Skip to main content
Log in

The unified ICE–CBF pathway provides a transcriptional feedback control of freezing tolerance during cold acclimation in Arabidopsis

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

During cold acclimation, C-repeat binding factors (CBFs) activate downstream targets, such as cold-regulated genes, leading to the acquisition of freezing tolerance in plants. Inducer of CBF expression 1 (ICE1) plays a key role by activating CBF3 expression in shaping the cold-induced transcriptome. While the ICE1–CBF3 regulon constitutes a major cold acclimation pathway, gene regulatory networks governing the CBF signaling are poorly understood. Here, we demonstrated that ICE1 and its paralog ICE2 induce CBF1, CBF2, and CBF3 by binding to the gene promoters. ICE2, like ICE1, was ubiquitinated by the high expression of osmotically responsive gene 1 (HOS1) E3 ubiquitin ligase. Whereas ICE2-defective ice2-2 mutant did not exhibit any discernible freezing-sensitive phenotypes, ice1-2 ice2-2/+ plant, which is defective in ICE1 and has a heterozygotic ice2 mutation, exhibited significantly reduced freezing tolerance. Accordingly, all three CBF genes were markedly down-regulated in the ice1-2 ice2-2/+ plant, indicating that ICE1 and ICE2 are functionally redundant with different implementations in inducing CBF genes. Together with the negative regulation of CBF3 by CBF2, we propose that the unified ICE–CBF pathway provides a transcriptional feedback of freezing tolerance to sustain plant development and survival during cold acclimation.

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

Access this article

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
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Agarwal M, Hao Y, Kapoor A, Dong CH, Fujii H, Zheng X, Zhu JK (2006) A R2R3 type MYB transcription factor is involved in the cold regulation of CBF genes and in acquired freezing tolerance. J Biol Chem 281:37636–37645

    Article  CAS  PubMed  Google Scholar 

  • Akhtar M, Jaiswal A, Taj G, Jaiswal JP, Qureshi MI, Singh NK (2012) DREB1/CBF transcription factors: their structure, function and role in abiotic stress tolerance in plants. J Genet 91:385–395

    Article  CAS  PubMed  Google Scholar 

  • Bond DM, Dennis ES, Finnegan EJ (2011) The low temperature response pathways for cold acclimation and vernalization are independent. Plant, Cell Environ 34:1737–1748

    Article  CAS  Google Scholar 

  • Briggs GC, Osmont KS, Shindo C, Sibout R, Hardtke CS (2006) Unequal genetic redundancies in Arabidopsis—a neglected phenomenon? Trends Plant Sci 11:492–498

    Article  CAS  PubMed  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 Central  CAS  PubMed  Google Scholar 

  • Chinnusamy V, Zhu J, Zhu JK (2007) Cold stress regulation of gene expression in plants. Trends Plant Sci 12:444–451

    Article  CAS  PubMed  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

    Article  CAS  PubMed  Google Scholar 

  • Ding Y, Li H, Zhang X, Xie Q, Gong Z, Yang S (2015) OST1 kinase modulates freezing tolerance by enhancing ICE1 stability in Arabidopsis. Dev Cell 32:278–289

    Article  CAS  PubMed  Google Scholar 

  • Doherty CJ, Van Buskirk HA, Myers SJ, Thomashow MF (2009) Roles for Arabidopsis CAMTA transcription factors in cold-regulated gene expression and freezing tolerance. Plant Cell 21:972–984

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Dong CH, Agarwal M, Zhang Y, Xie Q, Zhu JK (2006) The negative regulator of plant cold responses, HOS1, is a RING E3 ligase that mediates the ubiquitination and degradation of ICE1. Proc Natl Acad Sci USA 103:8281–8286

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Duarte JM, Cui L, Wall PK, Zhang Q, Zhang X, Leebens-Mack J, Ma H, Altman N, dePamphilis CW (2006) Expression pattern shifts following duplication indicative of subfunctionalization and neofunctionalization in regulatory genes of Arabidopsis. Mol Biol Evol 23:469–478

    Article  CAS  PubMed  Google Scholar 

  • Fursova OV, Pogorelko GV, Tarasov VA (2009) Identification of ICE2, a gene involved in cold acclimation which determines freezing tolerance in Arabidopsis thaliana. Gene 429:98–103

    Article  CAS  PubMed  Google Scholar 

  • Gendrel AV, Lippman Z, Martienssen R, Colot V (2005) Profiling histone modification patterns in plants using genomic tiling microarrays. Nat Methods 2:213–218

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Gilmour SJ, Sebolt AM, Salazar MP, Everard JD, Thomashow MF (2000) Overexpression of the Arabidopsis CBF3 transcriptional activator mimics multiple biochemical changes associated with cold acclimation. Plant Physiol 124:1854–1865

    Article  PubMed Central  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Guy C, Kaplan F, Kopka J, Selbig J, Hincha DK (2008) Metabolomics of temperature stress. Physiol Plant 132:220–235

    CAS  PubMed  Google Scholar 

  • Hofmann NR (2008) They all scream for ICE1/SCRM2: core regulatory units in stomatal development. Plant Cell 20:1732

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Holm M, Ma LG, Qu LJ, Deng XW (2002) Two interacting bZIP proteins are direct targets of COP1-mediated control of light dependent gene expression in Arabidopsis. Genes Dev 16:1247–1259

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6:3901–3907

    PubMed Central  CAS  PubMed  Google Scholar 

  • Jung JH, Seo PJ, Park CM (2012) The E3 ubiquitin ligase HOS1 regulates Arabidopsis flowering by mediating CONSTANS degradation under cold stress. J Biol Chem 287:43277–43287

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Jung JH, Park JH, Lee S, To TK, Kim JM, Seki M, Park CM (2013) The cold signaling attenuator HIGH EXPRESSION OF OSMOTICALLY RESPONSIVE GENE1 activates FLOWERING LOCUS C transcription via chromatin remodeling under short-term cold stress in Arabidopsis. Plant Cell 25:4378–4390

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kanaoka MM, Pillittere LJ, Fujii H, Yoshida Y, Bogenschutz NL, Takabayashi J, Zhu JK, Torii KU (2008) SCREAM/ICE1 and SCREAM2 specify three cell-state transitional steps leading to Arabidopsis stomatal differentiation. Plant Cell 20:1775–1785

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kempin SA, Savidge B, Yanofsky MF (1995) Molecular basis of the cauliflower phenotype in Arabidopsis. Science 267:522–525

    Article  CAS  PubMed  Google Scholar 

  • Kleinboelting N, Huep G, Kloetgen A, Viehoever P, Weisshaar B (2012) GABI-Kat SimpleSearch: new features of the Arabidopsis thaliana T-DNA mutant database. Nucleic Acids Res 40:D1211–D1215

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kosciuczuk EM, Lisowski P, Jarczak J, Strzalkowska N, Jozwik A, Horbanczuk J, Krzyzewski J, Zwierzchowski L, Bagnicka E (2012) Cathelicidins: family of antimicrobial peptides. Mol Biol Rep 39:10957–10970

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kurbidaeva A, Ezhova T, Novokreshchenova M (2014) Arabidopsis thaliana ICE2 gene: phylogeny, structural evolution and functional diversification from ICE1. Plant Sci 229:10–22

    Article  CAS  PubMed  Google Scholar 

  • Kuwabara C, Imai R (2009) Molecular basis of disease resistance acquired through cold acclimation in overwintering plants. J Plant Biol 52:19–26

    Article  CAS  Google Scholar 

  • Lee DH, Goldberg AL (1998) Proteasome inhibitors: valuable new tools for cell biologists. Trends Cell Biol 8:397–403

    Article  CAS  PubMed  Google Scholar 

  • Lee CM, Thomashow MF (2012) Photoperiodic regulation of the C-repeat binding factor (CBF) cold acclimation pathway and freezing tolerance in Arabidopsis thaliana. Proc Natl Acad Sci USA 109:15054–15059

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lee H, Xiong L, Gong Z, Ishitani M, Stevenson B, Zhu JK (2001) The Arabidopsis HOS1 gene negatively regulates cold signal transduction and encodes a RING finger protein that displays cold-regulated nucleo-cytoplasmic partitioning. Genes Dev 15:912–924

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Magadum S, Banerjee U, Murugan P, Gangapur D, Ravikesavan R (2013) Gene duplication as a major force in evolution. J Genet 92:155–161

    Article  PubMed  Google Scholar 

  • Matsui A, Ishida J, Morosawa T, Mochizuki Y, Kaminuma E, Endo TA, Okamoto M, Nambara E, Nakajima M, Kawashima M, Satou M, Kim JM, Kobayashi N, Toyoda T, Shinozaki K, Seki M (2008) Arabidopsis transcriptome analysis under drought, cold, high-salinity and ABA treatment conditions using a tiling array. Plant Cell Physiol 49:1135–1149

    Article  CAS  PubMed  Google Scholar 

  • Medina J, Catalá R, Salinas J (2011) The CBFs: three Arabidopsis transcription factors to cold acclimate. Plant Sci 180:3–11

    Article  CAS  PubMed  Google Scholar 

  • Meshi T, Iwabuchi M (1995) Plant transcription factors. Plant Cell Physiol 36:1405–1420

    CAS  PubMed  Google Scholar 

  • Miura K, Ohta M (2010) SIZ1, a small ubiquitin-related modifier ligase, controls cold signaling through regulation of salicylic acid accumulation. J Plant Physiol 167:555–560

    Article  CAS  PubMed  Google Scholar 

  • Miura K, Jin JB, Lee J, Yoo CY, Stirm V, Miura T, Ashworth EN, Bressan RA, Yun DJ, Hasegawa PM (2007) SIZ1-mediated sumoylation of ICE1 controls CBF3/DREB1A expression and freezing tolerance in Arabidopsis. Plant Cell 19:1403–1414

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Novillo F, Alonso JM, Ecker JR, Salinas J (2004) CBF2/DREB1C is a negative regulator of CBF1/DREB1B and CBF3/DREB1A expression and plays a central role in stress tolerance in Arabidopsis. Proc Natl Acad Sci USA 101:3985–3990

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Novillo F, Medina J, Salinas J (2007) Arabidopsis CBF1 and CBF3 have a different function than CBF2 in cold acclimation and define different gene classes in the CBF regulon. Proc Natl Acad Sci USA 104:21002–21007

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sakuma Y, Liu Q, Dubouzet JG, Abe H, Shinozaki K, Yamaguchi-Shinozaki K (2002) DNA-binding specificity of the ERF/AP2 domain of Arabidopsis DREBs, transcription factors involved in dehydration and cold-inducible gene expression. Biochem Biophys Res Commun 290:998–1009

    Article  CAS  PubMed  Google Scholar 

  • Tarasov VA, Khadeeva NV, Mel’nik VA, Ezhova TA, Shestakov SV (2009) The atlg12860 gene of Arabidopsis thaliana determines cathelicidin-like antimicrobial activity. Dokl Biol Sci 427:332–334

    Article  CAS  PubMed  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 Central  CAS  PubMed  Google Scholar 

  • Udvardi MK, Czechowski T, Scheible WR (2008) Eleven golden rules of quantitative RT-PCR. Plant Cell 20:1736–1737

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wardle DJ, Burgon J, Sabroe I, Bingle CD, Whyte MK, Renshaw SA (2011) Effective caspase inhibition blocks neutrophil apoptosis and reveals Mcl-1 as both a regulator and a target of neutrophil caspase activation. PLoS ONE 6:e15768

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Whelan JA, Russell NB, Whelan MA (2003) A method for the absolute quantification of cDNA using real-time PCR. J Immunol Methods 278:261–269

    Article  CAS  PubMed  Google Scholar 

  • Yoo SD, Cho YH, Sheen J (2007) Arabidopsis mesophyll protoplasts. A versatile cell system for transient gene expression analysis. Nat Protoc 2:1565–1572

    Article  CAS  PubMed  Google Scholar 

  • Zeller G, Henz SR, Widmer CK, Sachsenberg T, Rätsch G, Weigel D, Laubinger S (2009) Stress-induced changes in the Arabidopsis thaliana transcriptome analyzed using whole-genome tiling arrays. Plant J 58:1068–1082

    Article  CAS  PubMed  Google Scholar 

  • Zhu Y, Yang H, Mang HG, Hua J (2011) Induction of BAP1 by a moderate decrease in temperature is mediated by ICE1 in Arabidopsis. Plant Physiol 155:580–588

    Article  PubMed Central  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Keiko Torii and Julio Salinas for kindly providing ice2-1 and cbf2 mutants, respectively. This work was supported by the Leaping Research (NRF-2010-0014373) and Global Research Lab (NRF-2012K1A1A2055546) Programs provided by the National Research Foundation of Korea and the Next-Generation BioGreen 21 Program (PMBC No. PJ8103012014) provided by the Rural Development Administration of Korea. It was also supported in part by the Human Frontier Science Program (RGP0002/2012).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Chung-Mo Park.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kim, Y.S., Lee, M., Lee, JH. et al. The unified ICE–CBF pathway provides a transcriptional feedback control of freezing tolerance during cold acclimation in Arabidopsis . Plant Mol Biol 89, 187–201 (2015). https://doi.org/10.1007/s11103-015-0365-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-015-0365-3

Keywords

Navigation