Theoretical and Applied Genetics

, Volume 127, Issue 7, pp 1653–1666

Fine mapping of Co-x, an anthracnose resistance gene to a highly virulent strain of Colletotrichum lindemuthianum in common bean

  • Manon M. S. Richard
  • Stéphanie Pflieger
  • Mireille Sévignac
  • Vincent Thareau
  • Sophie Blanchet
  • Yupeng Li
  • Scott A. Jackson
  • Valérie Geffroy
Original Paper

Abstract

Key message

TheCo-xanthracnose R gene of common bean was fine-mapped into a 58 kb region at one end of chromosome 1, where no canonical NB-LRR-encoding genes are present in G19833 genome sequence.

Abstract

Anthracnose, caused by the phytopathogenic fungus Colletotrichum lindemuthianum, is one of the most damaging diseases of common bean, Phaseolus vulgaris. Various resistance (R) genes, named Co-, conferring race-specific resistance to different strains of C. lindemuthianum have been identified. The Andean cultivar JaloEEP558 was reported to carry Co-x on chromosome 1, conferring resistance to the highly virulent strain 100. To fine map Co-x, 181 recombinant inbred lines derived from the cross between JaloEEP558 and BAT93 were genotyped with polymerase chain reaction (PCR)-based markers developed using the genome sequence of the Andean genotype G19833. Analysis of RILs carrying key recombination events positioned Co-x at one end of chromosome 1 to a 58 kb region of the G19833 genome sequence. Annotation of this target region revealed eight genes: three phosphoinositide-specific phospholipases C (PI-PLC), one zinc finger protein and four kinases, suggesting that Co-x is not a classical nucleotide-binding leucine-rich encoding gene. In addition, we identified and characterized the seven members of common bean PI-PLC gene family distributed into two clusters located at the ends of chromosomes 1 and 8. Co-x is not a member of Co-1 allelic series since these two genes are separated by at least 190 kb. Comparative analysis between soybean and common bean revealed that the Co-x syntenic region, located at one end of Glycine max chromosome 18, carries Rhg1, a major QTL contributing to soybean cyst nematode resistance. The PCR-based markers generated in this study should be useful in marker-assisted selection for pyramiding Co-x with other R genes.

Supplementary material

122_2014_2328_MOESM1_ESM.pdf (183 kb)
Fig. S1 Fine mapping of Co-x and annotation of target region. a Physical map of Co-x region and graphical genotypes of RILs in which recombination occured between markers M5 and CV542014. Light grey and dark grey bars represent genomic regions derived from BAT93 and JaloEEP558, respectively. Phenotypes of resistance (R) and suceptibility (S) of RILs to C. lindemuthianum strain 100 are indicated below. For each RIL, a black arrow indicates the genetic interval carrying the inferred recombination breakpoint, represented by light/dark grey hatched motif. Location and name of markers are indicated on the left, in black when they are polymorphic and in grey when they are not polymorphic. b Annotation of the Co-x 58-kb target region between markers P05 and K06 in G19833. Predicted candidate genes for Co-x resistance are indicated by black or hatched arrows, for full-length and truncated genes, respectively. Loci names according to www.phytozome.net and putative gene function are indicated on the right. Location and name of markers are indicated on the right, in black when they are polymorphic and in grey when they are not polymorphic. (PDF 183 kb)
122_2014_2328_MOESM2_ESM.pdf (100 kb)
Fig. S2 Multiple sequence alignment of P. vulgaris PI-PLC gene products. The conserved PI-PLC-X, PI-PLC-Y and C2 domains are indicated below the alignment. (PDF 100 kb)
122_2014_2328_MOESM3_ESM.pptx (1.8 mb)
Fig. S3 Semi-quantitative RT-PCR analysis of the expression pattern of Co-x candidate genes during infection kinetics on JaloEEP558, at 24, 48, 72 and 96 h post infection (hpi), with an avirulent strain (strain 100) and a virulent strain (strain C531) of Colletotrichum lindemuthianum. Ubiquitine was used as an internal control to standardize cDNA input. (PPTX 1807 kb)
122_2014_2328_MOESM4_ESM.docx (17 kb)
Supplementary material 4 (DOCX 16 kb)
122_2014_2328_MOESM5_ESM.docx (31 kb)
Supplementary material 5 (DOCX 30 kb)
122_2014_2328_MOESM6_ESM.docx (15 kb)
Supplementary material 6 (DOCX 15 kb)

References

  1. Adamblondon AF, Sevignac M, Bannerot H, Dron M (1994) SCAR, RAPD and RFLP markers linked to a dominant gene (ARE) conferring resistance to anthracnose in common bean. Theor Appl Genet 88(6–7):865–870. doi:10.1007/bf01253998 CrossRefGoogle Scholar
  2. Altschul SF, Madden TL, Schaffer 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 25:3389–3402PubMedCentralPubMedCrossRefGoogle Scholar
  3. Alzate Marin AL, Baia GS, dePaula TJ, deCarvalho GA, deBarros EG, Moreira MA (1997) Inheritance of anthracnose resistance in common bean differential cultivar AB 136. Plant Dis 81(9):996–998. doi:10.1094/pdis.1997.81.9.996 CrossRefGoogle Scholar
  4. Alzate-Marin AL, de Souza KA, de Morais Silva MG, de Oliveira EJ, Moreira MA, de Barros EG (2007) Genetic characterization of anthracnose resistance genes Co-4(3) and Co-9 in common bean cultivar tlalnepantla 64 (PI 207262). Euphytica 154(1–2):1–8. doi:10.1007/s10681-006-9253-x CrossRefGoogle Scholar
  5. 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(1):5–21. doi:10.1104/pp.107.104588 PubMedCentralPubMedCrossRefGoogle Scholar
  6. Andolfo G, Sanseverino W, Rombauts S, Van de Peer Y, Bradeen JM, Carputo D, Frusciante L, Ercolano MR (2013) Overview of tomato (Solanum lycopersicum) candidate pathogen recognition genes reveals important Solanum R locus dynamics. New Phytol 197(1):223–237. doi:10.1111/j.1469-8137.2012.04380.x PubMedCrossRefGoogle Scholar
  7. Asano T, Masuda D, Yasuda M, Nakashita H, Kudo T, Kimura M, Yamaguchi K, Nishiuchi T (2008) AtNFXL1, an Arabidopsis homologue of the human transcription factor NF-X1, functions as a negative regulator of the trichothecene phytotoxin-induced defense response. Plant J 53(3):450–464. doi:10.1111/j.1365-313X.2007.03353.x PubMedCrossRefGoogle Scholar
  8. Bai JF, Pennill LA, Ning JC, Lee SW, Ramalingam J, Webb CA, Zhao BY, Sun Q, Nelson JC, Leach JE, Hulbert SH (2002) Diversity in nucleotide binding site-leucine-rich repeat genes in cereals. Genom Res 12(12):1871–1884CrossRefGoogle Scholar
  9. 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
  10. Barrus MF (1911) Variation of varieties of beans in their susceptibility to anthracnose. Phytopathology 1:190–195Google Scholar
  11. Barrus MF (1915) An anthracnose-resistant red kidney bean. Phytopathology 5:303–311Google Scholar
  12. Berridge MJ, Irvine RF (1989) Inositol phosphates and cell signalling. Nature 341(6239):197–205. doi:10.1038/341197a0 PubMedCrossRefGoogle Scholar
  13. Broughton WJ, Hernandez G, Blair M, Beebe S, Gepts P, Vanderleyden J (2003) Beans (Phaseolus spp.)––model food legumes. Plant Soil 252(1):55–128CrossRefGoogle Scholar
  14. Burset M, Guigo R (1996) Evaluation of gene structure prediction programs. Genomics 34(3):353–367PubMedCrossRefGoogle Scholar
  15. Buschges R, Hollricher K, Panstruga R, Simons G, Wolter M, Frijters A, vanDaelen R, vanderLee T, Diergaarde P, Groenendijk J, Topsch S, Vos P, Salamini F, Schulze-Lefert P (1997) The barley mlo gene: a novel control element of plant pathogen resistance. Cell 88(5):695–705. doi:10.1016/s0092-8674(00)81912-1 PubMedCrossRefGoogle Scholar
  16. Campa A, Giraldez R, Ferreira JJ (2009) Genetic dissection of the resistance to nine anthracnose races in the common bean differential cultivars MDRK and TU. Theor Appl Genet 119(1):1–11. doi:10.1007/s00122-009-1011-8 PubMedCrossRefGoogle Scholar
  17. Chen NWG, Sevignac M, Thareau V, Magdelenat G, David P, Ashfield T, Innes RW, Geffroy V (2010) Specific resistances against Pseudomonas syringae effectors AvrB and AvrRpm1 have evolved differently in common bean (Phaseolus vulgaris), soybean (Glycine max), and Arabidopsis thaliana. New Phytol 187(4):941–956. doi:10.1111/j.1469-8137.2010.03337.x PubMedCentralPubMedCrossRefGoogle Scholar
  18. Chisholm ST, Coaker G, Day B, Staskawicz BJ (2006) Host-microbe interactions: shaping the evolution of the plant immune response. Cell 124(4):803–814PubMedCrossRefGoogle Scholar
  19. Chou WM, Shigaki T, Dammann C, Liu YQ, Bhattacharyya MK (2004) Inhibition of phosphoinositide-specific phospholipase C results in the induction of pathogenesis-related genes in soybean. Plant Biol 6(6):664–672. doi:10.1055/s-2004-830351 PubMedCrossRefGoogle Scholar
  20. Cook DE, Lee TG, Guo XL, Melito S, Wang K, Bayless AM, Wang JP, Hughes TJ, Willis DK, Clemente TE, Diers BW, Jiang JM, Hudson ME, Bent AF (2012) Copy number variation of multiple genes at Rhg1 mediates nematode resistance in soybean. Science 338(6111):1206–1209. doi:10.1126/science.1228746 PubMedCrossRefGoogle Scholar
  21. Creusot F, Macadre C, Cana EF, Riou C, Geffroy V, Sevignac M, Dron M, Langin T (1999) Cloning 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(2):254–264. doi:10.1139/gen-42-2-254 PubMedCrossRefGoogle Scholar
  22. Dangl JL, Jones JDG (2001) Plant pathogens and integrated defence responses to infection. Nature 411(6839):826–833PubMedCrossRefGoogle Scholar
  23. Dangl JL, Horvath DM, Staskawicz BJ (2013) Pivoting the plant immune system from dissection to deployment. Science 341(6147):746–751. doi:10.1126/science.1236011 PubMedCrossRefGoogle Scholar
  24. David P, Sevignac M, Thareau V, Catillon Y, Kami J, Gepts P, Langin T, Geffroy V (2008) BAC end sequences corresponding to the B4 resistance gene cluster in common bean: a resource for markers and synteny analyses. Mol Genet Genom 280(6):521–533. doi:10.1007/s00438-008-0384-8 CrossRefGoogle Scholar
  25. David P, Chen NWG, Pedrosa-Harand A, Thareau V, Sevignac M, Cannon SB, Debouck D, Langin T, Geffroy V (2009) A nomadic subtelomeric disease resistance gene cluster in common bean. Plant Physiol 151(3):1048–1065. doi:10.1104/pp.109.142109 PubMedCentralPubMedCrossRefGoogle Scholar
  26. David P, des Francs-Small CC, Sevignac M, Thareau V, Macadre C, Langin T, Geffroy V (2010) Three highly similar formate dehydrogenase genes located in the vicinity of the B4 resistance gene cluster are differentially expressed under biotic and abiotic stresses in Phaseolus vulgaris. Theor Appl Genet 121(1):87–103. doi:10.1007/s00122-010-1293-x PubMedCrossRefGoogle Scholar
  27. Devoto A, Piffanelli P, Nilsson I, Wallin E, Panstruga R, von Heijne G, Schulze-Lefert P (1999) Topology, subcellular localization, and sequence diversity of the Mlo family in plants. J Biol Chem 274(49):34993–35004. doi:10.1074/jbc.274.49.34993 PubMedCrossRefGoogle Scholar
  28. Devoto A, Hartmann HA, Piffanelli P, Elliott C, Simmons C, Taramino G, Goh CS, Cohen FE, Emerson BC, Schulze-Lefert P, Panstruga R (2003) Molecular phylogeny and evolution of the plant-specific seven-transmembrane MLO family. J Mol Evol 56(1):77–88. doi:10.1007/s00239-002-2282-5 PubMedCrossRefGoogle Scholar
  29. Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15Google Scholar
  30. Edgar RC (2004a) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinform 5:1–19. doi:10.1186/1471-2105-5-113 CrossRefGoogle Scholar
  31. Edgar RC (2004b) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32(5):1792–1797. doi:10.1093/nar/gkh340 PubMedCentralPubMedCrossRefGoogle Scholar
  32. 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(2):251–261PubMedGoogle Scholar
  33. 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(5):895–905PubMedCrossRefGoogle Scholar
  34. Fisher RA (1937) The design of experiments. Edinburgh, LondonGoogle Scholar
  35. 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
  36. Freyre R, Skroch PW, 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(5–6):847–856. doi:10.1007/s001220050964 CrossRefGoogle Scholar
  37. Fu DL, Uauy C, Distelfeld A, Blechl A, Epstein L, Chen XM, Sela HA, Fahima T, Dubcovsky J (2009) A Kinase-START gene confers temperature-dependent resistance to wheat stripe rust. Science 323(5919):1357–1360. doi:10.1126/science.1166289 PubMedCrossRefGoogle Scholar
  38. Geffroy V, Creusot F, Falquet J, Sévignac 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 96:494–502PubMedCrossRefGoogle Scholar
  39. 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(9):774–784PubMedCrossRefGoogle Scholar
  40. 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(3):287–296. doi:10.1094/mpmi.2000.13.3.287 PubMedCrossRefGoogle Scholar
  41. 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(3):407–415. doi:10.1007/s00122-007-0678-y PubMedCrossRefGoogle Scholar
  42. Geffroy V, Macadre C, David P, Pedrosa-Harand A, Sevignac M, Dauga C, Langin T (2009) Molecular analysis of a large subtelomeric nucleotide-binding-site-leucine-rich-repeat family in two representative genotypes of the major gene pools of Phaseolus vulgaris. Genetics 181(2):405–419. doi:10.1534/genetics.108.093583 PubMedCentralPubMedCrossRefGoogle Scholar
  43. Goncalves-Vidigal MC, Kelly JD (2006) Inheritance of anthracnose resistance in the common bean cultivar Widusa. Euphytica 151(3):411–419. doi:10.1007/s10681-006-9164-x CrossRefGoogle Scholar
  44. Goncalves-Vidigal MC, Cruz AS, Garcia A, Kami J, Vidigal PS, Sousa LL, McClean P, Gepts P, Pastor-Corrales MA (2011) Linkage mapping of the Phg-1 and Co-1 (4) genes for resistance to angular leaf spot and anthracnose in the common bean cultivar AND 277. Theor Appl Genet 122(5):893–903. doi:10.1007/s00122-010-1496-1 PubMedCentralPubMedCrossRefGoogle Scholar
  45. Goodstein DM, Shu S, Howson R, Neupane R, Hayes RD, Fazo J, Mitros T, Dirks W, Hellsten U, Putnam N, Rokhsar DS (2012) Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res 40(D1):D1178–D1186. doi:10.1093/nar/gkr944 PubMedCentralPubMedCrossRefGoogle Scholar
  46. Gore MA, Chia J-M, Elshire RJ, Sun Q, Ersoz ES, Hurwitz BL, Peiffer JA, McMullen MD, Grills GS, Ross-Ibarra J, Ware DH, Buckler ES (2009) A first-generation haplotype map of maize. Science 326(5956):1115–1117. doi:10.1126/science.1177837 PubMedCrossRefGoogle Scholar
  47. Hammond-Kosack KE, Jones JDG (1997) Plant disease resistance genes. Ann Rev Plant Physiol Plant Mol Biol 48:575–607CrossRefGoogle Scholar
  48. Innes RW, Ameline-Torregrosa C, Ashfield T, Cannon E, Cannon SB, Chacko B, Chen NWG, Couloux A, Dalwani A, Denny R, Deshpande S, Egan AN, Glover N, Hans CS, Howell S, Ilut D, Jackson S, Lai H, Mammadov J, del Campo SM, Metcalf M, Nguyen A, O’Bleness M, Pfeil BE, Podicheti R, Ratnaparkhe MB, Samain S, Sanders I, Segurens B, Sevignac M, Sherman-Broyles S, Thareau V, Tucker DM, Walling J, Wawrzynski A, Yi J, Doyle JJ, Geffroy V, Roe BA, Maroof MAS, Young ND (2008) Differential accumulation of retroelements and diversification of NB-LRR disease resistance genes in duplicated regions following polyploidy in the ancestor of soybean. Plant Physiol 148(4):1740–1759. doi:10.1104/pp.108.127902 PubMedCentralPubMedCrossRefGoogle Scholar
  49. Jung GW, Coyne DP, Bokosi J, Steadman JR, Nienhuis J (1998) Mapping genes for specific and adult plant resistance to rust and abaxial leaf pubescence and their genetic relationships using randomly amplified polymorphic DNA (RAPD) markers in common bean. J Am Soc Hortic Sci 123(5):859–863Google Scholar
  50. Jupe F, Pritchard L, Etherington GJ, MacKenzie K, Cock PJA, Wright F, Sharma SK, Bolser D, Bryan GJ, Jones JDG, Hein I (2012) Identification and localisation of the NB-LRR gene family within the potato genome. BMC Genom 13:75. doi:10.1186/1471-2164-13-75 CrossRefGoogle Scholar
  51. Kim YJ, Kim JE, Lee JH, Lee MH, Jung HW, Bahk YY, Hwang BK, Hwang I, Kim WT (2004) The Vr-PLC3 gene encodes a putative plasma membrane-localized phosphoinositide-specific phospholipase C whose expression is induced by abiotic stress in mung bean (Vigna radiata L.). FEBS Lett 556(1–3):127–136. doi:10.1016/s0014-5793(03)01388-7 PubMedCrossRefGoogle Scholar
  52. Kim M, Hyten DL, Bent AF, Diers BW (2010) Fine mapping of the SCN resistance locus rhg1-b from PI 88788. Plant Genom 3(2):81–89. doi:10.3835/plantgenome2010.02.0001 CrossRefGoogle Scholar
  53. Kocourkova D, Krckova Z, Pejchar P, Veselkova S, Valentova O, Wimalasekera R, Scherer GFE, Martinec J (2011) The phosphatidylcholine-hydrolysing phospholipase C NPC4 plays a role in response of Arabidopsis roots to salt stress. J Exp Bot 62(11):3753–3763. doi:10.1093/jxb/err039 PubMedCentralPubMedCrossRefGoogle Scholar
  54. Kosambi DD (1944) The estimation of map distances from recombination values. Ann Eugen 12:172–175CrossRefGoogle Scholar
  55. Krattinger SG, Lagudah ES, Spielmeyer W, Singh RP, Huerta-Espino J, McFadden H, Bossolini E, Selter LL, Keller B (2009) A putative ABC transporter confers durable resistance to multiple fungal pathogens in wheat. Science 323(5919):1360–1363. doi:10.1126/science.1166453 PubMedCrossRefGoogle Scholar
  56. Lander ES, Green P, Abrahamson J, B 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
  57. Larkindale J, Vierling E (2008) Core genome responses involved in acclimation to high temperature. Plant Physiol 146(2):748–761. doi:10.1104/pp.107.112060 PubMedCentralPubMedCrossRefGoogle Scholar
  58. Lisso J, Altmann T, Muessig C (2006) The AtNFXL1 gene encodes a NF-X1 type zinc finger protein required for growth under salt stress. FEBS Lett 580(20):4851–4856. doi:10.1016/j.febslet.2006.07.079 PubMedCrossRefGoogle Scholar
  59. Lukashin AV, Borodovsky M (1998) GeneMark.hmm: new solutions for gene finding. Nucleic Acids Res 26(4):1107–1115. doi:10.1093/nar/26.4.1107 PubMedCentralPubMedCrossRefGoogle Scholar
  60. Martin GB, Brommonschenkel SH, Chunwongse J, Frary A, Ganal MW, Spivey R, Wu TY, Earle ED, Tanksley SD (1993) Map-based cloning of a protein kinase gene conferring disease resistance in tomato. Science 262(5138):1432–1436PubMedCrossRefGoogle Scholar
  61. Mastenbroek C (1960) A breeding programs for resistance to anthracnose in dry shell haricot beans, based on a new gene. Euphytica 9:177–184CrossRefGoogle Scholar
  62. McClean PE, Mamidi S, McConnell M, Chikara S, Lee R (2010) Synteny mapping between common bean and soybean reveals extensive blocks of shared loci. BMC Genom 11:184. doi:10.1186/1471-2164-11-184 CrossRefGoogle Scholar
  63. McDowell JM, Simon SA (2008) Molecular diversity at the plant-pathogen interface. Dev Comp Immunol 32(7):736–744. doi:10.1016/j.dci.2007.11.005 PubMedCrossRefGoogle Scholar
  64. McHale L, Tan XP, Koehl P, Michelmore RW (2006) Plant NBS-LRR proteins: adaptable guards. Genom Biol 7(4):11. doi:10.1186/gb-2006-7-4-212 CrossRefGoogle Scholar
  65. McRostie GP (1919) Inheritance of anthracnose resistance as indicated by a cross between a resistant and a susceptible bean. Phytopathology 9:141–148Google Scholar
  66. Melotto M, Kelly JD (2000) An allelic series at the Co-1 locus conditioning resistance to anthracnose in common bean of Andean origin. Euphytica 116(2):143–149. doi:10.1023/a:1004005001049 CrossRefGoogle Scholar
  67. 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(3):237–245CrossRefGoogle Scholar
  68. 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(3):317–332. doi:10.1046/j.1365-313X.1999.00606.x PubMedCrossRefGoogle Scholar
  69. Meyers BC, Kozik A, Griego A, Kuang HH, Michelmore RW (2003) Genome-wide analysis of NBS-LRR-encoding genes in Arabidopsis. Plant Cell 15(4):809–834PubMedCentralPubMedCrossRefGoogle Scholar
  70. Michelmore RW, Christopoulou M, Caldwell KS (2013) Impacts of resistance gene genetics, function, and evolution on a durable future. In: VanAlfen NK (ed) Annual review of phytopathology, vol 51. Annual Reviews, Palo Alto, pp 291–319. doi:10.1146/annurev-phyto-082712-102334 Google Scholar
  71. 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(1–2):105–131CrossRefGoogle Scholar
  72. Mucyn TS, Clemente A, Andriotis VME, Balmuth AL, Oldroyd GED, Staskawicz BJ, Rathjen JP (2006) The tomato NBARC-LRR protein Prf interacts with Pto kinase in vivo to regulate specific plant immunity. Plant Cell 18(10):2792–2806. doi:10.1105/tpc.106.044016 PubMedCentralPubMedCrossRefGoogle Scholar
  73. Mucyn TS, Wu AJ, Balmuth AL, Arasteh JM, Rathjen JP (2009) Regulation of tomato Prf by Pto-like protein kinases. Mol Plant-Microbe Interact 22(4):391–401. doi:10.1094/mpmi-22-4-0391 PubMedCrossRefGoogle Scholar
  74. Mudge J, Cannon SB, Kalo P, Oldroyd GE, Roe BA, Town CD, Young ND (2005) Highly syntenic regions in the genomes of soybean, Medicago truncatula, and Arabidopsis thaliana. BMC Plant Biol 5:15. doi:10.1186/1471-2229-5-15 PubMedCentralPubMedCrossRefGoogle Scholar
  75. Oh CS, Martin GB (2011) Effector-triggered immunity mediated by the Pto kinase. Trends Plant Sci 16(3):132–140. doi:10.1016/j.tplants.2010.11.001 PubMedCrossRefGoogle Scholar
  76. Pan QL, Liu YS, 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(1):309–322PubMedCentralPubMedGoogle Scholar
  77. Park SO, Coyne DP, Bokosi JM, Steadman JR (1999) Molecular markers linked to genes for specific rust resistance and indeterminate growth habit in common bean. Euphytica 105(2):133–141. doi:10.1023/a:1003477714349 CrossRefGoogle Scholar
  78. 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
  79. Pastor-Corrales MA, Erazo OA, Estrada EI, Singh SP (1994) Inheritance of anthracnose resistance in common bean accessions G2333. Plant Dis 78:959–962CrossRefGoogle Scholar
  80. Pedley KF, Martin GB (2003) Molecular basis of Pto-mediated resistance to bacterial speck disease in tomato. Annu Rev Phytopathol 41:215–243PubMedCrossRefGoogle Scholar
  81. Pflieger S, Richard MMS, Blanchet S, Meziadi C, Geffroy V (2013) VIGS technology: an attractive tool for functional genomics studies in legumes. Funct Plant Biol 40 (12):1234–1248. doi:http://dx.doi.org/10.1071/FP13089
  82. Ramirez M, Graham MA, Blanco-Lopez L, Silvente S, Medrano-Soto A, Blair MW, Hernandez G, Vance CP, Lara M (2005) Sequencing and analysis of common bean ESTs. Building a foundation for functional genomics. Plant Physiol 137(4):1211–1227PubMedCentralPubMedCrossRefGoogle Scholar
  83. Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol (Clifton, NJ) 132:365–386Google Scholar
  84. Ruben E, Jamai A, Afzal J, Njiti VN, Triwitayakorn K, Iqbal MJ, Yaegashi S, Bashir R, Kazi S, Arelli P, Town CD, Ishihara H, Meksem K, Lightfoot DA (2006) Genomic analysis of the rhg1 locus: candidate genes that underlie soybean resistance to the cyst nematode. Mol Genet Genom 276(6):503–516. doi:10.1007/s00438-006-0150-8 CrossRefGoogle Scholar
  85. Rutherford K, Parkhill J, Crook J, Horsnell T, Rice P, Rajandream MA, Barrell B (2000) Artemis: sequence visualization and annotation. Bioinformatics 16(10):944–945PubMedCrossRefGoogle Scholar
  86. Schlueter JA, Goicoechea JL, Collura K, Gill N, Lin J-Y, Yu Y, Kudrna D, Zuccolo A, Vallejos CE, Munoz-Torres M, Blair MW, Tohme J, Tomkins J, McClean P, Wing RA, Jackson SA (2008) BAC-end sequence analysis and a draft physical map of the common bean (Phaseolus vulgaris L.) genome. Trop Plant Biol 1:40–48CrossRefGoogle Scholar
  87. Schmutz J, Cannon SB, Schlueter J, Ma JX, Mitros T, Nelson W, Hyten DL, Song QJ, Thelen JJ, Cheng JL, Xu D, Hellsten U, May GD, Yu Y, Sakurai T, Umezawa T, Bhattacharyya MK, Sandhu D, Valliyodan B, Lindquist E, Peto M, Grant D, Shu SQ, Goodstein D, Barry K, Futrell-Griggs M, Abernathy B, Du JC, Tian ZX, Zhu LC, Gill N, Joshi T, Libault M, Sethuraman A, Zhang XC, Shinozaki K, Nguyen HT, Wing RA, Cregan P, Specht J, Grimwood J, Rokhsar D, Stacey G, Shoemaker RC, Jackson SA (2010) Genome sequence of the palaeopolyploid soybean. Nature 463(7278):178–183. doi:10.1038/nature08670 PubMedCrossRefGoogle Scholar
  88. Schmutz J, McClean P, Mamidi S, Wu AJ, Cannon SB, Grimwood J, Jenkins J, Shu SQ, Song QJ, Chavarro C, Torres-Torres M, Geffroy V, Moghaddam SM, Gao D, Abernathy B, Barry K, Blair M, Brick MA, Chovatia M, Gepts P, Goodstein DM, Gonzales M, Hellsten U, Hyten DL, Jia GF, Kelly JD, Kudrna D, Lee R, Richard MMS, Miklas PN, Osorno JM, Rodrigues J, Thareau V, Urrea CA, Wang M, Yu Y, Wing RA, Cregan PB, Rokhsar D, Jackson SA (2014) A reference genome for common bean and genome-wide analysis of dual domestications. Nat Genet (in press)Google Scholar
  89. Soderlund C, Bomhoff M, Nelson WM (2011) SyMAP v3.4: a turnkey synteny system with application to plant genomes. Nucleic Acids Res 39(10):e68. doi:10.1093/nar/gkr123 PubMedCentralPubMedCrossRefGoogle Scholar
  90. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28(10):2731–2739. doi:10.1093/molbev/msr121 PubMedCentralPubMedCrossRefGoogle Scholar
  91. Tasma IM, Brendel V, Whitham SA, Bhattacharyya MK (2008) Expression and evolution of the phosphoinositide-specific phospholipase C gene family in Arabidopsis thaliana. Plant Physiol Biochem 46(7):627–637. doi:10.1016/j.plaphy.2008.04.015 PubMedCrossRefGoogle Scholar
  92. Thareau V, Dehais P, Serizet C, Hilson P, Rouze P, Aubourg S (2003) Automatic design of gene-specific sequence tags for genome-wide functional studies. Bioinformatics 19(17):2191–2198. doi:10.1093/bioinformatics/btg286 PubMedCrossRefGoogle Scholar
  93. Vallejo V, Kelly JD (2009) New insights into the anthracnose resistance of common bean landrace G 2333. Open Hortic J 2(1):29–33. doi:10.2174/1874840600902010029 CrossRefGoogle Scholar
  94. Vallejos CE, Astua-Monge G, Jones V, Plyler TR, Sakiyama NS, Mackenzie SA (2006) Genetic and molecular characterization of the I locus of Phaseolus vulgaris. Genetics 172(2):1229–1242. doi:10.1534/genetics.105.050S15 PubMedCentralPubMedCrossRefGoogle Scholar
  95. Vossen JH, Abd-El-Haliem A, Fradin EF, van den Berg GCM, Ekengren SK, Meijer HJG, Seifi A, Bai YL, ten Have A, Munnik T, Thomma B, Joosten M (2010) Identification of tomato phosphatidylinositol-specific phospholipase-C (PI-PLC) family members and the role of PLC4 and PLC6 in HR and disease resistance. Plant J 62(2):224–239. doi:10.1111/j.1365-313X.2010.04136.x PubMedCrossRefGoogle Scholar
  96. Xiao SY, Ellwood S, Calis O, Patrick E, Li TX, Coleman M, Turner JG (2001) Broad-spectrum mildew resistance in Arabidopsis thaliana mediated by RPW8. Science 291(5501):118–120. doi:10.1126/science.291.5501.118 PubMedCrossRefGoogle Scholar
  97. Young RA, Kelly JD (1996) Characterization of the genetic resistance to Colletotrichum lindemuthianum in common bean differential cultivars. Plant Dis 80(6):650–654CrossRefGoogle Scholar
  98. Zhang CQ, Bradshaw JD, Whitham SA, Hill JH (2010) The development of an efficient multipurpose bean pod mottle virus viral vector set for foreign gene expression and RNA silencing. Plant Physiol 153(1):52–65. doi:10.1104/pp.109.151639 PubMedCentralPubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Manon M. S. Richard
    • 1
  • Stéphanie Pflieger
    • 1
    • 2
  • Mireille Sévignac
    • 1
  • Vincent Thareau
    • 1
  • Sophie Blanchet
    • 1
  • Yupeng Li
    • 3
  • Scott A. Jackson
    • 3
  • Valérie Geffroy
    • 1
    • 4
  1. 1.CNRS, Institut de Biologie des Plantes, UMR 8618Université Paris Sud, Saclay Plant Sciences (SPS)OrsayFrance
  2. 2.Univ Paris Diderot, Sorbonne Paris CitéParisFrance
  3. 3.Center for Applied Genetic Technologies and Institute for Plant Breeding Genetics, and GenomicsUniversity of GeorgiaAthensUSA
  4. 4.INRA, Unité Mixte de Recherche de Génétique Végétale, IDEEV FR3284Université Paris SudGif-sur-YvetteFrance

Personalised recommendations