Skip to main content
SpringerLink
Log in

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

  • Original Paper
  • Published:
Molecular Genetics and Genomics Aims and scope Submit manuscript

Abstract

The epistatic interaction of alleles at the VRN-H1 and VRN-H2 loci determines vernalization sensitivity in barley. To validate the current molecular model for the two-locus epistasis, we crossed homozygous vernalization-insensitive plants harboring a predicted “winter type” allele at either VRN-H1 (Dicktoo) or VRN-H2 (Oregon Wolfe Barley Dominant), or at both VRN-H (Calicuchima-sib) loci and measured the flowering time of unvernalized F2 progeny under long-day photoperiod. We assessed whether the spring growth habit of Calicuchima-sib is an exception to the two-locus epistatic model or contains novel “spring” alleles at VRN-H1 (HvBM5A) and/or VRN-H2 (ZCCT-H) by determining allele sequence variants at these loci and their effects relative to growth habit. We found that (a) progeny with predicted “winter type” alleles at both VRN-H1 and VRN-H2 alleles exhibited an extremely delayed flowering (i.e. vernalization-sensitive) phenotype in two out of the three F2 populations, (b) sequence flanking the vernalization critical region of HvBM5A intron 1 likely influences degree of vernalization sensitivity, (c) a winter habit is retained when ZCCT-Ha has been deleted, and (d) the ZCCT-H genes have higher levels of allelic polymorphism than other winterhardiness regulatory genes. Our results validate the model explaining the epistatic interaction of VRN-H2 and VRN-H1 under long-day conditions, demonstrate recovery of vernalization-sensitive progeny from crosses of vernalization-insensitive genotypes, show that intron length variation in VRN-H1 may account for a continuum of vernalization sensitivity, and provide molecular markers that are accurate predictors of “winter vs spring type” alleles at the VRN-H loci.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Bastow R, Mylne JS, Lister C, Lippman Z, Martienssen RA, Dean C (2004) Vernalization requires epigenetic silencing of FLC by histone methylation. Nature 427:164–167

    Article  CAS  PubMed  Google Scholar 

  • Ben-Naim O, Eshed R, Parnis A, Teper-Bamnolker P, Shalit A, Coupland G, Samach A, Lifschitz E (2006) The CCAAT binding factor can mediate interactions between CONSTANS-like proteins and DNA. Plant J 46:462–476

    Article  CAS  PubMed  Google Scholar 

  • Danyluk J, Kane ND, Breton G, Limin AE, Fowler DB, Sarhan F (2003) TaVRT-1, a putative transcription factor associated with vegetative to reproductive transition in cereals. Plant Physiol 132:1849–1860

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Dubcovsky J, Lijavetzky D, Appendino L, Tranquilli G (1998) Comparative RFLP mapping of Triticum monococcum genes controlling vernalization requirement. Theor Appl Genet 97:968–975

    Article  CAS  Google Scholar 

  • Dubcovsky J, Loukoianov A, Fu D, Valarik M, Sanchez A, Yan L (2006) Effect of photoperiod on the regulation of wheat vernalization genes VRN1 and VRN2. Plant Mol Biol 60:469–480

    Article  CAS  PubMed  Google Scholar 

  • Fu D, Szűcs P, Yan L, 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 Genomics 273:54–65

    Article  CAS  PubMed  Google Scholar 

  • Griffiths S, Dunford RP, Coupland G, Laurie DA (2003) The evolution of CONSTANS-like gene families in barley, rice, and Arabidopsis. Plant Physiol 131:1855–1867

    Article  CAS  PubMed  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Hayes PM, Corey AE, Dovel R, Karow R, Mundt C, Rhinart K, Vivar H (2000) Registration of Orca barley. Crop Sci 40:849

    Article  Google Scholar 

  • Iwaki K, Haruna S, Niwa T, Kato K (2001) Adaptation and ecological differentiation in wheat with special reference to geographical variation of growth habit and Vrn genotype. Plant Breed 120:107–114

    Article  CAS  Google Scholar 

  • Kane NA, Danyluk J, Tardif G, Ouellet F, Laliberté J, Limin AE, Fowler DB, Sarhan F (2005) TaVRT-2, a member of the StMADS-11 clade of flowering repressors, is regulated by vernalization and photoperiod in wheat. Plant Physiol 138:2354–2363

    Article  CAS  PubMed  Google Scholar 

  • Karl BN, Hugh BN (1997) GeneDoc: a tool for editing and annotating multiple sequence alignments. (Distributed by the author)

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

    Article  Google Scholar 

  • Karsai I, Mészáros K, Láng L, Hayes PM, Bedő Z (2001) Multivariate analysis of traits determining adaptation in cultivated barley. Plant Breed 120:217–222

    Article  Google Scholar 

  • Karsai I, Mészáros K, Szűcs P, Hayes PM, Láng L, Bedő Z (2006) The influence of photoperiod on the Vrn-H2 locus (4H) which is a major determinant of plant development and reproductive fitness traits in a facultative × winter barley (Hordeum vulgare L.) mapping population. Plant Breed 125:468–472

    Article  CAS  Google Scholar 

  • Karsai I, Szűcs P, Mészáros K, Filichkina T, Hayes PM, Skinner JS, Láng L, Bedő 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  CAS  PubMed  Google Scholar 

  • Kooiker M, Airoldi CA, Losa A, Manzotti PS, Finzi L, Kater MM, Colombo L (2005) BASIC PENTACYSTEINE1, a GA binding protein that induces conformational changes in the regulatory region of the homeotic Arabidopsis gene SEEDSTICK. Plant Cell 17:722–729

    Article  CAS  PubMed  Google Scholar 

  • Kóti K, Karsai I, Szűcs P, Horváth C, Mészáros K, Kiss GB, Bedő Z, Hayes PM (2006) Validation of the two-gene epistatic model for vernalization response in a winter × spring barley cross. Euphytica 152:17–24

    Article  CAS  Google Scholar 

  • Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163

    Article  CAS  PubMed  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  CAS  PubMed  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 3 spring barley (Hordeum vulgare L.) cross. Genome 38:575–585

    CAS  PubMed  Google Scholar 

  • Loukoianov A, Yan L, Blechl A, Sanchez A, Dubcovsky J (2005) Regulation of VRN-1 vernalization genes in normal and transgenic polyploid wheat. Plant Physiol 138:2364–2373

    Article  CAS  PubMed  Google Scholar 

  • Michaels SD, Amasino RM (1999) Flowering locus C encodes a novel MADS domain protein that acts as a repressor of flowering. Plant Cell 11:949–956

    Article  CAS  PubMed  Google Scholar 

  • Murai K, Miyamae M, Kato H, Takumi S, Ogihara Y (2003) WAP1, a wheat APETALA1 homolog, plays a central role in the phase transition from vegetative to reproductive growth. Plant Cell Physiol 44:1255–1265

    Article  CAS  PubMed  Google Scholar 

  • Reinheimer JL, Barr AR, Eglinton JK (2004) QTL mapping of chromosomal regions conferring reproductive frost tolerance in barley (Hordeum vulgare L.). Theor Appl Genet 109:1267–1274

    Article  CAS  PubMed  Google Scholar 

  • Robson F, Costa MMR, Hepworth SR, Vizir I, Pineiro M, Reeves PH, Putterill J, Coupland G (2001) Functional importance of conserved domains in the flowering-time gene CONSTANS demonstrated by analysis of mutant alleles and transgenic plants. Plant J 28:619–631

    Article  CAS  PubMed  Google Scholar 

  • Schmitz J, Franzen R, Ngyuen TH, Garcia-Maroto F, Pozzi C, Salamini F, Rohde W (2000) Cloning, mapping and expression analysis of barley MADS-box genes. Plant Mol Biol 42:899–913

    Article  CAS  PubMed  Google Scholar 

  • Sheldon CC, Conn AB, Dennis ES, Peacock WJ (2002) Different regulatory regions are required for the vernalization-induced repression of FLOWERING LOCUS C and for the epigenetic maintenance of repression. Plant Cell 14:2527–2537

    Article  CAS  PubMed  Google Scholar 

  • Skinner JS, Szűcs 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  CAS  PubMed  Google Scholar 

  • 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 112:1277–1285

    Article  PubMed  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

  • Takatsuji H (1998) Zinc-finger transcription factors in plants. Cell Mol Life Sci 54:582–596

    Article  CAS  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 

  • Tranquilli GE, Dubcovsky J (2000) Epistatic interactions between vernalization genes Vrn-A m 1 and Vrn-A m 2 in diploid wheat. J Hered 91:304–306

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Trevaskis B, Hemming MN, Peacock WJ, Dennis ES (2006) HvVRN2 responds to daylength, whereas HvVRN1 is regulated by vernalization and developmental status. Plant Physiol 140:1397–1405

    Article  CAS  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 

  • Wolfe RI, Franckowiak JD (1991) Multiple dominant and recessive genetic marker stocks in spring barley. Barley Genet Newsl 20:117–121

    Google Scholar 

  • Yan L, Helguera M, Kato K, Fukuyama S, Sherman J, Dubcovsky J (2004a) Allelic variation at the VRN-1 promoter region in polyploid wheat. Theor Appl Genet 109:1677–1686

    Article  CAS  Google Scholar 

  • Yan L, Loukoianov A, Blechl A, Tranquilli G, Ramakrishna W, SanMiguel P, Bennetzen JL, Echenique V, Dubcovsky J (2004b) The wheat VRN2 gene is a flowering repressor down-regulated by vernalization. Science 303:1640–1644

    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  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We wish to thank Douglas L. Heckart, John L. Helgesson, and Lauren A. Osborn for their technical assistance. This work was supported by the National Science Foundation Plant Genome Research Program (DBI 0110124) and the United States Barley Genome Project.

Author information

Authors and Affiliations

  1. Department of Crop and Soil Science, Oregon State University, 253 Crop Science Building, Corvallis, OR, 97331, USA

    Péter Szűcs, Jeffrey S. Skinner, Kale G. Haggard, Ann E. Corey & Patrick M. Hayes

  2. Agricultural Research Institute of the Hungarian Academy of Sciences, 2462, Martonvásár, Hungary

    Péter Szűcs & Ildikó Karsai

  3. Department of Horticulture, Oregon State University, Corvallis, OR, 97331, USA

    Jeffrey S. Skinner & Tony H. H. Chen

  4. Department of Genetics and Plant Production, Aula Dei Experimental Station, CSIC, 50080, Zaragoza, Spain

    Alfonso Cuesta-Marcos

Authors
  1. Péter Szűcs
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jeffrey S. Skinner
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ildikó Karsai
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Alfonso Cuesta-Marcos
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Kale G. Haggard
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Ann E. Corey
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Tony H. H. Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Patrick M. Hayes
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Patrick M. Hayes.

Additional information

Communicated by S. Hohmann.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Szűcs, P., Skinner, J.S., Karsai, I. et al. 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 (2007). https://doi.org/10.1007/s00438-006-0195-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00438-006-0195-8

Keywords

Search

Navigation