Skip to main content
Log in

Introgression of an intermediate VRNH1 allele in barley (Hordeum vulgare L.) leads to reduced vernalization requirement without affecting freezing tolerance

  • Published:
Molecular Breeding Aims and scope Submit manuscript

Abstract

The process of vernalization is mainly controlled by two genes in winter barley (Hordeum vulgare L.), VRNH1 and VRNH2. A recessive allele at VRNH1 and a dominant allele at VRNH2 must be present to induce a vernalization requirement. In addition, this process is usually associated with greater low-temperature tolerance. Spanish barleys originated in areas with mild winters and display a reduced vernalization requirement compared with standard winter cultivars. The objective of this study was to investigate the genetic origin of this reduced vernalization requirement and its effect on frost tolerance. We introgressed the regions of a typical Spanish barley line that carry VRNH1 and VRNH2 into a winter cultivar, Plaisant, using marker-assisted backcrossing. We present the results of a set of 12 lines introgressed with all four possible combinations of VRNH1 and VRNH2, which were evaluated for vernalization requirement and frost tolerance. The reduced vernalization requirement of the Spanish parent was confirmed, and was found to be due completely to the effect of the VRNH1 region. The backcross lines showed no decline in frost tolerance compared with that of the recurrent parent unless they carried an extra segment of chromosome 5H. This extra segment, a carryover of the backcross process, apparently contained the well-known frost tolerance quantitative trait locus Fr-H2. We demonstrate that it is possible to manipulate the vernalization requirement with only minor effects on frost tolerance. This finding opens the path to creating new types of barley cultivars that are better suited to specific environments, especially in a climate-change scenario.

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

  • Aghnoum R, Marcel TC, Johrde A, Pecchioni N, Schweizer P, Niks RE (2010) Basal host resistance of barley to powdery mildew: connecting quantitative trait loci and candidate genes. Mol Plant Microbe Interact 23:91–102

    Article  PubMed  CAS  Google Scholar 

  • Akar T, Francia E, Tondelli A, Rizza F, Stanca AM, Pecchioni N (2009) Marker-assisted characterization of frost tolerance in barley (Hordeum vulgare L.). Plant Breed 128:381–386

    Article  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, Szűcs 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 Genomics 10:582

    Article  PubMed  Google Scholar 

  • Cockram J, Chiapparino E, Taylor SA, Stamati K, Donini P, Laurie DA, O’Sullivan DM (2007) Haplotype analysis of vernalization loci in European barley germplasm reveals novel VRN-H1 alleles and a predominant winter VRN-H1/VRN-H2 multi-locus haplotype. Theor Appl Genet 115:993–1001

    Article  PubMed  CAS  Google Scholar 

  • Cuesta-Marcos A, Igartua E, Ciudad FJ, Codesal P, Russell JR, Molina-Cano JL, Moralejo MA, Szűcs 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 

  • Dhillon T, Pearce SP, Stockinger EJ, Distelfeld A, Li C, Knox AK, Vashegyi I, Vágújfalvi A, Galiba G, Dubcovsky J (2010) Regulation of freezing tolerance and flowering in temperate cereals: the VRN-1 connection. Plant Physiol. doi:10.1104/pp.110.159079

  • 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 

  • Flood RG, Halloran GM (1984) The nature and duration of gene action for vernalization response in wheat. Ann Bot 53:363–368

    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, 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 115:1083–1091

    Article  PubMed  CAS  Google Scholar 

  • Frisch M, Melchinger AE (2001) Marker-assisted backcrossing for simultaneous introgression of two genes. Crop Sci 41:1716–1725

    Article  Google Scholar 

  • Frisch M, Bohn M, Melchinger AE (1999) Comparison of selection strategies for marker-assisted backcrossing of a gene. Crop Sci 39:1295–1301

    Article  Google Scholar 

  • Galiba G, Quarrie SA, Sutka J, Morgaunov 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, Vágújfalvi A, Li C, Solté 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 

  • 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 winter hardiness. Genome 36:66–71

    Article  PubMed  CAS  Google Scholar 

  • Hemming MN, Fieg S, Peacock WJ, Dennis ES, Trevaskis B (2009) Regions associated with repression of the barley (Hordeum vulgare) VERNALIZATION1 gene are not required for cold induction. Mol Genet Genomics 282:107–117

    Article  PubMed  CAS  Google Scholar 

  • Igartua E, Gracia MP, Lasa JM, Medina B, Molina-Cano JL, Montoya JL, Romagosa I (1998) The Spanish barley core collection. Genet Resour Crop Evol 45:475–481

    Article  Google Scholar 

  • Izawa T, Takahashi Y, Yano M (2003) Comparative biology comes into bloom: genomic and genetic comparison of flowering pathways in rice and Arabidopsis. Curr Opin Plant Biol 6:113–120

    Article  PubMed  CAS  Google Scholar 

  • Karsai I, Hayes PM, Kling J, Matus IA, Mészáros K, Láng L, Bedő Z, Sato K (2004) Genetic variation in component traits of heading date in Hordeum vulgare subsp. spontaneum accessions characterized in controlled environments. Crop Sci 44:1622–1632

    Article  Google Scholar 

  • Kim DH, Doyle MR, Sung S, Amasino RM (2009) Vernalization: winter and the timing of flowering in plants. Annu Rev Cell Dev Biol 25:277–299

    Article  PubMed  CAS  Google Scholar 

  • Lasa JM, Igartua E, Ciudad FJ, Codesal P, Garcia EV, Gracia MP, Medina B, Romagosa I, Molina-Cano JL, Montoya JL (2001) Morphological and agronomical diversity patterns in the Spanish barley core collection. Hereditas 135:217–225

    Article  PubMed  CAS  Google Scholar 

  • Laurie DA, Pratchett N, Bezant JH, Snape JW (1995) RFLP mapping of five major genes and eight quantitative trait loci controlling flowering time in a winter × spring barley (Hordeum vulgare L) cross. Genome 38:575–585

    Article  PubMed  CAS  Google Scholar 

  • Levi A, Paterson AH, Barak V, Yakir D, Wang B, Chee PW, Saranga Y (2009) Field evaluation of cotton near-isogenic lines introgressed with QTLs for productivity and drought related traits. Mol Breed 23:179–195

    Article  CAS  Google Scholar 

  • Neeraja CN, Maghirang-Rodriguez R, Pamplona A, Heuer S, Collard BCY, Septiningsih EM, Vergara G, Sanchez D, Xu K, Ismail AM, Mackill DJ (2007) A marker-assisted backcross approach for developing submergence-tolerant rice cultivars. Theor Appl Genet 115:767–776

    Article  PubMed  CAS  Google Scholar 

  • Ribaut JM, Ragot M (2007) Marker-assisted selection to improve drought adaptation in maize: the backcross approach, perspectives, limitations, and alternatives. J Exp Bot 58:351–360

    Article  PubMed  CAS  Google Scholar 

  • Skinner JS, Szűcs P, von Zitzewitz J, Marquez-Cedillo L, Filichkin T, Stockinger EJ, Thomashow MF, Chen TH, 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 

  • 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 277:249–261

    Article  PubMed  Google Scholar 

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

    Google Scholar 

  • Tischner T, Kőszegi B, Veisz O (1997) Climatic programmes used in the Martonvásár phytotron most frequently in recent years. Acta Agron Hung 45:85–104

    Google Scholar 

  • Tondelli A, Francia E, Barabaschi D, Aprile A, Skinner JS, Stockinger EJ, Stanca AM, Pecchioni N (2006) Mapping regulatory genes as candidates for cold and drought stress tolerance in barley. Theor Appl Genet 112:445–454

    Article  PubMed  CAS  Google Scholar 

  • Tóth B, Galiba G, Fehér E, Sutka J, Snape JW (2003) Mapping genes affecting flowering time and frost resistance on chromosome 5B of wheat. Theor Appl Genet 107:509–514

    Article  PubMed  Google Scholar 

  • Tottman DR, Makepeace RJ (1979) An explanation of the decimal code for the growth stages of cereals, with illustrations. Ann Appl Biol 93:221–234

    Article  Google Scholar 

  • Trevaskis B, Bagnall DJ, Ellis MH, Peacock WJ, Dennis ES (2003) MADS box genes control vernalization-induced flowering in cereals. Proc Natl Acad Sci USA 100:13099–13104

    Article  PubMed  CAS  Google Scholar 

  • Vágújfalvi A, Galiba G, Cattivelli L, Dubcovsky J (2003) The cold regulated transcriptional activator Cbf3 is linked to the frost-tolerance locus Fr-A2 on wheat chromosome 5A. Mol Genet Genomics 269:60–67

    PubMed  Google Scholar 

  • Vágújfalvi A, Crosatti C, Galiba G, Dubcovsky J, Cattivelli L (2000) Two loci on wheat chromosome 5A regulate the differential cold-dependent expression of the cor14b gene in frost-tolerant and frost-sensitive genotypes. Mol Gen Genet 263:194–200

    Article  PubMed  Google Scholar 

  • von Zitzewitz J, Szűcs P, Dubcovsky J, Yan L, Pecchioni N, Francia E, Casas A, Chen THH, Hayes PM, Skinner JS (2005) Molecular and structural characterization of barley vernalization genes. Plant Mol Biol 59:449–467

    Article  CAS  Google Scholar 

  • Yan L, Loukoianov A, Tranquilli G, Helguera M, Fahima T, Dubcovsky J (2003) Positional cloning of the wheat vernalization gene VRN1. Proc Natl Acad Sci USA 100:6263–6268

    Article  PubMed  CAS  Google Scholar 

  • Yan L, Loukoianov A, Blech 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 303:1640–1644

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was funded by the Spanish Ministry of Science and Innovation (projects AGL2004-05311, GEN2006-28560-E, and AGL2007-63625), and co-funded by the European Regional Development Fund. CC was supported by an I3P predoctoral fellowship from CSIC.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ana M. Casas.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 104 kb)

11032_2010_9497_MOESM2_ESM.doc

Supplementary material 2 Fig. S1 PCR amplification of the region harbouring the 5.2 kb intron 1 InDel using primer set HvBM5A.055F/056R (von Zitzewitz et al. 2005). SBCC058 and Plaisant are depicted.(DOC 42 kb)

11032_2010_9497_MOESM3_ESM.xls

Supplementary material 3 Fig. S2 BOPA1 genotypes of BC3F3 NILs of the cross SBCC058 × Plaisant. 1 (green, Plaisant allele); 2 (red, SBCC058 allele); 3 (orange, heterozygous SNP).(XLS 127 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Casao, M.C., Igartua, E., Karsai, I. et al. Introgression of an intermediate VRNH1 allele in barley (Hordeum vulgare L.) leads to reduced vernalization requirement without affecting freezing tolerance. Mol Breeding 28, 475–484 (2011). https://doi.org/10.1007/s11032-010-9497-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11032-010-9497-y

Keywords

Navigation