BAC end sequences corresponding to the B4 resistance gene cluster in common bean: a resource for markers and synteny analyses

  • Perrine David
  • Mireille Sévignac
  • Vincent Thareau
  • Yann Catillon
  • Jim Kami
  • Paul Gepts
  • Thierry Langin
  • Valérie Geffroy
Original Paper

Abstract

In common bean, a complex disease resistance (R) gene cluster, harboring many specific R genes against various pathogens, is located at the end of the linkage group B4. A BAC library of the Meso-american bean genotype BAT93 was screened with PRLJ1, a probe previously shown to be specific to the B4 R gene cluster, leading to the identification of 73 positive BAC clones. BAC-end sequencing (BES) of the 73 positive BACs generated 75 kb of sequence. These BACs were organized into 6 contigs, all mapped at the B4 R gene cluster. To evaluate the potential of BES for marker development, BES-derived specific primers were used to check for linkage with two allelic anthracnose R specificities Co-3 and Co-32, through the analysis of pairs of Near Isogenic Lines (NILs). Out of 32 primer pairs tested, two revealed polymorphisms between the NILs, confirming the suspected location of Co-3 and Co-32 at the B4 cluster. In order to identify the orthologous region of the B4 R gene cluster in the two model legume genomes, bean BESs were used as queries in TBLASTX searches of Medicago truncatula and Lotus japonicus BAC clones. Putative orthologous regions were identified on chromosome Mt6 and Lj2, in agreement with the colinearity observed between Mt and Lj for these regions.

Keywords

Disease resistance gene Phaseolus vulgaris BAC-end sequence Near isogenic lines Synteny 

References

  1. Ashfield T, Danzer JR, Held D, Clayton K, Keim P, Saghai Maroof MA, Webb PM, Innes RW (1998) Rpg1, a soybean gene effective against races of bacterial blight, maps to a cluster of previously identified disease resistance genes. Theor Appl Genet 96:1013–1021CrossRefGoogle Scholar
  2. Ashfield T, Bocian A, Held D, Henk AD, Marek LF, Danesh D, Penuela S, Meksem K, Lightfoot DA, Young ND, Shoemaker RC, Innes RW (2003) Genetic and physical localization of the soybean Rpg1-b disease resistance gene reveals a complex locus containing several tightly linked families of NBS-LRR genes. Mol Plant-Microbe Interact 16:817–826PubMedCrossRefGoogle Scholar
  3. Ameline-Torregrosa C, Wang BB, O’Bleness MS, Deshpande S, Zhu HY, Roe B, Young ND, Cannon SB (2008) Identification and characterization of nucleotide-binding site-Leucine-rich repeat genes in the model plant Medicago truncatula. Plant Physiol 146:5–21PubMedCrossRefGoogle Scholar
  4. Bannerot H (1965) Résultat de l’infection d’une collection de haricots par six races physiologiques d’anthracnose. Ann Amélior Plantes 15:201–222Google Scholar
  5. Barrus MF (1911) Variation of varieties of beans in their susceptibility to anthracnose. Phytopathology 1:190–195Google Scholar
  6. Barrus MF (1915) An anthracnose-resistant red kidney bean. Phytopathology 5:303–311Google Scholar
  7. Broughton WJ, Hernandez G, Blair M, Beebe S, Gepts P, Vanderleyden J (2003) Beans (Phaseolus spp.)—model food legumes. Plant Soil 252:55–128CrossRefGoogle Scholar
  8. Cannon SB, Sterck L, Rombauts S, Sato S, Cheung F, Gouzy J, Wang XH, Mudge J, Vasdewani J, Scheix T, Spannagl M, Monaghan E, Nicholson C, Humphray SJ, Schoof H, Mayer KFX, Rogers J, Quetier F, Oldroyd GE, Debelle F, Cook DR, Retzel EF, Roe BA, Town CD, Tabata S, Van de Peer Y, Young ND (2006) Legume genome evolution viewed through the Medicago truncatula and Lotus japonicus genomes. Proc Natl Acad Sci USA 103:14959–14964PubMedCrossRefGoogle Scholar
  9. Cheung F, Town CD (2007) A BAC end view of the Musa acuminata genome. BMC Plant Biol 7:29PubMedCrossRefGoogle Scholar
  10. Chin DB, Arroyo Garcia R, Ochoa OE, Kesseli RV, Lavelle DO, Richelmore RW (2001) Recombination and spontaneous mutation at the major cluster of resistance genes in lettuce (Lactuca sativa). Genetics 157:831–849PubMedGoogle Scholar
  11. Choi HK, Mun JH, Kim DJ, Zhu HY, Baek JM, Mudge J, Roe B, Ellis N, Doyle J, Kiss GB, Young ND, Cook DR (2004) Estimating genome conservation between crop and model legume species. Proc Natl Acad Sci USA 101:15289–15294PubMedCrossRefGoogle Scholar
  12. Correa RX, Costa MR, Good-God PI, Ragagnin VA, Falejro FG, Moreira MA, De Barros EG (2000) Sequence characterized amplified regions linked to rust resistance genes in the common bean. Crop Sci 40:804–807Google Scholar
  13. Devereux J, Haeberli P, Smithies O (1984) A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res 11:387–395CrossRefGoogle Scholar
  14. Febrer M, Cheung F, Town CD, Cannon SB, Young ND, Abberton MT, Jenkins G, Milbourne D (2007) Construction, characterization, and preliminary BAC-end sequencing analysis of a bacterial artificial chromosome library of white clover (Trifolium repens L.). Genome 50:412–421PubMedCrossRefGoogle Scholar
  15. Ferrier Cana E, Geffroy V, Macadre C, Creusot F, Imbert Bollore P, Sevignac M, Langin T (2003) Characterization of expressed NBS-LRR resistance gene candidates from common bean. Theor Appl Genet 106:251–261PubMedGoogle Scholar
  16. Ferrier Cana E, Macadre C, Sevignac M, David P, Langin T, Geffroy V (2005) Distinct post-transcriptional modifications result into seven alternative transcripts of the CC-NBS-LRR gene JA1tr of Phaseolus vulgaris. Theor Appl Genet 110:895–905PubMedCrossRefGoogle Scholar
  17. Flor HH (1955) Host–parasite interaction in flax rust. Its genetics and other implications. Phytopathology 45:680–685Google Scholar
  18. Fouilloux G (1976) L’anthracnose du haricot (Colletotrichum lindemuthianum, Sacc et Magn.): nouvelles sources de résistance et nouvelles races physiologiques. Ann Amélior Plantes 26:443–453Google Scholar
  19. Fouilloux G (1979) New races of bean anthracnose and consequences on our breeding programs. In: Maraitre H, Meyer JA (eds) Disease of tropical food crops. Université Catholique de Louvain la Neuve, Belgium, pp 221–235Google Scholar
  20. Freyre R, Skroch P, Geffroy V, Adam-Blondon AF, Shirmohamadali A, Johnson WC, Llaca V, Nodari RO, Pereira PA, Tsai SM, Tohme J, Dron M, Nienhuis J, Vallejos CE, 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 97:847–856CrossRefGoogle Scholar
  21. Geffroy V, Creusot F, Falquet J, Sevignac M, Adam-Blondon AF, Bannerot H, Gepts P, Dron M (1998) A 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 96:494–502CrossRefGoogle Scholar
  22. Geffroy V, Sicard D, de Oliveira JCF, Sevignac M, Cohen S, Gepts P, Neema C, Langin T, Dron M (1999) Identification of an ancestral resistance gene cluster involved in the coevolution process between Phaseolus vulgaris and its fungal pathogen Colletotrichum lindemuthianum. Mol Plant-Microbe Interact 12:774–784PubMedCrossRefGoogle Scholar
  23. Geffroy V, Sevignac M, De Oliveira JCF, 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 13:287–296PubMedCrossRefGoogle Scholar
  24. Geffroy V, Sevignac M, Billant P, Dron M, Langin T (2008) Resistance to Colletotrichum lindemuthianum in Phaseolus vulgaris: a case study for mapping two independent genes. Theor Appl Genet 116:407–415PubMedCrossRefGoogle Scholar
  25. Graham PH, Vance CP (2003) Legumes: importance and constraints to greater use. Plant Physiol 131:872–877PubMedCrossRefGoogle Scholar
  26. Grant D, Cregan P, Shoemaker RC (2000) Genome organization in dicots: genome duplication in Arabidopsis and synteny between soybean and Arabidopsis. Proc Natl Acad Sci USA 97:4168–4173PubMedCrossRefGoogle Scholar
  27. Hammond-Kosack KE, Parker JE (2003) Deciphering plant–pathogen communication: fresh perspectives for molecular resistance breeding. Curr Opin Biotechnol 14:177–193PubMedCrossRefGoogle Scholar
  28. Hulbert SH, Webb CA, Smith SM, Sun Q (2001) Resistance gene complexes: evolution and utilization. Annu Rev Phytopathol 39:285–312PubMedCrossRefGoogle Scholar
  29. Jones JDG, Dangl JL (2006) The plant immune system. Nature 444:323–329PubMedCrossRefGoogle Scholar
  30. Kami J, Poncet V, Geffroy V, Gepts P (2006) Development of four phylogenetically-arrayed BAC libraries and sequence of the APA locus in Phaseolus vulgaris. Theor Appl Genet 112:987–998PubMedCrossRefGoogle Scholar
  31. Kosambi DD (1944) The estimation of map distances from recombination values. Ann Eugen 12:172–175Google Scholar
  32. Kuang H, Woo SS, Meyers BC, Nevo E, Michelmore RW (2004) Multiple genetic processes result in heterogeneous rates of evolution within the major cluster disease resistance genes in lettuce. Plant Cell 16:2870–2894PubMedCrossRefGoogle Scholar
  33. Kuang HH, Wei FS, Marano MR, Wirtz U, Wang XX, Liu J, Shum WP, Zaborsky J, Tallon LJ, Rensink W, Lobst S, Zhang PF, Tornqvist CE, Tek A, Bamberg J, Helgeson J, Fry W, You F, Luo MC, Jiang JM, Buell CR, Baker B (2005) 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 44:37–51PubMedCrossRefGoogle Scholar
  34. Kulikova O, Geurts R, Lamine M, Kim DJ, Cook DR, Leunissen J, de Jong H, Roe BA, Bisseling T (2004) Satellite repeats in the functional centromere and pericentromeric heterochromatin of Medicago truncatula. Chromosoma 113:276–283PubMedCrossRefGoogle Scholar
  35. Lai CW, Yu Q, Hou S, Skelton RL, Jones MR, Lewis KLT, Murray J, Eustice M, Guan P, Agbayani R, Moore PH, Ming R, Presting GG (2006) Analysis of papaya BAC end sequences reveals first insights into the organization of a fruit tree genome. Mol Gen Genomics 276:1–12CrossRefGoogle Scholar
  36. Lamoureux D, Bernole A, Le Clainche I, Tual S, Thareau V, Paillard S, Legeai F, Dossat C, Wincker P, Oswald M, Merdinoglu D, Vignault C, Delrot S, Caboche M, Chalhoub B, Adam-Blondon AF (2006) Anchoring of a large set of markers onto a BAC library for the development of a draft physical map of the grapevine genome. Theor Appl Genet 113:344–356PubMedCrossRefGoogle Scholar
  37. Lander ES, Green P, Abrahamson J, Barlow A, Daly MJ, Lincoln SE, Newburg L (1987) MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1:174–181PubMedCrossRefGoogle Scholar
  38. Leister D (2004) Tandem and segmental gene duplication and recombination in the evolution of plant disease resistance genes. Trends Genet 20:116–122PubMedCrossRefGoogle Scholar
  39. Leister D, Kurth J, Laurie DA, Yano M, Sasaki T, Devos K, Graner A, Schulze-Lefert P (1998) Rapid reorganization of resistance gene homologues in cereal genomes. Proc Natl Acad Sci USA 95:370–375PubMedCrossRefGoogle Scholar
  40. Lopez C, Piegu B, Cooke R, Delseny M, Tohme J, Verdier V (2005) Using cDNA and genomic sequences as tools to develop SNP strategies in cassava (Manihot esculenta Crantz). Theor Appl Genet 110:425–431PubMedCrossRefGoogle Scholar
  41. Lopez CE, Acosta IF, Jara C, Pedraza F, Gaitan-Solis E, Gallego G, Beebe S, Tohme J (2003) Identifying resistance gene analogs associated with resistances to different pathogens in common bean. Phytopathology 93:88–95PubMedCrossRefGoogle Scholar
  42. Mammadov JA, Brooks WS, Griffey CA, Maroof MAS (2007) Validating molecular markers for barley leaf rust resistance genes Rph5 and Rph7. Plant Breed 126:458–463CrossRefGoogle Scholar
  43. Mendez-Vigo B, Rodriguez-Suarez C, Paneda A, Ferreira JJ, Giraldez R (2005) Molecular markers and allelic relationships of anthracnose resistance gene cluster B4 in common bean. Euphytica 141:237–245CrossRefGoogle Scholar
  44. Meyers BC, Chin DB, Shen KA, Sivaramakrishnan S, Lavelle DO, Zhang Z, Michelmore RW (1998a) The major resistance gene cluster in lettuce is highly duplicated and spans several megabases. Plant Cell 10:1817–1832PubMedCrossRefGoogle Scholar
  45. Meyers BC, Kaushik S, Nandety RS (2005) Evolving disease resistance genes. Curr Opin Plant Biol 8:129–134PubMedCrossRefGoogle Scholar
  46. Meyers BC, Shen KA, Rohani P, Gaut BS, Michelmore RW (1998b) Receptor-like genes in the major resistance locus of lettuce are subject to divergent selection. Plant Cell 11:1833–1846CrossRefGoogle Scholar
  47. Meyers BC, Kozik A, Griego A, Kuang HH, Michelmore RW (2003) Genome-wide analysis of NBS–LRR-encoding genes in Arabidopsis. Plant Cell 15:809–834PubMedCrossRefGoogle Scholar
  48. Michelmore RW, Paran I, Kesseli RV (1991) Identification of markers linked to disease-resistance genes by bulked 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
  49. Mienie CM, Liedenberg MM, Pretorius ZA, Miklas PN (2005) SCAR markers linked to the common bean rust resistance gene Ur-13. Theor Appl Genet 111:972–979PubMedCrossRefGoogle Scholar
  50. Miklas PN, Kelly JD, Beebe SE, Blair MW (2006) Common bean breeding for resistance against biotic and abiotic stresses: from classical to MAS breeding. Euphytica 147:105–131CrossRefGoogle Scholar
  51. Nelson RT, Shoemaker R (2006) Identification and analysis of gene families from the duplicated genome of soybean using EST sequences. BMC Genomics 7:204PubMedCrossRefGoogle Scholar
  52. Nodari RO, Koinange EMK, Kelly JD, Gepts P (1992) Towards an integrated linkage map of common bean. 1. Development of genomic DNA probes and levels of restriction fragment length polymorphism. Theor Appl Genet 84:186–192CrossRefGoogle Scholar
  53. Pastor-Corrales MA, Tu JC (1989) Anthracnose. In: Schwartz HF, Pastor-Corrales MA (eds) Bean production problems in the tropics, 2nd edn. Centro Internacional de Agricultura Tropical (CIAT), Colombia, pp 77–104Google Scholar
  54. Paux E, Roger D, Badaeva E, Gay G, Bernard M, Sourdille P, Feuillet C (2006) Characterising the composition and evolution of homoeologous genomes in hexaploid wheat through BAC-end sequencing on chromosome 3B. Plant J 48:463–474PubMedCrossRefGoogle Scholar
  55. Pryor T, Ellis J (1993) The genetic complexity of fungal resistance genes in plants. Adv Plant Pathol 10:281–305Google Scholar
  56. Ron M, Avni A (2004) The receptor for the fungal elicitor ethylene-inducing xylanase is a member of a resistance-like gene family in tomato. Plant Cell 16:1604–1615PubMedCrossRefGoogle Scholar
  57. Sato S, Nakamura Y, Kaneko T, Asamizu E, Kato T, Nakao M, Sasamoto S, Watanabe A, Ono A, Kawashima K, Fujishiro T, Katoh M, Kohara M, Kishida Y, Minami C, Nakayama S, Nakazaki N, Shimizu Y, Shinpo S, Takahashi C, Wada T, Yamada M, Ohmido N, Hayashi M, Fukui K, Baba T, Nakamichi T, Mori H, Tabata S (2008) Genome structure of the legume, Lotus japonicus. DNA Res Adv. Access published online on May 28, 2008Google Scholar
  58. Scherrer B, Isidore E, Klein P, Kim JS, Bellec A, Chalhoub B, Keller B, Feuillet C (2005) Large intraspecific haplotype variability at the Rph7 locus results from rapid and recent divergence in the barley genome. Plant Cell 17:361–374PubMedCrossRefGoogle Scholar
  59. Seah S, Telleen AC, Williamson VM (2007) Introgressed and endogenous Mi-1 gene clusters in tomato differ by complex rearrangements in flanking sequences and show sequence exchange and diversifying selection among homologues. Theor Appl Genet 114:1289–1302PubMedCrossRefGoogle Scholar
  60. Simons G, Groenendijk J, Wijbrandi J, Reijans M, Groenen J, Diergaarde P, van der Lee T, Bleeker M, Onstenk J, De Both M, Haring M, Mes J, Cornelissen B, Zabeau M, Vos P (1998) Dissection of the fusarium I2 gene cluster in tomato reveals six homologs and one active gene copy. Plant Cell 10:1055–1068PubMedCrossRefGoogle Scholar
  61. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680PubMedCrossRefGoogle Scholar
  62. Vallejos CE, Sakiyama NS, Chase CD (1992) A molecular marker-based linkage map of Phaseolus vulgaris L. Genetics 131:733–740PubMedGoogle Scholar
  63. Webb CA, Richter TE, Collins NC, Nicolas M, Trick HN, Pryor T, Hulbert SH (2002) Genetic and molecular characterization of the maize rp3 rust resistance locus. Genetics 162:381–394PubMedGoogle Scholar
  64. Young ND, Cannon SB, Sato S, Kim D, Cook DR, Town CD, Roe BA, Tabata S (2005) Sequencing the genespaces of Medicago truncatula and Lotus japonicus. Plant Physiol 137:1174–1181PubMedCrossRefGoogle Scholar
  65. Young RA, Kelly JD (1997) RAPD markers linked to three major anthracnose resistance genes in common bean. Crop Sci 37:940–946Google Scholar
  66. Zhu HY, Cannon SB, Young ND, Cook DR (2002) Phylogeny and genomic organization of the TIR and non-TIR NBS–LRR resistance gene family in Medicago truncatula. Mol Plant-Microbe Interact 15:529–539PubMedCrossRefGoogle Scholar
  67. Zhu HY, Choi HK, Cook DR, Shoemaker RC (2005) Bridging model and crop legumes through comparative genomics. Plant Physiol 137:1189–1196PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Perrine David
    • 1
  • Mireille Sévignac
    • 1
  • Vincent Thareau
    • 1
  • Yann Catillon
    • 1
  • Jim Kami
    • 2
  • Paul Gepts
    • 2
  • Thierry Langin
    • 1
  • Valérie Geffroy
    • 1
  1. 1.Institut de Biotechnologie des PlantesINRA, UMR-CNRS 8618, LPPM, bât. 630, Université Paris-SudOrsayFrance
  2. 2.Department of Plant Sciences, Section of Crop and Ecosystem SciencesUniversity of CaliforniaDavisUSA

Personalised recommendations