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Haplotype structure at seven barley genes: relevance to gene pool bottlenecks, phylogeny of ear type and site of barley domestication

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Abstract

Archaeological remains indicate that the origin of western agriculture occurred in a brief period about 10,500 years ago in a region of the Middle East known as the Fertile Crescent, where the wild progenitors of several key agricultural cereal species are endemic. Domestication entailed the appearance of agronomic traits such as seed size and threshability. For a representative sample of 20 domesticated barley (Hordeum vulgare) lines, including 13 two-rowed and 7 six-rowed varieties, we determined the haplotypes at seven loci—Adh2, Adh3, Amy1, Dhn9, GAPDH, PEPC and WAXY encompassing 5,616 bases per line—and compared them to the haplotypes at the same loci for 25 wild forms (Hordeum spontaneum) collected within and outside the Fertile Crescent. In comparisons of wild versus domesticated barley, the number of haplotypes (70 vs. 17), average nucleotide diversity, π, (0.0077 vs. 0.0028), and Watterson’s theta at silent sites (0.0104 vs. 0.0028) was reduced in domesticated lines. Two loci, Amy1 and PEPC, were monomorphic in domesticated lines; Amy1 and GAPDH produced significant values of Tajima’s D. At GAPDH, π was slightly higher in domesticated than wild forms, due to divergent high-frequency haplotypes; for the remaining six loci, 87% of nucleotide diversity has been lost in the domesticated forms. Bottlenecks acting on neutrally evolving loci either during the domestication process, during subsequent breeding, or both, are sufficient to account for reduced diversity and the results of Tajima’s test, without the need to evoke selection at these loci. Phylogenetic networks data uncover distinct wild and domesticated barley genotypes and suggest that barley may have been domesticated in the Jordan valley. Because, based on AFLP data, the domesticated Turkish cultivars had a genetic basis as large as that present in large germplasm collections, all comparisons provided in this paper are of general value more than being restricted to the Turkish barley germplasm.

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References

  • Abdel-Ghani AH, Parzies HK, Omary A, Geiger HH (2004) Estimating the outcrossing rate of barley landraces and wild barley populations collected from ecologically different regions of Jordan. Theor Appl Genet 109:588–595

    Article  PubMed  Google Scholar 

  • Badr A, Müller KJ, Schäfer-Pregl R, El Rabey H, Effgen S, Ibrahim HH, Pozzi C, Rohde W, Salamini F (2000) On the origin and domestication history of barley (Hordeum vulgare). Mol Biol Evol 17:499–510

    PubMed  CAS  Google Scholar 

  • Bryant D, Moulton V (2004) Neighbor-Net: an agglomerative method for the construction of phylogenetic networks. Mol Biol Evol 21:255–265

    Article  PubMed  CAS  Google Scholar 

  • Buckler ES, Thornsberry JM, Kresovich S (2001) Molecular diversity, structure and domestication of grasses. Genet Res Camb 77:213–218

    CAS  Google Scholar 

  • Bundock P, Henry RJ (2004) Single nucleotide polymorphism, haplotype diversity and recombination in the Isa gene of barley. Theor Appl Genet 109:543–551

    Article  PubMed  CAS  Google Scholar 

  • Casas AM, Yahiaoui S, Ciudad F, Igartua E. (2005) Distribution of MWG699 polymorphism in Spanish European barleys. Genome 48:41–45

    Article  PubMed  CAS  Google Scholar 

  • Castiglioni P, Pozzi C, Heun M, Terzi V, Muller KJ, Rohde W, Salamini F (1998) An AFLP-based procedure for the efficient mapping of mutations and DNA probes in barley. Genetics 149:2039–2056

    PubMed  CAS  Google Scholar 

  • Chalmers KJ, Waugh R, Watters J, Forster BP, Nevo E, Abbott RJ, Powell W (1992) Grain isozyme and ribosomal DNA variability in Hordeum spontaneum populations from Israel. Theor Appl Genet 84:313–322

    Article  Google Scholar 

  • Dawson IK, Chalmers KJ, Waugh R, Powell W (1993) Detection and analysis of genetic variation in Hordeum spontaneum populations from Israel using RAPD markers. Mol Ecol 2:151–159

    Article  PubMed  CAS  Google Scholar 

  • Diamond J (1997) Guns, germs and steel. Random House, London

    Google Scholar 

  • Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–376

    Article  PubMed  CAS  Google Scholar 

  • Gaut BS, Morton BR, McCaig BC, Clegg MT (1996) Substitution rate comparisons between grasses and palms: synonymous rate differences at the nuclear gene Adh parallel rate differences at the plastid gene rbcL. Proc Natl Acad Sci USA 93:10274–10279

    Article  PubMed  CAS  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Harlan JR (1976) Barley. In: Simmonds NW (ed) Evolution of crop plants. Longman, London, pp 93–98

  • Huson DH (1998) SplitsTree: analyzing and visualizing evolutionary data. Bioinformatics 14:68–73

    Article  PubMed  CAS  Google Scholar 

  • Jana S, Pietrzak MI, Srivastava JP, Holwerda BC, Thai KM. (1987) Genetic diversity in wild barley (Hordeum spontaneum) populations of the Fertile Crescent. Barley Genet 5:63–73

    Google Scholar 

  • Kanazin V, Talbert H, See D, DeCamp P, Nevo E, Blake T (2002) Discovery and assay of single-nucleotide polymorphisms in barley (Hordeum vulgare). Plant Mol Biol 48:529–537

    Article  PubMed  CAS  Google Scholar 

  • Kolodinska Brantestam A, von Bothmer R, Dayteg C, Rashal I, Tuvesson S, Weibull J (2004) Inter simple sequence repeat analysis of genetic diversity and relationships in cultivated barley of Nordic and Baltic origin. Hereditas 141:186–192

    Article  PubMed  Google Scholar 

  • Komatsuda T, Maxim P, Senthil N, Mano Y (2004) High-density AFLP map of nonbrittle rachis 1 (btr1) and 2 (btr2) genes in barley (Hordeum vulgare L.). Theor Appl Genet 109:986–995

    Article  PubMed  CAS  Google Scholar 

  • Lev-Yadun S, Gopher A, Abbo S (2000) The cradle of agriculture. Science 288:1602–2603

    Article  PubMed  CAS  Google Scholar 

  • Lin J-Z, Brown AHD, Clegg MT (2001) Heterogeneous geographic patterns of nucleotide sequence diversity between two alcohol dehydrogenase genes in wild barley (Hordeum vulgare subspecies spontaneum). Proc Natl Acad Sci USA 98:531–536

    Article  PubMed  CAS  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 

  • Molina-Cano J-L, Russell JR, Moralejo MA, Escacena JL, Arias G, Powell W (2005) Chloroplast DNA microsatellite analysis supports a polyphyletic origin for barley. Theor Appl Genet 110:613–619

    Article  PubMed  CAS  Google Scholar 

  • Morrell PL, Lundy KE, Clegg MT (2003) Distinct geographic patterns of genetic diversity are maintained in wild barley (Hordeum vulgare ssp. spontaneum) despite migration. Proc Natl Acad Sci USA 100:10812–10817

    Article  PubMed  CAS  Google Scholar 

  • Morrell PL, Toleno DM, Lundy KE, Clegg MT (2005) Low levels of linkage disequilibrium in wild barley (Hordeum vulgare ssp. spontaneum) despite high rates of self-fertilization. Proc Natl Acad Sci USA 102:2442–2447

    Article  PubMed  CAS  Google Scholar 

  • Morgante M, Salamini F (2003) From plant genomics to breeding practice. Curr Opin Biotech 14:214–219

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Nevo E, Beiles A, Kaplan D, Starch N, Zohary D (1986a) Genetic diversity and environmental associations of wild barley, Hordeum spontaneum in Turkey. Genetica 68:203–213

    Article  Google Scholar 

  • Nevo E, Zohary D, Beiles A, Kaplan D (1986b) Genetic diversity and environmental associations of wild barley, Hordeum spontaneum (Poaceae) in Iran. Plant Syst Evol 153:141–164

    Article  Google Scholar 

  • Nevo E, Zohary D, Brown AHD, Harber M (1979) Genetic diversity and environmental associations of wild barley, Hordeum spontaneum, in Israel. Evolution 33:815–833

    Article  CAS  Google Scholar 

  • Paterson AH (2002) What has QTL mapping taught us about plant domestication? New Phytol 154:591–608

    Article  CAS  Google Scholar 

  • Paterson AH, Lin YR, Li Z, Schertz KF, Doebley JF, Pinson SRM, Liu SC, Stansel JW, Irvine JE (1995) Convergent domestication of cereal crops by independent mutations at corresponding genetic loci. Science 269:1714–1717

    Article  PubMed  CAS  Google Scholar 

  • Rafalski A (2002) Applications of single nucleotide polymorphisms in crop genetics. Curr Opin Plant Biol 5:94–100

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Rozen S, Skaletsky HJ (2000) Primer3 on the WWW for general users and for biologist programmers. In: Krawetz S, Misener S (eds) Bioinformatics methods and protocols: methods in molecular biology. Humana Press, Totowa, pp 365–386

    Google Scholar 

  • Russell J, Booth A, Fuller F, Harrower B, Hedley P, Machray G, Powell W (2004) A comparison of sequence-based polymorphism and haplotype content in transcribed and anonymous regions of the barley genome. Genome 47:389–398

    Article  PubMed  CAS  Google Scholar 

  • Salamini F, Özkan H, Brandolini A, Schäfer-Pregl R, Martin W (2002) Genetics and geography of wild cereal domestication in the Near East. Nat Genet Rev 3:429–441

    CAS  Google Scholar 

  • Salamini F, Heun M, Brandolini A, Ozkan H, Wunder J (2004) Comment on AFLP data and the origins of domesticated crops. Genome 47:615–620

    Article  PubMed  CAS  Google Scholar 

  • Schmidt HA, Strimmer K, Vingron M, von Haeseler A (2002) TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 18:502–504

    Article  PubMed  CAS  Google Scholar 

  • Schneider K, Borchardt DC, Schäfer-Pregl R, Nagl N, Glass C, Jeppson A, Gebhardt C, Salamini F (1999) PCR-based cloning and segregation analysis of functional gene homologues in Beta vulgaris. Mol Gen Genet 262:515–524

    Article  PubMed  CAS  Google Scholar 

  • Schneider K, Weisshaar B, Borchardt DC, Salamini F (2001) SNP frequency and allelic haplotype structure of Beta vulgaris expressed genes. Mol Breed 8:63–74

    Article  CAS  Google Scholar 

  • Snow L, Brody T (1984) Genetic variation of H. spontaneum in Israel Eco-Geographical Races, detected by trait measurements. Pl Syst Evol 145:15–28

    Article  Google Scholar 

  • Søgaard B, von Wettstein-Knowles P (1987) Barley: genes and chromosomes. Carlsberg Res Comm 52:123–196

    Article  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Taketa S, Kikuchi S, Awayama T, Yamamoto S, Ichii M, Kawasaki S (2004) Monophyletic origin of naked barley inferred from molecular analyses of a marker closely linked to the naked caryopsis gene (nud). Theor Appl Genet 108:1236–1242

    Article  PubMed  CAS  Google Scholar 

  • Tanno K, Takeda K (2004) On the origin of six-rowed barley with brittle rachis, agriocrithon [Hordeum vulgare ssp. vulgare f. agriocrithon (Aberg)]. Theor Appl Genet 110:145–150

    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  CAS  Google Scholar 

  • Vinh LS, von Haeseler A (2004) IQPNN: moving fast through tree space and stopping in time. Mol Biol Evol 21:1565–1571

    Article  CAS  Google Scholar 

  • Wright SI, Gaut BS (2005) Molecular population genetics and the search for adaptive evolution in plants. Mol Biol Evol 22:506–519

    Article  PubMed  CAS  Google Scholar 

  • Wright SI, Bi IV, Schroeder SG, Yamasaki M, Doebley JF, McMullen MD, Gaut BS (2005) The effects of artifical selection on the maize genome. Science 308:1310–1314

    Article  PubMed  CAS  Google Scholar 

  • Zabeau M, Vos P (1993) Selective restriction fragment amplification: a general method for DNA fingerprinting. European Patent Applification. Publication No:858A1

  • Zohary D, Hopf M (2000) Domestication of plants in the old world, 3rd edn. Oxford University Press, Oxford

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Acknowledgment

This work was supported by the Deutsche Forschungsgemeinschaft.

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Authors and Affiliations

  1. Max-Planck-Institute for Plant Breeding Research, Carl-von-Linné-Weg, 10, 50829, Koeln, Germany

    Benjamin Kilian & Francesco Salamini

  2. Department of Field Crops, Faculty of Agriculture, University of Cukurova, 01330, Adana, Turkey

    Hakan Özkan & Cemal Yucel

  3. Institute for Bioinformatics, Heinrich-Heine-Universitaet Duesseldorf, Universitätsstr., 1, 40225, Düsseldorf, Germany

    Jochen Kohl & Arndt von Haeseler

  4. Istituto Sperimentale per la Cerealicoltura - CRA, Via Mulino, 3, 26866, S. Angelo Lodigiano, (LO), Italy

    Andrea Brandolini

  5. Institute for Botany III, Heinrich-Heine-Universitaet Duesseldorf, Universitätsstr., 1, 40225, Düsseldorf, Germany

    Benjamin Kilian, Oliver Deusch & William Martin

  6. Fondazione Parco Tecnologico Padano, Via Einstein-Località Cascina Codazza, 26900, Lodi, Italy

    Francesca Barale & Francesco Salamini

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  1. Benjamin Kilian
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  2. Hakan Özkan
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  5. Francesca Barale
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Correspondence to Francesco Salamini.

Additional information

Communicated by R. McCombia

Manuscript information: Sequence data from this article have been deposited in GenBank Data library under accession nos. DQ195928 to DQ196067.

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Kilian, B., Özkan, H., Kohl, J. et al. Haplotype structure at seven barley genes: relevance to gene pool bottlenecks, phylogeny of ear type and site of barley domestication. Mol Genet Genomics 276, 230–241 (2006). https://doi.org/10.1007/s00438-006-0136-6

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  • DOI: https://doi.org/10.1007/s00438-006-0136-6

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