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Resistance Gene Analog Polymorphism (RGAP) Markers Co-Localize with Disease Resistance Genes and QTL in Common Bean

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Abstract

Resistance (R) genes containing nucleotide-binding site (NBS)-leucine rich repeats (LRR) are the most prevalent types of R gene in plants. The objective of this study was to develop PCR-based R-gene analog polymorphism (RGAP) markers for common bean (Phaseolus vulgaris L). Twenty degenerate primers were designed from the conserved kinase-1a (GVGKTT) and hydrophobic domains (GLPLAL) of known NBS-LRR type R-genes and from EST databases. Sixty-six of the 100 primer combinations tested yielded polymorphism. Thirty-two RGAP markers were mapped in the BAT 93/Jalo EEP558 core mapping population for common bean. The markers mapped to 10 of 11 linkage groups with a strong tendency for clustering. In addition, the RGAP markers co-located, on six linkage groups, with 15 resistance gene analogs (RGAs) that were previously mapped in other populations of common bean. The distance between the priming sites in NBS-LRR type R-genes is around 500 bp. Of the 32 RGAP markers, 19 had sizes larger and 13 less than 500 bp. RGAP markers mapped close to known R-genes on B11, and to QTLs for resistance on B1, B2, B6, B7, B8, B10, and B11. RGAP appears to provide a useful marker technique for tagging and mapping R-genes in segregating common bean populations, discovery of candidate genes underlying resistance QTL, and future cloning of R-genes in common bean.

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Abbreviations

HD:

Hydrophobic domain

K:

Kinase

LG:

Linkage group

QTL:

Quantitative trait locus/loci

RGAP:

Resistance gene analog polymorphism

References

  • M.G. Aarts B. Lintel Hekkert E.B. Holub J.L. Beynon W.J. Stiekema A. Pereira (1998) ArticleTitleIdentification of R-gene homologous DNA fragments genetically linked to disease resistance loci in Arabidopsis thaliana Mol. Plant Microb. Interact. 11 251–258 Occurrence Handle1:CAS:528:DyaK1cXitVGqsLc%3D

    CAS  Google Scholar 

  • P.A. Anderson G.J. Lawrence B.C. Morrish M.A. Ayliffe E.J. Finnegan J.G. Ellis (1997) ArticleTitleInactivation of the flax rust resistance gene M associated with loss of a repeated unit within the leucine-rich repeat coding region Plant Cell 9 641–651 Occurrence Handle1:CAS:528:DyaK2sXivFCrsLc%3D Occurrence Handle9144966

    CAS  PubMed  Google Scholar 

  • B. Baker P. Zambryski B. Staskawicz S.P. Dinesh-Kumar (1997) ArticleTitleSignaling in plant-microbe interactions Science 276 726–733 Occurrence Handle1:CAS:528:DyaK2sXivFOltLg%3D Occurrence Handle9115193

    CAS  PubMed  Google Scholar 

  • A.F. Bent (1996) ArticleTitlePlant disease resistance genes: Function meets structure Plant Cell 8 1757–1771 Occurrence Handle10.1105/tpc.8.10.1757 Occurrence Handle1:CAS:528:DyaK28Xmsl2mtbw%3D Occurrence Handle12239361

    Article  CAS  PubMed  Google Scholar 

  • Caranta C., Lefebvre V. and Palloix A. 1997. Polygenic resistance of pepper to potyviruses consist of a combination of isolate specific and broad-spectrum quantitative trait loci. Mol. Plant Microb. Interact. 872–878.

  • N.C. Collins C.A. Webb S. Seah J.G. Ellis S.H. Hulbert A. Pryor (1998) ArticleTitleThe isolation and mapping of disease resistance gene analogs in maize Mol. Plant Microb. Interact. 11 968–978 Occurrence Handle1:CAS:528:DyaK1cXmtlCqsL8%3D

    CAS  Google Scholar 

  • F. Creusot C. Macadre E. Ferrier Cana C. Riou V. Geffroy M. Sevignac M. Dron T. Langin (1999) ArticleTitleCloning and molecular characterization of three members of the NBS-LRR subfamily located in the vicinity of the Co-2 locus for anthracnose resistance in Phaseolus vulgaris Genome 42 254–264 Occurrence Handle10.1139/gen-42-2-254 Occurrence Handle1:CAS:528:DyaK1MXjtVGju70%3D Occurrence Handle10231959

    Article  CAS  PubMed  Google Scholar 

  • Z. Deng S. Huang P. Ling C. Chen C. Yu C.A. Weber G.A. Moore F.G. Gmitter SuffixJr. (2000) ArticleTitleCloning and characterization of NBS-LRR class resistance-gene candidate sequences in citrus Theor. Appl. Genet. 101 IssueID(5–6) 814–822 Occurrence Handle1:CAS:528:DC%2BD3cXosFyhu78%3D

    CAS  Google Scholar 

  • M.S. Dixon K. Hatzixanthis D.A. Jones K. Harrison J.D. Jones (1998) ArticleTitleThe tomato Cf-5 disease resistance gene and six homologs show pronounced allelic variation in leucine-rich repeat copy number Plant Cell 10 1915–1925 Occurrence Handle10.1105/tpc.10.11.1915 Occurrence Handle1:CAS:528:DyaK1MXptFSi Occurrence Handle9811798

    Article  CAS  PubMed  Google Scholar 

  • H.H. Flor (1956) ArticleTitleThe complementary genetic systems in flax and flax rust Adv. Genet. 8 29–54

    Google Scholar 

  • Freyre R., Skroch P.W., Geffroy V., Adam Blondon A.F., Shirmohamadali A., Johnson W.C., Llaca V., Nodari R.O., Pereira P.A., Tsai S.M., Tohme J., Dron M., Nienhuis J., Vallejos C.E. and Gepts P. 1998. Towards an integrated linkage map of common bean. 4. Development of a core linkage map and alignment of RFLP maps. Theor. Appl. Genet. 847–856.

  • C. Gebhardt J.P. Valkonen (2001) ArticleTitleOrganization of genes controlling disease resistance in the potato genome Annu. Rev. Phytopathol. 39 79–102 Occurrence Handle10.1146/annurev.phyto.39.1.79 Occurrence Handle1:CAS:528:DC%2BD3MXmvVygsrk%3D Occurrence Handle11701860

    Article  CAS  PubMed  Google Scholar 

  • V. Geffroy F. Creusot J. Falquet J. Sévignac A.F. Adam-Blonden H. Bannerot P. Gepts M. Dron (1998) ArticleTitleA family of LRR sequences in the vicinity of the Co-2 locus for anthracnose resistance in Phaseolus vulgaris and its potential use in marker-assisted selection Theor. Appl. Genet. 96 494–502 Occurrence Handle10.1007/s001220050766 Occurrence Handle1:CAS:528:DyaK1cXivVWlsLw%3D

    Article  CAS  Google Scholar 

  • V. Geffroy M. Sévignac J. Oliveira ParticleDe G. Fouilloux P. Skroch P. Thoquet P. Gepts T. Langin M. Dron (2000) ArticleTitleInheritance of partial resistance against Colletotrichum lindemuthianum Plant Microb. Interact. 13 287–296 Occurrence Handle1:CAS:528:DC%2BD3cXht1ymtbY%3D

    CAS  Google Scholar 

  • Gentzbittel L., Mouzeyar S., Badaoui S., Mestries E., Vear F., de Labrouhe D. and Nicolas P. 1998. Cloning of molecular markers for disease resistance in sunflowerHelianthus annuus L. Theor. Appl. Genet. 519–525.

  • Hammond-Kosack K. and Jones J.D.G. 1997. Plant disease resistance genes. Annu. Rev. Plant Physiol. Plant Mol. Biol. 575–607.

  • S. Hunger G. Gaspero Particledi S. Mohring D. Bellin R. Schafer-Pregl D.C. Borchardt C.E. Durel M. Werber (2003) ArticleTitleIsolation and linkage analysis of expressed disease-resistance gene analogues of sugar beet (Beta vulgaris L.) Genome 46 IssueID1 70–82 Occurrence Handle10.1139/g02-106 Occurrence Handle1:CAS:528:DC%2BD3sXlslartrs%3D Occurrence Handle12669798

    Article  CAS  PubMed  Google Scholar 

  • S.C. Jeong A.J. Hayes R.M. Biyashev M.A. Saghai Maroof (2001) ArticleTitleDiversity and evolution of a non-TIR-NBS sequence family that clusters to a chromosomal “hotspot” for disease resistance genes in soybean Theor. Appl. Genet. 103 IssueID2–3 406–414 Occurrence Handle1:CAS:528:DC%2BD3MXmvVeksbo%3D

    CAS  Google Scholar 

  • D.A. Jones C.M. Thomas K.E. Hammond-Kosack P.J. Balint-Kurti J.D. Jones (1994) ArticleTitleIsolation of the tomato Cf-9 gene for resistance to Cladosporium fulvum by transposon tagging Science 266 789–793 Occurrence Handle1:CAS:528:DyaK2MXitVGgtrg%3D Occurrence Handle7973631

    CAS  PubMed  Google Scholar 

  • V. Kanazin L.F. Marek R.C. Shoemaker (1996) ArticleTitleResistance gene analogs are conserved and clustered in soybean Proc. Natl. Acad. Sci. USA 93 11746–11750 Occurrence Handle10.1073/pnas.93.21.11746 Occurrence Handle1:CAS:528:DyaK28XmtlansLw%3D Occurrence Handle8876208

    Article  CAS  PubMed  Google Scholar 

  • J.D. Kelly P. Gepts P.N. Miklas D.P. Coyne (2003) ArticleTitleTagging and mapping of genes and QTL and molecular marker-assisted selection for traits of economic importance in bean and cowpea Field Crops Res. 82 135–154 Occurrence Handle10.1016/S0378-4290(03)00034-0

    Article  Google Scholar 

  • Kosambi D.D. 1944. The estimation of map distances from recombination values. Annu. Eugen. 172–175.

  • Lander E.S., Green P., Abrahamson J., Barlow A., Daly M., Lincoln S.E. and Newburg L. 1987. MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 174–181.

  • Lefebvre V. and Chevre A.-M. 1995. Tools for marking plant disease and pest resistance genes. Agronomie 3–19.

  • Lefebvre V. and Palloix A. 1996. Both epistatic and additive effects of QTLs are involved in polygenic induced resistance to disease: a case study, the interaction pepper-Phytophthora capsici Leonian. Theor. Appl. Genet. 503–511.

  • D. Leister A. Ballvora F. Salamini C. Gebhardt (1996) ArticleTitleA PCR-based approach for isolating pathogen resistance genes from potato with potential for wide application in plants Nat. Genet. 14 421–429 Occurrence Handle10.1038/ng1296-421 Occurrence Handle1:CAS:528:DyaK28XntlGgsb4%3D Occurrence Handle8944022

    Article  CAS  PubMed  Google Scholar 

  • D. Leister J. Kurth D.A. Laurie M. Yano T. Sasaki K. Devos A. Graner P. Schulze-Lefert (1998) ArticleTitleRapid reorganization of resistance gene homologues in cereal genomes Proc. Natl. Acad. Sci. USA 95 370–375 Occurrence Handle10.1073/pnas.95.1.370 Occurrence Handle1:CAS:528:DyaK1cXjtl2gsg%3D%3D Occurrence Handle9419382

    Article  CAS  PubMed  Google Scholar 

  • C. Leonards-Schippers W. Gieffers F. Salamini C. Gebhardt (1992) ArticleTitleThe R1 gene conferring race-specific resistance to Phytophthora infestans in potato is located on potato chromosome V Mol. Gen. Genet. 233 278–283 Occurrence Handle10.1007/BF00587589 Occurrence Handle1:CAS:528:DyaK38XkvVCntbk%3D Occurrence Handle1351246

    Article  CAS  PubMed  Google Scholar 

  • C.E. Lopez I.F. Acosta C. Jara F. Pedraza E. Gaitan-Solis G. Gallego S. Beebe J. Tohme (2003) ArticleTitleIdentifying resistance gene analogs associated with resistances to different pathogens in common bean Phytopathology 93 IssueID1 88–95 Occurrence Handle1:CAS:528:DC%2BD3sXksV2isw%3D%3D

    CAS  Google Scholar 

  • G.B. Martin (1999) ArticleTitleFunctional analysis of plant disease resistance genes and their downstream effectors Curr. Opin. Plant Biol. 2 273–279 Occurrence Handle10.1016/S1369-5266(99)80049-1 Occurrence Handle1:CAS:528:DyaK1MXls1Oqurg%3D Occurrence Handle10458999

    Article  CAS  PubMed  Google Scholar 

  • B.C. Meyers D.B. Chin K.A. Shen S. Sivaramakrishnan D.O. Lavelle Z. Zhang R.W. Michelmore (1998) ArticleTitleThe major resistance gene cluster in lettuce is highly duplicated and spans several megabases Plant Cell 10 1817–1832 Occurrence Handle1:CAS:528:DyaK1MXovF2j Occurrence Handle9811791

    CAS  PubMed  Google Scholar 

  • Nodari R.O. 1992. Towards an integrated map of common bean (Phaseolus vulgaris L.). PhD diss., University of CaliforniaDavis.

  • R.O. Nodari S.M. Tsai P. Guzman R.L.P. Gilbertsonand P. Gepts (1993) ArticleTitleToward an integrated linkage map of common bean. III. Mapping genetic factors controlling host-bacteria interactions Genetics. 134 341–350 Occurrence Handle1:CAS:528:DyaK3sXkvVyisbo%3D Occurrence Handle8514141

    CAS  PubMed  Google Scholar 

  • J.T. Ouedraogo B.S. Gowda M. Jean T.J. Close J.D. Ehlers A.E. Hall A.G. Gillaspie P.A. Roberts A.M. Ismail G. Bruening P. Gepts M.P. Timko F.J. Belzile (2002) ArticleTitleAn improved genetic linkage map for cowpea (Vigna unguiculata L.) combining AFLP, RFLP, RAPD and biochemical markers Genome 45 IssueID1 175–188 Occurrence Handle1:CAS:528:DC%2BD38Xhslarsbk%3D Occurrence Handle11908660

    CAS  PubMed  Google Scholar 

  • S. Pflieger V. Lefebvre C. Caranta A. Blattes B. Goffinet A. Palloix (1999) ArticleTitleDisease resistance gene analogs as candidates for QTLs involved in pepper-pathogen interactions Genome 42 1100–1110 Occurrence Handle10.1139/gen-42-6-1100 Occurrence Handle1:CAS:528:DC%2BD3cXpt12rsg%3D%3D Occurrence Handle10659776

    Article  CAS  PubMed  Google Scholar 

  • E. Ritter T. Debener A. Barone F. Salamini C. Gebhardt (1991) ArticleTitleRFLP mapping on potato chromosomes of two genes controlling extreme resistance to potato virus X (PVX) Mol. Gen. Genet. 227 81–85 Occurrence Handle1:CAS:528:DyaK3MXlvF2qt7c%3D Occurrence Handle1675423

    CAS  PubMed  Google Scholar 

  • M.I. Rivkin C.E. Vallejos P.E. McClean (1999) ArticleTitleDisease-resistance related sequences in common bean Genome 42 41–47 Occurrence Handle10.1139/gen-42-1-41 Occurrence Handle1:CAS:528:DyaK1MXhsVyqsbs%3D Occurrence Handle10208000

    Article  CAS  PubMed  Google Scholar 

  • Seah S., Sivasithamparam K., Karakousis A. and Lagudah E.S. 1998. Cloning and characterisation of a family of disease resistance gene analogs from wheat and barley. Theor. Appl. Genet. 937–945.

  • K.A. Shen B.C. Meyers M.N. Islam Faridi D.B. Chin D.M. Stelly R.W. Michelmore (1998) ArticleTitleResistance gene candidates identified by PCR with degenerate oligonucleotide primers map to clusters of resistance genes in lettuce Mol. Plant Mic. Int. 11 IssueID8 815–823 Occurrence Handle1:CAS:528:DyaK1cXkslWht7k%3D

    CAS  Google Scholar 

  • E. Speulman D. Bouchez E.B. Holub J.L. Beynon (1998) ArticleTitleDisease resistance gene homologs correlate with disease resistance loci of Arabidopsis thaliana Plant J. 14 467–474 Occurrence Handle10.1046/j.1365-313X.1998.00138.x Occurrence Handle1:CAS:528:DyaK1cXkt1Khtbc%3D Occurrence Handle9670562

    Article  CAS  PubMed  Google Scholar 

  • Spielmeyer W., Huang L., Bariana H., Laroche A., Gill B.S. and Lagudah E.S. 2000. NBS-LRR sequence family is associated with leaf and stripe rust resistance on the end of homoeologous chromosome group 1S of wheat. Theor. Appl. Genet. 1139–1144.

  • B.J. Staskawicz F.M. Ausubel B.J. Baker J.G. Ellis J.D. Jones (1995) ArticleTitleMolecular genetics of plant disease resistance Science 268 661–667 Occurrence Handle1:CAS:528:DyaK2MXlsVGjurg%3D Occurrence Handle7732374

    CAS  PubMed  Google Scholar 

  • C.E. Vallejos P.W. Skroch J. Nienhuis (2001) Phaseolus vulgaris – The common bean integration of RFLP and RAPD-based linkage maps R.L. Phillips I.K. Vasil (Eds) DNA-Based Markers in Plants Kluwer Academic Publishers Netherlands 301–317

    Google Scholar 

  • Y.G. Yu G.R. Buss M.A. Maroof (1996) ArticleTitleIsolation of a superfamily of candidate disease-resistance genes in soybean based on a conserved nucleotide-binding site Proc. Natl. Acad. Sci. USA 93 11751–11756 Occurrence Handle10.1073/pnas.93.21.11751 Occurrence Handle1:CAS:528:DyaK28XmtlansLs%3D Occurrence Handle8876209

    Article  CAS  PubMed  Google Scholar 

  • K. Yu S.J. Park V. Poysa (2000) ArticleTitleMarker-assisted selection of common beans for resistance to common bacterial blight: efficacy and economics Plant Breed. 119 411–415 Occurrence Handle10.1046/j.1439-0523.2000.00514.x Occurrence Handle1:CAS:528:DC%2BD3cXotV2itbg%3D

    Article  CAS  Google Scholar 

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Mutlu, N., Miklas, P.N. & Coyne, D.P. Resistance Gene Analog Polymorphism (RGAP) Markers Co-Localize with Disease Resistance Genes and QTL in Common Bean. Mol Breeding 17, 127–135 (2006). https://doi.org/10.1007/s11032-005-4474-6

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