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Common Bean Genomes: Mining New Knowledge of a Major Societal Crop

  • Phillip E. McCleanEmail author
  • Bodo Raatz
Chapter
Part of the Compendium of Plant Genomes book series (CPG)

Abstract

Common bean, Phaseolus vulgaris L., is the most consumed grain legume in the world. The continued improvement of this crop is necessary as it has historically been pushed to more marginal lands as other crops displace it. Genomic technologies are providing valuable information aid this process. This includes a reference and draft genome of representatives of the Andean and Mesoamerican gene pools, respectively. Early applications such as new marker development, marker development, transcriptomics, and comparative genomics. Future applications such as the need for a denser gene chip for fine-mapping are highlighted.

Keywords

Common bean Phaseolus vulgaris L. Genomics Sequencing Marker-assisted selection 

References

  1. Ariani A, Teran JCBM, Gepts P (2016) Genome-wide identification of SNPs and copy number variation in common bean (Phaseolus vulgaris L.) using genotyping-by-sequencing (GBS). Mol Breeding 36:87Google Scholar
  2. Bello MH, Moghaddam SM, Massoudi M, McClean PE, Cregan PB, Miklas PN (2014) Application of in silico bulked segregant analysis for rapid development of markers linked to bean common mosaic virus resistance in common bean. BMC Genom 15:903CrossRefGoogle Scholar
  3. Beebe S, Skroch PW, Tohme J, Duque MC, Pedraza F, Nienhuis J (2000) Structure of genetic diversity among common bean landraces of Middle American origin based on correspondence analysis of RAPD. Crop Sci 40:264–273CrossRefGoogle Scholar
  4. Beebe S, Ramírez J, Jarvis A, Rao IM, Mosquera G, Bueno JM, Blair MW (2011) Genetic improvement of common beans and the challenges of climate change. In: Yadav SS, Redden R, Hatfield JL, Lotze-Campen H, Hall A (eds) Crop adaptation to climate change. Wiley-Blackwell, Oxford, UK, pp 356–369CrossRefGoogle Scholar
  5. Berdegué JA, Fuentealba R 2011. Latin America: the state of smallholders in agriculture. A paper presented at the IFAD conference on new directions for smallholder agriculture 24–25 Jan, 2011, Rome: IFADGoogle Scholar
  6. Bitocchi E, Nanni L, Bellucci E, Rossi M, Giardini A, Zeuli PS, Logozzo G, Stougaard J, McClean PE, Attene G, Papa R (2012) Mesoamerican origin of the common bean (Phaseolus vulgaris L.) is revealed by sequence data. Proc Natl Acad Sci USA 109:E788–E796CrossRefPubMedPubMedCentralGoogle Scholar
  7. Blair MW, Pedraza F, Buendia HF, Gaitán-Solís E, Beebe SE, Gepts P, Tohme J (2003) Development of a genome-wide anchored microsatellite map for common bean (Phaseolus vulgaris L.). Theor Appl Genet 107:1362–1374CrossRefPubMedGoogle Scholar
  8. Brisco EI, Porch TG, Cregan PB, Kelly JD (2014) Quantitative trait loci associated with resistance to Empoasca in common bean. Crop Sci 54:2509–2519CrossRefGoogle Scholar
  9. Butare L, Rao I, Lepoivre P, Cajiao C, Polania J et al (2011) Phenotypic evaluation of interspecific recombinant inbred lines (RILs) of Phaseolus species for aluminium resistance and shoot and root growth response to aluminium-toxic acid soil. Euphytica 186:715–730CrossRefGoogle Scholar
  10. Cichy KA, Porch TG, Beaver JS, Cregan P, Fourie D, Glahn RP, Grusak MA, Kamfwa K, Katuuramu DN, McClean P, Mndolwa E, Nchimbi-Msolla S, Pastor-Corrales MA, Miklas PN (2015) A diversity panel for Andean bean improvement. Crop Sci 55:2149–2160CrossRefGoogle Scholar
  11. Cook OF (1919) Milpa agriculture, a primitive tropical system. Annual Report of the Board of Regents of the Smithsonian Institute pp 307–326. Government Printing Office, Washington, D.C.Google Scholar
  12. Córdoba JM, Chavarro C, Schlueter JA, Jackson SA, Blair MW (2010) Integration of physical and genetic maps of common bean through BAC-derived microsatellite markers. BMC Genom 11:436CrossRefGoogle Scholar
  13. Debouck DG, Toro O, Paredes OM, Johnson WC, Gepts P (1993) Genetic diversity and ecological distribution of Phaseolus vulgaris (Fabaceae) in northwestern South America. Econ Bot 47:408–423CrossRefGoogle Scholar
  14. Drijfhout E (1978) Genetic interaction between Phaseolus vulgaris and bean common mosaic virus with implications for strain identification and breeding for resistance. Verslagen van Landbouwkundige Onderzoekingen No. 872:1–89Google Scholar
  15. Ferreira JJ, Murube E, Campa A (2016) Introgressed genomic regions in a set of near-isogenic lines of common bean revealed by genotyping-by-sequencing. Plant Genome 9. doi: 10.3835/plantgenome2016.08.0081
  16. Fournier-Level A, Korte A, Cooper MD, Nordborg M, Schmitt J, Wilczek AM (2011) A map of local adaptation in Arabidopsis thaliana. Science 334:86–89CrossRefPubMedGoogle Scholar
  17. Freyre R, Skroch PW, Geffroy V, Adam-Blondon AF, Shirmohamadali A, Johnson WC, Llaca V, Nodari RO, Pereira PA, Tsai S-M, 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
  18. Gaut BS (2015) Evolution is an experiment: assessing parallelism in crop domestication and experimental evolution (Nei Lecture, SMBE 2014, Puerto Rico). Mol Biol Evol 32:1661–1671CrossRefPubMedGoogle Scholar
  19. Geraldes A, Difazio SP, Slavov GT, Ranjan P, Muchero W, Hannemann J, Gunter LE, Wymore AM, Grassa CUJ, Farzaneh N, Porth I, McKown AD, Skyba O, Li E, Fujita M, Klapste J, Martin J, Schackwitz W, Pennacchio C, Rokshar D, Friedmann MC, Wasteneys GO, Guy RD, El-Kassaby YA, Mansfield SD, Cronk QCB, Ehlting J, Douglas CJ, Tuskan GA (2013) A 34K SNP genotyping array for Populus trichocarpa: design, application to the study of natural populations and transferability to other Populus species. Mol Ecol Resour 13:306–323CrossRefPubMedGoogle Scholar
  20. Gourdji S, Läderach P, Valle AM, Martinez CZ, Lobell DB (2015) Historical climate trends, deforestation, and maize and bean yields in Nicaragua. Agric Forest Meteorol 200:270–281CrossRefGoogle Scholar
  21. Graham RD, Welch RW, Saunders DA, Ortiz-Monasterio I, Bouis HE, Bonierbale M, de Haan S, Bugos G, Thiele G, Liria R, Meisner AA, Beebe SE, Potts MJ, Kadian M, Hobbs PR, Gupta RK, Twomlow S (2007) Nutritious subsistence food systems. Adv Agron 92:1–74CrossRefGoogle Scholar
  22. Grisi MCM, Blair MW, Gepts P, Brondani C, Pereira PAA, Brondani RPV (2007) Genetic mapping of a new set of microsatellite markers in a reference common bean (Phaseolus vulgaris) population BAT93 × Jalo EEP558. Genet Mol Res 6:691–706PubMedGoogle Scholar
  23. Hagerty CH, Cuesta-Marcos A, Cregan P, Song Q, McClean P, Myers JR (2016) Mapping snap bean pod and color traits, in a dry bean × snap bean recombinant inbred population. J Am Soc Hort Sci 141:131–138Google Scholar
  24. Hagerty CH, Cuesta-Marcos A, Cregan PB, Song Q, McClean P, Noffsinger S, Myers JR (2015) Mapping and root rot resistance and root architecture quantitative trait loci in common bean. Crop Sci 55:1969–1977CrossRefGoogle Scholar
  25. Hancock AM, Brachi B, Faure N, Horton MW, Jarymowycz LB, Sperone FG, Toomajian C, RouxF Bergelson J (2011) Adaptation to climate across the Arabidopsis thaliana genome. Science 334:83–86CrossRefPubMedGoogle Scholar
  26. Heilig JA, Beaver JS, Wright EM, Song Q, Kelly JD (2016) QTL analysis of symbiotic nitrogen fixation in a black bean population. Crop Sci. doi: 10.2135/cropsci2016.05.0348 Google Scholar
  27. Hyten DL, Song Q, Fickus EW, Quigley CV, Lim JS, Choi IY, Hwang EY, Pastor-Corrales M, Cregan PB (2010) High-throughput SNP discovery and assay development in common bean. BMC Genom 11:475CrossRefGoogle Scholar
  28. Jiao Y, Wickett NJ, Ayyampalayam S, Chanderbali AS, Landherr L, Ralph PE, Tomsho PP, Hu Y, Liang H, Soltis PS, Soltis DE, Clkifton SW, Schlarbaum SE, Schuster SC, Ma H, Leebens-Mack J, de Pamphilis CW (2011) Ancestral polyploidy in seed plants and angiosperms. Nature 473:97–100CrossRefPubMedGoogle Scholar
  29. 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 112:987–998CrossRefPubMedGoogle Scholar
  30. Kami J, Velásquez VB, Debouck DG, Gepts P (1995) Identification of presumed ancestral DNA sequences of phaseolin in Phaseolus vulgaris. Proc Natl Acad Sci USA 92:1101–1104CrossRefPubMedPubMedCentralGoogle Scholar
  31. Kang YJ, Kim KH, Shim S, Yoon MY, Sun S, Kim MY et al (2012) Genome-wide mapping of NBS-LRR genes and their association with disease resistance in soybean. BMC Plant Biol 12:139CrossRefPubMedPubMedCentralGoogle Scholar
  32. Karaki L, Da Silva P, Rizk F, Chouabe C, Chantret N, Eyraud V, Gressent F, Sivignon C, Rahioui I, Kahn D, Brochier-Armanet CB, Rahbe Yl, Royer C (2016) Genome-wide analysis identifies gain and loss/change of function within the small multigenic insecticidal Albumin 1 family of Medicago truncatula. BMC Plant Biol 16:63Google Scholar
  33. Katungi E, Farrow A, Chianu J, Sperling L, Beebe S (2009) Common bean in Eastern and Southern Africa: a situation and outlook analysis. International Centre for Tropical Agriculture, Cali, ColombiaGoogle Scholar
  34. Katungi E, Sperling L, Karanja D, Farrow A, Beebe S (2011) Relative importance of common bean attributes and variety demand in the drought areas of Kenya. J Develop Agric Econ 3:411–422Google Scholar
  35. Kawecki TJ, Ebert D (2004) Conceptual issues in local adaptation. Ecol Lett 7:1225–1241CrossRefGoogle Scholar
  36. Keller B, Manzanares C, Jara C, Lobaton JD, Studer B, Raatz B (2015) Fine-mapping of a major QTL controlling angular leaf spot resistance in common bean (Phaseolus vulgaris L.). Theor Appl Genet 128:813–826CrossRefPubMedPubMedCentralGoogle Scholar
  37. Kelly JD, Gepts P, Miklas PN, Coyne DP (2003) Tagging and mapping of genes and QTL and molecular marker-assisted selection for traits of economic importance in bean and cowpea. Field Crops Res 82:135–154CrossRefGoogle Scholar
  38. Lavin M, Herendeen PS, Wojciechowski MF (2005) Evolutionary rates analysis of Leguminosae implicates a rapid diversification of lineages during the Tertiary. Syst Biol 54:575–594CrossRefPubMedGoogle Scholar
  39. Le B, Nawaz MA, Rehman HM, Le T, Yang SH, Golokhvast KS, Son E, Chung G (2016) Genome-wide characterization and expression pattern of auxin response factor (ARF) gene family in soybean and common bean. Genes Genom 38:1165–1178CrossRefGoogle Scholar
  40. Mamidi S, Miklas PN, Trapp J, Felicetti E, Grimwood J, Schmutz J, Lee R, McClean PE (2016) Sequence-based introgression mapping identifies candidate white mold tolerance genes in common bean. Plant Genome 9. doi: 10.3835/plantgenome2015.09.0092
  41. Mamidi S, Rossi M, Annam D, Moghaddam S, Lee R, Papa R, McClean P (2011) Investigation of the domestication of common bean (Phaseolus vulgaris) using multilocus sequence data. Funct Plant Biol 38:953–967CrossRefGoogle Scholar
  42. Mamidi S, Rossi M, Moghaddam SM, Annam D, Lee R, Papa R, McClean PE (2013) Demographic factors shaped diversity in the two gene pools of wild common bean Phaseolus vulgaris L. Heredity 110:267–276CrossRefPubMedGoogle Scholar
  43. McClean PE, Lee RK (2007) Genetic architecture of chalcone isomerase non-coding regions in common bean (Phaseolus vulgaris L.). Genome 50:203–214CrossRefPubMedGoogle Scholar
  44. McClean PE, Lee RK, Miklas PN (2004) Sequence diversity analysis of dihydroflavonol 4-reductase intron 1 in common bean. Genome 47:266–280CrossRefPubMedGoogle Scholar
  45. 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 11:184CrossRefGoogle Scholar
  46. McClean P, Cannon S, Gepts P, Hudson M, Jackson S, Rokhsar D, Schmutz J, Vance C (2008) Towards a whole genome sequence of common bean, (Phaseolus vulgaris L.): background, approaches, applications. http://bic.css.msu.edu/_pdf/Bean_Genomics_Status_2008.pdf
  47. McClean PE, Lee RK, Otto C, Gepts P, Bassett MJ (2002) Molecular and phenotypic mapping of genes controlling seed coat pattern and color in common bean (Phaseolus vulgaris L.). J Hered 93:148–152CrossRefPubMedGoogle Scholar
  48. McConnell M, Mamidi S, Lee R, Chikara S, Rossi M, Papa R, McClean P (2010) Syntenic relationships among legumes revealed using a gene-based genetic linkage map of common bean (Phaseolus vulgaris L.). Theor Appl Genet 121:1103–1116CrossRefPubMedGoogle Scholar
  49. Melotto M, Coelho MF, Pedrosa-Harand A, Kelly JD, Camargo LEA (2004) The anthracnose resistance locus Co-4 of common bean is located on chromosome 3 and contains putative disease resistance-related genes. Theor Appl Genet 109:690–699CrossRefPubMedGoogle Scholar
  50. Melotto M, Monteiro-Vitorello CB, Bruschi AG, Camargo LE (2005) Comparative bioinformatic analysis of genes expressed in common bean (Phaseolus vulgaris L.) seedlings. Genome 48:562–570CrossRefPubMedGoogle Scholar
  51. Meziadi C, Richard MM, Derquennes A, Thareau V, Blanchet S, Gratias A, Pflieger S, Geffroy V (2016) Development of molecular markers linked to disease resistance genes in common bean based on whole genome sequence. Plant Sci 242:351–357CrossRefPubMedGoogle Scholar
  52. Michael TP, Jackson S (2013) The first 50 plant genomes. Plant Genome 6. doi: 10.3835/plantgenome2013.03.0001in
  53. Miklas PN, Afanador L, Kelly JD (1996) Recombination-facilitated RAPD marker-assisted selection for disease resistance in common bean. Crop Sci 36:86–90CrossRefGoogle Scholar
  54. Miklas PN, Fourie D, Trapp J, Davis J, Myers JR (2014) New loci including conferring resistance to halo bacterial blight on chromosome Pv04 in common bean. Crop Sci 54:2099–2108CrossRefGoogle Scholar
  55. 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
  56. Moghaddam SM, Mamidi S, Osorno JM, Lee R, Brick M, Kelly J, Miklas P, Urrea C, Song Q, Cregan P, Grimwood J, Schmutz J, McClean PE (2016) Genome-wide association study identifies candidate loci underlying agronomic traits in a Middle American diversity panel of common bean. Plant Genome 9. doi: 10.3835/plantgenome2016.02.0012
  57. Moghaddam SM, Song Q, Mamidi S, Schmutz J, Lee R, Cregan P, Osorno J, McClean PE (2014) Developing market class specific InDel markers from next generation sequence data in Phaseolus vulgaris L. Front Plant Sci 5:185CrossRefPubMedPubMedCentralGoogle Scholar
  58. Muchero W, Guo J, Di Fazio SP, Chen JG, Ranjan P, Slavov GT, Gunter LE, Jawdy S, Bryan AC, Sykes R, Ziebell A, Klapste J, Porth I, Skyba O, Unda F, El-Kassaby YA, Douglas CA, Mansfield SD, Martin J, Schackwitz W, Evans LM, Czarnecki O, Tuskan GA (2015) High-resolution genetic mapping of allelic variants associated with cell wall chemistry in Populus. BMC Genom 16:1CrossRefGoogle Scholar
  59. Munishi LK, Lema AA, Ndakidemi PA (2015) Decline in maize and beans production in the face of climate change at Hai District in Kilimanjaro Region, Tanzania. Int J Climate Change Strat Manag 7:17–26CrossRefGoogle Scholar
  60. Naj AC, Jun G, Beecham GW, Wang L-S, Narayan B et al (2011) Common variants at MS4A4/MS4A6E, CD2AP, CD33 and EPHA1 are associated with late-onset Alzheimer’s disease. Nat Gene 43:436–441CrossRefGoogle Scholar
  61. Nakedde T, Ibarra-Perez FJ, Mukankusi C, Waines JG, Kelly JD (2016) Mapping of QTL associated with Fusarium root rot resistance and root architecture traits in black beans. Euphytica 212:51–63CrossRefGoogle Scholar
  62. Nodari RO, Tsail SM, Gilbertson RL, Gepts P (1993) Towards an integrated linkage map of common bean 2. Development of an RFLP-based linkage map. Theor Appl Genet 85:513–520CrossRefPubMedGoogle Scholar
  63. Nordborg M, Hu TT, Ishino Y, Jhaveri J, Toomajian C, Zheng H, Bakker E, Calabrese P, Gladstone J, Goyal R, Jakobsson M, Kim S, Morozov Y, Padhukasahasram B, Plagnol V, Rosenberg NA, Shah C, Wall JD, Wang J, Zhao K, Kalbfleisch T, Schlz V, Kreitman M, Bergelson J (2005) The pattern of polymorphism in Arabidopsis thaliana. PLoS Biol 3:e196CrossRefPubMedPubMedCentralGoogle Scholar
  64. O’Rourke JA, Iniguez LP, Fu F, Bucciarelli B, Miller SS, Jackson SA, McClean PE, Li J, Dai X, Zhao PX, Hernandez G, Vance CP (2014) An RNA-Seq based gene expression atlas of the common bean. BMC Genom 15:866CrossRefGoogle Scholar
  65. Papa R, Gepts P (2003) Asymmetry of gene flow and differential geographical structure of molecular diversity in wild and domesticated common bean (Phaseolus vulgaris L.) from Mesoamerica. Theor Appl Genet 106:239–250CrossRefPubMedGoogle Scholar
  66. Ramírez M, Graham MA, Blanco-López L, Silvente S, Medrano-Soto A, Blair MW et al (2005) Sequencing and analysis of common bean ESTs. Building a foundation for functional genomics. Plant Physiol 137:1211–1227CrossRefPubMedPubMedCentralGoogle Scholar
  67. Rodriguez M, Rau D, Bitocchi E, Bellucci E, Biagetti E, Carboni A, Gepts P, Nanni L, Papa R, Attene G (2016) Landscape genetics, adaptive diversity and population structure in Phaseolus vulgaris. New Phytol 209:1781–1794CrossRefPubMedGoogle Scholar
  68. Salami A, Kamara AB, Brixiova Z (2010) Smallholder agriculture in East Africa: trends, constraints and opportunities. Working Papers Series No. 105. African Development Bank, Tunis, TunisiaGoogle Scholar
  69. Schlueter JA, Goicoechea JL, Collura K, Gill N, Lin JY, 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
  70. Schmutz J, Cannon SB, Schlueter J, Ma J, Mitros T, Nelson W, Hyten DL, Song Q, Thelen JJ, Cheng J, 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 S, Goodstein D, Barry K, Futrell-Griggs M, Abernathy B, Du J, Tian Z, Zhu L, Gill N, Joshi T, Libault M, Sethuraman A, Zhang X-C, Shinozaki K, Nguyen HT, Wing RA, Cregan P, Specht J, Grimwood J, Rokshar D, Stacey G, Shoemaker RC, Jackson SA (2010) Genome sequence of the palaeopolyploid soybean. Nature 463:178–183CrossRefPubMedGoogle Scholar
  71. Schmutz J, McClean P, Mamidi S, Wu GA, Cannon SB, Grimwood J, Jenkins J, Shu S, Song Q, 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 G, Kelly JD, Kudrna D, Lee R, Richard MMS, Miklas PN, Osorno JM, Rodrigues J, Thareau V, Urrea CA, Want M, Yu Y, Zhang M, Wing RA, Cregan PB, Rokhsar DS, Jackson SA (2014) A reference genome for common bean and genome-wide analysis of dual domestications. Nat Genet 46:707–713CrossRefPubMedGoogle Scholar
  72. Schröder S, Mamidi S, Lee R, McKain MR, McClean PE, Osorno JM (2016) Optimization of genotyping by sequencing (GBS) data in common bean (Phaseolus vulgaris L.). Mol Breeding 36:1–9CrossRefGoogle Scholar
  73. Singh SP (2000) 50 years of the cooperative dry bean nursery. Annu Rep Bean Improv Cooperative 43:110–111Google Scholar
  74. Singh SP, Gepts P, Debouck DG (1991) Races of common bean (Phaseolus vulgaris, Fabaceae). Econ Bot 45:379–396CrossRefGoogle Scholar
  75. Singh SP, Munoz CG, TeraN H (2001) Registration of common bacterial blight resistant dry bean germplasm VAX 1, VAX 3, and VAX 4. Crop Sci 41:275–276CrossRefGoogle Scholar
  76. Slavov GT, Di Fazio SP, Martin J, Schackwitz W, Muchero W, Rodgers-Melnick E, Lipphardt MF, Pennacchio CP, Hellsten U, Pennacchio LA, Gunter LE, Ranjan P, Vining K, Pomraning KR, Wilhelm LJ, Pellegrini M, Mockler TC, Freitag M, Geraldes A, El-Kassaby YA, Mansfield SD, Cronk QCB, Douglas CJ, Strauss SH, Rokhsar D, Tuskan GA (2012) Genome resequencing reveals multiscale geographic structure and extensive linkage disequilibrium in the forest tree Populus trichocarpa. New Phytol 196:713–725CrossRefPubMedGoogle Scholar
  77. Soltani A, Bello M, Mndolwa E, Schroder S, Moghaddam SM, Osorno JM, Miklas PN, McClean PE (2016) Targeted analysis of dry bean growth habit: interrelationship among architectural, phenological, and yield components. Crop Sci 56:3005–3015CrossRefGoogle Scholar
  78. Song Q, Jia G, Hyten DL, Jenkins J, Hwang EY, Schroeder SG, Osorno JM, Schmutz J, Jackson SA, McClean PE, Cregan PB (2015) SNP Assay Development for linkage map construction, anchoring whole-genome sequence, and other genetic and genomic applications in common bean. G3: Genes Genom Genet 5:2285–2290Google Scholar
  79. Thibivilliers S, Joshi T, Campbell KB, Scheffler B, Xu D, Cooper B, Nguyen HT, Stacey G (2009) Generation of Phaseolus vulgaris ESTs and investigation of their regulation upon Uromyces appendiculatus infection. BMC Plant Biol 9:46CrossRefPubMedPubMedCentralGoogle Scholar
  80. Thornsberry JM, Goodman MM, Doebley J, Kresovich S, Nielsen D, Buckler ES (2001) Dwarf8 polymorphisms associate with variation in flowering time. Nat Genet 28:286–289CrossRefPubMedGoogle Scholar
  81. Tian D, Traw MB, Chen JQ, Kreitman M, Bergelson J (2003) Fitness costs of R-gene-mediated resistance in Arabidopsis thaliana. Nature 423:74–77CrossRefPubMedGoogle Scholar
  82. Tuskan GA, Difazio S, Jansson S, Bohlmann J, Grigoriev I, Hellsten U, Putnam N, Ralph S, Rombauts S, Salamov A, Schein J, Sterck I, Aerts A, Bhalerao RR, Bhalerao RP, Blaudez D, Boerjan W, Brun A, Brunner A, Busov V, Campbell M, Carlson J, Chalot M, Chapman J, Chen G–L, Cooper D, Coutinho PM, Couturier J, Covert S, Cronk Q, Cunningham R, Davis J, Degroeve S, Dejardin A, dePamphilis C, Detter J, Dirks B, Dubchak I, Duplessis, Ehlting J, Ellis B, Gendler K, Goodstein D, Gribskov M, Grimwood J, Groover A, Gunter L, Hamberger B, Heinze B, Helariutta Y, Henrissat B, Holligan D, Holt R, Huang W, Islam-Faridi N, Jones S, Jones-Rhoades M, Jorgensen R, Joshi C, Kangasjarvi J, Karlsson K, Kelleher C, Kirkpatrick R, Kirst M, Kohler A, Kalluri U, Larimer F, Leebens-Mack J, Leple L–C, Locascio P, Lou Yl, Lucas S, Martin F, Montanini B, Napoli C, Nelson DR, Nelson C, Nieminen K, Nilsson O, Pereda V, Peter G, Philippe R, Pilate G, Poliakov A, Razumovskaya J, Rihcardson P, Rinaldi C, Ritland L, Rouze P, Ryaboy D, Schmutz J, Scharader J, Segerman B, Shin H, Siddiqui A, Sterky F, Terry A, Tsai C, Uberbacher E, Unneberg P, Vahala J, Wall K, Wessler S, Yang G, Yin T, Douglas C, Marra M, Sandber G, Van de Peer Y, Rokshar D (2006) The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313:1596–1604Google Scholar
  83. Ugen M, Musoni A, Cheminingwa G, Kimani P, Mucharo M, Katafire M (2012) Utilization of common bean for improved health and nutrition in eastern and central Africa. Association for Strengthening Agricultural Research in Eastern and Central Africa, Entebbe, UgandaGoogle Scholar
  84. Viteri DM, Cregan PB, Trapp JJ, Miklas P, Singh SP (2014) A new common bacterial blight resistance QTL in VAX 1 common bean and interaction of the new QTL, SAP6, and SU91 with bacterial strains. Crop Sci 54:1598–1608CrossRefGoogle Scholar
  85. Vlasova A, Capella-Gutiérrez S, Rendón-Anaya M, Hernández-Oñate M, Minoche AE, Erb I, Camara F, Prieto-Barja P, Corvelo A, Sanseverino W, Westergaard G, Dohm J, Pappas GJ Jr, Saburido-Alvarez S, Kedra D, Gonzalez I, Cozzuto L, Gomez-Garrido J, Aguilar-Moron MA, Andreu N, Aguilar OM, Garcia-Mas J, Zehnsdorf M, Vazquez MP, Delgado-Salinas A, Delaye L, Lowy E, Mentaberry A, Vianello-Brondani RP, Garcia JL, Alioto T, Sanchez F, Himmelbauer H, Santalla M, Notredame C, Gabaldon T, Herrera-Estrella A, Guigo R (2016) Genome and transcriptome analysis of the Mesoamerican common bean and the role of gene duplications in establishing tissue and temporal specialization of genes. Genome Biol 17:32CrossRefPubMedPubMedCentralGoogle Scholar
  86. Weigel D, Nordborg M (2015) Population genomics for understanding adaptation in wild plant species. Annu Rev Genet 49:315–338CrossRefPubMedGoogle Scholar
  87. Zhang X, Zhai H, Wang Y, Tian X, Zhang Y, Wu H, Lu S, Yang G, Li Y, Wang L, Hu B, Bu Q, Xia Z (2016) Functional conservation and diversification of the soybean maturity gene E1 and its homologs in legumes. Scien Rep 6:29548CrossRefGoogle Scholar
  88. Zuiderveen GH, Padder BA, Kamfwa K, Song Q, Kelly JD (2016) Genome-wide association study of anthracnose resistance in Andean beans (Phaseolus vulgaris). PLoS ONE 11:e0156391CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  1. 1.Department of Plant SciencesNorth Dakota State UniversityFargoUSA
  2. 2.CIAT—International Center for Tropical AgricultureCaliColombia

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