Skip to main content
Log in

FR-H3: a new QTL to assist in the development of fall-sown barley with superior low temperature tolerance

  • Original Paper
  • Published:
Theoretical and Applied Genetics Aims and scope Submit manuscript

Abstract

Fall-sown barley will be increasingly important in the era of climate change due to higher yield potential and efficient use of water resources. Resistance/tolerance to abiotic stresses will be critical, and foremost among the abiotic stresses is low temperature. Simultaneous gene discovery and breeding will accelerate the development of agronomically relevant fall-sown barley germplasm with resistance to low temperature. We developed two doubled haploid mapping populations using two lines from the University of Nebraska (NE) and one line from Oregon State University (OR): NB3437f/OR71 (facultative × facultative) and NB713/OR71 (winter × facultative). Both were genotyped with a custom 384 oligonucleotide pool assay (OPA). QTL analyses were performed for low temperature tolerance (LTT) and vernalization sensitivity (VS). The role of VRN-H2 in VS was confirmed and a novel alternative winter allele at VRN-H3 was discovered in the Nebraska germplasm. FR-H2 was identified as a probable determinant of LTT and a new QTL, FR-H3, was discovered on chromosome 1H that accounted for up to 48 % of the phenotypic variation in field survival at St. Paul, MN, USA. The discovery of FR-H3 is a significant advancement in barley LTT genetics and will assist in developing the next generation of fall-sown varieties.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Baga M, Fowler DB, Chibbar RN (2009) Identification of genomic regions determining the phenological development leading to floral transition in wheat (Triticum aestivum L.). J Exp Bot 60:3575–3585

    Article  PubMed  CAS  Google Scholar 

  • Casas AM, Djemel A, Ciudad FJ, Yahiaoui S, Ponce LJ, Contreras-Moreira B, Pilar Gracia M, Lasa JM, Igartua E (2011) HvFT1 (VrnH3) drives latitudinal adaptation in Spanish barleys. Theor Appl Genet 122:1293–1304

    Article  PubMed  CAS  Google Scholar 

  • Cistué L, Vallés MP, Echávarri B, Sanz JM, Castillo AM (2003) Barley anther culture. In: Maluszynski M, Kasha KJ, Forster BP, Szarejko I (eds) Doubled haploid production in crop plants: a manual. Kluwer, Dordrecht, pp 29–35

    Google Scholar 

  • Close TJ, Bhat PR, Lonardi S, Wu Y, Rostoks N, Ramsay L, Druka A, Stein N, Svensson JT, Wanamaker S, Bozdag S, Roose ML, Moscou MJ, Chao S, Varshney RK, Szuecs P, Sato K, Hayes PM, Matthews DE, Kleinhofs A, Muehlbauer GJ, DeYoung J, Marshall DF, Madishetty K, Fenton RD, Condamine P, Graner A, Waugh R (2009) Development and implementation of high-throughput SNP genotyping in barley. BMC Genom. 10:582

    Article  Google Scholar 

  • Cuesta-Marcos A, Igartua E, Ciudad FJ, Codesal P, Russell JR, Molina-Cano JL, Moralejo M, Szucs P, Gracia MP, Lasa JM, Casas AM (2008) Heading date QTL in a spring × winter barley cross evaluated in Mediterranean environments. Mol Breed 21:455–471

    Article  Google Scholar 

  • Cuesta-Marcos A, Szucs P, Close TJ, Filichkin T, Muehlbauer GJ, Smith KP, Hayes PM (2010) Genome-wide SNPs and re-sequencing of growth habit and inflorescence genes in barley: implications for association mapping in germplasm arrays varying in size and structure. BMC Genom. 11:707

    Article  CAS  Google Scholar 

  • Distelfeld A, Li C, Dubcovsky J (2009) Regulation of flowering in temperate cereals. Curr Opin Plant Biol 12:178–184

    Article  PubMed  CAS  Google Scholar 

  • Dubcovsky J, Chen CL, Yan LL (2005) Molecular characterization of the allelic variation at the VRN-H2 vernalization locus in barley. Mol Breed 15:395–407

    Article  CAS  Google Scholar 

  • Faure S, Higgins J, Turner A, Laurie DA (2007) The FLOWERING LOCUS T-like gene family in barley (Hordeum vulgare). Genetics 176:599–609

    Article  PubMed  CAS  Google Scholar 

  • Fowler S, Thomashow MF (2002) Arabidopsis transcriptome profiling indicates that multiple regulatory pathways are activated during cold acclimation in addition to the CBF cold response pathway. Plant Cell 14:1675–1690

    Article  PubMed  CAS  Google Scholar 

  • 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 127:1676–1681

    Article  PubMed  CAS  Google Scholar 

  • Francia E, Rizza F, Cattivelli L, Stanca AM, Galiba G, Toth 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 108:670–680

    Article  PubMed  CAS  Google Scholar 

  • Francia E, Barabaschi D, Tondelli A, Laido 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 115:1083–1091

    Article  PubMed  CAS  Google Scholar 

  • Fu DL, Szucs P, Yan LL, Helguera M, Skinner JS, von Zitzewitz J, Hayes PM, Dubcovsky J (2005) Large deletions within the first intron in VRN-1 are associated with spring growth habit in barley and wheat. Mol Genet Genom. 273:54–65

    Article  CAS  Google Scholar 

  • Galiba G, Quarrie SA, Sutka J, Morgounov A, Snape JW (1995) RFLP mapping of the vernalization (VRN1) and frost-resistance (FR1) genes on chromosome 5a of wheat. Theor Appl Genet 90:1174–1179

    Article  CAS  Google Scholar 

  • Galiba G, Vagujfalvi A, Li CX, Soltesz A, Dubcovsky J (2009) Regulatory genes involved in the determination of frost tolerance in temperate cereals. Plant Sci 176:12–19

    Article  CAS  Google Scholar 

  • Greenup A, Peacock WJ, Dennis ES, Trevaskis B (2009) The molecular biology of seasonal flowering-responses in Arabidopsis and the cereals. Ann Bot 103:1165–1172

    Article  PubMed  CAS  Google Scholar 

  • Hayes PM, Blake T, Chen THH, Tragoonrung S, Chen F, Pan A, Liu B (1993) Quantitative trait loci on barley (Hordeum vulgare L.) chromosome-7 associated with components of winterhardiness. Genome 36:66–71

    Article  PubMed  CAS  Google Scholar 

  • 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 147:355–366

    Article  PubMed  CAS  Google Scholar 

  • Karsai I, Szucs P, Meszaros K, Filichkina T, Hayes PM, Skinner JS, Lang L, Bedo Z (2005) The Vrn-H2 locus is a major determinant of flowering time in a facultative × winter growth habit barley (Hordeum vulgare L.) mapping population. Theor Appl Genet 110:1458–1466

    Article  PubMed  CAS  Google Scholar 

  • Kikuchi R, Kawahigashi H, Ando T, Tonooka T, Handa H (2009) Molecular and functional characterization of PEBP genes in barley reveal the diversification of their roles in flowering. Plant Physiol 149(3):1341–1353. doi:10.1104/pp.108.132134

    Article  PubMed  CAS  Google Scholar 

  • Knox AK, Dhillon T, Cheng HM, Tondelli A, Pecchioni N, Stockinger EJ (2010) CBF gene copy number variation at Frost Resistance-2 is associated with levels of freezing tolerance in temperate-climate cereals. Theor Appl Genet 121:21–35

    Article  PubMed  Google Scholar 

  • Pan A, Hayes PM, Chen F, Chen THH, Blake T, Wright S, Karsai I, Bedo Z (1994) Genetic-analysis of the components of winterhardiness in barley (Hordeum vulgare L.). Theor Appl Genet 89:900–910

    Article  CAS  Google Scholar 

  • Rizza F, Pagani D, Gut M, Prasil IT, Lago C, Tondelli A, Orru L, Mazzucotelli E, Francia E, Badeck FW, Crosatti C, Terzi V, Cattivelli L, Stanca AM (2011) Diversity in the response to low temperature in representative barley genotypes cultivated in Europe. Crop Sci 51:2759–2779

    Article  CAS  Google Scholar 

  • SAS Institute (2006) The SAS system for Windows v. 9.1. SAS Institute Inc. Cary, USA

  • Sasani S, Hemming MN, Oliver SN, Greenup A, Tavakkol-Afshari R, Mahfoozi S, Poustini K, Sharifi H-R, Dennis ES, Peacock WJ, Trevaskis B (2009) The influence of vernalization and day length on expression of flowering-time genes in the shoot apex and leaves of barley (Hordeum vulgare). J Exp Bot 60:2169–2178

    Article  PubMed  CAS  Google Scholar 

  • Skinner JS, von Zitzewitz J, Szucs 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 59:533–551

    Article  PubMed  CAS  Google Scholar 

  • Skinner J, Szucs P, von Zitzewitz J, Marquez-Cedillo L, Filichkin T, Stockinger EJ, Thomashow MF, Chen THH, Hayes PM (2006) Mapping of barley homologs to genes that regulate low temperature tolerance in Arabidopsis. Theor Appl Genet 112:832–842

    Article  PubMed  CAS  Google Scholar 

  • 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 51:308–321

    Article  PubMed  CAS  Google Scholar 

  • Szucs P, Skinner JS, Karsai I, Cuesta-Marcos A, Haggard KG, Corey AE, Chen THH, Hayes PM (2007) Validation of the VNR-H2/VNR-H1 epistatic model in barley reveals that intron length variation in VNR-H1 may account for a continuum of vernalization sensitivity. Mol Genet Genom. 277:249–261

    Article  CAS  Google Scholar 

  • Takahashi R, Yasuda S (1971) Genetics of earliness and growth habit in barley. In: Nilan RA (ed) Barley genetics. II. Proceedings of the second international barley genetics symposium. Washington State University Press, Pullman, pp 388–408

    Google Scholar 

  • Trevaskis B (2010) The central role of the VERNALIZATION1 gene in the vernalization response of cereals. Funct Plant Biol 37:479–487

    Article  CAS  Google Scholar 

  • Trevaskis B, Hemming MN, Dennis ES, Peacock WJ (2007) The molecular basis of vernalization-induced flowering in cereals. Trends Plant Sci 12:352–357

    Article  PubMed  CAS  Google Scholar 

  • Turner A, Beales J, Faure S, Dunford RP, Laurie DA (2005) The pseudo-response regulator Ppd-H1 provides adaptation to photoperiod in barley. Science 310:1031–1034

    Article  PubMed  CAS  Google Scholar 

  • Van Ooijen JW (2006) JoinMap 4, Software for the calculation of genetic linkage maps in experimental populations. Kyazma BV, Wageningen

    Google Scholar 

  • von Zitzewitz J, Szucs P, Dubcovsky J, Yan LL, 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(3):449–467

    Article  CAS  Google Scholar 

  • von Zitzewitz J, Cuesta-Marcos A, Condon F, Castro AJ, Chao S, Corey A, Filichkin T, Fisk SP, Gutierrez L, Haggard K, Karsai I, Muehlbauer GJ, Smith KP, Veisz O, Hayes PM (2011) The genetics of winterhardiness in barley: perspectives from genome-wide association mapping. Plant Genome 4:76–91

    Article  Google Scholar 

  • Wang S, Basten CJ, Zeng Z-B (2010) Windows QTL Cartographer 2.5. Department of Statistics, North Carolina State University, Raleigh, NC. http://statgen.ncsu.edu/qtlcart/WQTLCart.htm

  • Yan LL, Loukoianov A, Blechl A, 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(5664):1640–1644

    Article  PubMed  CAS  Google Scholar 

  • 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 VRN3FT. Proc Natl Acad Sci USA 103:19581–19586

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We would like to thank Blake Cooper (Limagrain USA) and Chris Evans (Busch Agricultural Resources, Inc., USA) for the field phenotyping of LTT at Fort Collins, Colorado and Fairfield, Montana (USA). This work was supported by the Agriculture and Food Research Initiative Plant Genome, Genetics and Breeding Program of USDA’s National Institute of Food and Agriculture (2009-65300-05666).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Alfonso Cuesta-Marcos.

Additional information

Communicated by A. Graner.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Fisk, S.P., Cuesta-Marcos, A., Cistué, L. et al. FR-H3: a new QTL to assist in the development of fall-sown barley with superior low temperature tolerance. Theor Appl Genet 126, 335–347 (2013). https://doi.org/10.1007/s00122-012-1982-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-012-1982-8

Keywords

Navigation