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A genome-wide analysis of differentiation between wild and domesticated Phaseolus vulgaris from Mesoamerica

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Abstract

Lack of introgression or divergent selection may be responsible for the maintenance of phenotypic differences between sympatric populations of crops and their wild progenitors. To distinguish between these hypotheses, amplified fragment length polymorphism markers were located on a molecular linkage map of Phaseolus vulgaris relative to genes for the domestication syndrome and other traits. Diversity for these same markers was then analyzed in two samples of wild and domesticated populations from Mesoamerica. Differentiation between wild and domesticated populations was significantly higher in parapatric and allopatric populations compared to sympatric populations. It was also significantly higher near genes for domestication compared to those away from these genes. Concurrently, the differences in genetic diversity between wild and domesticated populations were strongest around such genes. These data suggest that selection in the presence of introgression appears to be a major evolutionary factor maintaining the identity of wild and domesticated populations in sympatric situations. Furthermore, alleles from domesticated populations appear to have displaced alleles in sympatric wild populations, thus leading to a reduction in genetic diversity in such populations. These results also provide a possible experimental framework for assessing the long-term risk of transgene escape and the targeting of transgenes inside the genome to minimize the survival of these transgenes into wild populations following introduction by gene flow.

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References

  • Burke JM, Tang S, Knapp SJ, Rieseberg LH (2002) Genetic analysis of sunflower domestication. Genetics 161:1257–1267

    PubMed  CAS  Google Scholar 

  • Cavalli-Sforza LL (1966) Population structure and human evolution. Proc R Soc Lond Ser B 164:362–379

    ADS  CAS  Google Scholar 

  • Charlesworth B, Nordborg M, Charlesworth D (1997) The effects of local selection, balanced polymorphism and background selection on equilibirum patterns of genetic diversity in subdivided populations. Genet Res 70:155–174

    Article  PubMed  CAS  Google Scholar 

  • Doebley J, Stec A (1991) Genetic analysis of the morphological differences between maize and teosinte. Genetics 129:285–295

    PubMed  CAS  Google Scholar 

  • Doebley J, Stec A, Wendel J, Edwards M (1990) Genetic and morphological analysis of a maize-teosinte F2 population:implications for the origin of maize. Proc Natl Acad Sci USA 87:9888–9892

    PubMed  ADS  CAS  Google Scholar 

  • Excoffier L, Smouse P, Quattro J (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491

    PubMed  CAS  Google Scholar 

  • Freyre R, Skroch P, Geffroy V, Adam-Blondon A-F, Shirmohamadali A, Johnson W, Llaca V, Nodari R, Pereira P, Tsai S-M, Tohme J, Dron M, Nienhuis J, Vallejos C, Gepts P (1998) Towards an integrated linkage map of common bean. 4. Development of a core map and alignment of RFLP maps. Theor Appl Genet 97:847–856

    Article  CAS  Google Scholar 

  • Geffroy V, Sévignac M, De Oliveira J, 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 QTL with genes involved in specific resistance. Mol Plant Microb Interact 13:287–296

    CAS  Google Scholar 

  • Gepts P (1988) Phaseolin as an evolutionary marker. In: Gepts P (ed) Genetic resources of Phaseolus beans. Kluwer, Dordrecht, pp 215–241

    Google Scholar 

  • Gepts P (1999) Development of an integrated genetic linkage map in common bean (Phaseolus vulgaris L.) and its use. In: Singh S (ed) Bean breeding for the 21st century Kluwer, Dordrecht, pp 53–91, 389–400

  • Gepts P (2004) Domestication as a long-term selection experiment. Plant Breed Rev 24(Part 2):1–44

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • González A, Wong A, Delgado-Salinas A, Papa R, Gepts P (2005) Assessment of inter simple sequence repeat markers to differentiate sympatric wild and domesticated populations of common bean (Phaseolus vulgaris L.). Crop Sci 35:606–615

    Article  Google Scholar 

  • Gressel J (1999) Tandem constructs: preventing the rise of superweeds. Trends Biotech 17:361–366

    Article  CAS  Google Scholar 

  • Ibarra-Pérez F, Ehdaie B, Waines G (1997) Estimation of outcrossing rate in common bean. Crop Sci 37:60–65

    Article  Google Scholar 

  • Kaplan L, Lynch T (1999) Phaseolus (Fabaceae) in archaeology: AMS radiocarbon dates and their significance for pre-Columbian agriculture. Econ Bot 53:261–272

    Google Scholar 

  • Koenig R, Gepts P (1989) Allozyme diversity in wild Phaseolus vulgaris: further evidence for two major centers of diversity. Theor Appl Genet 78:809–817

    Article  Google Scholar 

  • Koinange EMK, Singh SP, Gepts P (1996) Genetic control of the domestication syndrome in common-bean. Crop Sci 36:1037–1045

    Article  Google Scholar 

  • Lenormand T (2002) Gene flow and the limits to natural selection. Trends Ecol Evol 17:183–189

    Article  Google Scholar 

  • Lin J-Z, Morrell PL, Clegg MT (2002) The influence of linkage and inbreeding on patterns of nucleotide sequence diversity at duplicate alcohol dehydrogenase loci in wild barley (Hordeum vulgare ssp. spontaneum). Genetics 162:2007–2015

    PubMed  CAS  Google Scholar 

  • Llaca V, Gepts P (1996) Pulsed field gel electrophoresis analysis of the phaseolin locus region in Phaseolus vulgaris. Genome 39:722–729

    Article  PubMed  CAS  Google Scholar 

  • McKay JK, Latta RG (2002) Adaptive population divergence: markers, QTL and traits. Trends Ecol Evol 17:285–291

    Article  Google Scholar 

  • Merilä J, Crnokrak P (2001) Comparison of genetic differentiation at marker loci and quantitative traits. J Evol Biol 14:892–903

    Article  Google Scholar 

  • Miklas P, Johnson W, Delorme R, Gepts P (2001) QTL conditioning physiological resistance and avoidance to white mold in dry bean. Crop Sci 41:309–315

    Article  Google Scholar 

  • Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York, p 512

  • Nei M, Li W-H (1979) Mathematical models for studying genetic variation in terms of restriction endonucleases. Proc Natl Acad Sci USA 76:5269–5273

    PubMed  MATH  ADS  CAS  Google Scholar 

  • Nodari RO, Tsai SM, Guzmán P, Gilbertson RL, Gepts P (1993) Towards an integrated linkage map of common bean. 3. Mapping genetic factors controlling host-bacteria interactions. Genetics 134:341–350

    PubMed  CAS  Google Scholar 

  • Nordborg M, Borevitz JO, Bergelson J, Berry CC, Chory J, Hagenblad J, Kreitman M, Maloof JN, Noyes T, Oefner PJ, Stahl EA, Weigel D (2002) The extent of linkage disequilibrium in Arabidopsis thaliana. Nat Genet 30:190–193

    Article  PubMed  CAS  Google Scholar 

  • 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, Gepts P (2004) Asymmetric gene flow and introgression between wild and domesticated populations. In: Den Nijs D, Bartsch D, Sweet J (ed) Introgression from genetically modified plants into wild relatives and its consequences. CABI, Oxon, pp 125–138

    Google Scholar 

  • Payró de la Cruz E, Gepts P, Colunga GarciaMarín P, Zizumbo Villareal D (2005) Spatial distribution of genetic diversity in wild populations of Phaseolus vulgaris L. from Guanajuato and Michoacán, México. Genet Res Crop Evol (in press)

  • Poncet V, Lamy F, Enjalbert J, Joly H, Sarr A, Robert T (1998) Genetic analysis of the domestication syndrome in pearl millet (Pennisetum glaucum L, Poaceae): inheritance of the major characters. Heredity 81:648–658

    Article  Google Scholar 

  • Poncet V, Lamy F, Devos K, Gale M, Sarr A, Robert T (2000) Genetic control of domestication traits in pearl millet (Pennisetum glaucum L., Poaceae). Theor Appl Genet 100:147–159

    Article  CAS  Google Scholar 

  • Poncet V, Martel E, Allouis S, Devos K, Lamy F, Sarr A, Robert T (2002) Comparative analysis of QTLs affecting domestication traits between two domesticated × wild pearl millet (Pennisetum glaucum L., Poaceae) crosses. Theor Appl Genet 104:965–975

    Article  PubMed  CAS  Google Scholar 

  • Schlötterer C (2003) Hitchhiking mapping—functional genomics from the population genetics perspective. Trends Genet 19:32–38

    Article  PubMed  Google Scholar 

  • Singh SP, Nodari R, Gepts P (1991) Genetic diversity in cultivated common bean. I. Allozymes. Crop Sci 31:19–23

    Article  CAS  Google Scholar 

  • Sokal R, Rohlf F (1995) Biometry: the principles and practice of statistics in biological research, 3rd edn. Freeman, New York

    Google Scholar 

  • Sonnante G, Stockton T, Nodari RO, Becerra Velásquez VL, Gepts P (1994) Evolution of genetic diversity during the domestication of common-bean (Phaseolus vulgaris L.). Theor Appl Genet 89:629–635

    Article  Google Scholar 

  • Storz JF (2005) Using genome scans of DNA polymorphism to infer adaptive population divergence. Mol Ecol 14:671–688

    Article  PubMed  CAS  Google Scholar 

  • Tenaillon MI, U’Ren J, Tenaillon O, Gaut BS (2004) Selection versus demography: a multilocus investigation of the domestication process in maize. Mol Biol Evol 21:1214–1225

    Article  PubMed  CAS  Google Scholar 

  • Vigouroux Y, McMullen M, Hittinger CT, Houchins K, Schulz L, Kresovich S, Matsuoka Y, Doebley J (2002) Identifying genes of agronomic importance in maize by screening microsatellites for evidence of selection during domestication. Proc Natl Acad Sci USA 99:9650–9655

    Article  PubMed  ADS  CAS  Google Scholar 

  • Vos P, Hogers R, Bleeker M, Reijans M, Van de Lee T, Hornes M, Frijters A, Pot J, Peleman J, Kuiper M, Zabeau M (1995) AFLP: a new technique for DNA fingerprinting. Nucleic Acids Res 23:4407–4414

    PubMed  CAS  Google Scholar 

  • Weir BS, Cockerham C (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370

    Google Scholar 

  • Xiong L, Liu K, Dai X, Xu C, Zhang Q (1999) Identification of genetic factors controlling domestication-related traits of rice using an F2 population of a cross between Oryza sativa and O. rufipogon. Theor Appl Genet 98:243–251

    Article  CAS  Google Scholar 

  • Zizumbo-Villarreal D, Colunga-GarcíaMarín P, Payró de la Cruz E, Delgado-Valerio P, Gepts P (2005) Population structure and evolutionary dynamics of wild–weedy–domesticated complexes of common bean in a Mesoamerican region. Crop Sci 35 (in press)

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Acknowledgements

This work was supported by the McKnight Foundation. RP was supported by CNR (Italy) for his stay in Davis and work at Ancona. We thank Guido Barbujani, Thomas Bataillon, Isabelle Olivieri, Cal Qualset, Delphine Sicard, Julianno Sambatti, Don Strong, Fabio Veronesi and Renaud Vitalis for their useful comments on an early version of the manuscript.

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Correspondence to P. Gepts.

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Communicated by F. J. Muehlbauer

This article is dedicated to the memory of Epimaki M. K. Koinange.

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Papa, R., Acosta, J., Delgado-Salinas, A. et al. A genome-wide analysis of differentiation between wild and domesticated Phaseolus vulgaris from Mesoamerica. Theor Appl Genet 111, 1147–1158 (2005). https://doi.org/10.1007/s00122-005-0045-9

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  • DOI: https://doi.org/10.1007/s00122-005-0045-9

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