Abstract
Main conclusion
ICEs are key transcription factors in response to cold in plant, they also balance plant growth and stress tolerance. Thus, we systematize the information about ICEs published to date.
Abstract
Low temperature is an important factor affecting plant growth and development. Exposing to cold condition results in a suit of effects on plants including reduction of plant growth and reproduction, and decrease in crop yield and quality. Plants have evolved a series of strategies to deal with cold stress such as reprogramming of the expression of genes and transcription factors. ICEs (Inducer of CBF Expression), as transcription factors regulating CBFs (C-repeat binding factor), play key roles in balancing plant growth and stress tolerance. Studies on ICEs focused on the function of ICEs on cold tolerance, growth and development; post-translational modifications of ICEs and crosstalk between the ICEs and phytohormones. In this review, we focus on systematizing the information published to date. We summarized the main advances of the functions of ICEs on the cold tolerance, growth and development. And we also elaborated the regulation of ICEs protein stability including phosphorylation, ubiquitination and SUMOylation of ICE. Finally, we described the function of ICEs in the crosstalk among different phytohormone signaling pathway and cold stress. This review provides perspectives for ongoing research about cold tolerance, growth and development in plant.
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Change history
21 March 2022
A Correction to this paper has been published: https://doi.org/10.1007/s00425-022-03878-3
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(8):2117–2129. https://doi.org/10.1105/tpc.108.058941
An JP, Wang XF, Zhang XW, You CX, Hao YJ (2020) Apple B-box protein BBX37 regulates jasmonic acid mediated cold tolerance through the JAZ-BBX37-ICE1-CBF pathway and undergoes MIEL1-mediated ubiquitination and degradation. New Phytol 229(5):2707–2729. https://doi.org/10.1111/nph.17050
An JP, Xu RR, Liu X, Su L, Yang K, Wang XF, Wang GL, You CX (2021) ABI4 interacts with ICE1 and JAZ proteins to regulate abscisic acid signaling-mediated cold tolerance in apple. J Exp Bot. https://doi.org/10.1093/jxb/erab433
Baker SS, Wilhelm KS, Thomashow MF (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(5):701–713. https://doi.org/10.1007/BF00029852
Bremer A, Kent B, Hau T (2017) Intrinsically disordered stress protein COR15A resides at the membrane surface during dehydration. Biophys J 113(3):572–579. https://doi.org/10.1016/j.bpj.2017.06.027
Chen L, Guan LP, Qian PP, Xu F, Wu ZL, Wu YJ, He K, Gou XP, Li J, Hou SW (2016) NRPB3, the third largest subunit of RNA polymerase II, is essential for stomatal patterning and differentiation in Arabidopsis. Development 143(9):1600–1611. https://doi.org/10.1242/dev.129098
Chen K, Li GJ, Bressan RA, Song CP, Zhu JK, Zhao Y (2020) Abscisic acid dynamics, signaling, and functions in plants. J Integr Plant Biol 62(1):25–54. https://doi.org/10.1111/jipb.12899
Chen XX, Ding YL, Yang YQ, Song CP, Wang BS, Yang SH, Guo Y, Gong ZZ (2021) Protein kinases in plant responses to drought, salt, and cold stress. J Integr Plant Biol 63(1):53–78. https://doi.org/10.1111/jipb.13061
Cheng L, Zhang W, Hu J, Zhang Z, Lin Y (2020) Characterization of the key region and phosphorylation sites of EcaICE1 for its molecular interaction with EcaHOS1 protein in eucalyptus camaldulensis. Plant Biol 23(2):400–406. https://doi.org/10.1101/861088
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(8):1043–1054. https://doi.org/10.1101/gad.1077503
Clouse SD, Sasse JM (1998) BRSSINOSTEROIDS: essential regulators of plant growth and development. Annu Rev Plant Physiol Mol Biol 49(1):427–451. https://doi.org/10.1146/annurev.arplant.49.1.427
Colebrook EH, Thomas SG, Phillips AL, Hedden P (2014) The role of gibberellin signaling in plant responses to abiotic stress. J Exp Bot 217(1):67–75. https://doi.org/10.1242/jeb.089938
Daviere JM, Achard P (2013) Gibberellin signaling in plants. Development 140(6):1147–1151. https://doi.org/10.1242/dev.087650
Ding YL, Li H, Zhang XY, Xie Q, Gong ZZ, Yang SH (2015) OST1 kinase modulates freezing tolerance by enhancing ICE1 stability in Arabidopsis. Dev Cell 32(3):278–289. https://doi.org/10.1016/j.devcel.2014.12.023
Ding YL, Jia YX, Shi YT, Zhang XY, Song CP, Goong ZZ, Yang SH (2017) OST1-mediated BTF3L phosphorylation positively regulates CBFs during plant cold responses. EMBO J 37:e98228. https://doi.org/10.15252/embj.201798228
Ding YL, Lv J, Shi YT, Gao JP, Hua J, Song CP, Gong ZZ, Yang SH (2019) EGR2 phosphatase regulates OST1 kinase activity and freezing tolerance in Arabidopsis. EMBO J 38(1):e99819
Domagalska MA, Schomburg FM, Amasino RM, Vierstra RD, Nagy F, Davis SJ (2007) Attenuation of brassinosteroid signaling enhances FLC expression and delays flowering. Development 134(15):2841–2850. https://doi.org/10.1242/dev.02866
Dong CH, Agarwal M, Zhang YY, 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 ICE. Proc Natl Acad Sci 103(21):8281–8286. https://doi.org/10.1073/pnas.0602874103
Dong MA, Farré EM, Thomashow MF (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 108(17):7241–7246. https://doi.org/10.1073/pnas.1103741108
Elrouby N (2017) Regulation of plant cellular and organismal development by SUMO. Adv Exp Med Biol 963:227–247
Eremina M, Unterholzner SJ, Rathnayake AI, Castellanos M, Khan M, Kugler KG, May ST, Mayer KFX, Rozhon W, Poppenberger B (2016) Brassinosteroids participate in the control of basal and acquired freezing tolerance of plants. Proc Natl Acad Sci 113(40):e5982–e5991. https://doi.org/10.1073/pnas.1611477113
Fan ZQ, Chen JY, Kuang JF, Lu WJ, Shan W (2017) The banana fruit SINA ubiquitin ligase MaSINA1 regulates the stability of MaICE1 to be negatively involved in cold stress response. Front Plant Sci 8:995. https://doi.org/10.3389/fpls.2017.00995
Feng HL, Ma NN, Meng X, Zhang S, Wang JR, Chai S, Meng QW (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. https://doi.org/10.1016/j.plaphy.2013.09.014
Finkelstein RR (1994) Mutations at two new Arabidopsis ABA response loci are similar to the abi3 mutations. Plant J 5(6):765–771. https://doi.org/10.1046/j.1365-313X.1994.5060765.x
Finkelstein RR, Gampala SSL, Rock CD (2002) Abscisic acid signaling in seeds and seedlings. Plant Cell 14(1):S15–S45. https://doi.org/10.1105/tpc.010441
Frey A, Godin B, Bonnet M, Sotta B, Marion-Poll A (2004) Maternal synthesis of abscisic acid controls seeds development and yield in Nicotiana plumbaginifolia. Planta 218(6):958–964
Fukaki H, Fujisawa H, Tasaka M (1996) Gravitropic response of inflorescence stems in Arabidopsis thaliana. Plant Physiol 110(3):933–943
Furihata T, Maruyama K, Fujita Y, Umezawa T, Yoshida R, Shinozaki K, Shinozaki KY (2006) Abscisic acid-dependent multisite phosphorylation regulates the activity of a transcription activator AREB1. Proc Natl Acad Sci 103(6):1988–1993. https://doi.org/10.1073/pnas.0505667103
Fursova OV, Pogorelko G, Tarasov VA (2009) Identification of ICE2, a gene involved in cold acclimation which determines freezing tolerance in Arabidopsis thaliana. Gene 429(1–2):98–103. https://doi.org/10.1016/j.gene.2008.10.016
Furuya T, Matsuoka D, Nanmori T (2013) Phosphorylation of Arabidopsis thaliana MEKK1 via Ca2+ signaling as a part of the cold stress response. J Plant Res 126(6):833–840
Gilmour SJ, Hajela RK, Thomashow MF (1988) Cold acclimation in Arabidopsis thaliana. Plant Physiol 87(3):745–750. https://doi.org/10.1104/pp.87.3.745
Gilmour SJ, Zarka D, Stockinger EJ, Salazar M (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(4):433–442. https://doi.org/10.1046/j.1365-313x.1998.00310.x
Gong Z, Morales-Ruiz T, Ariza RR, Roldán-Arjona T, David L, Zhu JK (2002) ROS1, a repressor of transcriptional gene silencing in Arabidopsis, encodes a DNA glycosylase/lyase. Cell 111(6):803–814. https://doi.org/10.1016/s0092-8674
Gong ZZ, Xiong LM, Shi HZ, Yang SH, Herrera-Estrella LR, Xu GH, Chao DY, Li J, Wang PY, Qin F, Li JJ, Ding YL, Shi YT, Wang Y, Yang YQ, Guo Y, Zhu JK (2020) Plant abiotic stress response and nutrient use efficiency. Sci China Life Sci 63(5):635–674. https://doi.org/10.1007/s.11427-020-1683-x
Grégoire D, Audrey C, Steven M, Pauline W, Johanne T, Marie-France G, Pierre C, Bertrand D, Gwyneth I (2014) Endosperm breakdown in Arabidopsis requires heterodimers of the basic helix-loop-helix proteins ZHOUPI and INDUCER OF CBP EXPRESSION 1. Development 141(6):1222–1227. https://doi.org/10.1242/dev.103531
Han X, Zhang MH, Yang ML, Hu YR (2020) Arabidopsis JAZ proteins interact with and suppress RHD6 transcription factor to regulate jasmonate-stimulated root hair development. Plant Cell 32(4):1049–1062
He ZQ, Huang TT, Ao K, Yan XF, Huang Y (2017) Sumoylation, phosphorylation, and acetylation fine-tune the turnover of plant immunity components mediated by ubiquitination. Front Plant Sci 8:1682. https://doi.org/10.3389/fpls.2017.01682
Heidaand L, Amiri RM (2010) What happens in plant molecular responses to cold stress? Acta Physiol Plant 32(3):419–431
Hetherington AM, Woodward FI (2003) The role of stomata in sensing and driving environmental change. Nature 424(6951):901–908
Hu YR, Jiang LQ, Wang F, Yu DQ (2013) Jasmonate regulates the INDUCER OF CBF EXPRESSION-C-REPEAT BINDING FACTOR/DRE BIING FACTOR1 cascade and freezing tolerance in Arabidopsis. Plant Cell 25(8):2907–2924. https://doi.org/10.1105/tpc.113.112631
Huang JG, Yang M, Liu P, Yang GD, Wu CA, Zheng CC (2009) GhDREB1 enhances abiotic stress tolerance, delays GA-mediated development and represses cytokinin signalling in transgenic Arabidopsis. Plant Cell Environ 32(8):1132–1145. https://doi.org/10.1111/j.1365-3040.2009.01995.x
Ichimura K, Mizoguchi T, Yoshida R, Yuasa T, Shinozaki K (2010) Various abiotic stresses rapidly activate Arabidopsis MAP kinases AtMPK4 and AtMPK6. Plant J 24(5):655–665. https://doi.org/10.1046/j.1365-313x.2000.00913.x
Jung JH, Seo PJ, Park MJ (2013) The E3 ubiquitin ligase HOS1 regulates Arabidopsis flowering by mediating CONSTANS degradation under cold stress. J Biol Chem 287(4):43277–43287. https://doi.org/10.4161/psb.23780
Kagale S, Divi UK, Krochko JE, Keller WA, Krishna P (2007) Brassinosteroid confers tolerance in Arabidopsis thaliana and Brassica napus to a range of abiotic stresses. Planta 225(2):353–364
Kanaoka MM, Pillitteri LJ, Fujii H, Yoshida Y, Bogenschutz NL, Takabayashi J, Zhu JK, Toriia KU (2008) SCREAM/ICE1 and SCREAM2 specify three cell-state transitional steps leading to Arabidopsis stomatal differentiation. Plant Cell 20(7):1775–1785. https://doi.org/10.1105/tpc.108.060848
Kanno Y, Jikumaru Y, Hanada A, Nambara E, Abrams SR, Kamiya Y, Seo M (2010) Comprehensive hormone profiling in developing Arabidopsis seeds: Examination of the site of ABA biosynthesis, ABA transport and hormone interactions. Plant Cell Physiol 51(12):1988–2001. https://doi.org/10.1093/pcp/pcq158
Karssen CM, Brinkhorst-van der Swan DLC, Breekland AE, Koornneef M (1983) Induction of dormancy during seed development by endogenous abscisic acid: studies on abscisic acid deficient genotypes of Arabidopsis thaliana (L.) Heynh. Planta 157(2):158–165
Kidokoro S, Kim JS, Ishikawa T, Suzuki T, Shinozaki K, Yamaguchi-Shinozaki K (2020) DREB1A/CBF3 is repressed by transgene-induced DNA methylation in the arabidopsis ice1–1 mutant. Plant Cell 32(4):1035–1048. https://doi.org/10.1105/tpc.19.00532
Kim KN, Yong HC, Grant JJ, Pandey GK, Luan S (2003) CIPK3, a calcium sensor-associated protein kinase that regulates abscisic acid and cold signal transduction in Arabidopsis. Plant Cell 15(2):411–423. https://doi.org/10.1105/tpc.006858
Kim JM, Sasaki T, Ueda M, Sako K, Seki M (2015a) Chromatin changes in response to drought, salinity, heat, and cold stresses in plants. Front Plant Sci 6:114. https://doi.org/10.3389/fpls.2015.00114
Kim YS, Lee M, Lee JH, Lee HJ, Park CM (2015b) The unified ICE-CBF pathway provides a transcriptional feedback control of freezing tolerance during cold acclimation in Arabidopsis. Plant Mol Biol 89:187–201. https://doi.org/10.1007/s11103-015-0365-3
Kim JS, Kidokoro S, Shinozaki K, Yamaguchi-Shinozaki K (2020) DNA demethylase ROS1 prevents inheritable DREB1A/CBF3 repression by transgene-induced promoter methylation in the Arabidopsis ice1-1 mutant. Plant Mol Biol 104(6):1–8. https://doi.org/10.1007/s11103-020-01061-4
Klimecka M, Bucholc M, Maszkowska J, Szczegielniak J (2020) Regulation of ABA-Non-Activated SNF1-Related protein kinase 2 signaling pathways by phosphatidic acid. Int J Mol Sci 21(14):4984. https://doi.org/10.3390/ijms21144984
Kolesnikov YS, Nokhrina KP, Kretynin SV, Volotovski ID, Martinec J, Romanov GA, Kravets VS (2012) Molecular structure of phospholipase D and regulatory mechanisms of its activity in plant and animal cells. Biochemistry (mosc) 77(1):1–14
Kundu S, Gantait S (2017) Abscisic acid signal crosstalk during abiotic stress response. Plant Gene 11:61–69. https://doi.org/10.1016/j.plgene.2017.04.007
Lee JH, Park CM (2015) Integration of photoperiod and cold temperature signals into flowering genetic pathways in Arabidopsis. Plant Signal Behav 10(11):e1089373. https://doi.org/10.1080/15592324.2015.1089373
Lee JH, 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(7):912–924
Lee BH, Henderson DA, Zhu JK (2005) The Arabidopsis cold-responsive transcriptome and its regulation by ICE1. Plant Cell 17(11):3155–3175. https://doi.org/10.1105/tpc.105.035568
Li D, Liu C, Shen LS, Wu Y, Chen HY, Robertson M, Helliwell CA, Ito T, Meyerowitz E, Yu H (2008) A repressor complex governs the integration of flowering signals in Arabidopsis. Dev Cell 15(1):110–120
Li H, Ye KY, Shi YT, Cheng JK, Zhang XY, Yang SH (2017a) BZR1 positively regulates freezing tolerance via CBF-Dependent and CBF-independent pathways in Arabidopsis. Mol Plant 10(004):545–559. https://doi.org/10.1016/j.molp.2017.01.004
Li H, Ding Y, Shi Y, Zhang X, Zhang S, Gong Z, Yang S (2017b) MPK3- and MPK6-mediated ICE1 phosphorylation negatively regulates ICE1 stability and freezing tolerance in Arabidopsis. Dev Cell 43:630–642. https://doi.org/10.1016/j.devcel.2017.09.025
Li H, Ding YL, Shi YT, Zhang XY, Zhang SQ, Gong ZZ, Yang SH (2019) MPK3- and MPK6-mediated ICE1 phosphorylation negatively regulates ICE1 stability and freezing tolerance in Arabidopsis. Dev Cell 43(5):630–642. https://doi.org/10.1016/j.devcel.2017.09.025
Li M, Wang CH, Shi JL, Zhang YJ, Liu T, Qi HY (2021) Abscisic acid and putrescine synergistically regulate the cold tolerance of melon seedlings. Plant Physiol Biochem 166:1054–1064. https://doi.org/10.1016/j.plaphy.2021.07.011
Liang CH, Yang CC (2015) Identification of ICE1 as a negative regulator of ABA-dependent pathways in seeds and seedlings of Arabidopsis. Plant Mol Biol 88(4–5):459–470
Lu X, Yang L, Yu MY, Lai JB, Wang C, McNeil D, Zhou MX, Yang CW (2017) A novel Zea mays ssp. mexicana L. MYC-type ICE-like transcription factor gene ZmICE1, enhances freezing tolerance in transgenic Arabidopsis thaliana. Plant Physiol Biochem 113:78–88. https://doi.org/10.1016/j.plaphy.2017.02.002
Luo P, Li ZY, Chen W, Xing W, Yang J, Cui YY (2020) Overexpression of RmICE1, a bHLH transcription factor from Rosa multiflora, enhances cold tolerance via modulating ROS levels and activating the expression of stress-responsive genes. Environ Exp Bot 178:104160. https://doi.org/10.1016/j.envexpbot.2020.104160
Lv J, Liu JY, Ming YH, Shi YT, Song CP, Gong ZZ, Yang SH, Ding YL (2021) Reciprocal regulation between the negative regulator PP2CG1 phosphatase and the positive regulator OST1 kinase confers cold response in Arabidopsis. J Integr Plant Biol 63(08):1568–1587. https://doi.org/10.1111/jipb.13100
MacGregor DR, Zhang NC, Iwasaki M, Chen M, Dave A, Lopez-Molina L, Penfield S (2019) ICE1 and ZOU determine the depth of primary seed dormancy in Arabidopsis independently of their role in endosperm development. Plant J 98(2):277–290. https://doi.org/10.1111/tpj.14211
Mahajan S, Tuteja N (2005) Cold, salinity and drought stresses: An overview. Arch Biochem Biophys 444(2):139–158. https://doi.org/10.1016/j.abb.2005.10.018
Makoto S, Haruko U, Shimada T, Hara-Nishimura I (2016) FAMA: a molecular link between stomata and myrosin cells. Trends Plant Sci 21(10):861–871. https://doi.org/10.1016/j.tplants.2016.07.003
Martinez C, Espinosa-Ruiz A, de Lucas M, Bernardo-Garcia S, Franco-Zorrilla JM, Prat S (2018) PIF4-induced BR synthesis is critical to diurnal and thermomorphogenic growth. EMBO J 37:e99552. https://doi.org/10.15252/embj.201899552
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(7):555–560. https://doi.org/10.1016/j.jplph.2009.11.003
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(4):1403–1414. https://doi.org/10.1105/tpc.106.048397
Miura K, Lee J, Gong Q, Ma S, Jin JB, Yoo CY, Miura T, Sato A, Bohnert HJ, Hasegawa PM (2011a) SIZ1 regulation of phosphate starvation-induced root architecture remodeling involves the control of auxin accumulation. Plant Physiol 155(2):100–1012. https://doi.org/10.1104/pp.110.165191
Miura K, Ohta M, Nakazawa M, Hasegawa PM (2011b) ICE1 Ser403 is necessary for protein stabilization and regulation of cold signaling and tolerance. Plant J 67(2):269–279. https://doi.org/10.1111/j.1365-313X.2011.04589.x
Morris DA (1979) The effect of temperature on the velocity of exogenous auxin transport in intact chilling-sensitive and chilling-resistant plants. Planta 146(5):603–605
Müssig M, Altmann T (1999) Physiology and molecular mode of action of brassinosteroids. Plant Physiol Biochem 37(5):363–372. https://doi.org/10.1016/S0981-9428(99)80042-4
Mustilli AC, Merlot S, Vavasseur A, Fenzi F, Giraudata 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(12):089–3099. https://doi.org/10.1105/tpc.007906
Nadella V, Shipp MJ, Muday GK, Wyatt SE (2006) Evidence for altered polar and lateral auxin transport in the gravity persistent signal (gps) mutants of Arabidopsis. Plant Cell Environ 29(4):682–690. https://doi.org/10.1111/j.1365-3040.2005.01451.x
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(3):303–309. https://doi.org/10.5511/plantbiotechnology.11.0421a
Ohme-Takagi M, Shinshi H (1995) Ethylene-lnducible DNA binding proteins that lnteract with an ethylene-responsive element. Plant Cell 7(2):173–182. https://doi.org/10.1105/tpc.7.2.173
Okamuro JK, Caster B, Villarroel R (1997) The AP2 domain of APETALA2 defines a large new family of DNA binding proteins in Arabidopsis. Proc Natl Acad Sci 94(13):7076–7081
Penterman J, Zilberman D, Huh JH, Ballinger T, Henikoff S, Fischer RL (2007) DNA demethylation in the Arabidopsis genome. Proc Natl Acad Sci USA 104(16):6752–6757. https://doi.org/10.1073/pnas.0701861104
Pillitteri LJ, Torii KU (2012) Mechanisms of stomatal development. Annu Rev Plant Biol 63:591–614
Putterill J, Robson F, Lee K, Simon R, Coupland G (1995) The CONSTANS gene of Arabidopsis promotes flowering and encodes a protein showing similarities to zinc finger transcription factors. Cell 80(6):847–857. https://doi.org/10.1016/0092-8674(95)90288-0
Qi XY, Torii KU (2018) Hormonal and environmental signals guiding stomatal development. BMC Biol 16(1):21
Quesada V, Ponce MR, Micol JL (2000) Genetic analysis of salt-tolerant mutants in Arabidopsis thaliana. Genetics. 154(1):421–436. https://doi.org/10.1093/genetics/154.1.421
Riechmann JL, Meyerowitz EM (1998) The AP2/EREBP family of plant transcription factors. Biol Chem 379(6):633–646. https://doi.org/10.1515/bchm.1998.379.6.633
Rout GR, Bansal A, Swain D, Jadhao KR, Shelke RG, Panda SK (2020) Overexpression of ICE1 gene in mung bean (Vigna radiata L.) for cold tolerance. Plant Cell Tissue Organ Cult 143:593–608. https://doi.org/10.1007/s11240-020-01944-w
Sah SK, Reddy KR, Li J (2016) Abscisic acid and abiotic stress tolerance in crop plants. Front Plant Sci 7:571. https://doi.org/10.3389/fpls.2016.00571
Salomé PA (2017) This ICE/SCRM melts in the dark: light-dependent COP1-mediated protein degradation in stomatal formation. Plant Cell 29(11):2680–2681. https://doi.org/10.1105/tpc.17.00870
Seo M, Kanno Y, Frey A, North HM, Marion-Poll A (2016) Dissection of Arabidopsis NCED9 promoter regulatory regions reveal a role for ABA synthesized in embryos in the regulation of GA-dependent seed germination. Plant Sci 246:91–97. https://doi.org/10.1016/j.plantsci.2016.02.013
Shibasaki K, Uemura M, Tsurumi S, Rahman A (2009) Auxin response in Arabidopsis under cold stress: underlying molecular mechanisms. Plant Cell 21(12):3823–3838. https://doi.org/10.1105/tpc.109.069906
Shin JJ, Loewen CJ (2011) Putting the pH into phosphatidic acid signaling. BMC Biol 9:85
Song QP, Wang XP, Li J, Chen THH, Liu Y, Yang XH (2021) CBF1 and CBF4 in Solanum tuberosum L. differ in their effect on low-temperature tolerance and development. Environ Exp Bot 185:104416. https://doi.org/10.1016/j.envexpbot
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 94(3):1035–1040. https://doi.org/10.1073/pnas.94.3.1035
Strohm AK, Vaughn LM, Masson PH (2015) Natural variation in the expression of ORGANIC CATION TRANSPORTER 1 affects root length responses to cadaverine in Arabidopsis. J Exp Bot 66(3):853–862. https://doi.org/10.1093/jxb/eru444
Sun TP (2010) Gibberellin-GID1-DELLA: a pivotal regulatory module for plant growth and development. Plant Physiol 154(20):567–570. https://doi.org/10.1104/pp.110.161554
Takashi Y, Junya N, Yushi I, Mari I (2014) Tomato inducer of CBF expression 1 (SlICE1) is involved in cold and salt stress signaling. American Journal of Experimental Agriculture 4(7):785–796. http://www.sciencedomain.org/review-history/3923
Tang K, Zhao L, Ren YY, Yang SH, Zhu JK, Zhao CZ (2020) The transcription factor ICE1 functions in cold stress response by binding to the promoters of CBF and COR genes. J Integr Plant Biol 62(03):258–263
Tao Y (2009) ICE1 regulates plant growth and development by tuning gibberellin synthesis in Arabidopsis
Teige M, Scheikl E, Eulgem T, Dóczi R, Hirt H (2004) The MKK2 pathway mediates cold and salt stress signaling in Arabidopsis. Mol Cell 15(1):141–152. https://doi.org/10.1016/j.molcel.2004.06.023
Testerink C, Munnik T (2011) Molecular, cellular, and physiological responses to phosphatidic acid formation in plants. J Exp Bot 62(7):2349–2361. https://doi.org/10.1093/jxb/err079
Thines B, Katsir L, Melotto M, Niu YJ, Mandaokar A, Liu GH, Nomura K, He SY, Howe GA, Browse J (2007) JAZ repressor proteins are targets of the SCF(COI1) complex during jasmonate signaling. Nature 448(7154):661–665. https://doi.org/10.1038/nature05960
Thomashow MF (1999) Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annu Rev Plant Physiol Plant Mol Biol 50(1):571–599. https://doi.org/10.1146/annurev.arplant.50.1.571
To TK, Nakaminami K, Kim JM, Morosawa T, Ishida J, Tanaka M, Yokoyama S, Shinozaki K, Seki M (2011) Arabidopsis HDA6 is required for freezing tolerance. Biochem Biophys Res Commun 406(3):414–419. https://doi.org/10.1016/j.bbrc.2011.02.058
Ullah A, Manghwar H, Shaban M, Khan AH, Akbar A, Ali U, Ali E, Fahad S (2018) Phytohormones enhanced drought tolerance in plants: a coping strategy. Environ Sci Pollut Res 25(33):33103–33118. https://doi.org/10.1007/s11356-018-3364-5
Verm V, Ravindran P, Kumar PP (2016) Plant hormone-mediated regulation of stress responses. BMC Plant Biol 16:86
Verma RK, Venkata V, Kumar V, Shashank S, Senthil T, Venkateswara RM, Chinnusamy V (2020) Overexpression of Arabidopsis ICE1 enhances yield and multiple abiotic stress tolerance in indica rice. Plant Signal Behav 15:1814547. https://doi.org/10.1080/15592324.2020.1814547
Vertegaal ACO (2011) Uncovering ubiquitin and ubiquitin-like signaling networks. Chem Rev 111(12):7923–7940. https://doi.org/10.1021/cr200187e
Vishwakarma K, Upadhyay N, Kumar N, Yadav G, Singh J, Mishra RK, Kumar V, Verma R, Upadhyay RG, Pandey M, Sharma P (2017) Abscisic acid signaling and abiotic stress tolerance in plants: a review on current knowledge and future prospects. Front Plant Sci 8:161. https://doi.org/10.3389/fpls.2017.00161
Vlachonasios KE, Thomashow MF, Triezenberg SJ (2003) Disruption mutations of ADA2b and GCN5 transcriptional adaptor genes dramatically affect Arabidopsis growth, development, and gene expression. Plant Cell 15(3):626–638. https://doi.org/10.1105/tpc.007922
Wang YC, Xu HF, Liu WJ, Wang N, Qu CZ, Jiang SH, Fang HC, Zhang ZY, Chen XS (2019) Methyl jasmonate enhances apple cold tolerance through the JAZ-MYC2 pathway. Plant Cell Tissue Organ Cult 136(1):75–84. https://doi.org/10.1007/s11240-018-1493-7
Wang YM, Zhang YM, Zhang X, Zhao X, Zhang Y, Wang C, Wang YC, Wang LQ (2021) Poplar PsnICE1 enhances cold tolerance by binding to different cis-acting elements to improve reactive oxygen species-scavenging capability. Tree Physiol 00:1–14. https://doi.org/10.1093/treephys/tpab084
Wasternack C (2007) Jasmonates: An update on biosynthesis, signal transduction and action in plant stress response, growth and development. Ann Bot 100(4):681–697. https://doi.org/10.1093/aob/mcm079
Wasternack C, Hause B (2013) Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. An update to the 2007 review in Annals of Botany. Ann Bot 111(6):1021–1058. https://doi.org/10.1093/aob/mct067
Wen JQ, Oono K, Imai R (2002) Two novel mitogen-activated protein signaling components, OsMEK1 and OsMAP1, are involved in a moderate low-temperature signaling pathway in rice. Plant Physiol 129(4):1880–1891. https://doi.org/10.1104/pp.006072
Wild M, Daviere JM, Cheminant S, Regnault T, Baumberger N, Heintz D, Baltz R, Genschik P, Achard P (2012) The Arabidopsis DELLA RGA-LIKE3 is a direct target of MYC2 and Modulates Jasmonate Signaling Responses. Plant Cell 24(8):3307–3319. https://doi.org/10.1105/tpc.112.1014289
Wyatt SE, Rashotte AM, Shipp MJ, Robertson D, Muday GK (2002) Mutations in the gravity persistence signal loci in Arabidopsis disrupt the perception and/or signal transduction of gravitropic stimuli. Plant Physiol 130(3):1426–1435. https://doi.org/10.1104/pp.102.010579
Xu WR, Jiao YT, Li RM, Zhang NB, Xiao DM, Ding XL, Wang ZP (2014) Chinese wild-growing Vitis amurensis ICE1 and ICE2 encode MYC-type bHLH transcription activators that regulate cold tolerance in Arabidopsis. PLoS ONE 9(7):e102303. https://doi.org/10.1371/journal.pone.0102303
Yang TB, Ali GS, Yang LH, Du LQ, Reddy ASN, Poovaiah BW (2010) Calcium/calmodulin-regulated receptor-like kinase CRLK1 interacts with MEKK1 in plants. Plant Signal Behav 5(8):991–994
Ye KY, Li H, Ding YL, Shi YT, Song CP, Gong ZZ, Yang SH (2019) BRASSINOSTEROID-INSENSITIVE2 negatively regulates the stability of transcription factor ICE1 in response to cold stress in Arabidopsis. Plant Cell 31(9):2682–2696. https://doi.org/10.1105/tpc.19.00058
Yin X, Yang Y, Lv Y, Li Y, Yang Y (2020) BrrICE1.1 is associated with putrescine synthesis through regulation of the arginine decarboxylase gene in freezing tolerance of turnip (Brassica rapa var. rapa). BMC Plant Biol 20(1):504–504. https://doi.org/10.1186/s12870-020-02697-6
Zhang ZY, Li JH, Li F, Liu HH, Yang WS, Chong K, Xu YY (2017) OsMAPK3 phosphorylates OsbHLH002/OsICE1 and inhibits its ubiquitination to activate OsTPP1 and enhances rice chilling tolerance. Dev Cell 43(6):731–743. https://doi.org/10.1016/j.devcel.2017.11.016
Zhang TG, Mo JG, Zhou K, Chang Y, Liu ZG (2018) Overexpression of Brassica campestris BcICE1 gene increases abiotic stress tolerance in tobacco. Plant Physiol Biochem 132:515–523. https://doi.org/10.1016/j.plaphy.2018.09.039
Zhang H, Zhao Y, Zhu JK (2020a) Thriving under stress: how plants balance growth and the stress response. Dev Cell 55(5):529–543. https://doi.org/10.1016/j.devcel.2020.10.012
Zhang ZY, Cheng L, Zhang WH, Hu JL, Liu Y, Lin YZ (2020b) Characterization of transcription activation domain of EcaICE1 and its interaction with EcaSIZ1 in Eucalyptus camaldulensis. Trees 34(5):1243–1253. https://doi.org/10.1007/s00468-020-01994-9
Zhang HM, Zhu JH, Gong ZZ, Zhu JK (2021) Abiotic stress responses in plants. Nat Rev Genet. https://doi.org/10.1038/s41576-021-00413-0
Zhao C, Wang P, Si T, Hsu CC, Wang L, Zayed O, Yu Z, Zhu Y, Dong J, Tao WA (2017) MAP Kinase cascades regulate the cold response by modulating ICE1 protein stability. Dev Cell 43(5):618–629. https://doi.org/10.1016/j.devcel.2017.09.024
Zhou L, He YJ, Li J, Li LZ, Liu Y, Chen HY (2020) An eggplant SmICE1a gene encoding MYC-type ICE1-like transcription factor enhances freezing tolerance in transgenic Arabidopsis thaliana. Plant Biol 22(3):450–458. https://doi.org/10.1111/plb.13095
Zhu JK (2016) Abiotic stress signaling and responses in plants. Cell 167(2):313–324. https://doi.org/10.1016/j.cell.2016.08.029
Zhu JH, Dong CH, Zhu JK (2007) Interplay between cold-responsive gene regulation, metabolism and RNA processing during plant cold acclimation. Curr Opin Plant Biol 10(3):290–295. https://doi.org/10.1016/j.pbi.2007.04.010
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This work was supported by the project EPPN2020-OPVaI-VA—ITMS313011T813 and VEGA 1/0589/19.
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Wang, X., Song, Q., Liu, Y. et al. The network centered on ICEs play roles in plant cold tolerance, growth and development. Planta 255, 81 (2022). https://doi.org/10.1007/s00425-022-03858-7
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DOI: https://doi.org/10.1007/s00425-022-03858-7