Theoretical and Applied Genetics

, Volume 125, Issue 5, pp 1069–1085 | Cite as

Nucleotide diversity patterns at the drought-related DREB2 encoding genes in wild and cultivated common bean (Phaseolus vulgaris L.)

  • Andrés J. Cortés
  • Dominique This
  • Carolina Chavarro
  • Santiago Madriñán
  • Matthew W. BlairEmail author
Original Paper


Common beans are an important food legume faced with a series of abiotic stresses the most severe of which is drought. The crop is interesting as a model for the analysis of gene phylogenies due to its domestication process, race structure, and origins in a group of wild common beans found along the South American Andes and the region of Mesoamerica. Meanwhile, the DREB2 transcription factors have been implicated in controlling non-ABA dependent responses to drought stress. With this in mind our objective was to study in depth the genetic diversity for two DREB2 genes as possible candidates for association with drought tolerance through a gene phylogenetic analysis. In this genetic diversity assessment, we analyzed nucleotide diversity at the two candidate genes Dreb2A and Dreb2B, in partial core collections of 104 wild and 297 cultivated common beans with a total of 401 common bean genotypes from world-wide germplasm analyzed. Our wild population sample covered a range of semi-mesic to very dry habitats, while our cultivated samples presented a wide spectrum of low to high drought tolerance. Both genes showed very different patterns of nucleotide variation. Dreb2B exhibited very low nucleotide diversity relative to neutral reference loci previously surveyed in these populations. This suggests that strong purifying selection has been acting on this gene. In contrast, Dreb2A exhibited higher levels of nucleotide diversity, which is indicative of adaptive selection and population expansion. These patterns were more distinct in wild compared to cultivated common beans. These approximations suggested the importance of Dreb2 genes in the context of drought tolerance, and constitute the first steps towards an association study between genetic polymorphism of this gene family and variation in drought tolerance traits. We discuss the utility of allele mining in the DREB gene family for the discovery of new drought tolerance traits from wild common bean.


Drought Tolerance Common Bean Selective Sweep Mismatch Distribution Wild Accession 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



The authors wish to thank A. Soler and L. Díaz for DNA extractions and the personnel of the CIAT Genetic Resource Unit and CIAT bean program for seed characterization and multiplication. They also acknowledge the Cornell Biotechnology Center for support in sequencing. Sequencing by D. Brunel and team is gratefully acknowledged, too. This research was supported by the Generation Challenge Program and had technical support from the ICRISAT genomics center.

Supplementary material

122_2012_1896_MOESM1_ESM.docx (212 kb)
Supplementary material 1 (DOCX 211 kb) List of 401 wild and cultivated accessions from the FAO germplasm collection selected for the gene phylogeny analysis
122_2012_1896_MOESM2_ESM.docx (145 kb)
Supplementary material 2 (DOCX 145 kb). Details of nucleotide diversity and neutrality tests for Dreb2A and Dreb2B genes in the wild collection. Cultivated common bean were not considered because of their low polymorphism
122_2012_1896_MOESM3_ESM.pdf (221 kb)
Supplementary material 3 (PDF 221 kb) Alignment of the P. vulgaris a) DREB2A and b) DREB2B proteins. In each case, only the analyzed region in our survey is shown. Long boxes below amino acid codons correspond to the AP2 protein domain. Marked amino acids correspond to non-synonymous mutations according to our survey
122_2012_1896_MOESM4_ESM.pdf (142 kb)
Supplementary material 4 (PDF 141 kb). Mismatch distributions for (a–c) Dreb2A and (d–e) Dreb2B. All common beans (subfigures a and d), only the Andean genepool (subfigures b and e), and only the Mesoamerican genepool (subfigures c and f) are considered separately. Continuous line: simulated distribution using the Wright–Fisher neutral model. Dotted line: observed distribution


  1. Afanador LK, Hadley SD, Kelly JD (1993) Adoption of a mini-prep DNA extraction method for RAPD marker analysis in common bean. Bean Improv Cooperative 35:10–11Google Scholar
  2. Agarwal PK, Agarwal P, Reddy MK, Sopory SK (2006) Role of DREB transcription factors in abiotic and biotic stress tolerance in plants. Plant Cell Rep 25:1263–1274PubMedCrossRefGoogle Scholar
  3. Asfaw A, Blair MW, Almekinders C (2009) Genetic diversity and population structure of common bean (Phaseolus vulgaris L.) landraces from the East African Highlands. Theor Appl Genet 120:1–12PubMedCrossRefGoogle Scholar
  4. Bandelt HJ, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Bio Evol 16:37–48CrossRefGoogle Scholar
  5. Bartels D, Sunkar R (2005) Drought and salt tolerance in plants. Critical Rev Plant Sci 24:23–58CrossRefGoogle Scholar
  6. Becerra V, Paredes M, Rojo C, Díaz LM, Blair MW (2010) Microsatellite marker characterization of Chilean common bean (Phaseolus vulgaris L.) germplasm. Crop Sci 50:1–10CrossRefGoogle Scholar
  7. Beebe S, Rao IM, Cajiao C, Grajales M (2008) Selection for drought resistance in common bean also improves yield in phosphorus limited and favorable environments. Crop Sci 48:582–592CrossRefGoogle Scholar
  8. Benchimol LL, de Campos T, Carbonell SAM, Colombo CA, Chioratto AF, Formighieri EF, Gouvea LRL, de Souza AP (2007) Structure of genetic diversity among common bean (Phaseolus vulgaris L.) varieties of Mesoamerican and Andean origins using new developed microsatellite markers. Genet Res Crop Evol 54:1747–1762CrossRefGoogle Scholar
  9. Blair MW, Giraldo MC, Buendia HF, Tovar E, Duque MC, Beebe SE (2006a) Microsatellite marker diversity in common bean (Phaseolus vulgaris L.). Theor Appl Genet 113:100–109PubMedCrossRefGoogle Scholar
  10. Blair MW, Iriarte G, Beebe S (2006b) QTL analysis of yield traits in an advanced backcross population derived from a cultivated Andean x wild common bean (Phaseolus vulgaris L.) cross. Theor Appl Genet 112:1149–1163PubMedCrossRefGoogle Scholar
  11. Blair MW, Diaz JM, Hidalgo R, Diaz LM, Duque MC (2007) Microsatellite characterization of Andean races of common bean (Phaseolus vulgaris L.). Theor Appl Genet 116:29–43PubMedCrossRefGoogle Scholar
  12. Blair M, Diaz LM, Buendia HF, Duque MC (2009) Genetic diversity, seed size associations and population structure of a core collection of common beans (Phaseolus vulgaris L.). Theor Appl Genet 119:955–972PubMedCrossRefGoogle Scholar
  13. Blair MW, Medina JI, Astudillo C, Rengifo J, Beebe SE, Machado G, Graham R (2010) QTL for seed iron and zinc concentration and content in a Mesoamerican common bean (Phaseolus vulgaris L.) population. Theor Appl Genet 121:1059–1070PubMedCrossRefGoogle Scholar
  14. Blair MW, Galeano CH, Tovar E, Muñoz-Torres MC, Velasco A, Beebe SE, Rao IM (2012) Development of a Mesoamerican intra-genepool genetic map for QTL detection in a drought tolerant x susceptible common bean (Phaseolus vulgaris L.) cross. Mol Breed 29:71–88PubMedCrossRefGoogle Scholar
  15. Bradbury PJ, Zhang Z, roon DE, Casstevens RM, Ramdoss Y, Buckler ES (2007) TASSELL Software for association mapping of complex traits in diverse samples. Bioinformatics 23:2633–2635Google Scholar
  16. 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
  17. Caicedo AL, Williamson SH, Hernandez RD, Boyko A, Fledel-Alon A, York TL, Polato NR, Olsen KM, Nielsen R, McCouch SR, Bustamante CD, Purugganan MD (2007) Genome-wide patterns of nucleotide polymorphism in domesticated rice. PLoS Genet 3:1745–1756PubMedCrossRefGoogle Scholar
  18. Camus L, Chevin LM, Cordet CT, Charcosset A, Manicacci D, Tenaillon MI (2008) Patterns of molecular evolution associated with two selective sweeps in the Tb1-Dwarf8 region in maize. Genetics 180:1107–1121CrossRefGoogle Scholar
  19. Chacón MI, Pickersgill B, Debouck DG (2005) Domestication patterns in common bean (Phaseolus vulgaris L.) and the origin of the Mesoamerican and Andean cultivated races. Theor Appl Genet 110:432–444CrossRefGoogle Scholar
  20. Chacón MI, Pickersgill B, Debouck DG, Arias JS (2007) Phylogeographic analysis of the chloroplast DNA variation in wild common bean (Phaseolus vulgaris L.) in the Americas. Plant Syst Evol 266:175–195CrossRefGoogle Scholar
  21. Chai TY, Zhang YX (1999) Gene expression analysis of a proline-rich protein from bean under biotic and abiotic stress acta botanica sínica 41:111–113Google Scholar
  22. Chen JQ, Meng XP, Zhang Y, Xia M, Wang XP (2008) Over-expression of OsDREB genes lead to enhanced drought tolerance in rice. Biotechnol Lett 30:2191–2198PubMedCrossRefGoogle Scholar
  23. Cortés AJ, Chavarro MC, Blair MW (2011) SNP marker diversity in common bean (Phaseolus vulgaris L.). Theor Appl Genet doi. doi: 10.1007/s00122-011-1630-8 Google Scholar
  24. Diaz LM, Blair MW (2006) Race structure within the Mesoamerican gene pool of common bean (Phaseolus vulgaris L.) as determined by microsatellite markers. Theor Appl Genet 114:143–154PubMedCrossRefGoogle Scholar
  25. Edgar RC (2004) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5:113PubMedCrossRefGoogle Scholar
  26. Frankel N, Hasson E, Iusem ND, Rossi M (2003) Adaptive evolution of the eater stress—induced gene Asr2 in Lycopersicon species dwelling in arid habitats. Mol Bio Evol 20:1955–1962CrossRefGoogle Scholar
  27. Frankel N, Carrari F, Hasson E, Iusem ND (2006) Evolutionary history of the Asr gene family. Gene 378:74–83PubMedCrossRefGoogle Scholar
  28. Gepts P (1998) Origin and evolution of common bean : past events and recent trends. HortScience 33:1119–1135Google Scholar
  29. Gepts P, Debouck DG (1991) Origin, domestication, and evolution of the common bean. In: van Schoonhaven A, Voysest O (eds) Common beans: research for Crop Improvement Centro Internacional de Agricultura Tropical (CIAT), Cali, ColombiaGoogle Scholar
  30. Gepts P, Osborn TC, Rashka K, Bliss FA (1986) Phaseolin-protein variability in wild forms and landraces of the common bean (Phaseolus vulgaris): evidence for multiple centers of domestication. Econ Bot 40:451–468CrossRefGoogle Scholar
  31. Gepts P, Aragão F, Barros E, Blair M, Brondani R, Broughton W, Galasso I, Hernandez G, Kami J, Lariguet P, McClean P, Melotto M, Miklas P, Pauls P, Pedrosa-Harand A, Porch T, Sánchez F, Sparvoli F, Yu K (2008) Genomics of Phaseolus beans, a major source of dietary protein and micronutrients in the tropics. In: Moore P, Ming R (eds) Genomics of tropical crop plants. Springer, New YorkGoogle Scholar
  32. Hudson RR (2000) A new statistic for detecting genetic differentiation. Genetics 155:2011–2014PubMedGoogle Scholar
  33. Hudson RR, Kreitman M, Aguade M (1987) A test of neutral molecularevolution based on nucleotide data. Genetics 116:153–159PubMedGoogle Scholar
  34. Kelly JD (2000) Remaking bean plant architecture for efficient production. Adv Agron 71:109–143CrossRefGoogle Scholar
  35. Kim J-S, Mizoi J, Yoshida T, Fujita Y, Nakajima J, Ohori T, Todaka D, Nakashima K, Hirayama T, Shinozaki K, Yamaguchi-Shinozaki K (2012) An ABRE promoter sequence is involved in osmotic stress-responsive expression of the DREB2A gene, which encodes a transcription factor regulating drought-inducible genes in Arabidopsis. Plant Cell Physiol 52:2136–2146Google Scholar
  36. Kizis D, Lumbreras V, Pagès M (2001) Role of AP2/EREBP transcription factors in gene regulation during abiotic stress. FEBS Lett 498:187–189PubMedCrossRefGoogle Scholar
  37. Kwak M, Gepts P (2009) Structure of genetic diversity in the two major gene pools of common bean (Phaseolus vulgaris L., Fabaceae). Theor Appl Genet 118:979–992PubMedCrossRefGoogle Scholar
  38. Li ZM, Zheng XM, Ge S (2011) Genetic diversity and domestication history of African rice (Oryza glaberrima) as inferred from multiple gene sequences. Theor Appl Genet 123:21–31PubMedCrossRefGoogle Scholar
  39. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452PubMedCrossRefGoogle Scholar
  40. Morran S, Eini O, Pyvovarenko T, Parent B, Singh R, Ismagul A, Eliby S, Shirley N, Landridge P, Lopato S (2011) Improvement of stress tolerance of wheat and barley by modulation of expression of DREB/CBF factors. Plant Biotechnol J 9:230–249PubMedCrossRefGoogle Scholar
  41. Nayak SN, Balaji J, Upadhyaya HD, Hash T, Kishor K, Chattopadhyay D, Rodriguez LM, Blair MW, Baume M, McNally K, This D, Hoisington DA, Varshney RK (2009) Isolation and sequence analysis of DREB2A homologues in three cereal and two legume species. Plant Sci 177:460–467CrossRefGoogle Scholar
  42. Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New YorkGoogle Scholar
  43. 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 106:239–250PubMedGoogle Scholar
  44. Papa R, Bellucci E, Rossi M, Leonardi S, Rau D, Gepts P, Nanni L, Attene G (2007) Tagging the signatures of domestication in common bean (Phaseolus vulgaris) by means of pooled DNA samples. Ann Bot 100:1039–1051PubMedCrossRefGoogle Scholar
  45. Paredes M, Becerra V, Tay J, Blair MW, Bascur G (2010) Selection of a representative core collection from the Chilean common bean germplasm. Chil J Agric Res 70:3–15Google Scholar
  46. Payró E, Gepts P, Colunga P, Zizumbo D (2005) Spatial distribution of genetic diversity in wild populations of Phaseolus vulgaris L. from Guanajuato and Michoacán, México. Genet Resour Crop Evol 52:589–599CrossRefGoogle Scholar
  47. Pérez JC, Monserrate F, Beebe S, Blair M (2008) Field evaluation of a common bean reference collection for drought tolerance. In: CIAT (ed) Annual report outcome line SBA-1 product 2: beans that are more productive in smallholder systems of poor farmers. CIAT, Palmira, ColombiaGoogle Scholar
  48. Philippe R, Courtois B, McNally KL, Mournet P, El-Malki R, Le Paslier MC, Fabre D, Billot C, Brunel D, Glaszmann JC, This D (2010) Structure, allelic diversity and selection of Asr genes, candidate for drought tolerance, in Oryza sativa L. and wild relatives. Theor Appl Genet 121:769–787PubMedCrossRefGoogle Scholar
  49. Rafalski JA (2010) Association genetics in crop improvement. Curr Opin Plant Biol 13:174–180PubMedCrossRefGoogle Scholar
  50. Ramírez-Villegas J, Khoury C, Jarvis A, Debouck DG, Guarino L (2010) A gap analysis methodology for collecting crop genepools: a case study with Phaseolus beans. PLoS ONE 5:e13497PubMedCrossRefGoogle Scholar
  51. Riechmann JL, Meyerowitz EM (1998) The AP2/EREBP family of plant transcription factors. Biol Chem 379:633–646PubMedCrossRefGoogle Scholar
  52. Rosales R, Ramírez P, Acosta JA, Castillo F, Kelly JD (2000) Grain yield and drought tolerance of common bean under field conditions. Agrociencia 34:153–165Google Scholar
  53. Rossi M, Bitocchi E, Bellucci E, Nanni L, Rau D, Attene G, Papa R (2009) Linkage disequilibrium and population structure in wild and domesticated populations of Phaseolus vulgaris L. Evol Appl 2:504–522CrossRefGoogle Scholar
  54. Rozas J, Sanchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497PubMedCrossRefGoogle Scholar
  55. Sahana G, Guldbrandtsen B, Janss L, Lund MS (2010) Comparison of association mapping methods in a complex pedigreed population. Genet Epidemiol 34:455–462PubMedCrossRefGoogle Scholar
  56. Singh SP (2001) Broadening the genetic base of common bean cultivars: a review. Crop Sci 41:1659–1675CrossRefGoogle Scholar
  57. Singh SP (2005) Common bean (Phaseolus vulgaris L.). In: Singh RJ, Jauhar PP (eds) Genetic resources, chromosome engineering, and crop improvement, grain legumes. CRC Press, LondonCrossRefGoogle Scholar
  58. Stephens M, Donnelly P (2003) A comparison of Bayesian methods for haplotype reconstruction from population genotype data. Amer J Hum Genet 73:1162–1169PubMedCrossRefGoogle Scholar
  59. Taiz L, Zeiger E (2006) Plant physiology, 4th edn. Sinauer Associates, Sunderland, MAGoogle Scholar
  60. Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595PubMedGoogle Scholar
  61. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599Google Scholar
  62. Thornthwaite, CW, Mather JR (1955) The water balance. Climatology 8(1):1–104Google Scholar
  63. Tiana F, Stevensa NM, Buckler ES (2009) Tracking footprints of maize domestication and evidence for a massive selective sweep on chromosome 10. Proc Nat Acad Sci USA 106:9979–9986CrossRefGoogle Scholar
  64. Tohme J, Jones P, Beebe S, Iwanaga M (1995) The combined use of agroecological and characterization data to establish the CIAT Phaseolus vulgaris core collection. In: Hodgkin T, Brown AH, van Hintum JL, Morales EA (eds) Core collections of plant genetic resources. John Wiley & Sons, New YorkGoogle Scholar
  65. Tohme J, Gonzalez O, Beebe S, Duque MC (1996) AFLP analysis of gene pools of a wild bean core collection Crop Sci 36:1375–1384Google Scholar
  66. Wakeley J (2008) Coalescent theory: an introduction. Harvard University, CambridgeGoogle Scholar
  67. Wang Y-M, He C-F (2007) Isolation and characterization of a cold-induced DREB gene from Aloe vera L. Plant Mol Biol Rep 25:121–132CrossRefGoogle Scholar
  68. Wang Q, Guan Y, Wu Y, Chen H, Chen F, Chu C (2008) Overexpression of a rice OsDREB1F gene increases salt, drought, and low temperature tolerance in both Arabidopsis and rice. Plant Mol Biol 67:589–602PubMedCrossRefGoogle Scholar
  69. Watterson GA (1975) Number of segregating sites in genetic models without recombination. Theor Popul Biol 7:256–276PubMedCrossRefGoogle Scholar
  70. Xia H, Camus-Kulandaivelu LT, Stephan W, Tellier AL, Zhang Z (2010) Nucleotide diversity patterns of local adaptation at drought-related candidate genes in wild tomatoes. Mol Ecol (Online version)Google Scholar
  71. Yang Y, Wu J, Zhu K, Liu L, Chen F, Yu D (2009) Identification and characterization of two chrysanthemum (Dendronthema x moriforlium) DREB genes, belonging to the AP2/EREBP family. Mol Biol Rep 36:71–81PubMedCrossRefGoogle Scholar
  72. Zhang XY, Blair MW, Wang SM (2008) Genetic diversity of chinese common bean (Phaseolus vulgaris L.) landraces assessed with simple sequence repeat markers. Theor Appl Genet 117:629–640PubMedCrossRefGoogle Scholar
  73. Zhao J, Ren W, Zhi D, Wang L, Xia G (2007) Arabidopsis DREB1A / CBF3 bestowed transgenic tall fescue increased tolerance to drought stress. Plant Cell Rep 26:1521–1528PubMedCrossRefGoogle Scholar
  74. Zhao KY, Wright M, Kimball J, Eizenga G, McClung A, Kovach M, Tyagi W, Ali ML, Tung CW, Reynolds A, Bustamante CD, McCouch SR (2010a) Genomic diversity and introgression in O. sativa reveal the impact of domestication and breeding on the rice genome. Plos One 5(5):e10780Google Scholar
  75. Zhao L, Hu Y, Chong K, Wang T (2010b) ARAG1, an ABA-responsive DREB gene, plays a role in seed germination and drought tolerance of rice. Ann Bot 105:401–409PubMedCrossRefGoogle Scholar
  76. Zhuang J, Xiong AS, Peng RH, Gao F, Zhu B, Zhang JA, Fu XY, Jin XF, Chen JM, Zhang Z, Qiao YS, Yao QH (2010) Analysis of Brassica rapa ESTs: gene discovery and expression patterns of AP2/ERF family genes. Mol Biol Rep 37:2485–2492PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • Andrés J. Cortés
    • 1
  • Dominique This
    • 2
    • 3
  • Carolina Chavarro
    • 2
  • Santiago Madriñán
    • 4
  • Matthew W. Blair
    • 2
    • 5
    Email author
  1. 1.Evolutionary Biology CentreUppsala UniversityUppsalaSweden
  2. 2.ADOC ProjectGeneration Challenge ProgramMontpellierFrance
  3. 3.CIRADUMR Développement et Amélioration des PlantesMontpellierFrance
  4. 4.Laboratorio de Botánica y SistemáticaUniversidad de los AndesBogotáColombia
  5. 5.Department of Plant Breeding and GeneticsCornell UniversityIthacaUSA

Personalised recommendations