Cereal Research Communications

, Volume 46, Issue 4, pp 591–603 | Cite as

Genome-wide Scan Using DArT Markers for Selection Footprints in Six-rowed Naked Barley from the Tibetan Plateau

  • J. Q. Xu
  • L. Wang
  • B. L. Liu
  • T. F. Xia
  • D. C. Liu
  • X. Chang
  • T. W. Zhang
  • H. G. ZhangEmail author
  • Y. H. ShenEmail author


As one of the world’s earliest domesticated crops, barley is a model species for the study of evolution and domestication. Domestication is an evolutionary process whereby a population adapts, through selection; to new environments created by human cultivation. We describe the genome-scanning of molecular diversity to assess the evolution of barley in the Tibetan Plateau. We used 667 Diversity Arrays Technology (DArT) markers to genotype 185 barley landraces and wild barley accessions from the Tibetan Plateau. Genetic diversity in wild barley was greater than in landraces at both genome and chromosome levels, except for chromosome 3H. Landraces and wild barley accessions were clearly differentiated genetically, but a limited degree of introgression was still evident. Significant differences in diversity between barley subspecies at the chromosome level were observed for genes known to be related to physiological and phenotypical traits, disease resistance, abiotic stress tolerance, malting quality and agronomic traits. Selection on the genome of six-rowed naked barley has shown clear multiple targets related to both its specific end-use and the extreme environment in Tibet. Our data provide a platform to identify the genes and genetic mechanisms that underlie phenotypic changes, and provide lists of candidate domestication genes for modified breeding strategies.


domestication Hordeum vulgare selective sweep 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Supplementary material

42976_2018_4604591_MOESM1_ESM.pdf (253 kb)
Genome-wide Scan Using DArT Markers for Selection Footprints in Six-rowed Naked Barley from the Tibetan Plateau


  1. Åberg E. 1938. Hordeum agriocrithon nova sp.: a wild six-rowed barley. Ann. Roy. Agric. Coll. Sweden 6:159–216.Google Scholar
  2. Badr, A., Sch. R., Rabey, H.El., Effgen, S., Ibrahim, H., Pozzi, C., Rohde, W., Salamini, F. 2000. On the origin and domestication history of barley (Hordeum vulgare). Mol. Biol. Evol. 17:499–510.PubMedCrossRefPubMedCentralGoogle Scholar
  3. Bauer, E., Weyen, J., Schiemann, A., Graner, A., Ordon, F. 1997. Molecular mapping of novel resistance genes against Barley Mild Mosaic Virus (BaMMV). Theor. Appl. Genet. 95:1263–1269.CrossRefGoogle Scholar
  4. Beattie, A.D., Edney, M.J., Scoles, G.J., Rossnagel, B.G. 2010. Association mapping of malting quality data from Western Canadian two-row barley cooperative trials. Crop Sci. 50:1649–1663.CrossRefGoogle Scholar
  5. Boyd, W.J.R., Li, C.D., Grime, C.R., Cakir, M., Potipibool, S., Kaveeta, L., Men, S., Kamali, M.R., Barr, A.R., Moody, D.B., Lance, R.C.M., Logue, S.J., Raman, H., Read, B.J. 2003. Conventional and molecular genetic analysis of factors contributing to variation in the timing of heading among spring barley (Hordeum vulgare L.) genotypes grown over a mild winter growing season. Aust. J. Agric. Res. 54:1277–1301.CrossRefGoogle Scholar
  6. Bradbury, P.J., Zhang, Z., Kroon, D.E., Casstevens, T.M., Ramdoss, Y., Buckler, E.S. 2007. TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 23:2633–2635.CrossRefGoogle Scholar
  7. Brueggeman, R., Rostoks, N., Kudrna, D., Kilian, A., Han, F., Chen, J., Druka, A., Steffenson, B., Kleinhofs, A. 2002. The barley stem rust-resistance gene Rpg1 is a novel disease-resistance gene with homology to receptor kinases. Proc. Natl Acad. Sci. USA 99:9328–9333.PubMedCrossRefPubMedCentralGoogle Scholar
  8. Cai, S., Wu, D., Jabeen, Z., Huang, Y., Huang, Y., Zhang, G. 2013. Genome-wide association analysis of aluminum tolerance in cultivated and Tibetan wild barley. PLoS ONE 8:e69776.PubMedPubMedCentralCrossRefGoogle Scholar
  9. Cakir, M., Poulsen, D., Galwey, N.W., Ablett, G.A., Chalmers, K.J., Platz, G.J., Park, R.F., Lance, R.C.M., Panozzo, J.F., Read, B.J., Moody, D.B., Barr, A.R., Johnston, P., Li, C.D., Boyd, W.J.R., Grime, C.R., Appels, R., Jones, M.G.K, Langridge, P. 2003. Mapping and QTL analysis of the barley population Tallon × Kaputar. Aust. J. Agric. Res. 54:1155–1162.CrossRefGoogle Scholar
  10. Collins, H.M., Panozzo, J.F., Logue, S.J., Jefferies, S.P., Barr, A.R. 2003. Mapping and validation of chromosome regions associated with high malt extract in barley (Hordeum vulgare L.). Aust. J. Agric. Res. 54:1223–1240.CrossRefGoogle Scholar
  11. Coventry, S.J., Barr, A.R., Eglinton, J.K., Mcdonald, G.K. 2003. The determinants and genome locations influencing grain weight and size in barley (Hordeum vulgare L.). Aust. J. Agric. Res. 54:1103–1115.CrossRefGoogle Scholar
  12. Dai, F., Nevo, E., Wu, D., Comadran, J., Zhou, M., Qiu L., Chen, Z., Beiles, A., Chen, G., Zhang, G. 2012. Tibet is one of the centers of domestication of cultivated barley. Proc. Natl Acad. Sci. USA. 109:16969–16973.PubMedCrossRefPubMedCentralGoogle Scholar
  13. Doebley, J.F., Gaut, B.S., Smith, B.D. 2006. The molecular genetics of crop domestication. Cell 127:1309–1321.PubMedCrossRefPubMedCentralGoogle Scholar
  14. Doyle, J.J. 1990. Isolation of plant DNA from fresh tissue. Focus 12:13–15.Google Scholar
  15. Edwards, M.C., Steffenson, B.J. 1996. Genetics and mapping of barley stripe mosaic virus resistance in barley. Phytopathol. 86:184–187.CrossRefGoogle Scholar
  16. Excoffier, L., Lischer, H.E. 2010. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol. Ecol. Resour. 10:564–567.PubMedCrossRefPubMedCentralGoogle Scholar
  17. Faure, S., Turner, A.S., Gruszka, D., Christodoulou, V., Davis, S.J., von Korff, M., Laurie, D.A. 2012. Mutation at the circadian clock gene EARLY MATURITY 8 adapts domesticated barley (Hordeum vulgare) to short growing seasons. Proc. Natl. Acad. Sci. USA. 109:8328–8333.PubMedCrossRefPubMedCentralGoogle Scholar
  18. Garvin, D.F., Millergarvin, J.E., Viccars, E.A., Jacobsen, J.V., Brown, A.H.D. 1998. Identification of molecular markers linked to ant28–484, a mutation that eliminates proanthocyanidin production in barley seeds. Crop Sci. 38:1250–1255.CrossRefGoogle Scholar
  19. Genger, R.K., Williams, K.J., Raman, H., Read, B.J., Wallwork, H., Burdon, J.J., Brown, A.H.D. 2003. Leaf scald resistance genes in Hordeum vulgare and Hordeum vulgare ssp. spontaneum: parallels between cultivated and wild barley. Aust. J. Agric. Res. 54:1335–1342.CrossRefGoogle Scholar
  20. Graner, A., Tekauz, A. 1996. RFLP mapping in barely of a dominant gene conferring resistance to scald (Rhynchosporium secalis). Theor. Appl. Genet. 93: 421–425.PubMedCrossRefPubMedCentralGoogle Scholar
  21. Hill, W.G., Robertson, A. 1968. Linkage disequilibrium in finite populations. Theor. Appl. Genet. 38:226–231.PubMedCrossRefPubMedCentralGoogle Scholar
  22. Holsinger, K.E., Lewis, P.O., Dey, D.K. 2002. A Bayesian approach to inferring population structure from dominant markers. Mol. Ecol. 11:1157–1164.PubMedCrossRefPubMedCentralGoogle Scholar
  23. Hsu, T.W. 1975. On the origin and phylogeny of cultivated barley with reference to the discovery of Ganze wild two-rowed barley Hordeum spontaneum C. Koch. Acta Genet. Sin. 2:129–137. (in Chinese with English abstract)Google Scholar
  24. Igartua, E., Moralejo, M., Casas, A.M., Torres, L., Molina-Cano, J.L. 2012. Whole-genome analysis with SNPs from BOPA1 shows clearly defined groupings of Western Mediterranean, Ethiopian, and Fertile Crescent barleys. Genet. Resour. Crop. Evol. 60:251–264.CrossRefGoogle Scholar
  25. Jefferies, S.P., Barr, A.R., Karakousis, A., Kretschmer, J.M., Manning, S., Chalmers, K.J., Nelson, J.C., Islam, A.K.M.R., Langridge, P. 1999. Mapping of chromosome regions conferring boron toxicity tolerance in barley (Hordeum vulgare L.). Theor. Appl. Genet. 98:1293–1303.CrossRefGoogle Scholar
  26. Kikuchi, R., Kawahigashi, H., Oshima, M., Ando, T., Handa, H. 2012. The differential expression of HvCO9, a member of the CONSTANS-like gene family, contributes to the control of flowering under short-day conditions in barley. J. Exp. Bot. 63:773–784.PubMedCrossRefPubMedCentralGoogle Scholar
  27. Larson, S.R., Kadyrzhanova, D., Mcdonald, C., Sorrells, M., Blake, T.K. 1996. Evaluation of barley chromosome- 3 yield QTLs in a backcross F2 population using STS-PCR. Theor. Appl. Genet. 93:618–625.PubMedCrossRefPubMedCentralGoogle Scholar
  28. Li, C., Ni, P., Francki, M., Hunter, A., Zhang, Y., Schibeci, D., Li, H., Tarr, A., Wang, J., Cakir, M., Yu, J., Bellgard, M. Lance, R., Appels, R. 2004. Genes controlling seed dormancy and pre-harvest sprouting in a rice-wheat-barley comparison. Funct. Integr. Genomics. 4:84–93.PubMedCrossRefPubMedCentralGoogle Scholar
  29. Li, C.D., Lance, R.C.M., Collins, H.M., Tarr, A., Roumeliotis, S., Harasymow, S., Cakir, M., Fox, G.P., Grime, C.R., Broughton, S., Young, K.J., Raman, H., Barr, A.R., Moody, D.B., Read, B.J. 2003. Quantitative trait loci controlling kernel discoloration in barley (Hordeum vulgare L.). Aust. J. Agric. Res. 54:1251–1259.CrossRefGoogle Scholar
  30. Lonergan, P. F. 2001. Genetic characterisation and QTL mapping of zinc nutrition in barley (Hordeum vulgare). Ph.D. thesis, University of Adelaide, Australia. http://hdl.handle.net2440/21718Google Scholar
  31. Mano, Y., Takeda, K. 1997. Mapping quantitative trait loci for salt tolerance at germination and the seedling stage in barley (Hordeum vulgare L.). Euphytica 94:263–272.CrossRefGoogle Scholar
  32. Meyer, R.C., Swanston, J.S., Young, G.R., Lawrence, P.E., Bertie, A., Ritchie, J., Wilson, A., Brosnan, J., Pearson, S., Bringhurst, T., Steele, G., Aldis, P.R., Filed, M., Jolliffe, T., Powell, W., Thomas, W.T.B. 2001. A genome based approach to improving barley for the malting and distilling industries. HGCA Project Report 264. Scottish Crop Research Institute pp. 70–74.
  33. Nei, M. 1978. Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590.PubMedPubMedCentralGoogle Scholar
  34. Nevo, E. 2013. Evolution of wild barley and barley improvement. In: Zhang, G.P., Li, C.D., Liu, X. (eds), Advance in barley sciences. Springer. Dordrecht, The Netherlands. pp. 1–23.Google Scholar
  35. Park, R.F., Karakousis, A. 2002. Characterization and mapping of gene Rph19 conferring resistance to Puccinia hordei in the cultivar ‘Reka 1’ and several Australian barleys. Plant Breed. 121:232–236.CrossRefGoogle Scholar
  36. Pourkheirandish, M., Hensel, G., Kilian, B., Senthil, N., Chen, G., Sameri, M., Azhaguvel, P., Sakuma, S., Dhanagond, S., Sharma, R., Mascher, M., Himmelbach, A., Gottwald, S., Nair, S.K., Tagiri, A., Yukuhiro, F., Nagamura, Y., Kanamori, H., Matsumoto, T., Willcox, G., Middleton, C.P., Wicker, T., Walther, A., Waugh, R., Fincher, G.B., Stein, N., Kumlehn, J., Sato, K., Komatsuda, T. 2015. Evolution of the grain dispersal system in barley. Cell 162:527–539.PubMedCrossRefPubMedCentralGoogle Scholar
  37. Pourkheirandish, M., Komatsuda, T. 2007. The importance of barley genetics and domestication in a global perspective. Ann. Bot. 100:999–1008.PubMedPubMedCentralCrossRefGoogle Scholar
  38. Pritchard, J.K., Wen, X., Falush, D. 2010. Documentation for structure software: Version 2.3. University of Chicago, Chicago, IL. Raman, H., Platz, G.J., Chalmers, K.J., Raman, R., Read, B.J., Barr, A.R., Moody, D.B. 2003. Mapping of genomic regions associated with net form of netblotch resistance in barley. Aust. J. Agric. Res. 54:1359–1367.Google Scholar
  39. Read, B.J., Raman, H., Mcmichael, G., Chalmers, K.J., Ablett, G.A., Platz, G.J., Raman, R., Genger, R.K., Boyd, W.J.R., Li, C.D., Grime, C.R., Park, R.F., Wallwork, H., Prangnell, R., Lance, R.C.M. 2003. Mapping and QTL analysis of the barley population Sloop × Halcyon. Aust. J. Agric. Res. 54:1145–1153.CrossRefGoogle Scholar
  40. Ren, X., Nevo, E., Sun, D., Sun, G. 2013. Tibet as a potential domestication center of cultivated barley of China. PLoS ONE 8:e62700.PubMedPubMedCentralCrossRefGoogle Scholar
  41. Rohlf, F.J. 2000. NTSYS-pc Numerical taxonomy and multivariate analysis system, version 2.1. Exeter Software, New York.Google Scholar
  42. Rostoks, N., Ramsay, L., MacKenzie, K., Cardle, L., Bhat, P.R., Roose, M.L., Svensson, J.T., Stein, N., Varshney, R.K., Marshall, D.F., Graner, A., Close, T.J., Waugh, R. 2006. Recent history of artificial out-crossing facilitates whole-genome association mapping in elite inbred crop varieties. Proc. Natl Acad. Sci. USA. 103:18656–18661.PubMedCrossRefPubMedCentralGoogle Scholar
  43. Roy, J.K., Smith, K.P., Muehlbauer, G.J., Chao, S., Close, T.J., Steffenson, B.J. 2010. Association mapping of spot blotch resistance in wild barley. Mol. Breed. 26:243–256.PubMedPubMedCentralCrossRefGoogle Scholar
  44. Russell, J., Dawson, I.K., Flavell, A.J., Steffenson, B., Weltzien, E., Booth, A., Ceccarelli, S., Grando, S., Waugh, R. 2011. Analysis of >1000 single nucleotide polymorphisms in geographically matched samples of landrace and wild barley indicates secondary contact and chromosome-level differences in diversity around domestication genes. New Phytol. 191:564–578.PubMedCrossRefPubMedCentralGoogle Scholar
  45. Shoeva, O.Y., Mock, H.-P., Kukoeva, T.V., Börner, A., Khlestkina, E.K. 2016. Regulation of the flavonoid Biosynthesis Pathway Genes in Purple and Black Grains of Hordeum vulgare. PloS one 11:e0163782PubMedPubMedCentralCrossRefGoogle Scholar
  46. Spaner, D., Shugar, L.P., Choo, T.M., Falak, I., Briggs, K.G., Legge, W.G., Falk, D.E., Ullrich, S.E., Tinker, N.A., Steffenson, B.J., Mather, D.E. 1998. Mapping of disease resistance loci in barley on the basis of visual assessment of naturally occurring symptoms. Crop. Sci. 38:843–850.CrossRefGoogle Scholar
  47. Steffenson, B.J., Hayes, P. M., Kleinhofs, A. 1996. Genetics of seedling and adult plant resistance to net blotch (Pyrenophora teres f. teres) and spot blotch (Cochliobolus sativus) in barley. Theor. Appl. Genet. 92:552–558.PubMedPubMedCentralCrossRefGoogle Scholar
  48. Tanno, K., Taketa, S., Takeda, K., Komatsuda, T. 2002. A DNA marker closely linked to the vrs1 locus (row-type gene) indicates multiple origins of six-rowed cultivated barley (Hordeum vulgare L.). Theor. Appl. Genet. 104:54–60.PubMedCrossRefPubMedCentralGoogle Scholar
  49. Tashi, N., Tang, Y., Zeng, X. 2013. Food preparation from hulless barley in Tibet. In: Zhang, G.P., Li, C.D., Liu, X. (eds), Advance in barley sciences. Springer. Dordrect, The Netherlands. pp. 151–158.CrossRefGoogle Scholar
  50. Varshney, R.K., Paulo, M.J., Grando, S., van Eeuwijk, F.A., Keizer, L.C.P., Guo, P., Ceccarelli, S., Kilian, A., Baum, M., Graner, A. 2012. Genome wide association analyses for drought tolerance related traits in barley (Hordeum vulgare L.). Field Crop Res. 126:171–180.CrossRefGoogle Scholar
  51. von Bothmer, R., Sato, K., Komatsuda, T., Yasuda, S., Fischbeck, G. 2003. The domestication of cultivated barley. In: von Bothmer, R., van Hintum, T., Knüpffer, H., Sato, K. (eds), Diversity in barley (Hordeum vulgare). Elsevier, Amsterdam. pp. 9–27.CrossRefGoogle Scholar
  52. Wang, L., Xu, J.Q., Xia, T.F., Zhang, H.G., Liu, D.C., Shen, Y.H. 2014. Population structure and linkage disequilibrium in six-rowed barley landraces from the Qinghai-Tibetan Plateau. Crop. Sci. 54:2011–2022.CrossRefGoogle Scholar
  53. Wenzl, P., Li, H., Carling, J., Zhou, M., Raman, H., Paul, E., Hearnden, P., Maier, C., Xia, L., Caig, V., Ovesná, J., Cakir, M., Poulsen, D., Wang, J., Raman, R., Smith, K.P., Muehlbauer, G.J., Chalmer, K.J., Kleinhofs, A., Huttner, E., Kilian, A. 2006. A high-density consensus map of barley linking DArT markers to SSR, RFLP and STS loci and agricultural traits. BMC Genomics 7:206.PubMedPubMedCentralCrossRefGoogle Scholar
  54. Williams, K.J., Lichon, A., Gianquitto, P., Kretschmer, J.M., Karakousis, A., Manning, S., Langridge, P., Wallwork, H. 1999 Identification and mapping of a gene conferring resistance to the spot form of net blotch (Pyrenophora teres f. maculata) in barley. Theor. Appl. Genet. 99:323–327.CrossRefGoogle Scholar
  55. Wu, D., Qiu, L., Xu, L., Ye, L., Chen, M., Sun, D., Chen, Z., Zhang, H., Jin, X., Dai, F., Zhang, G. 2011. Genetic variation of HvCBF genes and their association with salinity tolerance in Tibetan annual wild barley. PLoS ONE 6:e22938.PubMedPubMedCentralCrossRefGoogle Scholar
  56. Zhang, F., Chen, G., Huang, Q., Orion, O., Krugman, T., Fahima, T., Korol, A.B., Nevo, E., Gutterman, Y. 2005. Genetic basis of barley caryopsis dormancy and seedling desiccation tolerance at the germination stage. Theor. Appl. Genet. 110:445–453.PubMedCrossRefPubMedCentralGoogle Scholar
  57. Zhou, T.-S., Takashi, I., Ryouichi, K., Naohiko, H., Makoto, K., Takehiro, H., Kazuhiro, S. 2012. Malting quality quantitative trait loci on a high-density map of Mikamo golden × Harrington cross in barley (Hordeum vulgare L.). Mol. Breed. 30:103–112.CrossRefGoogle Scholar

Copyright information

© Akadémiai Kiadó, Budapest 2018

Authors and Affiliations

  • J. Q. Xu
    • 1
    • 2
  • L. Wang
    • 1
  • B. L. Liu
    • 1
  • T. F. Xia
    • 1
    • 2
  • D. C. Liu
    • 1
    • 3
  • X. Chang
    • 4
  • T. W. Zhang
    • 5
  • H. G. Zhang
    • 1
    Email author
  • Y. H. Shen
    • 1
    Email author
  1. 1.Key Laboratory of Adaptation and Evolution of Plateau Biota, Key Laboratory of Crop Molecular Breeding of Qinghai Province, Northwest Institute of Plateau BiologyChinese Academy of SciencesXiningChina
  2. 2.University of Chinese Academy of SciencesBeijingChina
  3. 3.Triticeae Research Institute, Sichuan Agricultural UniversityWenjiangChina
  4. 4.Department of Plant SciencesTibet Agriculture and Animal Husbandry CollegeLinzhiChina
  5. 5.Institute of Agricultural Product Quality Standard and Testing ResearchTibet Academy of Agricultural and Animal Husbandry SciencesLhasaChina

Personalised recommendations