Abstract
Increasing the vulnerability of plants especially crops to a wide range of cold stress reduces plant growth, development, yield production, and plant distribution. Cold stress induces physiological, morphological, biochemical, phenotypic, and molecular changes in plants. Transcription factor (TF) is one of the most important regulators that mediate gene expression. TF is activated by the signal transduction pathway, together with cis-acting element modulate the transcription of cold-responsive genes which contribute to increasing cold tolerance in plants. Here, AP2/ERF TF family is one of the most important cold stress-related TF families that along with other TF families, such as WRKY, bHLH, bZIP, MYB, NAC, and C2H2 interrelate to enhance cold stress tolerance. Over the past decade, significant progress has been found to solve the role of transcription factors (TFs) in improving cold tolerance in plants, such as omics analysis. Furthermore, numerous studies have identified and characterized the complexity of cold stress mechanisms among TFs or between TFs and other factors (endogenous and exogenous) including phytohormones, eugenol, and light. The role, function, and relationship among these TFs or between TFs and other factors to enhance cold tolerance still need to be clarified. Here, the current study analysed the role of AP2/ERF TF and the linkages among AP2/ERF with MYB, WRKY, bZIP, bHLH, C2H2, or NAC against cold stress tolerance.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Abbreviations
- CA:
-
Cold acclimation
- TF:
-
Transcription factor
- TFs:
-
Transcription factors
- ABA:
-
Abscisic acid
- JA:
-
Jasmonic acid
- SA:
-
Salicylic acid
- CAMP:
-
Cyclic adenosine monophosphate
- ROS:
-
Reactive oxygen species
- CBL:
-
Calcineurin-B Like proteins
- CPKs/CDPKs:
-
Ca2+-dependent protein kinases
- CIPKs:
-
CBL-interacting protein kinases
- CBF:
-
C-repeat Binding Factor
- DREB:
-
Dehydration-Responsive Element-Binding-Factor
- ICE1:
-
CBF expression 1
- COR:
-
Cold regulated genes
- AP2/ERF:
-
APETALA2/Ethylene responsive factor
- DRE/CRT:
-
Dehydration-responsive C-repeat
- ChIP-seq:
-
Chromatin Immunoprecipitation-sequencing
- ChIP-PCR:
-
Chromatin Immunoprecipitation Polymerase Chain Reaction
- SOD:
-
Superoxide
- POD:
-
Peroxide
- CAT:
-
Catalase
- APX:
-
Ascorbate peroxidase
- BIN2:
-
Brassinosteroid-Insensitive2
- HOS1:
-
Osmotically Responsive Gene1
- GA:
-
Gibberellic Acid
- phyA:
-
Phytochrome A
- phyB:
-
Phytochrome B
- PIFs:
-
Phytochrome-Interacting Factors
- bHLH:
-
Basic helix-loop-helix
- LEA:
-
Late embryogenesis abundant
- bZIP:
-
Basic leucine zipper
- MYB:
-
Myeloblastosis
References
Alisoltani A, Karimi M, Ravash R, Fallahi H, Shiran B (2019). Molecular responses to cold stress in temperate fruit crops with focus on rosaceae family," in Genomics Assisted Breeding of Crops for Abiotic Stress Tolerance, Vol. II. Springer), 105–130
An JP, Yao JF, Wang XN, You CX, Wang XF, Hao YJ (2017) MdHY5 positively regulates cold tolerance via CBF-dependent and CBF-independent pathways in apple. J Plant Physiol 218:275–281. https://doi.org/10.1016/j.jplph.2017.09.001
An JP, Li R, Qu FJ, You CX, Wang XF, Hao YJ (2018) An apple NAC transcription factor negatively regulates cold tolerance via CBF-dependent pathway. J Plant Physiol 221:74–80. https://doi.org/10.1016/j.jplph.2017.12.009
Artlip TS, Wisniewski ME, Norelli JL (2014) Field evaluation of apple overexpressing a peach CBF gene confirms its effect on cold hardiness, dormancy, and growth. Environ Exp Bot 106:79–86. https://doi.org/10.1016/j.envexpbot.2013.12.008
Barrero-Gil J, Salinas J (2017) CBFs at the crossroads of plant hormone signaling in cold stress response. Mol Plant 10(4):542–544. https://doi.org/10.1016/j.molp.2017.03.004
Barrero-Gil J, Huertas R, Rambla JL, Granell A, Salinas J (2016) Tomato plants increase their tolerance to low temperature in a chilling acclimation process entailing comprehensive transcriptional and metabolic adjustments. Plant Cell Environ 39(10):2303–2318. https://doi.org/10.1111/pce.12799
Beloiu M, Stahlmann R, Beierkuhnlein C (2020) High recovery of saplings after severe drought in temperate deciduous forests. Forests 11(5):546. https://doi.org/10.3390/f11050546
Byun MY, Lee J, Cui LH, Kang Y, Oh TK, Park H, Kim WT et al (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. https://doi.org/10.1016/j.plantsci.2015.03.020
Cai WT, Yang YL, Wang WW, Guo GY, Liu W, Bi CL (2018) Overexpression of a wheat (Triticum aestivum L.) bZIP transcription factor gene, TabZIP6, decreased the freezing tolerance of transgenic Arabidopsis seedlings by down-regulating the expression of CBFs. Plant Physiol Biochem 124:100–111. https://doi.org/10.1016/j.plaphy.2018.01.008
Carlow CE, Faultless JT, Lee C, Siddiqua M, Edge A, Nassuth A (2017) Nuclear localization and transactivation by Vitis CBF transcription factors are regulated by combinations of conserved amino acid domains. Plant Physiol Biochem 118:306–319. https://doi.org/10.1016/j.plaphy.2017.06.027
Carvallo MA, Pino M-T, Jeknić Z, Zou C, Doherty CJ, Shiu S-H, Thomashow MF et al (2011) A comparison of the low temperature transcriptomes and CBF regulons of three plant species that differ in freezing tolerance: Solanum commersonii, Solanum tuberosum, and Arabidopsis thaliana. J Exp Bot 62(11):3807–3819. https://doi.org/10.1093/jxb/err066
Chen HY, Chen XL, Chai XF, Qiu YW, Gong C, Zhang ZZ, Wang AX et al (2015a) Effects of low temperature on mRNA and small RNA transcriptomes in Solanum lycopersicoides leaf revealed by RNA-Seq. Biochem Biophys Res Commun 464(3):768–773. https://doi.org/10.1016/j.bbrc.2015.07.029
Chen QF, Xu L, Tan WJ, Chen L, Qi H, Xie LJ, Yao N et al (2015b) Disruption of the Arabidopsis defense regulator genes SAG101, EDS1, and PAD4 confers enhanced freezing tolerance. Mol Plant 8(10):1536–1549. https://doi.org/10.1016/j.molp.2015.06.009
Chen L, Zhao Y, Xu S, Zhang Z, Xu Y, Zhang J, Chong K (2018) OsMADS57 together with OsTB1 coordinates transcription of its target OsWRKY94 and D14 to switch its organogenesis to defense for cold adaptation in rice. New Phytol 218(1):219–231. https://doi.org/10.1111/nph.14977
Chen S, Wang Y, Yu L, Zheng T, Wang S, Yue Z, Yang C et al (2021) Genome sequence and evolution of Betula platyphylla. Hortic Res 8(1):37. https://doi.org/10.1038/s41438-021-00481-7
Djemal R, Mila I, Bouzayen M, Pirrello J, Khoudi H (2018) Molecular cloning and characterization of novel WIN1/SHN1 ethylene responsive transcription factor HvSHN1 in barley (Hordeum vulgare L.). J Plant Physiol 228:39–46
Djemal R, Khoudi H (2016) TdSHN1, a WIN1/SHN1-type transcription factor, imparts multiple abiotic stress tolerance in transgenic tobacco. Environ Exp Bot 131:89–100. https://doi.org/10.1016/j.envexpbot.2016.07.005
Eulgem T, Somssich IE (2007) Networks of WRKY transcription factors in defense signaling. Curr Opin Plant Biol 10(4):366–371. https://doi.org/10.1016/j.pbi.2007.04.020
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
Feng WQ, Li J, Long SX, Wei SJ (2019) A DREB1 gene from zoysiagrass enhances Arabidopsis tolerance to temperature stresses without growth inhibition. Plant Sci 278:20–31. https://doi.org/10.1016/j.plantsci.2018.10.009
Gamboa MC, Rasmussen-Poblete S, Valenzuela PD, Krauskopf E (2007) Isolation and characterization of a cDNA encoding a CBF transcription factor from E. globulus. Plant Physiol Biochem 45(1):1–5. https://doi.org/10.1016/j.plaphy.2006.12.006
Govardhana M, Kumudini BS (2020) In-silico analysis of cucumber (Cucumis sativus L) Genome for WRKY transcription factors and cis-acting elements. Comput Biol Chem 85:107212. https://doi.org/10.1016/j.compbiolchem.2020.107212
Gu H, Yang Y, Xing M, Yue C, Wei F, Zhang Y, Huang J et al (2019) Physiological and transcriptome analyses of Opisthopappus taihangensis in response to drought stress. Cell & Biosci 9(1):56. https://doi.org/10.1186/s13578-019-0318-7
Gualerzi CO, Giuliodori AM, Pon CL (2003) Transcriptional and post-transcriptional control of cold-shock genes. J Mol Biol 331(3):527–539. https://doi.org/10.1016/s0022-2836(03)00732-0
Guo H, Li Z, Han Z, Xin Y, Cheng H (2011) Cloning of cotton CBF gene for cold tolerance and its expression in transgenic tobacco. Acta Agro Sin 37(2):286–293. https://doi.org/10.1016/S1875-2780(11)60009-6
Han YC, Fu CC (2019) Cold-inducible MaC2H2s are associated with cold stress response of banana fruit via regulating MaICE1. Plant Cell Rep 38(5):673–680. https://doi.org/10.1007/s00299-019-02399-w
Hao YJ, Wei W, Song QX, Chen HW, Zhang YQ, Wang F, Zhang WK et al (2011) Soybean NAC transcription factors promote abiotic stress tolerance and lateral root formation in transgenic plants. Plant J 68(2):302–313. https://doi.org/10.1111/j.1365-313X.2011.04687.x
Hao JJ, Yang JL, Dong JL, Fei SZ (2017) Characterization of BdCBF genes and genome-wide transcriptome profiling of BdCBF3-dependent and-independent cold stress responses in Brachypodium distachyon. Plant Sci 262:52–61. https://doi.org/10.1016/j.plantsci.2017.06.001
Hu Y, Jiang Y, Han X, Wang H, Pan J, Yu D (2017) Jasmonate regulates leaf senescence and tolerance to cold stress: crosstalk with other phytohormones. J Exp Bot 68(6):1361–1369
Hu Y, Jiang L, Wang F, Yu D (2013) Jasmonate regulates the inducer of cbf expression-C-repeat binding factor/DRE binding factor1 cascade and freezing tolerance in Arabidopsis. Plant Cell 25(8):2907–2924. https://doi.org/10.1105/tpc.113.112631
Hu ZR, Huang XB, Amombo E, Liu A, Fan JB, Bi AY, Fu JM et al (2020) The ethylene responsive factor CdERF1 from bermudagrass (Cynodon dactylon) positively regulates cold tolerance. Plant Sci 294:110432. https://doi.org/10.1016/j.plantsci.2020.110432
Huang J, Wang JF, Wang QH, Zhang HS (2005) Identification of a rice zinc finger protein whose expression is transiently induced by drought, cold but not by salinity and abscisic acid. DNA Seq 16(2):130–136. https://doi.org/10.1080/10425170500061590
Huang J, Sun SJ, Xu DQ, Lan HX, Sun H, Wang ZF, Zhang HS et al (2012) A TFIIIA-type zinc finger protein confers multiple abiotic stress tolerances in transgenic rice (Oryza sativa L). Plant Mol Biol 80(3):337–350. https://doi.org/10.1007/s11103-012-9955-5
Huang XS, Li KQ, Jin C, Zhang SL (2015) ICE1 of Pyrus ussuriensis functions in cold tolerance by enhancing PuDREBa transcriptional levels through interacting with PuHHP1. Sci Rep 5:17620. https://doi.org/10.1038/srep17620
Huang QH, Qian XC, Jiang TJ, Zheng XL (2019) Effect of eugenol fumigation treatment on chilling injury and CBF gene expression in eggplant fruit during cold storage. Food Chem 292:143–150. https://doi.org/10.1016/j.foodchem.2019.04.048
Iida A, Kazuoka T, Torikai S, Kikuchi H, Oeda K (2000) A zinc finger protein RHL41 mediates the light acclimatization response in Arabidopsis. Plant J 24(2):191–203. https://doi.org/10.1046/j.1365-313x.2000.00864.x
Jeon J, Cho C, Lee MR, Van Binh N, Kim J (2016) Cytokinin Response Factor2 (CRF2) and CRF3 regulate lateral root development in response to cold stress in Arabidopsis. Plant Cell 28(8):1828–1843. https://doi.org/10.1105/tpc.15.00909
Jiang BC, Shi YT, Peng Y, Jia Y, Yan Y, Dong XJ, Gong ZZ et al (2020) Cold-Induced CBF-PIF3 Interaction Enhances Freezing Tolerance by Stabilizing the phyB Thermosensor in Arabidopsis. Mol Plant. https://doi.org/10.1016/j.molp.2020.04.006
Jin C, Li KQ, Xu XY, Zhang HP, Chen HX, Chen YH, Zhang SL et al (2017) A novel NAC transcription factor, PbeNAC1, of Pyrus betulifolia confers cold and drought tolerance via interacting with PbeDREBs and activating the expression of stress-responsive genes. Front Plant Sci 8:1049. https://doi.org/10.3389/fpls.2017.01049
Ju YL, Yue XF, Min Z, Wang XH, Fang YL, Zhang JX (2020) VvNAC17, a novel stress-responsive grapevine (Vitis vinifera L.) NAC transcription factor, increases sensitivity to abscisic acid and enhances salinity, freezing, and drought tolerance in transgenic Arabidopsis. Plant Physiol Biochem 146:98–111. https://doi.org/10.1016/j.plaphy.2019.11.002
Jung WJ, Seo YW (2019) Identification of novel C-repeat binding factor (CBF) genes in rye (Secale cereale L.) and expression studies. Gene 684:82–94. https://doi.org/10.1016/j.gene.2018.10.055
Kang HG, Kim JK, Kim BH, Jeong HN, Choi SH, Kim EK, Lim PO et al (2011) Overexpression of FTL1/DDF1, an AP2 transcription factor, enhances tolerance to cold, drought, and heat stresses in Arabidopsis thaliana. Plant Sci 180(4):634–641. https://doi.org/10.1016/j.plantsci.2011.01.002
Kang WH, Sim YM, Koo NJ, Nam JY, Js L, Kim NY, Yeom SI et al (2020) Transcriptome profiling of abiotic responses to heat, cold, salt, and osmotic stress of Capsicum annuum L. Sci Data 7(1):1–7. https://doi.org/10.1038/s41597-020-0352-7
Kargiotidou A, Kappas I, Tsaftaris A, Galanopoulou D, Farmaki T (2010) Cold acclimation and low temperature resistance in cotton: Gossypium hirsutum phospholipase Dα isoforms are differentially regulated by temperature and light. J Exp Bot 61(11):2991–3002. https://doi.org/10.1093/jxb/erq124
Kashyap P, Deswal R (2017) A novel class I Chitinase from Hippophae rhamnoides: Indications for participating in ICE-CBF cold stress signaling pathway. Plant Sci 259:62–70. https://doi.org/10.1016/j.plantsci.2017.03.004
Kashyap P, Deswal R (2019) Two ICE isoforms showing differential transcriptional regulation by cold and hormones participate in Brassica juncea cold stress signaling. Gene 695:32–41. https://doi.org/10.1016/j.gene.2019.02.005
Kazemi-Shahandashti SS, Maali-Amiri R (2018) Global insights of protein responses to cold stress in plants: signaling, defence, and degradation. J Plant Physiol 226:123–135. https://doi.org/10.1016/j.jplph.2018.03.022
Klay I, Gouia S, Liu M, Mila I, Khoudi H, Bernadac A, Pirrello J et al (2018) Ethylene Response Factors (ERF) are differentially regulated by different abiotic stress types in tomato plants. Plant Sci 274:137–145. https://doi.org/10.1016/j.plantsci.2018.05.023
Li KL, Bai X, Li Y, Cai H, Ji W, Tang LL, Zhu YM et al (2011) GsGASA1 mediated root growth inhibition in response to chronic cold stress is marked by the accumulation of DELLAs. J Plant Physiol 168(18):2153–2160. https://doi.org/10.1016/j.jplph.2011.07.006
Li XD, Zhuang KY, Liu ZM, Yang DY, Ma NN, Meng QW (2016) Overexpression of a novel NAC-type tomato transcription factor, SlNAM1, enhances the chilling stress tolerance of transgenic tobacco. J Plant Physiol 204:54–65. https://doi.org/10.1016/j.jplph.2016.06.024
Li H, Ye KY, Shi YT, Cheng JK, Zhang XY, Yang SH (2017) BZR1 positively regulates freezing tolerance via CBF-dependent and CBF-independent pathways in Arabidopsis. Mol Plant 10(4):545–559. https://doi.org/10.1016/j.molp.2017.01.004
Li R, Zhang LX, Wang L, Chen L, Zhao RR, Sheng JP, Shen L (2018) Reduction of tomato-plant chilling tolerance by CRISPR–Cas9-mediated SlCBF1 mutagenesis. J Agric Food Chem 66(34):9042–9051. https://doi.org/10.1021/acs.jafc.8b02177
Liu H, Timko MP (2021) Jasmonic acid signaling and molecular crosstalk with other phytohormones. Int J Mol Sci. https://doi.org/10.3390/ijms22062914
Liu ZY, Jia YX, Ding YL, Shi YT, Li Z, Guo Y, Yang SH et al (2017) Plasma membrane CRPK1-mediated phosphorylation of 14–3–3 proteins induces their nuclear import to fine-tune CBF signaling during cold response. Mol Cell 66(1):117–128. https://doi.org/10.1016/j.molcel.2017.02.016
Liu C, Ou S, Mao B, Tang J, Wang W, Wang H, Xiao G et al (2018a) Early selection of bZIP73 facilitated adaptation of japonica rice to cold climates. Nat Commun 9(1):1–12. https://doi.org/10.1038/s41467-018-05753-w
Liu H, Zhou Y, Li H, Wang T, Zhang J, Ouyang B, Ye Z (2018b) Molecular and functional characterization of ShNAC1, an NAC transcription factor from Solanum habrochaites. Plant Sci 271:9–19. https://doi.org/10.1016/j.plantsci.2018.03.005
Londo JP, Kovaleski AP, Lillis JA (2018) Divergence in the transcriptional landscape between low temperature and freeze shock in cultivated grapevine (Vitis vinifera). Hortic Res 5(1):1–14. https://doi.org/10.1038/s41438-018-0020-7
Luo C, Liu H, Ren J, Chen D, Cheng X, Sun W, Huang C et al (2020a) Cold-inducible expression of an Arabidopsis thaliana AP2 transcription factor gene, AtCRAP2, promotes flowering under unsuitable low-temperatures in chrysanthemum. Plant Physiol Biochem 146:220–230. https://doi.org/10.1016/j.plaphy.2019.11.022
Luo P, Li Z, Chen W, Xing W, Yang J, Cui Y (2020b) 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 Y, Yang M, Hu D, Yang Z, Ma S, Li X, Xiong L (2017) The OsMYB30 transcription factor suppresses cold tolerance by interacting with a JAZ protein and suppressing β-amylase expression. Plant Physiol 173(2):1475–1491. https://doi.org/10.1104/pp.16.01725
Lv K, Li J, Zhao K, Chen S, Nie J, Zhang W, Wei H et al (2019) Overexpression of an AP2/ERF family gene, BpERF13, in birch enhances cold tolerance through upregulating CBF genes and mitigating reactive oxygen species. Plant Sci. https://doi.org/10.1016/j.plantsci.2019.110375
Ma Y, Zhang L, Zhang J, Chen J, Wu T, Zhu S, Zhong G et al (2014) Expressing a citrus ortholog of arabidopsis ERF1 enhanced cold-tolerance in tobacco. Sci Hortic 174:65–76. https://doi.org/10.1016/j.scienta.2014.05.009
Medina J, Catalá R, Salinas J (2011) The CBFs: three Arabidopsis transcription factors to cold acclimate. Plant Sci 180(1):3–11. https://doi.org/10.1016/j.plantsci.2010.06.019
Mehrotra S, Verma S, Kumar S, Kumari S, Mishra BN (2020) Transcriptional regulation and signalling of cold stress response in plants: an overview of current understanding. Environ Exp Bot 180:104243. https://doi.org/10.1016/j.envexpbot.2020.104243
Mitsis T, Efthimiadou A, Bacopoulou F, Vlachakis D, Chrousos GP, Eliopoulos E (2020) Transcription factors and evolution: An integral part of gene expression. World Acad Sci Eng Technol 2(1):3–8. https://doi.org/10.3892/wasj.2020.32
Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K (2012) AP2/ERF family transcription factors in plant abiotic stress responses. Biochimica et Biophysica Acta (BBA)-Gene Regulatory Mechanisms 1819(2): 86–96 https://doi.org/10.1016/j.bbagrm.2011.08.004
Mizuno S, Hirasawa Y, Sonoda M, Nakagawa H, Sato T (2006) Isolation and characterization of three DREB/ERF-type transcription factors from melon (Cucumis melo). Plant Sci 170(6):1156–1163. https://doi.org/10.1016/j.plantsci.2006.02.005
Monteagudo A, Forcada CF, Estopañán G, Dodd RS, Alonso JM, Rubio-Cabetas MJ, Marti ÁF (2018) Biochemical analyses and expression of cold transcription factors of the late PDO ‘Calanda’peach under different post-harvest conditions. Sci Hortic 238:116–125. https://doi.org/10.1016/j.scienta.2018.04.043
Nakashima K, Takasaki H, Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K (2012) NAC transcription factors in plant abiotic stress responses. Biochimica et Biophysica Acta (BBA)-Gene Regulatory Mechanisms 1819(2): 97–103. https://doi.org/10.1016/j.bbagrm.2011.10.005
Niu Y, Hu T, Zhou Y, Hasi A (2010) Isolation and characterization of two Medicago falcate AP2/EREBP family transcription factor cDNA, MfDREB1 and MfDREB1s. Plant Phys Biochem 48(12):971–976. https://doi.org/10.1016/j.plaphy.2010.08.009
Ohta M, Sato A, Renhu N, Yamamoto T, Oka N, Zhu JK, Miura K et al (2018) MYC-type transcription factors, MYC67 and MYC70, interact with ICE1 and negatively regulate cold tolerance in Arabidopsis. Sci Rep 8(1):1–12. https://doi.org/10.1038/s41598-018-29722-x
Pan XW, Li YC, Li XX, Liu WQ, Jun M, Lu TT, Sheng XN et al (2013) Differential regulatory mechanisms of CBF regulon between Nipponbare (Japonica) and 93–11 (Indica) during cold acclimation. Rice Sci 20(3):165–172. https://doi.org/10.1016/S1672-6308(13)60121-3
Peng HH, Shan W, Kuang JF, Lu WJ, Chen JY (2013a) Molecular characterization of cold-responsive basic helix-loop-helix transcription factors MabHLHs that interact with MaICE1 in banana fruit. Planta 238(5):937–953. https://doi.org/10.1007/s00425-013-1944-7
Peng YL, Wang YS, Cheng H, Sun CC, Wu P, Wang LY, Fei J (2013b) Characterization and expression analysis of three CBF/DREB1 transcriptional factor genes from mangrove Avicennia marina. Aquat Toxicol 140:68–76. https://doi.org/10.1016/j.aquatox.2013.05.014
Prerostova S, Zupkova B, Petrik I, Simura J, Nasinec I, Kopecky D, Vankova R et al (2021) Hormonal responses associated with acclimation to freezing stress in Lolium perenne. Environ Exp Bot 182:104295. https://doi.org/10.1016/j.envexpbot.2020.104295
Puhakainen T, Li C, Boije-Malm M, Kangasjärvi J, Heino P, Palva ET (2004) Short-day potentiation of low temperature-induced gene expression of a C-repeat-binding factor-controlled gene during cold acclimation in silver birch. Plant Physiol 136(4):4299–4307
Qu YT, Duan M, Zhang ZQ, Dong JL, Wang T (2016) Overexpression of the Medicago falcata NAC transcription factor MfNAC3 enhances cold tolerance in Medicago truncatula. Environ Exp Bot 129:67–76. https://doi.org/10.1016/j.envexpbot.2015.12.012
Rapacz M, Jurczyk B, Krępski T, Płażek A (2018) C-repeat binding transcription factors from Miscanthus× giganteus and their expression at a low temperature. Ind Crops Prod 113:283–287. https://doi.org/10.1016/j.indcrop.2018.01.058
Rasmussen S, Barah P, Suarez-Rodriguez MC, Bressendorff S, Friis P, Costantino P, Mundy J et al (2013) Transcriptome responses to combinations of stresses in Arabidopsis. Plant Physiol 161(4):1783–1794. https://doi.org/10.1104/pp.112.210773
Raza A, Tabassum J, Kudapa H, Varshney RK (2021) Can omics deliver temperature resilient ready-to-grow crops? Crit Rev Biotechnol https://doi.org/10.1080/07388551.2021.1898332
Razzaq MK, Aleem M, Mansoor S, Khan MA, Rauf S, Iqbal S, Siddique KHM (2021) Omics and CRISPR-Cas9 approaches for molecular insight, functional gene analysis, and stress tolerance development in crops. Int J Mol Sci. https://doi.org/10.3390/ijms22031292
Ritonga FN, Chen S (2020) Physiological and molecular mechanism involved in cold stress tolerance in plants. Plants 9(560):13. https://doi.org/10.3390/plants9050560
Ritonga FN, Ngatia JN, Song RX, Farooq U, Somadona S, Andi TL, Chen S (2021) Abiotic stresses induced physiological, biochemical, and molecular changes in Betula platyphylla a review. Silva Fenn. https://doi.org/10.14214/sf.10516
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(3):998–1009. https://doi.org/10.1006/bbrc.2001.6299
Shahzad R, Jamil S, Ahmad S, Nisar A, Amina Z, Saleem S, Wang X et al (2021) Harnessing the potential of plant transcription factors in developing climate resilient crops to improve global food security: Current and future perspectives. Saudi J Biol Sci 28(4):2323–2341. https://doi.org/10.1016/j.sjbs.2021.01.028
Sharma KD, Nayyar H (2016) Regulatory networks in pollen development under cold stress. Front Plant Sci 7:402–402. https://doi.org/10.3389/fpls.2016.00402
Shi YT, Ding YL, Yang SH (2018) Molecular regulation of CBF signaling in cold acclimation. Trends Plant Sci 23(7):623–637. https://doi.org/10.1016/j.tplants.2018.04.002
STRING (2021). Protein-protein Interaction networks, Functional enrichment analysis [Online]. Available: (https://string-db.org/cgi/) [Accessed 21 June, 2021].
Su LT, Li JW, Liu DQ, Zhai Y, Zhang HJ, Li XW, Wang QY et al (2014) A novel MYB transcription factor, GmMYBJ1, from soybean confers drought and cold tolerance in Arabidopsis thaliana. Gene 538(1):46–55. https://doi.org/10.1016/j.gene.2014.01.024
Sun XM, Zhu ZF, Zhang LL, Fang LC, Zhang JS, Wang QF, Xin HP et al (2019) Overexpression of ethylene response factors VaERF080 and VaERF087 from Vitis amurensis enhances cold tolerance in Arabidopsis. Sci Hortic 243:320–326. https://doi.org/10.1016/j.scienta.2018.08.055
Thakur P, Kumar S, Malik JA, Berger JD, Nayyar H (2010) Cold stress effects on reproductive development in grain crops: an overview. Environ Exp Bot 67(3):429–443. https://doi.org/10.1016/j.envexpbot.2009.09.004
Wang Z, Liu J, Guo H, He X, Wu W, Du J, An X et al (2014) Characterization of two highly similar CBF/DREB1-like genes, PhCBF4a and PhCBF4b, in Populus hopeiensis. Plant Physiol Biochem 83:107–116. https://doi.org/10.1016/j.plaphy.2014.07.012
Wang GD, Xu XP, Wang H, Liu Q, Yang XT, Liao LX, Cai GH (2019a) A tomato transcription factor, SlDREB3 enhances the tolerance to chilling in transgenic tomato. Plant Physiol Biochem 142:254–262. https://doi.org/10.1016/j.plaphy.2019.07.017
Wang WD, Gao T, Chen JF, Yang JK, Huang HY, Yu YB (2019b) The late embryogenesis abundant gene family in tea plant (Camellia sinensis): Genome-wide characterization and expression analysis in response to cold and dehydration stress. Plant Physiol Biochem 135:277–286. https://doi.org/10.1016/j.plaphy.2018.12.009
Wang X, Ding Y, Li Z, Shi Y, Wang J, Hua J, Yang S et al (2019c) PUB25 and PUB26 promote plant freezing tolerance by degrading the cold signaling negative regulator MYB15. Dev Cell 51(2):222–235. https://doi.org/10.1016/j.devcel.2019.08.008
Wang Y, Mao Z, Jiang H, Zhang Z, Chen X (2019d) A feedback loop involving MdMYB108L and MdHY5 controls apple cold tolerance. Biochem Biophys Res Commun 512(2):381–386. https://doi.org/10.1016/j.bbrc.2019.03.101
Watt C, Zhou G, Li C (2020) Harnessing transcription factors as potential tools to enhance grain size under stressful abiotic conditions in cereal crops. Front Plant Sci 11(1273). https://doi.org/10.3389/fpls.2020.01273
Winfield MO, Lu C, Wilson ID, Coghill JA, Edwards KJ (2010) Plant responses to cold: transcriptome analysis of wheat. Plant Biotechnol J 8(7):749–771
Xie Y, Chen P, Yan Y, Bao C, Li X, Wang L, Niu C et al (2018) An atypical R2R3 MYB transcription factor increases cold hardiness by CBF-dependent and CBF-independent pathways in apple. New Phytol 218(1):201–218. https://doi.org/10.1111/nph.14952
Xu D, Deng XW (2020) CBF-phyB-PIF module links light and low temperature signaling. Trends Plant Sci. https://doi.org/10.1016/j.tplants.2020.06.010
Xu YC, Hou XL, Xu WW, Shen LL, Lü SW, Zhang SL, Hu CM (2016) Isolation and characterization of an ERF-B3 gene associated with flower abnormalities in non-heading Chinese cabbage. J Integr Agric 15(3):528–536. https://doi.org/10.1016/S2095-3119(15)61203-5
Xu H, Yang G, Zhang J, Wang Y, Zhang T, Wang N, Chen X et al (2018) Overexpression of a repressor MdMYB15L negatively regulates anthocyanin and cold tolerance in red-fleshed callus. Biochem Biophys Res Commun 500(2):405–410. https://doi.org/10.1016/j.bbrc.2018.04.088
Yadav SK (2010) Cold stress tolerance mechanisms in plants A review. Agronomy Sustain Develop 30(3):515–527. https://doi.org/10.1051/agro/2009050
Yamasaki Y, Randall SK (2016) Functionality of soybean CBF/DREB1 transcription factors. Plant Sci 246:80–90. https://doi.org/10.1016/j.plantsci.2016.02.007
Yao PF, Sun ZX, Li CL, Zhao XR, Li MF, Deng RY, Wu Q et al (2018) Overexpression of Fagopyrum tataricum FtbHLH2 enhances : tolerance to cold stress in transgenic Arabidopsis. Plant Physiol Biochem 125:85–94. https://doi.org/10.1016/j.plaphy.2018.01.028
Yang T, Zhang L, Zhang T, Zhang H, Xu S, An L (2005) Transcriptional regulation network of cold-responsive genes in higher plants. Plant Sci 169(6):987–995. https://doi.org/10.1016/j.plantsci.2005.07.005
Yang Xy, Wang R, Hu Ql, Li SL, Mao XD, Jing HH, Liu CM et al (2019) DlICE1, a stress-responsive gene from Dimocarpus longan, enhances cold tolerance in transgenic Arabidopsis. Plant Physiol Biochem 142:490–499. https://doi.org/10.1016/j.plaphy.2019.08.007
Ye K, Li H, Ding Y, Shi Y, Song C, Gong Z, Yang S (2019) BRASSINOSTEROID-INSENSITIVE2 negatively regulates the stability of transcription factor ICE1 in response to cold stress in Arabidopsis. The Plant Cell 31(11), 2682-2696
Yin XR, Allan AC, Xu Q, Burdon J, Dejnoprat S, Ks C, Ferguson IB (2012) Differential expression of kiwifruit ERF genes in response to postharvest abiotic stress. Postharvest Biol Technol 66:1–7
Yong YB, Zhang Y, Lyu YM (2019) A Stress-Responsive NAC transcription factor from tiger lily (LlNAC2) interacts with LlDREB1 and LlZHFD4 and enhances various abiotic stress tolerance in Arabidopsis. Int J Mol Sci 20(13):3225. https://doi.org/10.3390/ijms20133225
Yu ZC, Wang TQ, Luo YN, Zheng XT, He W, Chen LB, Peng CL (2021) Overexpression of the V-ATPase c subunit gene from Antarctic notothenioid fishes enhances freezing tolerance in transgenic Arabidopsis plants. Plant Physiol Biochem 160:365–376. https://doi.org/10.1016/j.plaphy.2021.01.038
Yuan P, Yang T, Poovaiah BW (2018) Calcium signaling-mediated plant response to cold stress. Int J Mol Sci 19(12):3896. https://doi.org/10.3390/ijms19123896
Zandalinas SI, Fritschi FB, Mittler R (2021) Global warming, climate change, and environmental pollution: recipe for a multifactorial stress combination disaster. Trends Plant Sci 26(6):588–599. https://doi.org/10.1016/j.tplants.2021.02.011
Zeng Y, Wen J, Zhao W, Wang Q, Huang W (2020) Rational Improvement of Rice Yield and Cold Tolerance by Editing the Three Genes OsPIN5b, GS3, and OsMYB30 With the CRISPR–Cas9 System. Front Plant Sci 10(1663). https://doi.org/10.3389/fpls.2019.01663
Zhang X, Guo XP, Lei CL, Cheng ZJ, Lin QB, Wang JL, Wan JM et al (2011) Overexpression of SlCZFP1, a novel TFIIIA-type zinc finger protein from tomato, confers enhanced cold tolerance in transgenic Arabidopsis and rice. Plant Mol Biol Rep 29(1):185–196. https://doi.org/10.1007/s11105-010-0223-z
Zhang Y, Yu HJ, Yang XY, Li Q, Ling J, Wang H, Jiang WJ et al (2016) CsWRKY46, a WRKY transcription factor from cucumber, confers cold resistance in transgenic-plant by regulating a set of cold-stress responsive genes in an ABA-dependent manner. Plant Physiol Biochem 108:478–487. https://doi.org/10.1016/j.plaphy.2016.08.013
Zhang QY, Yu JQ, Wang JH, Hu DG, Hao YJ (2017) Functional characterization of MdMYB73 reveals its involvement in cold stress response in apple calli and Arabidopsis. J Integr Agric. https://doi.org/10.1007/s11103-019-00846-6
Zhang CY, Liu HC, Zhang XS, Guo QX, Bian SM, Wang JY, Zhai LL (2020) VcMYB4a, an R2R3-MYB transcription factor from Vaccinium corymbosum, negatively regulates salt, drought, and temperature stress. Gene 757:144935. https://doi.org/10.1016/j.gene.2020.144935
Zhao H, Wang S, Chen S, Jiang J, Liu GF (2015) Phylogenetic and stress-responsive expression analysis of 20 WRKY genes in Populus simonii× Populus nigra. Gene 565(1):130–139. https://doi.org/10.1016/j.gene.2015.04.002
Zhao X, Yang XW, Pei SQ, He G, Wang XY, Tang Q, Zhou GK et al (2016) The Miscanthus NAC transcription factor MlNAC9 enhances abiotic stress tolerance in transgenic Arabidopsis. Gene 586(1):158–169. https://doi.org/10.1016/j.gene.2016.04.028
Zhao C, Liu XF, He JQ, Xie YP, Xu Y, Ma FW, Guan QM (2021) Apple TIME FOR COFFEE contributes to freezing tolerance by promoting unsaturation of fatty acids. Plant Sci 302:110695. https://doi.org/10.1016/j.plantsci.2020.110695
Zhou MQ, Chen H, Wei DH, Ma H, Lin J (2017) Arabidopsis CBF3 and DELLAs positively regulate each other in response to low temperature. Sci Rep 7(1):1–13. https://doi.org/10.1038/srep39819
Zhou L, Li J, He YJ, Liu Y, Chen HY (2018) Functional characterization of SmCBF genes involved in abiotic stress response in eggplant (Solanum melongena). Sci Hortic 233:14–21. https://doi.org/10.1016/j.scienta.2018.01.043
Zhu Z, Shi J, Xu W, Li H, He M, Xu Y, Wang Y et al (2013) Three ERF transcription factors from Chinese wild grapevine Vitis pseudoreticulata participate in different biotic and abiotic stress-responsive pathways. J Plant Physiol 170(10):923–933
Zhu YY, Liu XL, Gao YD, Li K, Guo WD (2020) Transcriptome-based identification of AP2/ERF family genes and their cold-regulated expression during the dormancy phase transition of Chinese cherry flower buds. Sci Hortic, 109666. https://doi.org/10.1016/j.scienta.2020.109666
Zuo ZF, Kang HG, Park MY, Jeong H, Sun HJ, Song PS, Lee HY (2019) Zoysia japonica MYC type transcription factor ZjICE1 regulates cold tolerance in transgenic Arabidopsis. Plant Sci 289:110254. https://doi.org/10.1016/j.plantsci.2019.110254
Zwack PJ, Compton MA, Adams CI, Rashotte AM (2016) Cytokinin response factor 4 (CRF4) is induced by cold and involved in freezing tolerance. Plant Cell Rep 35(3):573–584. https://doi.org/10.1007/s00299-015-1904-8
Acknowledgements
The authors appreciate the reviewers for their comments and suggestions.
Funding
This review was funded by the Fundamental Research Funds for the Central Universities, grant number 2572019CG08, the National Natural Science Foundation of China, Grant Number 31870659 and Heilongjiang Touyan Innovation Team Program (Tree Genetics and Breeding Innovation Team).
Author information
Authors and Affiliations
Contributions
FNR had contributed to writing, editing, and original draft preparation. JNN, YRW, MAK, and UF contributed to editing the manuscript. SC had contributed to supervision, project administration, funding acquisition, review, and editing manuscript. All authors have read and agreed to the published version of the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Ritonga, F.N., Ngatia, J.N., Wang, Y. et al. AP2/ERF, an important cold stress-related transcription factor family in plants: A review. Physiol Mol Biol Plants 27, 1953–1968 (2021). https://doi.org/10.1007/s12298-021-01061-8
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12298-021-01061-8