Skip to main content
SpringerLink
Log in

ICE1, a Transcription Factor Involved in Cold Signaling and Tolerance

  • Conference paper
  • First Online:
Plant and Microbe Adaptations to Cold in a Changing World

Abstract

Cold stress is a major factor that limits the development, productivity, and geographical distribution of plants. To adapt to a low temperature, plants have developed mechanisms to tolerate cold stress. Cold signals in plants are transmitted to inducer of CBF expression1 (ICE1), a basic helix-loop-helix transcription factor, which activates the C-repeat-binding factor/dehydration-responsive element-binding protein regulon. ICE1 is posttranslationally regulated by ubiquitylation, mediated by the high expression of osmotically responsive gene1 (HOS1) ubiquitin E3 ligase, and sumoylation, mediated by the SIZ1 small ubiquitin-related modifier E3 ligase. ICE1 is functionally conserved in different plant species and its overexpression in tomato and cucumber increases chilling tolerance. The introduction of wheat ICE1 enhances cold tolerance in Arabidopsis. In this chapter, the recent progress in studying ICE1-dependent cold signaling in Arabidopsis and its functional conservation in crops will be summarized.

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

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 219.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 279.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 279.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Badawi M, Reddy YV, Agharbaoui Z, Tominaga Y, Danyluk J, Sarhan F, Houde M (2008) Structure and functional analysis of wheat ICE (inducer of CBF expression) genes. Plant Cell Physiol 49:1237–1249

    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. Gene Dev 17:1043–1054

    Article  PubMed  CAS  Google Scholar 

  • Chinnusamy V, Zhu JK, Sunkar R (2010) Gene regulation during cold stress acclimation in plants. Methods Mol Biol 639:39–55

    Article  PubMed  CAS  Google Scholar 

  • Davis LJ, Halazonetis TD (1993) Both the helix-loop-helix and the leucine zipper motifs of c-Myc contribute to its dimerization specificity with Max. Oncogene 8:125–132

    PubMed  CAS  Google Scholar 

  • Doherty CJ, Buskirk HA van, 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  CAS  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 U S A 103:8281–8286

    Article  PubMed  CAS  Google Scholar 

  • Du L, Ali GS, Simons KA, Hou J, Yang T, Reddy ASN, Poovaiah BW (2009) Ca2+/calmodulin regulates salicylic acid-mediated plant immunity. Nature 457:1154–1158

    Article  PubMed  CAS  Google Scholar 

  • Ferré-D’Amaré AR, Prendergast GC, Ziff EB, Burley SK (1993) Recognition by max of its cognate DNA through a dimeric b/HLH/Z domain. Nature 363:38–45

    Article  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  PubMed  CAS  Google Scholar 

  • Hara M, Furukawa J, Sato A, Mizoguchi T, Miura K (2011) Abiotic stress and role of salicylic acid in plants. In: Ahmad P, Prasad MNV (eds) Abiotic stress responses in plants: metabolism, productivity, and sustainability. Springer, New York, pp 235–251

    Google Scholar 

  • Hu Y, Zhang L, Zhao L, Li J, He S, Zhou K, Yang F, Huang M, Jiang L, Li L (2011) Trichostatin A selectively suppresses the cold-induced transcription of the ZmDREB1 gene in maize. PLoS One:e22132

    Google Scholar 

  • Janda T, Szalai G, Leskó K, Yordanova R, Apostol S, Popova LP (2007) Factors contributing to enhanced freezing tolerance in wheat during frost hardening in the light. Phytochemistry 68:1674-1682

    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  CAS  Google Scholar 

  • Kang HM, Saltveit ME (2002) Chilling tolerance of maize, cucumber and rice seedling leaves and roots are differentially affected by salicylic acid. Physiol Plantarum 115:571–576

    Article  CAS  Google Scholar 

  • Kosová K, Prášil IT, Vítámvás P, Dobrev P, Motyka V, Floková K, Novák O, Turečková V, Rolčík J, Pešek B, Trávničková A, Gaudinová A, Galiba G, Janda T, Vlasáková E, Prášilová P, Vanková R (2012) Complex phytohormone responses during the cold acclimation of two wheat cultivars differing in cold tolerance, winter Samanta and spring Sandra. J Plant Physiol 169:567–576

    Article  PubMed  Google Scholar 

  • Laudencia-Chngcuanco D, Ganeshan S, You F, Fowler B, Chibbar R, Anderson O (2011) Genome-wide gene expression analysis supports a developmental model of low temperature tolerance gene regulation in wheat (Triticum aestivum L. ). BMC Genomics 12:299

    Article  Google Scholar 

  • Lee BH, Henderson DA, Zhu JK (2005) The Arabidopsis cold-responsive transcriptome and its regulation by ICE1. Plant Cell 17:3155–3175

    Article  PubMed  CAS  Google Scholar 

  • Lissarre M, Ohta M, Sato A, Miura K (2010) Cold-responsive gene regulation during cold acclimation in plants. Plant Signal Behav 5:948–952

    Google Scholar 

  • Liu L, Duan L, Zhang J, Zhang Z, Mi G, Ren H (2010) Cucumber (Cucumis sativus L.) over-expressing cold-induced Transcriptome regulator ICE1 exhibits changed morphological characters and enhances chilling tolerance. Sci Hortic 124:29–33

    Article  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

    Google Scholar 

  • Miura K, Rus A, Sharkhuu A, Yokoi S, Karthikeyan AS, Raghothama KG, Baek D, Koo YD, Jin JB, Bressan RA, Yun DJ, Hasegawa PM (2005) The Arabidopsis SUMO E3 ligase SIZ1 controls phosphate deficiency responses. Proc Natl Acad Sci U S A 102:7760–7765

    Article  PubMed  CAS  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  CAS  Google Scholar 

  • Miura K, Hasegawa PM (2010) Sumoylation and other ubiquitin-like post-translational modifications in plants. Trends Cell Biol 20:223–232

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Miura K, Ohta M, Nakazawa M, Ono M, Hasegawa PM (2011) ICE1 Ser403 is necessary for protein stabilization and regulation of cold signaling and tolerance. Plant J 67:269–279

    Article  PubMed  CAS  Google Scholar 

  • Miura K, Shiba H, Ohta M, Kang SW, Sato A, Yuasa T, Iwaya-Inoue M, Kamada H, Ezura H (2012a) SlICE1 encoding a MYC-type transcription factor controls cold tolerance in tomato, Solanum lycopersicum. Plant Biotechnol 29:253–260

    Google Scholar 

  • Miura K, Sato A, Shiba H, Kang SW, Kamada H, Ezura H (2012b) Accumulation of antioxidants and antioxidant activity in tomato, Solanum lycopersicum, are enhanced by the transcription factor SlICE1. Plant Biotechnol 29:261–269

    Google Scholar 

  • Mora-Herrera ME, Lopez-Delgado H, Castillo-Morales A, Foyer CH (2005) Salicylic acid and H2O2 function by independent pathways in the induction of freezing tolerance in potato. Physiol Plantanum 125:430–440

    CAS  Google Scholar 

  • Nakamura J, Yuasa T, Huong TT, Harano K, Tanaka S, Iwata T, Phan T, Iwaya-Inoue M (2011) Rice homologs of inducer of CBF expression (OsICE) are involved in cold acclimation. Plant Biotechnol 28:303–309

    Article  CAS  Google Scholar 

  • Nawrath C, Métraux JP (1999) Salicylic acid induction-deficient mutants of Arabidopsis express PR-2 and PR-5 and accumulate high levels of camalexin after pathogene inoculation. Plant Cell 11:1393–1404

    PubMed  CAS  Google Scholar 

  • Orvar BL, Sangwan V, Omann F, Dhindsa R (2000) Early steps in cold sensing by plant cells: the role of actin cytoskeleton and membrane fluidity. Plant J 23:785–794

    Article  PubMed  CAS  Google Scholar 

  • Qiu D, Xiao J, Xie W, Liu H, Li X, Xiong L, Wang S (2008) Rice gene network inferred from expression profiling of plants overexpressing OsWRKY13, a positive regulator of disease resistance. Mol Plant 3:538–551

    Article  Google Scholar 

  • Scott IM, Clark SM, Wood JE, Mur LAJ (2004) Salicyliate accumulation inhibits growth at chilling temperature in Arabidopsis. Plant Physiol 135:1040–1049

    Google Scholar 

  • Sangwan V, Foulds I, Singh J, Dhindsa RJ (2001) Cold activation of Brassica napus BN115 promoter is mediated by structural changes in membranes and cytoskeleton, and requires Ca2+ influx. Plant J 27:1–12

    Article  PubMed  CAS  Google Scholar 

  • Stockinger EJ, Gilmour SJ, Thomashow MF (1997) Arabidopsis thaliana CBF1encodes 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. 94:1035–1040

    Google Scholar 

  • Strawn MA, Marr SK, Inoue K, Inada N, Zubieta C, Wildermuth MC (2007) Arabidopsis isochorismate synthase functional in pathogen-induced salicylate biosynthesis exhibits properties consistent with a role in diverse stress responses. J Biol Chem 282:5919–5933

    Article  PubMed  CAS  Google Scholar 

  • Tasgin E, Atici O, Nalbantoglu B (2003) Effects of salicylic acid and cold on freezing tolerance in winter wheat leaves. Plant Growth Regul 41:231–236

    Article  CAS  Google Scholar 

  • Tsutsui T, Kato W, Asada Y, Sako K, Sato T, Sonoda Y, Kidokoro S, Yamaguchi-Shinozaki K, Tamaoki M, Arakawa K, Ichikawa T, Nakazawa M, Seki M, Shinozaki K, Matsui M, Ikeda A, Yamaguchi J (2009) DEAR1, a transcriptional repressor of DREB protein that mediates plant defense and freezing stress responses in Arabidopsis. J Plant Res 122:633–643

    Article  PubMed  CAS  Google Scholar 

  • Wan SB, Tian L, Tian RR, Pan QH, Zhan JC, Wen PF, Chen JY, Zhang P, Wang W, Huang WD (2009) Involvement of phospholipase D in the low temperature acclimation-induced thermotolerance in grape berry. Plant Physiol Biochem 47:504–510

    Google Scholar 

  • Yun KY, Park MR, Mohanty B, Herath V, Xu F, Mauleon R, Wijaya E, Bajic VB, Bruskiewich R, los Reyes BG de (2010) Transcriptional regulatory network triggered by oxidative signals configures the early response mechanisms of japonica rice to chilling stress. BMC Plant Biol 10:16

    Article  PubMed  Google Scholar 

  • Zhou MQ, Shen C, Wu LH, Tang KX, Lin J (2011) CBF-dependent signaling pathway: a key responder to low temperature stress in plants. Crit Rev Biotechnol 31:186–192

    Article  PubMed  CAS  Google Scholar 

  • Zhao ML, Wang JN, Shan W, Fan JG, Kuang JF, Wu KQ, Li XP, Chen WX, He FY, Chen JY, Lu WJ (2012) Induction of jasmonate signalling regulators MaMYC2s and their physical interactions with MaICE1 in methyl jasmonate-induced chilling tolerance in banana fruit. Plant Cell Environ 36(1):30–51. doi:10.1111/j.1365–3040.2012.02551.x

    Article  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 155:1580–1588

    Google Scholar 

Download references

Acknowledgments

The laboratory is supported by a Grant-in-Aid for Scientific Research on Innovative Areas from Japanese Ministry of Education, Culture, Sports, Science and Technology on “Environmental Sensing of Plants: Signal Perception, Processing Cellular Responses”, Grant-in-Aid for Challenging Exploratory Research, Research Grant from Inamori Foundation, and Corporative Research Grant of the Gene Research Center, the University of Tsukuba.

Author information

Authors and Affiliations

  1. Faculty of Life and Environmental Sciences, University of Tsukuba, Tsukuba, Japan

    Kenji Miura

Authors
  1. Kenji Miura
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kenji Miura .

Editor information

Editors and Affiliations

  1. Crop Breeding Research Division, NARO Hokkaido Agricultural Research Center, Sapporo, Japan

    Ryozo Imai

  2. Crop Breeding Research Division, NARO Hokkaido Agricultural Research Center, Sapporo, Japan

    Midori Yoshida

  3. Silviculture & Forest Ecology Studies, Hokkaido University Graduate School of Agriculture, Sapporo, Japan

    Naoyuki Matsumoto

Rights and permissions

Reprints and permissions

Copyright information

© 2013 Springer Science+Business Media New York

About this paper

Cite this paper

Miura, K. (2013). ICE1, a Transcription Factor Involved in Cold Signaling and Tolerance. In: Imai, R., Yoshida, M., Matsumoto, N. (eds) Plant and Microbe Adaptations to Cold in a Changing World. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-8253-6_16

Download citation

Publish with us

Policies and ethics

Search

Navigation