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The expression of several Cbf genes at the Fr-A2 locus is linked to frost resistance in wheat

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Abstract

The C-repeat binding factor (Cbf) gene family has been shown to have a critical role in the regulation of low-temperature stress response in Arabidopsis. In Triticum monococcum, a locus carrying a family of Cbf-like genes, orthologs of Arabidopsis Cbf genes, is tightly linked to the frost tolerance locus Fr-A m 2, representing candidates for the differences in frost tolerance mapped at this locus. In this work we show that several Cbf genes have dramatically different levels of induction after cold exposure in hexaploid wheat. The Cbf-transcription levels differ between substitution and single chromosome recombinant lines carrying different 5A chromosomes or chromosome segments of the chromosome 5A from frost-tolerant and frost-sensitive wheat varieties. When the expression of eight Cbf genes, previously mapped at the Fr-A2 locus was investigated with gene specific primers using real-time RT-PCR, three Cbf sequences (Cbf1A, Cbf1C, Cbf7) showed a significantly higher relative transcription level (more than fourfold change) in lines differing for the Fr-A2 region. Differences in Cbf expression were also associated with a variation in frost tolerance. These results suggest that the amount of some Cbf mRNAs might be a critical factor for determining the level of frost tolerance in wheat.

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References

  • Baldi P, Vale G, Mazzucotelli E, Govoni C, Faccioli P, Stanca AM, Cattivelli L (2001) The transcripts of several components of the protein synthesis machinery are cold-regulated in a chloroplast-dependent manner in barley and wheat. J Plant Physiol 158:1541–1546

    Article  CAS  Google Scholar 

  • Chinnusamy V, Ohta M, Kanrar S, Lee BH, Hong XH, 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 D-W, Rodriguez EM, Close TJ (2002) Barley Cbf3 gene identification, expression pattern, and map location. Plant Physiol 129:1–7

    Article  Google Scholar 

  • Cook D, Fowler S, Fiehn O, Thomashow MF (2004) A prominent role for the CBF cold response pathway in configuring the low-temperature metabolome of Arabidopsis. Proc Natl Acad Sci USA 101:15243–15248

    Article  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 

  • 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 

  • 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 

  • Galiba G, Quarrie SA, Sutka J, Morgounov A (1995) RFLP mapping of the vernalization (Vrn) 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, Sebolt AM, Salazar MP, Everard JD, Thomashow MF (2000) Overexpression of the Arabidopsis CBF3 trascriptional activator mimics multiple biochemical changes associated with cold acclimation. Plant Physiol 124:1854–1865

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Guo Y, Xiong LM, Ishitani M, Zhu JK (2002) An Arabidopsis mutation in translation elongation factor 2 causes superinduction of CBF/DREB1 transcription factor genes but blocks the induction of their downstream targets under low temperatures. Proc Natl Acad Sci USA 99:7786–7791

    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 

  • 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 

  • McIntosh RA, Devos KM, Dubcovsky J, Rogers WJ (2004) Catalogue of gene symbols for wheat: 2004 supplement. Wheat Information Service (in press). http://wheat.pw.usda.gov/ggpages/awn/50/Textfiles/WGC.html

  • Medina J, Bargues M, Terol J, Perez-Alonso M, Salinas J (1999) The Arabidopsis CBF gene family is composed of three genes encoding AP2 domain-containing proteins whose expression is regulated by low temperature but not by abscisic acid or dehydration. Plant Physiol 119:463–469

    Article  PubMed  CAS  Google Scholar 

  • Miller AK, Galiba G, Dubcovsky J (2005) A cluster of eleven Cbf transcription factors is located at the frost tolerance locus Fr-A m 2 in Triticum monococcum. MGG (in press)

  • Nagy Z, Galiba G (1995) Drought and salt tolerance are not necessarily linked: a study on wheat varieties differing in drought tolerance under consecutive water and salinity stresses. J Plant Physiol 145:168–174

    CAS  Google Scholar 

  • 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 Breed 14:153–170

    Article  CAS  Google Scholar 

  • Shen YG, Zhang WK, He SJ, Zhang JS, Liu Q, Chen SY (2003) An EREBP/AP2-type protein in Triticum aestivum was a DRE-binding transcription factor induced by cold, dehydration and ABA stress. Theor Appl Genet 106:923–930

    PubMed  CAS  Google Scholar 

  • Shinozaki K, Yamaguchi-Shinozaki K, Seki M (2003) Regulatory network of gene expression in the drought and cold stress responses. Curr Opin Plant Biol 6:410–417

    Article  PubMed  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 Natl Acad Sci USA 94:1035–1040

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Thomashow MF, Gilmour SJ, Stockinger EJ, Jaglo-Ottosen KR, Zarka DG (2001) Role of the Arabidopsis CBF transcriptional activators in cold acclimation. Physiol Plant 112:171–175

    Article  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 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 

  • Veisz O, Sutka J (1989) The relationships of hardening period and the expression of frost resistance in chromosome substitution lines of wheat. Euphytica 43:41–45

    Article  Google Scholar 

  • Vogel JT, Zarka DG, Van Buskirk HA, Fowler SG, Thomashow MF (2005) Roles of the CBF2 and ZAT12 transcription factors in configuring the low temperature transcriptome of Arabidopsis. Plant J 41:195–211

    Article  PubMed  CAS  Google Scholar 

  • Xue GP (2002) An AP2 domain transcription factor HvCBF1 activates expression of cold-responsive genes in barley through interaction with a (G/a)(C/t)CGAC motif. Biochim Biophys Acta 1577:63–72

    PubMed  CAS  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 

  • Zarka DG, Vogel JT, Cook D, Thomashow MF (2003) Cold induction of Arabidopsis Cbf genes involves multiple ice (inducer of Cbf expression) promoter elements and a cold-regulatory circuit that is desensitized by low temperature. Plant Physiol 133:910–918

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

This work was supported by the Italian Ministry of Agriculture (Project FRUMISIS), by Italian Ministry of Education (FIRB program N RBNE01LACT-plant-stress), by the National Research Council of Italy (CNR-MTA bilateral project) by the Hungarian National Research Fund Nos. T046573, by the Hungarian Wheat Spike Consortia NKFP 406404 and by the National Research Initiative of the USDA Cooperative State Research, Education and Extension Service, grant number 2004-41783.

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Author notes

  1. Alessio Aprile

    Present address: Department of Biological and Environmental Sciences, University of Lecce, 73100, Lecce, Italy

Authors and Affiliations

  1. Agricultural Research Institute of the Hungarian Academy of Sciences, 2462, Martonvasar, Hungary

    Attila Vágújfalvi & Gábor Galiba

  2. CRA- Experimental Institute for Cereal Research, 29017, Fiorenzuola d’Arda, Italy

    Alessio Aprile, Giovanni Delugu & Luigi Cattivelli

  3. Department of Agronomy& Range Science, University of California, Davis, CA, 95616, USA

    Andrea Miller & Jorge Dubcovsky

Authors
  1. Attila Vágújfalvi
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  2. Alessio Aprile
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  3. Andrea Miller
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  4. Jorge Dubcovsky
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  5. Giovanni Delugu
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  6. Gábor Galiba
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  7. Luigi Cattivelli
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Corresponding author

Correspondence to Luigi Cattivelli.

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Communicated by R. Hagemann

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Vágújfalvi, A., Aprile, A., Miller, A. et al. The expression of several Cbf genes at the Fr-A2 locus is linked to frost resistance in wheat. Mol Genet Genomics 274, 506–514 (2005). https://doi.org/10.1007/s00438-005-0047-y

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  • DOI: https://doi.org/10.1007/s00438-005-0047-y

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