Skip to main content
SpringerLink
Log in

A cluster of 11 CBF transcription factors is located at the frost tolerance locus Fr-A m 2 in Triticum monococcum

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

Abstract

Due to the adverse effects of cold temperatures on winter wheat, frost tolerance is an important trait for breeding programs in regions with severe winters. Frost tolerance locus Fr-A m 2 was recently discovered in diploid wheat (Triticum monococcum L.). This locus was mapped as a QTL on chromosome 5Am in the same region as a QTL for the level of transcription of the cold-regulated gene COR14b at 15°C. A CBF transcription factor was mapped in the center of these two overlapping QTLs. However, since the CBF gene family in wheat has numerous members, it was possible that multiple CBF genes were present at Fr-A m 2. To investigate this possibility we initiated a systematic characterization of the CBF family in T. monococcum. Here we report the molecular characterization of thirteen TmCBF genes. Nine of them were numbered according to the closest barley HvCBF gene, and the other four that have no clear barley orthologues were assigned numbers TmCBF15 to TmCBF18. TmCBF5 and TmCBF18 were mapped on T. monococcum chromosomes 7Am and 6Am, respectively, and are thus not candidates for the Fr-A m 2 gene. The remaining eleven TmCBF genes are clustered at the Fr-A m 2 locus within five different Bacterial Artificial Chromosome (BAC) clones. These BACs were mapped using a high-density map and recombination events were found between most BACs. Lines carrying these recombination events will be useful to identify which of the CBF genes is responsible for the differences in frost tolerance between the T. monococcum parental lines at the Fr-A m 2 locus.

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

Similar content being viewed by others

References

  • Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  PubMed  CAS  Google Scholar 

  • Chinnusamy V, Ohta M, Kanrar S, Lee BH, Hong X, Agarwal M, Zhu JK (2003) ICE1: a regulator of cold-induced transcriptome and freezing tolerance in Arabidopsis. Genes Dev 17:1043–1054

    Article  PubMed  CAS  Google Scholar 

  • Choi DW, Rodriguez EM, Close TJ (2002) Barley Cbf3 gene identification, expression pattern and map location. Plant Physiol 129:1781–1787

    Article  PubMed  CAS  Google Scholar 

  • Crosatti C, Polverino de Laureto P, Bassi R, Cattivelli L (1999) The interaction between cold and light controls the expression of the cold-regulated barley gene cor14b and the accumulation of the corresponding protein. Plant Physiol 119:671–680

    Article  PubMed  CAS  Google Scholar 

  • Danyluk J, Kane NA, 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  PubMed  CAS  Google Scholar 

  • Doll H, Haahr V, Sogaard B (1989) Relationship between vernalization requirement and winter hardiness in doubled haploids of barley. Euphytica 42:209–213

    Google Scholar 

  • Dubcovsky J, Lou MC, Dvorak J (1995) Linkage relationships among stress-induced genes in wheat. Theor Appl Genet 91:795–801

    Article  CAS  Google Scholar 

  • Dubcovsky J, Luo MC, Zhong GY, Bransteiter R, Desai A, Kilian A, Kleinhofs A, Dvorak J (1996) Genetic map of diploid wheat, Triticum monococcum L., and its comparison with maps of Hordeum vulgare L. Genetics 143:983–999

    PubMed  CAS  Google Scholar 

  • Dubcovsky J, Lijavetsky 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, Ramakrishna W, SanMiguel PJ, Busso CS, Yan L, Shiloff BA, Bennetzen JL (2001) Comparative sequence analysis of colinear barley and rice bacterial artificial chromosomes. Plant Physiol 125:1342–1353

    Article  PubMed  CAS  Google Scholar 

  • Dubouzet JG, Sakuma Y, Ito Y, Kasuga M, Dubouzet EG, Miura S, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) OsDREB genes in rice, Oryza sativa L., encode transcription activators that function in drought-, high-salt- and cold-responsive gene expression. Plant J 33:751–763

    Article  PubMed  CAS  Google Scholar 

  • Ewing B, Green P (1998) Base-calling of automated sequencer traces using PHRED: II. Error probabilities. Genome Res 8:186–194

    PubMed  CAS  Google Scholar 

  • Feinberg AP, Vogelstein P (1983) A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem 132:6–13

    Article  PubMed  CAS  Google Scholar 

  • 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) x ‘Tremois’ (spring) barley map. Theor Appl Genet 108:670–680

    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 

  • 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 

  • Gilmour SJ, Zarka DG, Stockinger EJ, Salazar MP, Houghton JM, Thomashow MF (1998) Low temperature regulation of the Arabidopsis CBF family of AP2 transcriptional activators as an early step in cold-induced COR gene expression. Plant J 16:433–442

    Article  PubMed  CAS  Google Scholar 

  • Gilmour SJ, Fowler SG, Thomashow MF (2004) Arabidopsis transcriptional activators CBF1, CBF2, and CBF3 have matching functional activities. Pl Mol Biol 54:767–781

    Article  CAS  Google Scholar 

  • Gordon D, Abajian C, Green P (1998) CONSED: a graphical tool for sequencing finishing. Genome Res 8:195–202

    PubMed  CAS  Google Scholar 

  • Hayes PM, Chen FQ, Corey A, Pan A, Chen THH, Baird E, Powell W, Thomas W, Waugh R, Bedo Z, Karsai I, Blake T, Oberthur L (1997) The Dicktoo × Morex population: a model for dissecting components of winterhardiness in barley. In: Li PH, Chen THH (eds) Plant cold hardiness. Plenum Press, New York, pp 77–87

    Google Scholar 

  • Hossain KG, Kalavacharla V, Lazo GR, Hegstad J, Wentz MJ, Kianian PM, Simons K, Gehlhar S, Rust JL, Syamala RR, Obeori K, Bhamidimarri S, Karunadharma P, Chao S, Anderson OD, Qi LL, Echalier B, Gill BS, Linkiewicz AM, Ratnasiri A, Dubcovsky J, Akhunov ED, Dvorák J, Miftahudin, Ross K, Gustafson JP, Radhawa HS, Dilbirligi M, Gill KS, Peng JH, Lapitan NL, Greene RA, Bermudez-Kandianis CE, Sorrells ME, Feril O, Pathan MS, Nguyen HT, Gonzalez-Hernandez JL, Conley EJ, Anderson JA, Choi DW, Fenton D, Close TJ, McGuire PE, Qualset CO, Kianian SF (2004) A chromosome bin map of 2148 expressed sequence tag loci of wheat homoeologous group 7. Genetics 168:687–699

    Article  PubMed  CAS  Google Scholar 

  • Jaglo KR, Kleff S, Amundsen KL, Zhang X, Haake V, Zhang JZ, Deits T, Thomashow MF (2001) Components of the Arabidopsis C-repeat/dehydration-responsive element binding factor cold-response pathway are conserved in Brassica napus and other plant species. Plant Physiol 127:910–917

    Article  PubMed  CAS  Google Scholar 

  • Kobayashi F, Takumi S, Kume S, Ishibashi M, Ohno R, Murai K, Nakamura C (2005) Regulation by Vrn-1/Fr-1 chromosomal intervals of CBF-mediated Cor/Lea gene expression and freezing tolerance in common wheat. J Exp Bot 56:887–895

    Article  PubMed  Google Scholar 

  • Kumar S, Tamura K, Jakobsen I, Nei M (2001) MEGA2: molecular evolutionary genetics analysis software. Bioinformatics 17:1244–1245

    Article  PubMed  CAS  Google Scholar 

  • Law C, Worland A, Giorgi B (1976) The genetic control of ear-emergence time by chromosomes 5A and 5D of wheat. Heredity 36:49–58

    Google Scholar 

  • Lijavetzky D, Muzzi G, Wicker T, Keller B, Wing R, Dubcovsky J (1999) Construction and characterization of a bacterial artificial chromosome (BAC) library for the A genome of wheat. Genome 42:1176–1182

    Article  PubMed  CAS  Google Scholar 

  • Linkiewicz AM, Qi LL, Gill BS, Echalier B, Chao S, Lazo GR, Hummel DD, Anderson OD, Akhunov ED, Dvorak J, Pathan MS, Nguyen HT, Peng JH, Lapitan NL, Miftahudin, Gustafson JP, La Rota CM, Sorrells ME, Hossain KG, Kalavacharla V, Kianian SF, Sandhu D, Bondareva SN, Gill KS, Conley EJ, Anderson JA, Fenton RD, Close TJ, McGuire PE, Qualset CO, Dubcovsky J (2004) A 2500-loci bin map of wheat homoeologous group 5 provides insights on gene distribution and colinearity with rice. Genetics 168:665–676

    Article  PubMed  CAS  Google Scholar 

  • Liu Q, Kasuga M, Sakuma Y, Abe H, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (1998) Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought- and low-temperature-responsive gene expression, respectively, in Arabidopsis. Plant Cell 10:1391–1406

    Article  PubMed  CAS  Google Scholar 

  • McIntosh RA, Devos KM, Dubcovsky J, Rogers WJ (2004) Catalogue of gene symbols for wheat: 2004 supplement. Wheat Information Service. http://wheat.pw.usda.gov/ggpages/wgc/2004upd.html

  • Miller AK (2005) Characterization of the CBF family of transcription factors in diploid wheat. MS Thesis, University of California, Davis, CA, 57pp

  • Roberts D (1990) Identification of a locus on chromosome-5A of wheat involved in control of cold hardiness, vernalization, leaf length, rosette growth habit, and height of hardened plants. Genome 33:247–259

    Google Scholar 

  • Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. In: Krawetz S, Misener S (eds) Bioinformatics methods and protocols: methods in molecular biology. Humana Press, Totowa, NJ, pp 365–386

    Google Scholar 

  • Sakai A, Larcher V (1985) Frost survival of plants. Responses and adaptation to freezing stress. Ecological studies, vol 62. Springer-Verlag. Berlin, Heidelberg, New York

  • Shinwari Z, Nakashima K, Miura S, Kasuga M, Seki M, Yamaguchi-Shinozaki K, Shinozaki K (1998) An Arabidopsis gene family encoding DRE/CRT binding proteins involved in low-temperature-responsive gene expression. Biochem Biophys Res Comm 250:161–170

    Article  PubMed  CAS  Google Scholar 

  • 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 Bio 59:533–551

    Article  CAS  Google Scholar 

  • Snape JW, Sarma RN, Quarrie SA, Fish LJ, Galiba G, Sutka J (2001) Mapping genes for flowering time and frost tolerance in cereals using precise genetic stocks. Euphytica 120:309–315

    Article  CAS  Google Scholar 

  • Stockinger EJ, Gilmour SJ, Thomashow MF (1997) Arabidopsis thaliana CBF1 encodes an AP2 domain-containing transcriptional activator that binds to the C-repeat/DRE, a cis-acting DNA regulatory element that stimulates transcription in response to low temperature and water deficit. Proc Nat Acad Sci USA 94:1035–1040

    Article  PubMed  CAS  Google Scholar 

  • Sutka J, Snape JW (1989) Location of a gene for frost resistance on chromosome 5A of wheat. Euphytica 42:41–44

    Article  Google Scholar 

  • Sutka J (1994) Genetic control of frost resistance in wheat (Triticum aestivum L.). Euphytica 77:277–282

    Article  Google Scholar 

  • Sutka J, Galiba G, Vágújfalvi A, Gill BS, Snape JW (1999) Physical mapping of the VRN-A1 and Fr1 genes on chromosome 5A of wheat using deletion lines. Theor Appl Genet 99:199–202

    Article  CAS  Google Scholar 

  • Thomashow MF (2001) So what’s new in the field of plant cold acclimation? Lots! Plant Physiol 125:89–93

    Article  CAS  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucl Acids Res 22:4673–4680

    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 

  • 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 

  • 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 Gen Genomics 269:60–67

    Google Scholar 

  • Vágújfalvi A, Aprile A, Miller AK, Dubcovsky J, Delugu G, Galiba G, Cattivelli L (2005) The expression of several Cbf genes at the Fr-A2 locus is linked to frost resistance in wheat. Mol Gen Genomics 274:506–514

    Article  CAS  Google Scholar 

  • Vogel JT, Zarka DG, Van Buskirk HA, Fowler SG, Thomashow MF (2005) Roles of CBF2 and ZAT12 transcription factors in configuring the low temperature transcriptome of Arabidopsis. Plant J 41:196–211

    Article  CAS  Google Scholar 

  • Wang Y, Ribot C, Rezzonico E, Poirier Y (2004) Structure and expression profile of the Arabidopsis PHO1 gene family indicates a broad role in inorganic phosphate homeostasis. Plant Physiol 135:400–411

    Article  PubMed  CAS  Google Scholar 

  • Wang Z, Triezenberg SJ, Thomashow MF, Stockinger EJ (2005) Multiple hydrophobic motifs in Arabidopsis CBF1 COOH-terminus provide functional redundancy in trans-activation. Plant Mol Biol 58:543–559

    Article  PubMed  CAS  Google Scholar 

  • Xue GP (2002) Characterisation of the DNA-binding profile of barley HvCBF1 using an enzymatic method for rapid, quantitative and high-throughput analysis of the DNA-binding activity. Nucl Acids Res 30:e77

    Article  PubMed  Google Scholar 

  • Xue GP (2003) The DNA-binding activity of an AP2 transcriptional activator HvCBF2 involved in regulation of low-temperature responsive genes in barley is modulated by temperature. Plant J 33:373–383

    Article  PubMed  CAS  Google Scholar 

  • Yan L, Loukoianov A, Tranquilli G, Helguera M, Fahima T, Dubcovsky J (2003) Positional cloning of wheat vernalization gene Vrn1. Proc Natl Acad Sci USA 100:6263–6268

    Article  PubMed  CAS  Google Scholar 

  • Yan L, Loukoianov A, Blechl A, Tranquilli G, Ramakrishna W, SanMiguel PJ, 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

Acknowledgment

The project was supported by the National Research Initiative of the USDA Cooperative State Research, Education and Extension Service, grant number 2004-01783, NSF-Plant Genome grant DBI-0321462, and by the Hungarian Wheat Spike Consortia NKFP 406404.

Author information

Author notes

  1. Andrea K. Miller

    Present address: Department of Horticulture and Crop Science, The Ohio State University/OARDC, Wooster, OH, 44261, USA

  2. Gabor Galiba

    Present address: Agricultural Research Institute of the Hungarian Academy of Sciences, 2462, Martonvásár, Hungary

Authors and Affiliations

  1. Department of Plant Sciences, University of California, Davis, CA, 95616, USA

    Andrea K. Miller, Gabor Galiba & Jorge Dubcovsky

Authors
  1. Andrea K. Miller
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Gabor Galiba
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jorge Dubcovsky
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jorge Dubcovsky.

Additional information

Communicated by R. Hagemann

ACCESSION NUMBERS: Sequence data for the T. monococcum CBF genes is recorded in GenBank under accession numbers AY951944, AY951945, AY951946, AY951947, AY951948, AY951949, AY951950, and AY951951.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Miller, A.K., Galiba, G. & Dubcovsky, J. A cluster of 11 CBF transcription factors is located at the frost tolerance locus Fr-A m 2 in Triticum monococcum . Mol Genet Genomics 275, 193–203 (2006). https://doi.org/10.1007/s00438-005-0076-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00438-005-0076-6

Keywords

Search

Navigation