Theoretical and Applied Genetics

, Volume 120, Issue 5, pp 971–984 | Cite as

Structural and functional characterization of a winter malting barley

  • María Muñoz-Amatriaín
  • L. Cistué
  • Y. Xiong
  • H. Bilgic
  • A. D. Budde
  • M. R. Schmitt
  • K. P. Smith
  • P. M. Hayes
  • G. J. MuehlbauerEmail author
Original Paper


The development of winter malting barley (Hordeum vulgare L.) varieties is emerging as a worldwide priority due to the numerous advantages of these varieties over spring types. However, the complexity of both malting quality and winter hardiness phenotypes makes simultaneous improvement a challenge. To obtain an understanding of the relationship between loci controlling winter hardiness and malt quality and to assess the potential for breeding winter malting barley varieties, we structurally and functionally characterized the six-row accession “88Ab536”, a cold-tolerant line with superior malting quality characteristics that derives from the cross of NE76129/Morex//Morex. We used 4,596 SNPs to construct the haplotype structure of 88Ab536 on which malting quality and winter hardiness loci reported in the literature were aligned. The genomic regions determining malting quality and winter hardiness traits have been defined in this founder germplasm, which will assist breeders in targeting regions for marker-assisted selection. The Barley1 GeneChip array was used to functionally characterize 88Ab536 during malting. Its gene expression profile was similar to that of the archetypical malting variety Morex, which is consistent with their similar malting quality characteristics. The characterization of 88Ab536 has increased our understanding of the genetic relationships of malting quality and winter hardiness, and will provide a genetic foundation for further development of more cold-tolerant varieties that have malt quality characteristics that meet or exceed current benchmarks.


Quantitative Trait Locus Haplotype Structure Malting Barley Winter Hardiness Malting Quality 
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.



We thank Dr. Darrell Wesenberg for the persistence and skillful plant breeding that led to the development of 88Ab536. We also appreciate the resources provided by the University of Minnesota Supercomputing Institute. L. Cistué is recipient of a Senior Research Fellow at the Oregon State University from the Spanish Ministry of Science and Innovation. This research was supported by grants from the USDA-CSREES United States Barley Genome Project to GJM and KPS. SNP genotyping of 88Ab536 and Morex was supported by the Barley Coordinated Agriculture Project grant (USDA-CSREES-NRI Grant No 2006-55606-16722).

Supplementary material

122_2009_1225_MOESM1_ESM.xls (43 kb)
Supplementary material 1 (XLS 43 kb)
122_2009_1225_MOESM2_ESM.xls (373 kb)
Supplementary material 2 (XLS 373 kb)
122_2009_1225_MOESM3_ESM.xls (22 kb)
Supplementary material 3 (XLS 22.5 kb)


  1. American Society of Brewing Chemists (2004) Methods of analysis, 9th ed. Barley-7C protein by combustion; malt-4 extract, -6a diastatic power, -7a alpha amylase, -17 protein in unhopped wort by spectrophotometry, -18 β-glucan in congress wort by fluorescence. The Society, St. PaulGoogle Scholar
  2. Baik B-K, Ullrich SE (2008) Barley for food: characteristics, improvement and renewed interest. J Cereal Sci 48:223–242CrossRefGoogle Scholar
  3. Bamforth CW, Barclay AHP (1993) Malting technology and the uses of malt. In: McGregor A, Bhatty RS (eds) Barley: chemistry and technology. American Association of Cereal Chemists, St. Paul, pp 297–354Google Scholar
  4. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B 57:289–300Google Scholar
  5. Burger WC, LaBerge DE (1985) Malting and brewing quality. In: Rasmusson DC (ed) Barley. Agronomy monograph No. 26. ASA-CSSA-SSSA, Madison, pp 367–401Google Scholar
  6. Chen A, Reinheimer J, Brûlé-Babel A, Baumann U, Pallotta M, Fincher GB, Collins NC (2009) Genes and traits associated with chromosome 2H and 5H regions controlling sensitivity of reproductive tissues to frost in barley. Theor Appl Genet 118:1465–1476CrossRefPubMedGoogle Scholar
  7. Clark S, Hayes PM, Henson CA (2003) Effects of single nucleotide polymorphisms in β-amylase1 alleles from barley on functional properties of the enzymes. Plant Physiol Biochem 41:798–804CrossRefGoogle Scholar
  8. Close TJ, Wanamaker S, Caldo RA, Turner SM, Ashlock DA, Dickerson JA, Wing RA, Muehlbauer GJ, Kleinhofs A, Wise RP (2004) A new resource for cereal genomics: 22 K barley GeneChip comes of age. Plant Physiol 134:960–968CrossRefPubMedGoogle Scholar
  9. Devaux D, Kilian A, Kleinhofs A (1995) Comparative mapping of the barley genome with male and female recombination-derived, doubled haploid populations. Mol Gen Genet 249:600–608CrossRefPubMedGoogle Scholar
  10. Faure S, Higgins J, Turner A, Laurie DA (2007) The FLOWERING LOCUS T-like gene family in barley (Hordeum vulgare). Genetics 176:599–609CrossRefPubMedGoogle Scholar
  11. Fowler DB, Breton G, Limin AE, Mahfoozi S, Sarhan F (2001) Photoperiod and temperature interactions regulate low-temperature-induced gene expression in barley. Plant Physiol 127:1676–1681CrossRefPubMedGoogle Scholar
  12. Fox GP, Panozzo JF, Li CD, Lance RCM, Inkerman PA, Henry RJ (2003) Molecular basis of barley quality. Aust J Agric Res 54:1081–1101CrossRefGoogle Scholar
  13. Francia E, Rizza F, Cattivelli L, Stanca AM, Galiba G, Tóth B, Hayes PM, Skinner JS, Pecchioni N (2004) Two loci on chromosome 5H determine low-temperature tolerance in a ‘Nure’ (winter) × ‘Tremois’ (spring) barley map. Theor Appl Genet 108:670–680CrossRefPubMedGoogle Scholar
  14. Francia E, Barabaschi D, Tondelli A, Laidò G, Rizza F, Stanca AM, Busconi M, Fogher C, Stockinger EJ, Pecchioni N (2007) Fine mapping of a HvCBF gene cluster at the frost resistance locus Fr-H2 in barley. Theor Appl Genet 115:1083–1091CrossRefPubMedGoogle Scholar
  15. Galiba G, Vágújfalvi A, Li C, Soltész A, Dubcovsky J (2009) Regulatory genes involved in the determination of frost tolerance in temperate cereals. Plant Sci 176:12–19CrossRefGoogle Scholar
  16. Hayes PM, Jones BL (2000) Malting quality from a QTL perspective. In: 8th International barley genetics symposium, vol 8, Adelaide Convention Centre, Adelaide, South Australia, pp 99–105Google Scholar
  17. Hayes PM, Liu BH, Knapp SJ, Chen F, Jones B, Blake T, Frankckowiak J, Rasmusson D, Sorrells M, Ullrich SE, Wesenberg D, Kleinhofs A (1993) Quantitative trait locus effects and environmental interaction in a sample of North American barley germ plasm. Theor Appl Genet 87:392–401CrossRefGoogle Scholar
  18. Hayes MP, Castro A, Marquez-Cedillo L, Corey A, Henson C, Jones BL, Kling J, Mather D, Matus I, Rossi C, Sato K (2003) Genetic diversity for quantitatively inherited agronomic and malting quality traits. In: von Bothmer R, van Hintum T, Knüpffer H, Sato K (eds) Diversity in barley (Hordeum vulgare). Elsevier Science, Amsterdam, pp 201–226CrossRefGoogle Scholar
  19. Hemming MN, Peacock WJ, Dennis ES, Trevaskis B (2008) Low-temperature and daylength cues are integrated to regulate FLOWERING LOCUS T in barley. Plant Physiol 147:355–366CrossRefPubMedGoogle Scholar
  20. Karsai I, Szűcs P, Kőszegi B, Hayes PM, Casas A, Bedő Z, Veisz O (2008) Effects of photo and thermo cycles on flowering time in barley: a genetical phenomics approach. J Exp Bot 59:2707–2715CrossRefPubMedGoogle Scholar
  21. Kliebenstein D (2009) Quantitative genomics: analyzing intraspecific variation using global gene expression polymorphisms or eQTLs. Annu Rev Plant Biol 60:93–114CrossRefPubMedGoogle Scholar
  22. Kreis M, Williamson M, Shewry PR, Sharp P, Gale M (1988) Identification of a second locus encoding β-amylase on chromosome 2 of barley. Genetical Res 51:13–16CrossRefGoogle Scholar
  23. Lapitan NLV, Hess A, Cooper B, Botha AM, Badillo D, Iyer H, Menert J, Close TJ, Wright L, Hanning G, Tahir M, Lawrence C (2009) Differentially expressed genes during malting and correlation with malting quality phenotypes in barley (Hordeum vulgare L.). Theor Appl Genet 118:937–952CrossRefPubMedGoogle Scholar
  24. Obert DE, Wesenberg DM, Burrup DE, Jones BE, Erickson CA (2006) Registration of ‘Charles’ barley. Crop Sci 46:468–469CrossRefGoogle Scholar
  25. Pan A, Hayes PM, Chen F, Chen THH, Blake T, Wright S, Karsai I, Bedö Z (1994) Genetic analysis of the components of winterhardiness in barley (Hordeum vulgare L.). Theor Appl Genet 89:900–910CrossRefGoogle Scholar
  26. Potokina E, Sreenivasulu N, Altschmied L, Michalek W, Graner A (2002) Differential gene expression during seed germination in barley (Hordeum vulgare L.). Funct Integr Genomics 2:28–39CrossRefPubMedGoogle Scholar
  27. Potokina E, Caspers M, Prasad M, Kota R, Zhang H, Sreenivasulu N, Wang M, Graner A (2004) Functional association between malting quality trait components and cDNA array based expression patterns in barley (Hordeum vulgare L.). Mol Breeding 14:153–170CrossRefGoogle Scholar
  28. Potokina E, Prasad M, Malysheva L, Röder MS, Graner A (2006) Expression genetics and haplotype analysis reveal cis regulation of serine carboxypeptidase I (Cxp1), a candidate gene for malting quality in barley (Hordeum vulgare L.). Funct Integr Genomics 6:25–35CrossRefPubMedGoogle Scholar
  29. Reinheimer JL, Barr AR, Eglinton JK (2004) QTL mapping of chromosomal regions conferring reproductive frost tolerance in barley (Hordeum vulgare L.). Theor Appl Genet 109:1267–1274CrossRefPubMedGoogle Scholar
  30. Sall T, Flink J, Bengtsson BO (1990) Genetic control of recombination in barley. I. Variation in recombination frequency measured with inversion heterozygotes. Hereditas 112:171–178CrossRefGoogle Scholar
  31. Schmitt MR, Budde AD (2007) Improved methods for high-throughput extraction and assay of green barley malt proteinase activity facilitating examination of proteinase activity across large-scale populations. Cereal Chem 84:313–319CrossRefGoogle Scholar
  32. Schmitt MR, Marinac L (2008) Beta-amylase degradation by serine endoproteinases from green barley malt. J Cereal Sci 47:480–488CrossRefGoogle Scholar
  33. Skinner JS, von Zitzewitz J, Szűcs P, Marquez-Cedillo L, Filichkin T, Amundsen K, Stockinger EJ, Thomashow MF, Chen THH, Hayes PM (2005) Structural, functional, and phylogenetic characterization of a large CBF gene family in barley. Plant Mol Biol 59:533–551CrossRefPubMedGoogle Scholar
  34. Stockinger EJ, Skinner JS, Gardner KG, Francia E, Pecchioni N (2007) Expression levels of barley Cbf genes at the Frost resistance-H2 locus are dependent upon alleles at Fr-H1 and Fr-H2. Plant J 51:308–321CrossRefPubMedGoogle Scholar
  35. Szűcs P, Karsai I, von Zitzewitz J, Mészáros K, Cooper LLD, Gu YQ, Chen THH, Hayes PM, Skinner JS (2006) Positional relationships between photoperiod response QTL and photoreceptor and vernalization genes in barley. Theor Appl Genet 112:1277–1285CrossRefPubMedGoogle Scholar
  36. Szűcs P, Skinner JS, Karsai I, Cuesta-Marcos A, Haggard KG, Corey AE, Chen THH, Hayes PM (2007) Validation of the VRN-H2/VRN-H1 epistatic model in barley reveals that intron length variation in VRN-H1 may account for a continuum of vernalization sensitivity. Mol Genet Genomics 277:249–261CrossRefPubMedGoogle Scholar
  37. Szűcs P, Filichkin T, Cuesta-Marcos A, Hayes PM, Barley CAP (2008) Allele structure of the vernalization and photoperiod loci in the barley CAP core germplasm array. In: Plant and animal genome XV conference, January 12–16, San Diego, CA, USAGoogle Scholar
  38. Szűcs P, Blake VC, Bhat PR, Chao S, Close TJ, Cuesta-Marcos A, Muehlbauer GJ, Ramsay L, Waugh R, Hayes PM (2009) An integrated resource for barley linkage map and malting quality QTL alignment. Plant Genome 2:1–7CrossRefGoogle Scholar
  39. Trevaskis B, Hemming MN, Dennis ES, Peacock WJ (2007) The molecular basis of vernalization-induced flowering in cereals. Trends Plant Sci 12:352–357CrossRefPubMedGoogle Scholar
  40. Turner A, Beales J, Faure S, Dunford RP, Laurie DA (2005) The pseudo-response regulator Ppd-H1 provides adaptation to photoperiod in barley. Science 310:1031–1034CrossRefPubMedGoogle Scholar
  41. von Zitzewitz J, Szűcs P, Dubcovsky J, Yan L, Francia E, Pecchioni N, Casas A, Chen THH, Hayes PM, Skinner JS (2005) Molecular and structural characterization of barley vernalization genes. Plant Mol Biol 59:449–467CrossRefGoogle Scholar
  42. Watson L, Henry RJ (2005) Microarray analysis of gene expression in germinating barley embryos (Hordeum vulgare L.). Funct Integr Genomics 5:155–162CrossRefPubMedGoogle Scholar
  43. Wesenberg DM, Baenzinger PS, Rasmusson DC, Burrup DE, Jones BL (1998) Registration of 88Ab536-B barley germplasm. Crop Sci 38:559CrossRefGoogle Scholar
  44. White J, Pacey-Miller T, Crawford A, Cordeiro G, Barbary D, Bundock P, Henry R (2006) Abundant transcripts of malting barley identified by serial analysis of gene expression (SAGE). Plant Biotech J 4:289–301CrossRefGoogle Scholar
  45. Yan L, Loukoinov A, Blechl AE, Tranquilli G, Ramakrishna W, Sanmiguel P, Bennetzen JL, Echenique V, Dubcovsky J (2004) The wheat VRN2 gene is a flowering repressor down-regulated by vernalization. Science 303:1640–1644CrossRefPubMedGoogle Scholar
  46. Yan L, Fu D, Li C, Blechl A, Tranquilli G, Bonafede M, Sanchez A, Valarik M, Yasuda S, Dubcovsky J (2006) The wheat and barley vernalization gene VRN3 is an orthologue of FT. Proc Natl Acad Sci USA 103:19581–19586CrossRefPubMedGoogle Scholar
  47. Yasuda S, Hayashi J, Moriya I (1993) Genetic constitution for spring growth habit and some other characters in barley cultivars in the Mediterranean coastal regions. Euphytica 70:77–83CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • María Muñoz-Amatriaín
    • 1
  • L. Cistué
    • 3
  • Y. Xiong
    • 1
    • 4
  • H. Bilgic
    • 1
    • 5
  • A. D. Budde
    • 2
  • M. R. Schmitt
    • 2
  • K. P. Smith
    • 1
  • P. M. Hayes
    • 3
  • G. J. Muehlbauer
    • 1
    Email author
  1. 1.Department of Agronomy and Plant GeneticsUniversity of MinnesotaSaint PaulUSA
  2. 2.Cereal Crop Research UnitUSDA-ARSMadisonUSA
  3. 3.Department of Crop and Soil ScienceOregon State UniversityCorvallisUSA
  4. 4.Pioneer Hi-Bred Int’l Inc.Dallas CenterUSA
  5. 5.Department of Medicine/RheumatologyUniversity of MinnesotaMinneapolisUSA

Personalised recommendations