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

Theoretical and Applied Genetics volume 125, pages 1069–1085 (2012)Cite this article

Abstract

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.

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References

  • 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 35:10–11

    Google Scholar 

  • 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 25:1263–1274

    PubMed  Article  CAS  Google Scholar 

  • 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 120:1–12

    PubMed  Article  Google Scholar 

  • Bandelt HJ, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Bio Evol 16:37–48

    Article  CAS  Google Scholar 

  • Bartels D, Sunkar R (2005) Drought and salt tolerance in plants. Critical Rev Plant Sci 24:23–58

    Article  CAS  Google Scholar 

  • Becerra V, Paredes M, Rojo C, Díaz LM, Blair MW (2010) Microsatellite marker characterization of Chilean common bean (Phaseolus vulgaris L.) germplasm. Crop Sci 50:1–10

    Article  Google Scholar 

  • 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 48:582–592

    Article  Google Scholar 

  • 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 54:1747–1762

    Article  CAS  Google Scholar 

  • 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 113:100–109

    PubMed  Article  CAS  Google Scholar 

  • 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 112:1149–1163

    PubMed  Article  CAS  Google Scholar 

  • 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 116:29–43

    PubMed  Article  CAS  Google Scholar 

  • 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 119:955–972

    PubMed  Article  CAS  Google Scholar 

  • 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 121:1059–1070

    PubMed  Article  CAS  Google Scholar 

  • 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 29:71–88

    PubMed  Article  Google Scholar 

  • 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 23:2633–2635

    Google Scholar 

  • Broughton WJ, Hernandez G, Blair M, Beebe S, Gepts P, Vanderleyden J (2003) Beans (Phaseolus spp.)—model food legumes. Plant Soil 252:55–128

    Article  CAS  Google Scholar 

  • 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 3:1745–1756

    PubMed  Article  CAS  Google Scholar 

  • 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 180:1107–1121

    Article  Google Scholar 

  • 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 110:432–444

    Article  Google Scholar 

  • 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 266:175–195

    Article  Google Scholar 

  • Chai TY, Zhang YX (1999) Gene expression analysis of a proline-rich protein from bean under biotic and abiotic stress acta botanica sínica 41:111–113

    CAS  Google Scholar 

  • 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 30:2191–2198

    PubMed  Article  Google Scholar 

  • 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 

  • 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 114:143–154

    PubMed  Article  CAS  Google Scholar 

  • Edgar RC (2004) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5:113

    PubMed  Article  Google Scholar 

  • 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 20:1955–1962

    Article  CAS  Google Scholar 

  • Frankel N, Carrari F, Hasson E, Iusem ND (2006) Evolutionary history of the Asr gene family. Gene 378:74–83

    PubMed  Article  CAS  Google Scholar 

  • Gepts P (1998) Origin and evolution of common bean : past events and recent trends. HortScience 33:1119–1135

    Google Scholar 

  • 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, Colombia

  • 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 40:451–468

    Article  CAS  Google Scholar 

  • 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 York

    Google Scholar 

  • Hudson RR (2000) A new statistic for detecting genetic differentiation. Genetics 155:2011–2014

    PubMed  CAS  Google Scholar 

  • Hudson RR, Kreitman M, Aguade M (1987) A test of neutral molecularevolution based on nucleotide data. Genetics 116:153–159

    PubMed  CAS  Google Scholar 

  • Kelly JD (2000) Remaking bean plant architecture for efficient production. Adv Agron 71:109–143

    Article  Google Scholar 

  • 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 52:2136–2146

    Google Scholar 

  • Kizis D, Lumbreras V, Pagès M (2001) Role of AP2/EREBP transcription factors in gene regulation during abiotic stress. FEBS Lett 498:187–189

    PubMed  Article  CAS  Google Scholar 

  • 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 118:979–992

    PubMed  Article  CAS  Google Scholar 

  • 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 123:21–31

    PubMed  Article  Google Scholar 

  • Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452

    PubMed  Article  CAS  Google Scholar 

  • 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 9:230–249

    PubMed  Article  CAS  Google Scholar 

  • 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 177:460–467

    Article  CAS  Google Scholar 

  • Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York

  • 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 106:239–250

    PubMed  CAS  Google Scholar 

  • 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 100:1039–1051

    PubMed  Article  CAS  Google Scholar 

  • 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 70:3–15

    Google Scholar 

  • 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 52:589–599

    Article  Google Scholar 

  • 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, Colombia

  • 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 121:769–787

    PubMed  Article  CAS  Google Scholar 

  • Rafalski JA (2010) Association genetics in crop improvement. Curr Opin Plant Biol 13:174–180

    PubMed  Article  CAS  Google Scholar 

  • 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:e13497

    PubMed  Article  Google Scholar 

  • Riechmann JL, Meyerowitz EM (1998) The AP2/EREBP family of plant transcription factors. Biol Chem 379:633–646

    PubMed  Article  CAS  Google Scholar 

  • Rosales R, Ramírez P, Acosta JA, Castillo F, Kelly JD (2000) Grain yield and drought tolerance of common bean under field conditions. Agrociencia 34:153–165

    Google Scholar 

  • 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 2:504–522

    Article  Google Scholar 

  • Rozas J, Sanchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497

    PubMed  Article  CAS  Google Scholar 

  • Sahana G, Guldbrandtsen B, Janss L, Lund MS (2010) Comparison of association mapping methods in a complex pedigreed population. Genet Epidemiol 34:455–462

    PubMed  Article  Google Scholar 

  • Singh SP (2001) Broadening the genetic base of common bean cultivars: a review. Crop Sci 41:1659–1675

    Article  Google Scholar 

  • 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, London

    Chapter  Google Scholar 

  • Stephens M, Donnelly P (2003) A comparison of Bayesian methods for haplotype reconstruction from population genotype data. Amer J Hum Genet 73:1162–1169

    PubMed  Article  CAS  Google Scholar 

  • Taiz L, Zeiger E (2006) Plant physiology, 4th edn. Sinauer Associates, Sunderland, MA

  • Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595

    PubMed  CAS  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

  • Thornthwaite, CW, Mather JR (1955) The water balance. Climatology 8(1):1–104

    Google Scholar 

  • 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 106:9979–9986

    Article  Google Scholar 

  • 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 York

  • Tohme J, Gonzalez O, Beebe S, Duque MC (1996) AFLP analysis of gene pools of a wild bean core collection Crop Sci 36:1375–1384

    Google Scholar 

  • Wakeley J (2008) Coalescent theory: an introduction. Harvard University, Cambridge

    Google Scholar 

  • Wang Y-M, He C-F (2007) Isolation and characterization of a cold-induced DREB gene from Aloe vera L. Plant Mol Biol Rep 25:121–132

    Article  Google Scholar 

  • 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 67:589–602

    PubMed  Article  CAS  Google Scholar 

  • Watterson GA (1975) Number of segregating sites in genetic models without recombination. Theor Popul Biol 7:256–276

    PubMed  Article  CAS  Google Scholar 

  • 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)

  • 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 36:71–81

    PubMed  Article  CAS  Google Scholar 

  • 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 117:629–640

    PubMed  Article  CAS  Google Scholar 

  • 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 26:1521–1528

    PubMed  Article  CAS  Google Scholar 

  • 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):e10780

  • 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 105:401–409

    PubMed  Article  Google Scholar 

  • 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 37:2485–2492

    PubMed  Article  CAS  Google Scholar 

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Acknowledgments

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.

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Authors and Affiliations

  1. Evolutionary Biology Centre, Uppsala University, 751 05, Uppsala, Sweden

    Andrés J. Cortés

  2. ADOC Project, Generation Challenge Program, Montpellier, France

    Dominique This, Carolina Chavarro & Matthew W. Blair

  3. CIRAD, UMR Développement et Amélioration des Plantes, TA-A 96/03, 34398, Montpellier, France

    Dominique This

  4. Laboratorio de Botánica y Sistemática, Universidad de los Andes, Apartado Aéreo, 4976, Bogotá, Colombia

    Santiago Madriñán

  5. Department of Plant Breeding and Genetics, Cornell University, 242 Emerson Hall, Ithaca, NY, 14853, USA

    Matthew W. Blair

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  1. Andrés J. Cortés
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  3. Carolina Chavarro
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  4. Santiago Madriñán
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Correspondence to Matthew W. Blair.

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Communicated by H. Becker.

Electronic supplementary material

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122_2012_1896_MOESM1_ESM.docx

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

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

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

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

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Cortés, A.J., This, D., Chavarro, C. et al. Nucleotide diversity patterns at the drought-related DREB2 encoding genes in wild and cultivated common bean (Phaseolus vulgaris L.). Theor Appl Genet 125, 1069–1085 (2012). https://doi.org/10.1007/s00122-012-1896-5

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Keywords

  • Drought Tolerance
  • Common Bean
  • Selective Sweep
  • Mismatch Distribution
  • Wild Accession