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Large deletions in the CBF gene cluster at the Fr-B2 locus are associated with reduced frost tolerance in wheat

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Abstract

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.

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References

  • Achard P, Gong F, Cheminant S, Alioua M, Hedden P, Genschik P (2008) The cold-inducible CBF1 factor-dependent signaling pathway modulates the accumulation of the growth-repressing DELLA proteins via its effect on gibberellin metabolism. Plant Cell 20:2117–2129

    Article  PubMed  CAS  Google Scholar 

  • 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 11:702

    Article  CAS  Google Scholar 

  • Badawi M, Danyluk J, Boucho B, Houde M, Sarhan F (2007) The CBF gene family in hexaploid wheat and its relationship to the phylogenetic complexity of cereal CBFs. Mol Genet Genom 277:533–554

    Article  CAS  Google Scholar 

  • Båga M, Chodaparambil SV, Limin AE, Pecar M, Fowler DB, Chibbar RN (2007) Identification of quantitative trait loci and associated candidate genes for low-temperature tolerance in cold-hardy winter wheat. Funct Integr Genom 7:53–68

    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 153:1846–1858

    Article  PubMed  CAS  Google Scholar 

  • Dubcovsky J, Dvorak J (2007) Genome plasticity a key factor in the success of polyploid wheat under domestication. Science 316:1862–1866

    Article  PubMed  CAS  Google Scholar 

  • Fowler DB, Limin AE (2004) Interactions among factors regulating phenological development and acclimation rate determine low-temperature tolerance in wheat. Ann Bot 94:717–724

    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, Barabaschi D, Tondelli A, Laido 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 

  • Fu DL, Szucs P, Yan LL, 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 Genom 273:54–65

    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. Plant Mol Biol 54:767–781

    Article  PubMed  CAS  Google Scholar 

  • Jaglo-Ottosen KR, Gilmour SJ, Zarka DG, Schabenberger O, Thomashow MF (1998) Arabidopsis CBF1 overexpression induces COR genes and enhances freezing tolerance. Science 280:104–106

    Article  PubMed  CAS  Google Scholar 

  • Knox AK, Li C, Vágújfalvi A, Galilba G, Stockinger EJ, Dubcovsky J (2008) Identification of candidate CBF genes for the frost tolerance locus Fr-A m 2 in Triticum monococcum. Plant Mol Biol 67:257–270

    Article  PubMed  CAS  Google Scholar 

  • Knox AK, Dhillon T, Cheng H, Tondelli A, Pecchioni N, Stockinger EJ (2010) CBF gene copy number variation at Frost Resistance-2 is associated with levels of freezing tolerance in temperate-climate cereals. Theor Appl Genet 121:21–35

    Article  PubMed  Google Scholar 

  • Kocsy G, Athmer B, Perovic D, Himmelbach A, Szűcs A, Vashegyi I, Schweizer P, Galiba G, Stein N (2010) Regulation of gene expression by chromosome 5A during cold hardening in wheat. Mol Genet Genom 283:351–363

    Article  CAS  Google 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 10:1391–1406

    PubMed  CAS  Google Scholar 

  • Luo MC, Yang ZL, You FM, Kawahara T, Waines JG, Dvorak J (2007) The structure of wild and domesticated emmer wheat populations, gene flow between them, and the site of emmer domestication. Theor Appl Genet 114:947–959

    Article  PubMed  Google Scholar 

  • McIntosh R, Devos K, Dubcovsky J, Rogers W (2004) Catalogue of gene symbols for wheat

  • 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 (2006) A cluster of 11 CBF transcription factors is located at the frost tolerance locus Fr-A m 2 in Triticum monococcum. Mol Genet Genom 275:193–203

    Article  CAS  Google 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 40:590–591

    Google Scholar 

  • Nevo E, Beiles A (1989) Genetic diversity of wild emmer wheat in Israel and Turkey—structure, evolution and applications in breeding. Theor Appl Genet 77:421–455

    Article  Google Scholar 

  • Ozkan H, Brandolini A, Schafer-Pregl R, Salamini F (2002) AFLP analysis of a collection of tetraploid wheats indicates the origin of emmer and hard wheat domestication in southeast Turkey. Mol Biol Evol 19:1797–1801

    Article  PubMed  CAS  Google Scholar 

  • Peleg Z, Fahima T, Abbo S, Krugman T, Nevo E, Yakir D, Saranga Y (2005) Genetic diversity for drought resistance in wild emmer wheat and its ecogeographical associations. Plant Cell Environ 28:176–191

    Article  Google Scholar 

  • Sandve SR, Fjellheim S (2010) Did gene family expansions during the Eocene–Oligocene boundary climate cooling play a role in Pooideae adaptation to cool climates? Mol Ecol 19:2075–2088

    Article  PubMed  CAS  Google Scholar 

  • Skinner JS, von Zitzewitz J, Szucs 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 Biol 59:533–551

    Article  PubMed  CAS  Google 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 45:265–270

    Google Scholar 

  • Sorrells ME, Gustafson JP, Somers D, Chao S, Benscher D, Guedira-Brown G, Huttner E, Kilian A, McGuire PE, Ross K, Tanaka J, Wenzl P, Williams K, Qualset CO (2011) Reconstruction of the Synthetic W7984 × Opata M85 wheat reference population. Genome 54:875–882

    Article  PubMed  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 (1981) Genetic studies of frost resistance in wheat. Theor Appl Genet 59:145–152

    Article  Google Scholar 

  • Thomashow MF (2010) Molecular basis of plant cold acclimation: insights gained from studying the CBF cold response pathway. Plant Physiol 154:571–577

    Article  PubMed  CAS  Google Scholar 

  • Toth B, Galiba G, Feher 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  CAS  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 Genet Genom 269:60–67

    Google Scholar 

  • Vágújfalvi A, Aprile A, Miller A, 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 Genet Genom 274:506–514

    Article  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 

  • Warburton ML, Crossa J, Franco J, Kazi M, Trethowan R, Rajaram S, Pfeiffer W, Zhang P, Dreisigacker S, van Ginkel M (2006) Bringing wild relatives back into the family: recovering genetic diversity in CIMMYT improved wheat germplasm. Euphytica 149:289–301

    Article  CAS  Google Scholar 

  • Wilhelm EP, Turner AS, Laurie DA (2009) Photoperiod insensitive Ppd-A1a mutations in tetraploid wheat (Triticum durum Desf.). Theor Appl Genet 118:285–294

    Article  PubMed  CAS  Google Scholar 

  • Winfield MO, Lu C, Wilson ID, Coghill JA, Edwards KJ (2010) Plant responses to cold: transcriptome analysis of wheat. Plant Biotechnol J 8:749–771

    Article  PubMed  CAS  Google Scholar 

  • Yan L, Fu D, Li C, Blechl A, Tranquilli G, Bonafede M, Sanchez A, Valarik M, Yasuda S, Dubcovsky J (2006) The wheat and barley vernalization gene VRN3 is an orthologue of FT. Proc Natl Acad Sci USA 103:19581–19586

    Article  PubMed  CAS  Google 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)

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Acknowledgments

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).

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Correspondence to Jorge Dubcovsky.

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Communicated by H.-C. Jing.

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Pearce, S., Zhu, J., Boldizsár, Á. et al. Large deletions in the CBF gene cluster at the Fr-B2 locus are associated with reduced frost tolerance in wheat. Theor Appl Genet 126, 2683–2697 (2013). https://doi.org/10.1007/s00122-013-2165-y

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  • DOI: https://doi.org/10.1007/s00122-013-2165-y

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