Skip to main content
SpringerLink
Log in

Gene regulation and signal transduction in the ICE–CBF–COR signaling pathway during cold stress in plants

  • Review
  • Published:
Biochemistry (Moscow) Aims and scope Submit manuscript

Abstract

Low temperature is an abiotic stress that adversely affects the growth and production of plants. Resistance and adaptation of plants to cold stress is dependent upon the activation of molecular networks and pathways involved in signal transduction and the regulation of cold-stress related genes. Because it has numerous and complex genes, regulation factors, and pathways, research on the ICE–CBF–COR signaling pathway is the most studied and detailed, which is thought to be rather important for cold resistance of plants. In this review, we focus on the function of each member, interrelation among members, and the influence of manipulators and repressors in the ICE–CBF–COR pathway. In addition, regulation and signal transduction concerning plant hormones, circadian clock, and light are discussed. The studies presented provide a detailed picture of the ICE–CBF–COR pathway.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

ABA:

abscisic acid

ABF:

ABRE-binding factor

ABRE:

ABA-responsive element

AHK:

Arabidopsis histidine kinase

AHPs:

Arabidopsis histidine phosphotransfer proteins

AP2/ERF:

apetala2/ethylene-responsive element binding protein

AREB/ABF:

ABRE-binding protein/ABRE-binding factor

ARRs:

Arabidopsis response regulators

BA:

brassinosteroids

BIN2:

brassinosteroid-insensitive 2

BZR1:

brassinazole-resistant 1

CAMTA:

calmodulin-binding transcription activator

CBF:

C-repeat-binding factor

CCA1:

circadian and clock-associated 1

CK:

cytokinin

COR/COR :

cold-regulated proteins/cold-responsive genes

CRPK1:

cold-responsive protein kinase 1

CRT/DRE:

C-repeat/dehydration responsive element

CSP2:

cold shock domain protein 2

DHN:

dehydrins

DREBs:

dehydration responsive element binding factors

EE:

evening element

EIN3:

ethylene-insensitive 3

GA:

gibberellic acid

HHP:

heptahelical transmembrane protein

HOS1:

high expression of osmotically respon-sive gene 1

HY5:

elongated hypocotyls 5

ICE:

inducer of CBF expression

JA:

jasmonates

KIN:

cold induced

LEA:

late embryo-genesis abundant

LHY:

late elongated hypocotyl

LUX:

LUX ARRYHTHMO

OST1:

open stomata 1

PP2C:

2C type protein phosphatases

RD:

responsive to dehydration

RDM4:

RNA-directed DNA methylation 4

ROC1:

regulator of CBF1

SOC1:

sup-pressor of overexpression of constans 1

References

  1. Thomashow, M. F. (1999) Plant cold acclimation: freezing tolerance genes and regulatory mechanisms, Plant Mol. Biol., 50, 571–599.

    CAS  Google Scholar 

  2. Huang, G. T., Ma, S. L., Bai, L. P., Zhang, L., Ma, H., Jia, P., Liu, J., Zhong, M., and Guo, Z. F. (2012) Signal transduction during cold, salt, and drought stresses in plants, Mol. Biol. Rep., 39, 969–987.

    Article  PubMed  CAS  Google Scholar 

  3. Kim, Y. S., Lee, M., Lee, J. H., Lee, H. J., and Park, C. M. (2015) The unified ICE–CBF pathway provides a tran-scriptional feedback control of freezing tolerance during cold acclimation in Arabidopsis, Plant Mol. Biol., 89, 187–201.

    Article  CAS  PubMed  Google Scholar 

  4. Chinnusamy, V., Zhu, J. K., and Sunkar, R. (2010) Gene regulation during cold stress acclimation in plants, Methods Mol. Biol., 639, 39–55.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Theocharis, A., Clement, C., and Barka, E. A. (2012) Physiological and molecular changes in plants grown at low temperatures, Planta, 235, 1091–1105.

    Article  CAS  PubMed  Google Scholar 

  6. Jiang, Y., Peng, D., Bai, L. P., Ma, H., Chen, L. J., Zhao, M. H., Xu, Z. J., and Guo, Z. F. (2013) Molecular switch for cold acclimation–anatomy of the cold-inducible pro-moter in plants, Biochemistry (Moscow), 78, 342–354.

    Article  CAS  Google Scholar 

  7. Shi, Y., Ding, Y., and Yang, S. (2015) Cold signal transduction and its interplay with phytohormones during cold acclimation, Plant Cell Physiol., 56, 7–15.

    Article  CAS  PubMed  Google Scholar 

  8. Verma, V., Ravindran, P., and Kumar, P. P. (2016) Plant hormone-mediated regulation of stress responses, BMC Plant Biol., 16, 86.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  9. Gilmour, S. J., Zarka, D. G., Stockinger, E. J., Salazar, M. P., Houghton, J. M., and Thomashow, M. F. (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 

  10. Chinnusamy, V., Ohta, M., Kanrar, S., Lee, B. H., Hong, X., Agarwal, M., and Zhu, J. K. (2003) ICE1: a regulator of cold-induced transcriptome and freezing tolerance in Arabidopsis, Genes Dev., 17, 1043–1054.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Sakuma, Y., Liu, Q., Dubouzet, J. G., Abe, H., Shinozaki, K., and 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 

  12. Thomashow, M. F. (2001) So what’s new in the field of plant cold acclimation? Lots! Plant Physiol., 125, 89–93.

    Article  CAS  PubMed  Google Scholar 

  13. Zarka, D. G., Vogel, J. T., Cook, D., and Thomashow, M. F. (2003) Cold induction of Arabidopsis CBF genes involves multiple ICE (inducer of CBF expression) promoter ele-ments and a cold-regulatory circuit that is desensitized by low temperature, Plant Physiol., 133, 910–918.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Gehan, M. A., Park, S., Gilmour, S. J., An, C., Lee, C. M., and Thomashow, M. F. (2015) Natural variation in the C-repeat binding factor cold response pathway correlates with local adaptation of Arabidopsis ecotypes, Plant J., 84, 682–693.

    Article  CAS  PubMed  Google Scholar 

  15. Yamaguchi-Shinozaki, K., and Shinozaki, K. (1994) A novel cis-acting element in an Arabidopsis gene is involved in responsiveness to drought, low-temperature, or high-salt stress, Plant Cell, 6, 251–264.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Uemura, M., Gilmour, S. J., Thomashow, M. F., and Steponkus, P. L. (1996) Effects of COR6.6 and COR15am polypeptides encoded by COR (cold-regulated) genes of Arabidopsis thaliana on the freeze-induced fusion and leakage of liposomes, Plant Physiol., 111, 313–327.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Lee, H., Xiong, L., Ishitani, M., Stevenson, B., and Zhu, J. K. (1999) Cold-regulated gene expression and freezing tol-erance in an Arabidopsis thaliana mutant, Plant J., 17, 301–308.

    Article  CAS  PubMed  Google Scholar 

  18. Thalhammer, A., Bryant, G., Sulpice, R., and Hincha, D. K. (2014) Disordered cold-regulated 15 proteins protect chloroplast membranes during freezing through binding and folding, but do not stabilize chloroplast enzymes in vivo, Plant Physiol., 166, 190–201.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  19. Shi, Y., Huang, J., Sun, T., Wang, X., Zhu, C., Ai, Y., and Gu, H. (2017) The precise regulation of different COR genes by individual CBF transcription factors in Arabidopsis thaliana, J. Iintegr. Plant Biol., 59, 118–133.

    Article  CAS  Google Scholar 

  20. Ganeshan, S., Vitamvas, P., Fowler, D. B., and Chibbar, R. N. (2008) Quantitative expression analysis of selected COR genes reveals their differential expression in leaf and crown tissues of wheat (Triticum aestivum L.) during an extended low temperature acclimation regimen, J. Exp. Bot., 59, 2393–2402.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Soltesz, A., Smedley, M., Vashegyi, I., Galiba, G., Harwood, W., and Vagujfalvi, A. (2013) Transgenic barley lines prove the involvement of TaCBF14 and TaCBF15 in the cold acclimation process and in frost tolerance, J. Exp. Bot., 64, 1849–1862.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Talanova, V. V., Titov, A. F., Repkina, N. S., and Topchieva, L. V. (2013) Cold-responsive COR/LEA genes participate in the response of wheat plants to heavy metals stress, Dokl. Biol. Sci., 448, 28–31.

    Article  CAS  PubMed  Google Scholar 

  23. Li, X. W., Feng, Z. G., Yang, H. M., Zhu, X. P., Liu, J., and Yuan, H. Y. (2010) A novel cold-regulated gene from Camellia sinensis, CsCOR1, enhances salt- and dehydration-tolerance in tobacco, Biochem. Biophys. Res. Commun., 394, 354–359.

    Article  CAS  PubMed  Google Scholar 

  24. Liu, S., Wang, X., Fan, Z., Pang, Y., Sun, X., Wang, X., and Tanga, K. (2004) Molecular cloning and characterization of a novel cold-regulated gene from Capsella bursa-pastoris, DNA Seq., 15, 262–268.

    Article  CAS  PubMed  Google Scholar 

  25. Lu, Y., Sun, X., Yao, J., Chai, Y., Zhao, X., Zhang, L., Song, J., Pang, Y. Z., Wu, W., and Tang, K. (2003) Isolation and expression of cold-regulated cDNA from Chinese cabbage (Brassica pekinensis), DNA Seq., 14, 219–222.

    Article  CAS  PubMed  Google Scholar 

  26. Haake, V., Cook, D., Riechmann, J. L., Pineda, O., Thomashow, M. F., and Zhang, J. Z. (2002) Transcription factor CBF4 is a regulator of drought adaptation in Arabidopsis, Plant Physiol., 130, 639–648.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Stockinger, E. J., Gilmour, S. J., and Thomashow, M. F. (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  CAS  PubMed  PubMed Central  Google Scholar 

  28. Liu, Q., Kasuga, M., Sakuma, Y., Abe, H., Miura, S., Yamaguchi-Shinozaki, K., and 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.

    Article  CAS  PubMed  Google Scholar 

  29. Medina, J., Bargues, M., Terol, J., Perez-Alonso, M., and 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, 463–470.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Jaglo, K. R., Kleff, S., Amundsen, K. L., Zhang, X., Haake, V., Zhang, J. Z., Deits, T., and Thomashow, M. F. (2001) Components of the Arabidopsis C-repeat/dehydra-tion-responsive element binding factor cold-response path-way are conserved in Brassica napus and other plant species, Plant Physiol., 127, 910–917.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Park, S., Lee, C. M., Doherty, C. J., Gilmour, S. J., Kim, Y., and Thomashow, M. F. (2015) Regulation of the Arabidopsis CBF regulon by a complex low-temperature regulatory network, Plant J., 82, 193–207.

    Article  CAS  PubMed  Google Scholar 

  32. Jia, Y., Ding, Y., Shi, Y., Zhang, X., Gong, Z., and Yang, S. (2016) The cbfs triple mutants reveal the essential functions of CBFs in cold acclimation and allow the definition of CBF regulons in Arabidopsis, New Phytol., 212, 345–353.

    Article  CAS  PubMed  Google Scholar 

  33. Novillo, F., Alonso, J. M., Ecker, J. R., and 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  CAS  PubMed  PubMed Central  Google Scholar 

  34. Novillo, F., Medina, J., and 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  CAS  PubMed  PubMed Central  Google Scholar 

  35. Zhao, C., Zhang, Z., Xie, S., Si, T., Li, Y., and Zhu, J. K. (2016) Mutational evidence for the critical role of CBF transcription factors in cold acclimation in Arabidopsis, Plant Physiol., 171, 2744–2759.

    CAS  PubMed  PubMed Central  Google Scholar 

  36. Ito, Y., Katsura, K., Maruyama, K., Taji, T., Kobayashi, M., Seki, M., Shinozaki, K., and Yamaguchi-Shinozaki, K. (2006) Functional analysis of rice DREB1/CBF-type transcription factors involved in cold-responsive gene expression in transgenic rice, Plant Cell Physiol., 47, 141–153.

    Article  CAS  PubMed  Google Scholar 

  37. Zhuang, L., Yuan, X., Chen, Y., Xu, B., Yang, Z., and Huang, B. (2015) PpCBF3 from cold-tolerant krtucky bluegrass involved in freezing tolerance associated with up-regulation of cold-related genes in transgenic Arabidopsis thaliana, PLoS One, 10, e0132928.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  38. Huang, Z., He, J., Zhong, X. J., Guo, H. D., Jin, S. H., Li, X., and Sun, L. X. (2016) Molecular cloning and characterization of a novel freezing-inducible DREB1/CBF transcription factor gene in boreal plant iceland poppy (Papaver nudicaule), Genet. Mol. Biol., 39, 616–628.

    Article  PubMed  PubMed Central  Google Scholar 

  39. Du, F., Xu, J. N., Li, D., and Wang, X. Y. (2015) The identification of novel and differentially expressed apple-tree genes under low-temperature stress using high-throughput Illumina sequencing, Mol. Biol. Rep., 42, 569–580.

    Article  CAS  PubMed  Google Scholar 

  40. Byun, M. Y., Lee, J., Cui, L. H., Kang, Y., Oh, T. K., Park, H., Lee, H., and Kim, W. T. (2015) Constitutive expression of DaCBF7, an Antarctic vascular plant Deschampsia antarctica CBF homolog, resulted in improved cold tolerance in transgenic rice plants, Plant Sci., 236, 61–74.

    Article  CAS  PubMed  Google Scholar 

  41. Yamasaki, Y., and Randall, S. K. (2016) Functionality of soybean CBF/DREB1 transcription factors, Plant Sci., 246, 80–90.

    Article  CAS  PubMed  Google Scholar 

  42. Alisoltani, A., Shiran, B., Fallahi, H., and Ebrahimie, E. (2015) Gene regulatory network in almond (Prunus dulcis Mill.) in response to frost stress, Tree Genet. Gen., 11, 100.

    Article  Google Scholar 

  43. Fang, Z. W., Xu, X. Y., Gao, J. F., Wang, P. K., Liu, Z. X., and Feng, B. L. (2015) Characterization of FeDREB1 pro-moter involved in cold- and drought-inducible expression from common buckwheat (Fagopyrum esculentum), Genet. Mol. Res., 14, 7990–8000.

    Article  CAS  PubMed  Google Scholar 

  44. Li, J., Qin, R. Y., Li, H., Xu, R. F., Yang, Y. C., Ni, D. H., Ma, H., Li, L., Wei, P. C., and Yang, J. B. (2015) Low-tem-perature-induced expression of rice ureidoglycolate amido-hydrolase is mediated by a C-repeat/dehydration-responsive element that specifically interacts with rice C-repeat-binding factor 3, Front. Plant Sci., 6, 1011.

    PubMed  PubMed Central  Google Scholar 

  45. Wang, L., Gao, J., Qin, X., Shi, X., Luo, L., Zhang, G., Yu, H., Li, C., Hu, M., Liu, Q., Xu, Y., and Chen, F. (2015) JcCBF2 gene from Jatropha curcas improves freezing toler-ance of Arabidopsis thaliana during the early stage of stress, Mol. Biol. Rep., 42, 937–945.

    Article  CAS  PubMed  Google Scholar 

  46. Ebrahimi, M., Abdullah, S. N., Abdul Aziz, M., and Namasivayam, P. (2016) Oil palm EgCBF3 conferred stress tolerance in transgenic tomato plants through modulation of the ethylene signaling pathway, J. Plant Physiol., 202, 107–120.

    Article  CAS  PubMed  Google Scholar 

  47. Nguyen, H. C., Cao, P. B., San Clemente, H., Ployet, R., Mounet, F., Ladouce, N., Harvengt, L., Marque, C., and Teulieres, C. (2017) Special trends in CBF and DREB2 groups in Eucalyptus gunnii vs Eucalyptus grandis suggest that CBF are master players in the trade-off between growth and stress resistance, Physiol. Plant., 159, 445–467.

    Article  CAS  PubMed  Google Scholar 

  48. Kashyap, P., Sehrawat, A., and Deswal, R. (2015) Nitric oxide modulates Lycopersicon esculentum C-repeat binding factor 1 (LeCBF1) transcriptionally as well as post-translationally by nitrosylation, Plant Physiol. Biochem., 96, 115–123.

    Article  CAS  PubMed  Google Scholar 

  49. Lee, B. H., Henderson, D. A., and Zhu, J. K. (2005) The Arabidopsis cold-responsive transcriptome and its regulation by ICE1, Plant Cell, 17, 3155–3175.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Fursova, O. V., Pogorelko, G. V., and Tarasov, V. A. (2009) Identification of ICE2, a gene involved in cold acclimation which determines freezing tolerance in Arabidopsis thaliana, Gene, 429, 9–103.

    Article  CAS  Google Scholar 

  52. Kurbidaeva, A., Ezhova, T., and 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 

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

    Article  CAS  PubMed  Google Scholar 

  54. Man, L., Xiang, D., Wang, L., Zhang, W., Wang, X., and Qi, G. (2017) Stress-responsive gene RsICE1 from Raphanus sativus increases cold tolerance in rice, Protoplasma, 254, 945–956.

    Article  CAS  PubMed  Google Scholar 

  55. Lu, X., Yang, L., Yu, M., Lai, J., Wang, C., McNeil, D., Zhou, M., and Yang, C. (2017) A novel Zea mays ssp. mexicana L. MYC-type ICE-like transcription factor gene ZmmICE1 enhances freezing tolerance in transgenic Arabidopsis thaliana, Plant Physiol. Biochem., 113, 78–88.

    Article  CAS  PubMed  Google Scholar 

  56. Rahman, M. A., Moody, M. A., and Nassuth, A. (2014) Grape contains 4 ICE genes whose expression includes alternative polyadenylation, leading to transcripts encoding at least 7 different ICE proteins, Environ. Exp. Bot., 106, 70–78.

    Article  CAS  Google Scholar 

  57. Liu, S., Wang, X., Fan, Z., Pang, Y., Sun, X., Wang, X., and Tanga, K. (2004) Molecular cloning and characterization of a novel cold-regulated gene from Capsella bursa-pastoris, DNA Seq., 15, 262–268.

    Article  CAS  PubMed  Google Scholar 

  58. Wang, Y., Jiang, C. J., Li, Y. Y., Wei, C. L., and Deng, W. W. (2012) CsICE1 and CsCBF1: two transcription factors involved in cold responses in Camellia sinensis, Plant Cell Rep., 31, 27–34.

    Article  PubMed  CAS  Google Scholar 

  59. Chen, Y., Jiang, J., Song, A., Chen, S., Shan, H., Luo, H., Gu, C., Sun, J., Zhu, L., Fang, W., and Chen, F. (2013) Ambient temperature enhanced freezing tolerance of Chrysanthemum dichrum CdICE1 Arabidopsis via miR398, BMC Biol., 11, 121.

    Article  PubMed  PubMed Central  Google Scholar 

  60. Feng, H. L., Ma, N. N., Meng, X., Zhang, S., Wang, J. R., Chai, S., and Meng, Q. W. (2013) A novel tomato MYC-type ICE1-like transcription factor, SlICE1a, confers cold, osmotic and salt tolerance in transgenic tobacco, Plant Physiol. Biochem., 73, 309–320.

    CAS  PubMed  Google Scholar 

  61. Xu, W., Jiao, Y., Li, R., Zhang, N., Xiao, D., Ding, X., and Wang, Z. (2014) Chinese wild-growing Vitis amurensis ICE1 and ICE2 encode MYC-type bHLH transcription activators that regulate cold tolerance in Arabidopsis, PLoS One, 9, e102303.

    Article  PubMed  PubMed Central  Google Scholar 

  62. Ishitani, M., Xiong, L., Lee, H., Stevenson, B., and Zhu, J. K. (1998) HOS1, a genetic locus involved in cold-responsive gene expression in Arabidopsis, Plant Cell, 10, 1151–1161.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Dong, C. H., Agarwal, M., Zhang, Y., Xie, Q., and Zhu, J. K. (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  CAS  PubMed  PubMed Central  Google Scholar 

  64. Miura, K., Jin, J. B., Lee, J., Yoo, C. Y., Stirm, V., Miura, T., Ashworth, E. N., Bressan, R. A., Yun, D. J., and Hasegawa, P. M. (2007) SIZ1-mediated sumoylation of ICE1 controls CBF3/DREB1A expression and freezing tolerance in Arabidopsis, Plant Cell, 19, 1403–1414.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  66. Mustilli, A. C., Merlot, S., Vavasseur, A., Fenzi, F., and Giraudat, J. (2002) Arabidopsis OST1 protein kinase mediates the regulation of stomatal aperture by abscisic acid and acts upstream of reactive oxygen species production, Plant Cell, 14, 3089–3099.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Kanaoka, M. M., Pillitteri, L. J., Fujii, H., Yoshida, Y., Bogenschutz, N. L., Takabayashi, J., Zhu, J. K., and Torii, K. U. (2008) SCREAM/ICE1 and SCREAM2 specify three cell-state transitional steps leading to Arabidopsis stomatal differentiation, Plant Cell, 20, 1775–1785.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Seo, E., Lee, H., Jeon, J., Park, H., Kim, J., Noh, Y. S., and Lee, I. (2009) Crosstalk between cold response and flowering in Arabidopsis is mediated through the flowering-time gene SOC1 and its upstream negative regulator FLC, Plant Cell, 21, 3185–3197.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Lee, J. H., Jung, J. H., and Park, C. M. (2015) Inducer of CBF expression 1 integrates cold signals into flowering locus C-mediated flowering pathways in Arabidopsis, Plant J., 84, 29–40.

    Article  CAS  PubMed  Google Scholar 

  70. Liu, J., Whalley, H. J., and Knight, M. R. (2015) Combining modelling and experimental approaches to explain how calcium signatures are decoded by calmod-ulin-binding transcription activators (CAMTAs) to pro-duce specific gene expression responses, New Phytol., 208, 174–187.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Eckardt, N. A. (2009) CAMTA proteins: a direct link between calcium signals and cold acclimation? Plant Cell, 21, 697.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Doherty, C. J., Van Buskirk, H. A., Myers, S. J., and Thomashow, M. F. (2009) Roles for Arabidopsis CAMTA transcription factors in cold-regulated gene expression and freezing tolerance, Plant Cell, 21, 972–984.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Shen, C., Yang, Y., Du, L., and Wang, H. (2015) Calmodulin-binding transcription activators and perspectives for applications in biotechnology, Appl. Microbiol. Biotechnol., 99, 10379–10385.

    Article  CAS  PubMed  Google Scholar 

  74. Kim, Y., Park, S., Gilmour, S. J., and Thomashow, M. F. (2013) Roles of CAMTA transcription factors and salicylic acid in configuring the low-temperature transcriptome and freezing tolerance of Arabidopsis, Plant J., 75, 364–376.

    Article  CAS  PubMed  Google Scholar 

  75. Shinwari, Z. K., Nakashima, K., Miura, S., Kasuga, M., Seki, M., Yamaguchi-Shinozaki, K., and Shinozaki, K. (1998) An Arabidopsis gene family encoding DRE/CRT binding proteins involved in low-temperature-responsive gene expression, Biochem. Biophys. Res. Commun., 250, 161–170.

    Article  CAS  PubMed  Google Scholar 

  76. Agarwal, M., Hao, Y., Kapoor, A., Dong, C. H., Fujii, H., Zheng, X., and Zhu, J. K. (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 

  77. Chen, Y., Chen, Z., Kang, J., Kang, D., Gu, H., and Qin, G. (2013) AtMYB14 regulates cold tolerance in Arabidopsis, Plant Mol. Biol. Rep., 31, 87–97.

    Article  CAS  PubMed  Google Scholar 

  78. Lee, H. G., and Seo, P. J. (2015) The MYB96-HHP module integrates cold and abscisic acid signaling to activate the CBF–COR pathway in Arabidopsis, Plant J., 82, 962–977.

    Article  CAS  PubMed  Google Scholar 

  79. Chen, C. C., Liang, C. S., Kao, A. L., and Yang, C. C. (2009) HHP1 is involved in osmotic stress sensitivity in Arabidopsis, J. Exp. Bot., 60, 1589–1604.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Chen, C. C., Liang, C. S., Kao, A. L., and Yang, C. C. (2010) HHP1, a novel signalling component in the cross-talk between the cold and osmotic signalling pathways in Arabidopsis, J. Exp. Bot., 61, 3305–3320.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Mittler, R., Kim, Y., Song, L., Coutu, J., Coutu, A., Ciftci-Yilmaz, S., Lee, H., Stevenson, B., and Zhu, J. K. (2006) Gain- and loss-of-function mutations in Zat10 enhance the tolerance of plants to abiotic stress, FEBS Lett., 580, 6537–6542.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Davletova, S., Schlauch, K., Coutu, J., and Mittler, R. (2005) The zinc-finger protein Zat12 plays a central role in reactive oxygen and abiotic stress signaling in Arabidopsis, Plant Phys., 139, 847–856.

    Article  CAS  Google Scholar 

  83. Vogel, J. T., Zarka, D. G., Van Buskirk, H. A., Fowler, S. G., and Thomashow, M. F. (2005) Roles of the CBF2 and ZAT12 transcription factors in configuring the low temperature transcriptome of Arabidopsis, Plant J., 41, 195–211.

    Article  CAS  PubMed  Google Scholar 

  84. Lee, H., Guo, Y., Ohta, M., Xiong, L., Stevenson, B., and Zhu, J. K. (2002) LOS2, a genetic locus required for cold-responsive gene transcription encodes a bi-functional enolase, EMBO J., 21, 2692–2702.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  86. Zhou, M. Q., Shen, C., Wu, L. H., Tang, K. X., and Lin, J. (2011) CBF-dependent signaling pathway: a key responder to low temperature stress in plants, Crit. Rev. Biotech., 31, 186–192.

    Article  CAS  Google Scholar 

  87. He, X. J., Hsu, Y. F., Zhu, S., Liu, H. L., Pontes, O., Zhu, J., Cui, X., Wang, C. S., and Zhu, J. K. (2009) A conserved transcriptional regulator is required for RNA-directed DNA methylation and plant development, Genes Dev., 23, 2717–2722.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Chan, Z., Wang, Y., Cao, M., Gong, Y., Mu, Z., Wang, H., Hu, Y., Deng, X., He, X. J., and Zhu, J. K. (2016) RDM4 modulates cold stress resistance in Arabidopsis partially through the CBF-mediated pathway, New Phytol., 209, 1527–1539.

    Article  CAS  PubMed  Google Scholar 

  89. Sasaki, K., Kim, M. H., Kanno, Y., Seo, M., Kamiya, Y., and Imai, R. (2015) Arabidopsis cold shock domain protein 2 influences ABA accumulation in seed and negatively regulates ger-mination, Biochem. Biophys. Res. Commun., 456, 380–384.

    Article  CAS  PubMed  Google Scholar 

  90. Liu, Z., Jia, Y., Ding, Y., Shi, Y., Li, Z., Guo, Y., Gong, Z., and Yang, S. (2017) Plasma membrane CRPK1-medi-ated phosphorylation of 14-3-3 proteins induces their nuclear import to fine-tune CBF signaling during cold response, Mol. Cell, doi: 10.1016/j.molcel.

    Google Scholar 

  91. Cotelle, V., Meek, S. E., Provan, F., Milne, F. C., Morrice, N., and MacKintosh, C. (2000) 14-3-3s regulate global cleavage of their diverse binding partners in sugar-starved Arabidopsis cells, EMBO J., 19, 2869–2876.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Catala, R., Lopez-Cobollo, R., Mar Castellano, M., Angosto, T., Alonso, J. M., Ecker, J. R., and Salinas, J. (2014) The Arabidopsis 14-3-3 protein rare cold inducible 1A links low-temperature response and ethylene biosynthesis to regulate freezing tolerance and cold acclimation, Plant Cell, 26, 3326–3342.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Baker, S. S., Wilhelm, K. S., and Thomashow, M. F. (1994) The 5′-region of Arabidopsis thaliana cor15a has cis-acting elements that confer cold-, drought- and ABA-regulated gene expression, Plant Mol. Biol., 24, 701–713.

    Article  CAS  PubMed  Google Scholar 

  94. Nakashima, K., and Yamaguchi-Shinozaki, K. (2013) ABA signaling in stress-response and seed development, Plant Cell Rep., 32, 959–970.

    Article  CAS  PubMed  Google Scholar 

  95. Knight, H., Zarka, D. G., Okamoto, H., Thomashow, M. F., and Knight, M. R. (2004) Abscisic acid induces CBF gene transcription and subsequent induction of cold-regulated genes via the CRT promoter element, Plant Physiol., 135, 1710–1717.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Yamaguchi-Shinozaki, K., and Shinozaki, K. (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses, Ann. Rev. Plant Biol., 57, 781–803.

    Article  CAS  Google Scholar 

  97. Roychoudhury, A., Paul, S., and Basu, S. (2013) Cross-talk between abscisic acid-dependent and abscisic acid-independent pathways during abiotic stress, Plant Cell Rep., 32, 985–1006.

    Article  CAS  PubMed  Google Scholar 

  98. Lee, S. J., Kang, J. Y., Park, H. J., Kim, M. D., Bae, M. S., Choi, H. I., and Kim, S. Y. (2010) DREB2C interacts with ABF2, a bZIP protein regulating abscisic acid-responsive gene expression, and its overexpression affects abscisic acid sensitivity, Plant Physiol., 153, 716–727.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. An, D., Ma, Q., Wang, H., Yang, J., Zhou, W., and Zhang, P. (2017) Cassava C-repeat binding factor 1 gene responds to low temperature and enhances cold tolerance when overexpressed in Arabidopsis and cassava, Plant Mol. Biol., doi: 10.1007/s11103-017-0596-6.

    Google Scholar 

  100. Poppenberger, B., Rozhon, W., Khan, M., Husar, S., Adam, G., Luschnig, C., Fujioka, S., and Sieberer, T. (2011) CESTA, a positive regulator of brassinosteroid biosynthesis, EMBO J., 30, 1149–1161.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Khan, M., Rozhon, W., Unterholzner, S. J., Chen, T., Eremina, M., Wurzinger, B., Bachmair, A., Teige, M., Sieberer, T., Isono, E., and Poppenberger, B. (2014) Interplay between phosphorylation and SUMOylation events determines CESTA protein fate in brassinosteroid signalling, Nat. Commun., 5, 4687.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Eremina, M., Unterholzner, S. J., Rathnayake, A. I., Castellanos, M., Khan, M., Kugler, K. G., May, S. T., Mayer, K. F., Rozhon, W., and Poppenberger, B. (2016) Brassinosteroids participate in the control of basal and acquired freezing tolerance of plants, Proc. Natl. Acad. Sci. USA, 113, 5982–5991.

    Article  CAS  Google Scholar 

  103. Li, H., Ye, K., Shi, Y., Cheng, J., Zhang, X., and Yang, S. (2017) BZR1 positively regulates freezing tolerance via CBF-dependent and CBF-independent pathways in Arabidopsis, Mol. Plant., 10, 545–559.

    Article  CAS  PubMed  Google Scholar 

  104. Zentella, R., Zhang, Z. L., Park, M., Thomas, S. G., Endo, A., Murase, K., Fleet, C. M., Jikumaru, Y., Nambara, E., Kamiya, Y., and Sun, T. P. (2007) Global analysis of della direct targets in early gibberellin signaling in Arabidopsis, Plant Cell, 19, 3037–3057.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Ravid, J., Spitzer-Rimon, B., Takebayashi, Y., Seo, M., Can’ani, A., Aravena-Calvo, J., Masci, T., Farhi, M., and Vainstein, A. (2017) GA as a regulatory link between the showy floral traits color and scent, New Phytol., doi: 10.1111/nph.14504.

    Google Scholar 

  106. Achard, P., Renou, J. P., Berthome, R., Harberd, N. P., and Genschik, P. (2008) Plant DELLAs restrain growth and promote survival of adversity by reducing the levels of reactive oxygen species, Curr. Biol., 18, 656–660.

    Article  CAS  PubMed  Google Scholar 

  107. Li, K. L., Bai, X., Li, Y., Cai, H., Ji, W., Tang, L. L., Wen, Y. D., and Zhu, Y. M. (2011) GsGASA1 mediated root growth inhibition in response to chronic cold stress is marked by the accumulation of DELLAs, J. Plant Physiol., 168, 2153–2160.

    Article  CAS  PubMed  Google Scholar 

  108. Zhang, Y. Q., Liu, Z. J., Liu, J. P., Lin, S., Wang, J. F., Lin, W. X., and Xu, W. F. (2017) GA–DELLA pathway is involved in regulation of nitrogen deficiency-induced anthocyanin accumulation, Plant Cell Rep., doi: 10.1007/s00299-017-2102–2107.

    Google Scholar 

  109. Achard, P., Gong, F., Cheminant, S., Alioua, M., Hedden, P., and 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  CAS  PubMed  PubMed Central  Google Scholar 

  110. Niu, S. H., Gao, Q., Li, Z. X., Chen, X. Y., and Li, W. (2014) The role of gibberellin in the CBF1-mediated stress-response pathway, Plan. Mol. Biol. Rep., 32, 852–863.

    Article  CAS  Google Scholar 

  111. Zhou, M., Chen, H., Wei, D., Ma, H., and Lin, J. (2017) Arabidopsis CBF3 and DELLAs positively regulate each other in response to low temperature, Sci. Rep., 7, 39819.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Yang, D. L., Yao, J., Mei, C. S., Tong, X. H., Zeng, L. J., Li, Q., Xiao, L. T., Sun, T. P., Li, J., Deng, X. W., Lee, C. M., Thomashow, M. F., Yang, Y., He, Z., and He, S. Y. (2012) Plant hormone jasmonate prioritizes defense over growth by interfering with gibberellin signaling cascade, Proc. Natl. Acad. Sci. USA, 109, 1192–1200.

    Article  Google Scholar 

  113. Wild, M., Daviere, J. M., Cheminant, S., Regnault, T., Baumberger, N., Heintz, D., Baltz, R., Genschik, P., and Achard, P. (2012) The Arabidopsis DELLA RGA-LIKE3 is a direct target of MYC2 and modulates jasmonate signal-ing responses, Plant Cell, 24, 3307–3319.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. Hu, Y., Jiang, L., Wang, F., and Yu, D. (2013) Jasmonate regulates the inducer of cbf expression-C-repeat binding factor/DRE binding factor 1 cascade and freezing tolerance in Arabidopsis, Plant Cell, 25, 2907–2924.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. Shi, Y., Tian, S., Hou, L., Huang, X., Zhang, X., Guo, H., and Yang, S. (2012) Ethylene signaling negatively regulates freezing tolerance by repressing expression of CBF and type-A ARR genes in Arabidopsis, Plant Cell, 24, 2578–2595.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  116. Chao, Q., Rothenberg, M., Solano, R., Roman, G., Terzaghi, W., and Ecker, J. R. (1997) Activation of the eth-ylene gas response pathway in Arabidopsis by the nuclear protein ethylene-insensitives and related proteins, Cell, 89, 1133–1144.

    Article  CAS  PubMed  Google Scholar 

  117. Bolt, S., Zuther, E., Zintl, S., Hincha, D. K., and Schmulling, T. (2017) ERF105 is a transcription factor gene of Arabidopsis thaliana required for freezing tolerance and cold acclimation, Plant. Cell. Environ., 40, 108–120.

    Article  CAS  PubMed  Google Scholar 

  118. Vanneste, S., and Friml, J. (2009) Auxin: a trigger for change in plant development, Cell, 136, 1005–1016.

    Article  CAS  PubMed  Google Scholar 

  119. Eremina, M., Rozhon, W., and Poppenberger, B. (2016) Hormonal control of cold stress responses in plants, Cell. Mol. Life Sci., 73, 797–810.

    Article  CAS  PubMed  Google Scholar 

  120. Gaveliene, V., Novickiene, L., and Pakalniskyte, L. (2013) Effect of auxin physiological analogues on rapeseed (Brassica napus) cold hardening, seed yield and quality, J. Plant Res., 126, 283–292.

    Article  CAS  PubMed  Google Scholar 

  121. Dou, M., Cheng, S., Zhao, B., Xuan, Y., and Shao, M. (2016) The indeterminate domain protein ROC1 regulates chilling tolerance via activation of DREB1B/CBF1 in rice, Intern. J. Mol. Sci., 17, 233.

    Article  CAS  Google Scholar 

  122. Park, S. J., Kim, S. L., Lee, S., Je, B. I., Piao, H. L., Park, S. H., Kim, C. M., Ryu, C. H., Park, S. H., Xuan, Y. H., Colasanti, J., An, G., and Han, C. D. (2008) Rice indeterminate 1 (OsId1) is necessary for the expression of Ehd1 (early heading date 1) regardless of photoperiod, Plant J., 56, 1018–1029.

    Article  CAS  PubMed  Google Scholar 

  123. Feurtado, J. A., Huang, D., Wicki-Stordeur, L., Hemstock, L. E., Potentier, M. S., Tsang, E. W., and Cutler, A. J. (2011) The Arabidopsis C2H2 zinc finger indeterminate domain 1/enhydrous/promotes the transition to germination by regulating light and hormonal signaling during seed maturation, Plant Cell, 23, 1772–1794.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  124. Seo, P. J., Ryu, J., Kang, S. K., and Park, C. M. (2011) Modulation of sugar metabolism by an indeterminate domain transcription factor contributes to photoperiodic flowering in Arabidopsis, Plant J., 65, 418–429.

    Article  CAS  PubMed  Google Scholar 

  125. Veselov, D. S., Kudoyarova, G. R., Kudryakova, N. V., and Kusnetsov, V. V. (2017) Role of cytokinins in stress resistance of plants, Rus. J. Plant Physiol., 64, 15–27.

    Article  CAS  Google Scholar 

  126. Jeon, J., Kim, N. Y., Kim, S., Kang, N. Y., Novak, O., Ku, S. J., Cho, C., Lee, D. J., Lee, E. J., Strnad, M., and Kim, J. (2010) A subset of cytokinin two-component signaling system plays a role in cold temperature stress response in Arabidopsis, J. Biol. Chem., 285, 23371–23386.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  127. Huang, J. G., Yang, M., Liu, P., Yang, G. D., Wu, C. A., and Zheng, C. C. (2009) GhDREB1 enhances abiotic stress tolerance, delays GA-mediated development and represses cytokinin signalling in transgenic Arabidopsis, Plant Cell. Environ., 32, 1132–1145.

    Article  CAS  PubMed  Google Scholar 

  128. Wang, Q., An, B., Wei, Y., Reiter, R. J., Shi, H., Luo, H., and He, C. (2016) Melatonin regulates root meristem by repressing auxin synthesis and polar auxin transport in Arabidopsis, Front. Plant Sci., 7, 1882.

    PubMed  PubMed Central  Google Scholar 

  129. Zhao, H., Ye, L., Wang, Y., Zhou, X., Yang, J., Wang, J., Cao, K., and Zou, Z. (2016) Melatonin icreases the chill-ing tlerance of chloroplast in cucumber seedlings by regu-lating photosynthetic electron flux and the ascorbate-glu-tathione cycle, Front. Plant Sci., 7, 1814.

    PubMed  PubMed Central  Google Scholar 

  130. Shi, H., Qian, Y., Tan, D. X., Reiter, R. J., and He, C. (2015) Melatonin induces the transcripts of CBF/DREB1s and their involvement in both abiotic and biotic stresses in Arabidopsis, J. Pineal. Res., 59, 334–342.

    Article  CAS  PubMed  Google Scholar 

  131. Pruneda-Paz, J. L., and Kay, S. A. (2010) An expanding universe of circadian networks in higher plants, Trends Plant Sci., 15, 259–265.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  132. Nakamichi, N., Takao, S., Kudo, T., Kiba, T., Wang, Y., Kinoshita, T., and Sakakibara, H. (2016) Improvement of Arabidopsis biomass and cold, drought and salinity stress tolerance by modified circadian clock-associated pseudo-response regulators, Plant Cell. Physiol., 57, 1085–1097.

    Article  CAS  PubMed  Google Scholar 

  133. Pokhilko, A., Fernandez, A. P., Edwards, K. D., Southern, M. M., Halliday, K. J., and Millar, A. J. (2012) The clock gene circuit in Arabidopsis includes a repressilator with additional feedback loops, Mol. Systems Biol., 8, 574.

    Article  CAS  Google Scholar 

  134. Nakamichi, N., Kiba, T., Henriques, R., Mizuno, T., Chua, N. H., and Sakakibara, H. (2010) Pseudo-response regulators 9, 7, and 5 are transcriptional repressors in the Arabidopsis circadian clock, Plant Cell, 22, 594–605.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  135. Pokhilko, A., Hodge, S. K., Stratford, K., Knox, K., Edwards, K. D., Thomson, A. W., Mizuno, T., and Millar, A. J. (2010) Data assimilation constrains new connections and components in a complex, eukaryotic circadian clock model, Mol. Systems Biol., 6, 416.

    Article  CAS  Google Scholar 

  136. Seo, P. J., Park, M. J., Lim, M. H., Kim, S. G., Lee, M., Baldwin, I. T., and Park, C. M. (2012) A self-regulatory circuit of circadian clock-associated1 underlies the circadian clock regulation of temperature responses in Arabidopsis, Plant Cell, 24, 2427–2442.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  137. Fowler, S. G., Cook, D., and Thomashow, M. F. (2005) Low temperature induction of Arabidopsis CBF1, 2, and 3 is gated by the circadian clock, Plant Physiol., 137, 961–968.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  138. Dong, M. A., Farre, E. M., and Thomashow, M. F. (2011) Circadian clock-associated 1 and late elongated hypocotyl regulate expression of the C-repeat binding factor (CBF) pathway in Arabidopsis, Proc. Natl. Acad. Sci. USA, 108, 7241–7246.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  139. Chow, B. Y., Sanchez, S. E., Breton, G., Pruneda-Paz, J. L., Krogan, N. T., and Kay, S. A. (2014) Transcriptional regulation of LUX by CBF1 mediates cold input to the cir-cadian clock in Arabidopsis, Curr. Biol., 24, 1518–1524.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  140. Maibam, P., Nawkar, G. M., Park, J. H., Sahi, V. P., Lee, S. Y., and Kang, C. H. (2013) The influence of light quality, circadian rhythm, and photoperiod on the CBF-mediated freezing tolerance, Int. J. Mol. Sci., 14, 11527–11543.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  141. Moglich, A., Yang, X., Ayers, R. A., and Moffat, K. (2010) Structure and function of plant photoreceptors, Ann. Rev. Plant Biol., 61, 21–47.

    Article  CAS  Google Scholar 

  142. Wisniewski, M., Nassuth, A., Teulieres, C., Marque, C., Rowland, J., Cao, P. B., and Brown, A. (2014) Genomics of cold hardiness in woody plants, Crit. Rev. Plant Sci., 33, 92–124.

    Article  CAS  Google Scholar 

  143. Wang, F., Guo, Z., Li, H., Wang, M., Onac, E., Zhou, J., Xia, X., Shi, K., Yu, J., and Zhou, Y. (2016) Phytochrome A and B function antagonistically to regulate cold tolerance via abscisic acid-dependent jasmonate signaling, Plant Physiol., 170, 459–471.

    Article  CAS  PubMed  Google Scholar 

  144. Catala, R., Medina, J., and Salinas, J. (2011) Integration of low temperature and light signaling during cold acclimation response in Arabidopsis, Proc. Natl. Acad. Sci. USA, 108, 16475–16480.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Author notes

  1. These authors contributed equally to this work.

Authors and Affiliations

  1. College of Bioscience and Biotechnology, Shenyang Agricultural University, Shenyang, Liaoning, 110866, China

    Da-Zhi Wang, Ya-Nan Jin, Xi-Han Ding, Shan-Shan Zhai & Zhi-Fu Guo

  2. College of Agronomy, Shenyang Agricultural University, Shenyang, 110866, China

    Ya-Nan Jin

  3. Key Laboratory of Agricultural Biotechnology of Liaoning Province, Shenyang Agricultural University, Shenyang, Liaoning, 110866, China

    Wen-Jia Wang & Li-Ping Bai

Authors
  1. Da-Zhi Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ya-Nan Jin
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xi-Han Ding
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Wen-Jia Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Shan-Shan Zhai
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Li-Ping Bai
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Zhi-Fu Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Li-Ping Bai or Zhi-Fu Guo.

Additional information

Published in Russian in Biokhimiya, 2017, Vol. 82, No. 10, pp. 1444-1462.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, DZ., Jin, YN., Ding, XH. et al. Gene regulation and signal transduction in the ICE–CBF–COR signaling pathway during cold stress in plants. Biochemistry Moscow 82, 1103–1117 (2017). https://doi.org/10.1134/S0006297917100030

Download citation

  • Received:

  • Revised:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0006297917100030

Keywords

Search

Navigation