi.org/10.1007/s00122-004-1891-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-004-1891-6

Keywords

Navigation