Large deletions in the CBF gene cluster at the Fr-B2 locus are associated with reduced frost tolerance in wheat
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Wheat plants which are exposed to periods of low temperatures (cold acclimation) exhibit increased survival rates when they are subsequently exposed to freezing temperatures. This process is associated with large-scale changes in the transcriptome which are modulated by a set of tandemly duplicated C-repeat Binding Factor (CBF) transcription factors located at the Frost Resistance-2 (Fr-2) locus. While Arabidopsis has three tandemly duplicated CBF genes, the CBF family in wheat has undergone an expansion and at least 15 CBF genes have been identified, 11 of which are present at the Fr-2 loci on homeologous group 5 chromosomes. We report here the discovery of three large deletions which eliminate 6, 9, and all 11 CBF genes from the Fr-B2 locus in tetraploid and hexaploid wheat. In wild emmer wheat, the Fr-B2 deletions were found only among the accessions from the southern sub-populations. Among cultivated wheats, the Fr-B2 deletions were more common among varieties with a spring growth habit than among those with a winter growth habit. Replicated freezing tolerance experiments showed that both the deletion of nine CBF genes in tetraploid wheat and the complete Fr-B2 deletion in hexaploid wheat were associated with significant reductions in survival after exposure to freezing temperatures. Our results suggest that selection for the wild-type Fr-B2 allele may be beneficial for breeders selecting for varieties with improved frost tolerance.
KeywordsCold Acclimation Wheat Variety Hexaploid Wheat Freezing Tolerance Tetraploid Wheat
This project was supported by the National Research Initiative grants number 2008-35100-04562 and 2011-68002-30029 from the USDA National Institute of Food and Agriculture and by the Howard Hughes Medical Institute and the Gordon and Betty Moore Foundation. Dr. Gábor Galiba’s group acknowledges support from the Hungarian Research Fund ‘OTKA’ No K75528 and CNK80781 and from the National Development Agency (TÁMOP-4.2.2/B-10/1-2010-0025, University of Pannonia).
- Akhunov ED, Akhunova AR, Anderson OD, Anderson JA, Blake N, Clegg MT, Coleman-Derr D, Conley EJ, Crossman CC, Deal KR, Dubcovsky J, Gill BS, Gu YQ, Hadam J, Heo H, Huo N, Lazo GR, Luo M-C, Ma YQ, Matthews DE, McGuire PE, Morrell PL, Qualset CO, Renfro J, Tabanao D, Talbert LE, Tian C, Toleno DM, Warburton ML, You FM, Zhang W, Dvorak J (2010) Nucleotide diversity maps reveal variation in diversity among wheat genomes and chromosomes. BMC Genom 11:702CrossRefGoogle Scholar
- Krasileva KV, Buffalo V, Bailey P, Pearce S, Soria M, Tabbita F, Uauy C, Consortium IWGS, Dubcovsky J (2013) Separating homeologs by phasing in the tetraploid wheat transcriptome. Genome Biology 14:R66. doi: 10.1186/gb-2013-14-6-r66
- 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 10:1391–1406PubMedGoogle Scholar
- McIntosh R, Devos K, Dubcovsky J, Rogers W (2004) Catalogue of gene symbols for wheatGoogle Scholar
- 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 119:463–469PubMedCrossRefGoogle Scholar
- Mujeeb-Kazi A, Gilchrist LI, Villareal RL, Delgado R (2000) Registration of ten wheat germplasm lines resistant to Septoria tritici leaf blotch. Crop Sci 40:590–591Google Scholar
- Snape JW, Semikhodskii A, Fish L, Sarma RN, Quarrie SA, Galiba G, Sutka J (1997) Mapping frost tolerance loci in wheat and comparative mapping with other cereals. Acta Agron Hung 45:265–270Google 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 94:1035–1040PubMedCrossRefGoogle 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 Genom 269:60–67Google Scholar
- Zhu J, Pearce S, Burke A, See DR, Skinner DZ, Dubcovsky J, Garland-Campbell K (2013) Copy number variation at VRN-A1 and central Fr-A2 loci are associated with frost tolerance in hexaploid wheat (submitted)Google Scholar