Skip to main content

Advertisement

Log in

A pervasive phosphorylation cascade modulation of plant transcription factors in response to abiotic stress

  • Review
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Main conclusion

Transcriptional regulation of stress-responsive genes is a crucial step in establishing the mechanisms behind plant abiotic stress tolerance. A sensitive method of regulating transcription factors activity, stability, protein interaction, and subcellular localization is through phosphorylation. This review highlights a widespread regulation mechanism that involves phosphorylation of plant TFs in response to abiotic stress.

Abstract

Abiotic stress is one of the main components limiting crop yield and sustainability on a global scale. It greatly reduces the land area that is planted and lowers crop production globally. In all living organisms, transcription factors (TFs) play a crucial role in regulating gene expression. They participate in cell signaling, cell cycle, development, and plant stress response. Plant resilience to diverse abiotic stressors is largely influenced by TFs. Transcription factors modulate gene expression by binding to their target gene's cis-elements, which are impacted by genomic characteristics, DNA structure, and TF interconnections. In this review, we focus on the six major TFs implicated in abiotic stress tolerance, namely, DREB, bZIP, WRKY, ABF, MYB, and NAC, and the cruciality of phosphorylation of these transcription factors in abiotic stress signaling, as protein phosphorylation has emerged as one of the key post-translational modifications, playing a critical role in cell signaling, DNA amplification, gene expression and differentiation, and modification of other biological configurations. These TFs have been discovered after extensive study as stress-responsive transcription factors which may be major targets for crop development and important contributors to stress tolerance and crop production.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Data Availability

Data sharing does not apply to this article as no datasets were generated or analyzed during the current study.

References

  • Adachi H, Nakano T, Miyagawa N, Ishihama N, Yoshioka M, Katou Y, Yaeno T, Shirasu K, Yoshioka H (2015) WRKY transcription factors phosphorylated by MAPK regulate a plant immune NADPH oxidase in Nicotiana benthamiana. Plant Cell 27(9):2645–2663

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Agarwal M, Hao Y, Kapoor A, Dong C-H, Fujii H, Zheng X, 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(49):37636–37645

    Article  CAS  PubMed  Google Scholar 

  • Agarwal P, Agarwal PK, Nair S, Sopory S, Reddy M (2007) Stress-inducible DREB2A transcription factor from Pennisetum glaucum is a phosphoprotein and its phosphorylation negatively regulates its DNA-binding activity. Mol Genet Genomics 277:189–198

    Article  CAS  PubMed  Google Scholar 

  • Agarwal P, Agarwal PK, Joshi AJ, Sopory SK, Reddy MK (2010) Overexpression of PgDREB2A transcription factor enhances abiotic stress tolerance and activates downstream stress-responsive genes. Mol Biol Rep 37:1125–1135

    Article  CAS  PubMed  Google Scholar 

  • Ahuja I, de Vos RC, Bones AM, Hall RD (2010) Plant molecular stress responses face climate change. Trends Plant Sci 15(12):664–674

    Article  CAS  PubMed  Google Scholar 

  • Akhtar M, Jaiswal A, Taj G, Jaiswal J, Qureshi M, Singh N (2012) DREB1/CBF transcription factors: their structure, function and role in abiotic stress tolerance in plants. J Genet 91(3):385–395

    Article  CAS  PubMed  Google Scholar 

  • Araki S, Ito M, Soyano T, Nishihama R, Machida Y (2004) Mitotic cyclins stimulate the activity of c-Myb-like factors for transactivation of G2/M phase-specific genes in tobacco. J Biol Chem 279(31):32979–32988

    Article  CAS  PubMed  Google Scholar 

  • Baillo EH, Kimotho RN, Zhang Z, Xu P (2019) Transcription factors associated with abiotic and biotic stress tolerance and their potential for crops improvement. Genes 10(10):771

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bethke G, Unthan T, Uhrig JF, Pöschl Y, Gust AA, Scheel D, Lee J (2009) Flg22 regulates the release of an ethylene response factor substrate from MAP kinase 6 in Arabidopsis thaliana via ethylene signaling. Proc Natl Acad Sci 106(19):8067–8072

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bhadouria R, Singh R, Singh VK, Borthakur A, Ahamad A, Kumar G, Singh P (2019) Agriculture in the era of climate change: consequences and effects. In: Climate change and agricultural ecosystems. Elsevier, pp 1–23

  • Bundó M, Coca M (2017) Calcium-dependent protein kinase OsCPK10 mediates both drought tolerance and blast disease resistance in rice plants. J Exp Bot 68(11):2963–2975

    Article  PubMed  PubMed Central  Google Scholar 

  • Busk PK, Jensen AB, Pagès M (1997) Regulatory elements in vivo in the promoter of the abscisic acid responsive gene rab17 from maize. Plant J 11(6):1285–1295

    Article  CAS  PubMed  Google Scholar 

  • Cao X-y, Ming C, Xu Z-s, Chen Y-f, Li L-c, Yu Y-h, Liu Y-n (2012) Isolation and functional analysis of the bZIP transcription factor gene TaABP1 from a Chinese wheat landrace. J Integr Agric 11(10):1580–1591

    Article  CAS  Google Scholar 

  • Chae M-J, Lee J-S, Nam M-H, Cho K, Hong J-Y, Yi S-A, Suh S-C, Yoon I-S (2007) A rice dehydration-inducible SNF1-related protein kinase 2 phosphorylates an abscisic acid responsive element-binding factor and associates with ABA signaling. Plant Mol Biol 63(2):151–169

    Article  CAS  PubMed  Google Scholar 

  • Chinnusamy V, Ohta M, Kanrar S, Lee B-h, Hong X, Agarwal M, Zhu J-K (2003) ICE1: a regulator of cold-induced transcriptome and freezing tolerance in Arabidopsis. Genes Dev 17(8):1043–1054

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Choi H-i, Hong J-h, Ha J-o, Kang J-y, Kim SY (2000) ABFs, a family of ABA-responsive element binding factors. J Biol Chem 275(3):1723–1730

    Article  CAS  PubMed  Google Scholar 

  • Choi H-i, Park H-J, Park JH, Kim S, Im M-Y, Seo H-H, Kim Y-W, Hwang I, Kim SY (2005) Arabidopsis calcium-dependent protein kinase AtCPK32 interacts with ABF4, a transcriptional regulator of abscisic acid-responsive gene expression, and modulates its activity. Plant Physiol 139(4):1750–1761

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chu X, Wang C, Chen X, Lu W, Li H, Wang X, Hao L, Guo X (2015) The cotton WRKY gene GhWRKY41 positively regulates salt and drought stress tolerance in transgenic Nicotiana benthamiana. PLoS ONE 10(11):e0143022

    Article  PubMed  PubMed Central  Google Scholar 

  • Ciceri P, Gianazza E, Lazzari B, Lippoli G, Genga A, Hoscheck G, Schmidt RJ, Viotti A (1997) Phosphorylation of Opaque2 changes diurnally and impacts its DNA binding activity. Plant Cell 9(1):97–108

    CAS  PubMed  PubMed Central  Google Scholar 

  • Colcombet J, Hirt H (2008) Arabidopsis MAPKs: a complex signalling network involved in multiple biological processes. Biochemical Journal 413(2):217–226

    Article  CAS  PubMed  Google Scholar 

  • Cominelli E, Galbiati M, Vavasseur A, Conti L, Sala T, Vuylsteke M, Leonhardt N, Dellaporta SL, Tonelli C (2005) A guard-cell-specific MYB transcription factor regulates stomatal movements and plant drought tolerance. Curr Biol 15(13):1196–1200

    Article  CAS  PubMed  Google Scholar 

  • Cristina MS, Petersen M, Mundy J (2010) Mitogen-activated protein kinase signaling in plants. Annu Rev Plant Biol 61:621–649

    Article  Google Scholar 

  • Dai X, Wang Y, Zhang W-H (2016) OsWRKY74, a WRKY transcription factor, modulates tolerance to phosphate starvation in rice. J Exp Bot 67(3):947–960

    Article  CAS  PubMed  Google Scholar 

  • Danquah A, de Zelicourt A, Colcombet J, Hirt H (2014) The role of ABA and MAPK signaling pathways in plant abiotic stress responses. Biotechnol Adv 32(1):40–52

    Article  CAS  PubMed  Google Scholar 

  • Danquah A, de Zélicourt A, Boudsocq M, Neubauer J, Frei Frey N, Leonhardt N, Pateyron S, Gwinner F, Tamby JP, Ortiz-Masia D (2015) Identification and characterization of an ABA-activated MAP kinase cascade in Arabidopsis thaliana. Plant J 82(2):232–244

    Article  CAS  PubMed  Google Scholar 

  • Ding ZJ, Yan JY, Li CX, Li GX, Wu YR, Zheng SJ (2015) Transcription factor WRKY 46 modulates the development of Arabidopsis lateral roots in osmotic/salt stress conditions via regulation of ABA signaling and auxin homeostasis. Plant J 84(1):56–69

    Article  CAS  PubMed  Google Scholar 

  • Dong C-H, Agarwal M, Zhang Y, Xie Q, 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 103(21):8281–8286

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dröge-Laser W, Kaiser A, Lindsay WP, Halkier BA, Loake GJ, Doerner P, Dixon RA, Lamb C (1997) Rapid stimulation of a soybean protein-serine kinase that phosphorylates a novel bZIP DNA-binding protein, G/HBF-1, during the induction of early transcription-dependent defenses. EMBO J 16(4):726–738

    Article  PubMed  PubMed Central  Google Scholar 

  • Dubouzet JG, Sakuma Y, Ito Y, Kasuga M, Dubouzet EG, Miura S, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) OsDREB genes in rice, Oryza sativa L., encode transcription activators that function in drought-, high-salt-and cold-responsive gene expression. Plant J 33(4):751–763

    Article  CAS  PubMed  Google Scholar 

  • Easterling DR, Meehl GA, Parmesan C, Changnon SA, Karl TR, Mearns LO (2000) Climate extremes: observations, modeling, and impacts. Science 289(5487):2068–2074

    Article  CAS  PubMed  Google Scholar 

  • Erpen L, Devi HS, Grosser JW, Dutt M (2018) Potential use of the DREB/ERF, MYB, NAC and WRKY transcription factors to improve abiotic and biotic stress in transgenic plants. Plant Cell Tissue Organ Cult (PCTOC) 132(1):1–25

    Article  CAS  Google Scholar 

  • Fang Y, You J, Xie K, Xie W, Xiong L (2008) Systematic sequence analysis and identification of tissue-specific or stress-responsive genes of NAC transcription factor family in rice. Mol Genet Genomics 280(6):547–563

    Article  CAS  PubMed  Google Scholar 

  • Fujita Y, Fujita M, Satoh R, Maruyama K, Parvez MM, Seki M, Hiratsu K, Ohme-Takagi M, Shinozaki K, Yamaguchi-Shinozaki K (2005) AREB1 is a transcription activator of novel ABRE-dependent ABA signaling that enhances drought stress tolerance in Arabidopsis. Plant Cell 17(12):3470–3488

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fujita Y, Fujita M, Shinozaki K, Yamaguchi-Shinozaki K (2011) ABA-mediated transcriptional regulation in response to osmotic stress in plants. J Plant Res 124(4):509–525

    Article  CAS  PubMed  Google Scholar 

  • Furihata T, Maruyama K, Fujita Y, Umezawa T, Yoshida R, Shinozaki K, Yamaguchi-Shinozaki K (2006) Abscisic acid-dependent multisite phosphorylation regulates the activity of a transcription activator AREB1. Proc Natl Acad Sci 103(6):1988–1993

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gao X, He P (2013) Nuclear dynamics of Arabidopsis calcium-dependent protein kinases in effector-triggered immunity. Plant Signal Behav 8(4):e23868

    Article  PubMed  PubMed Central  Google Scholar 

  • Gilmour SJ, Zarka DG, Stockinger EJ, Salazar MP, Houghton JM, Thomashow MF (1998) Low temperature regulation of the Arabidopsis CBF family of AP2 transcriptional activators as an early step in cold-induced COR gene expression. Plant J 16(4):433–442

    Article  CAS  PubMed  Google Scholar 

  • Gilmour SJ, Sebolt AM, Salazar MP, Everard JD, Thomashow MF (2000) Overexpression of the Arabidopsis CBF3 transcriptional activator mimics multiple biochemical changes associated with cold acclimation. Plant Physiol 124(4):1854–1865

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gish LA, Clark SE (2011) The RLK/Pelle family of kinases. Plant J 66(1):117–127

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Göhre V, Jones AM, Sklenář J, Robatzek S, Weber AP (2012) Molecular crosstalk between PAMP-triggered immunity and photosynthesis. Mol Plant Microbe Interact 25(8):1083–1092

    Article  PubMed  Google Scholar 

  • Gong X, Zhang J, Hu J, Wang W, Wu H, Zhang Q, Liu JH (2015) FcWRKY 70, a WRKY protein of F. ortunella crassifolia, functions in drought tolerance and modulates putrescine synthesis by regulating arginine decarboxylase gene. Plant, Cell Environ 38(11):2248–2262

    Article  CAS  PubMed  Google Scholar 

  • Gong Q, Li S, Zheng Y, Duan H, Xiao F, Zhuang Y, He J, Wu G, Zhao S, Zhou H (2020) SUMOylation of MYB30 enhances salt tolerance by elevating alternative respiration via transcriptionally upregulating AOX1a in Arabidopsis. Plant J 102(6):1157–1171

    Article  CAS  PubMed  Google Scholar 

  • Gonzalez DH (2016) Introduction to transcription factor structure and function. In: Plant transcription factors. Elsevier, pp 3–11

  • Guo H-S, Xie Q, Fei J-F, Chua N-H (2005) MicroRNA directs mRNA cleavage of the transcription factor NAC1 to downregulate auxin signals for Arabidopsis lateral root development. Plant Cell 17(5):1376–1386

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guo L, Yang H, Zhang X, Yang S (2013) Lipid transfer protein 3 as a target of MYB96 mediates freezing and drought stress in Arabidopsis. J Exp Bot 64(6):1755–1767

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Haga N, Kato K, Murase M, Araki S, Kubo M, Demura T, Suzuki K, Müller I, Voß U, Jürgens G (2007) R1R2R3-Myb proteins positively regulate cytokinesis through activation of KNOLLE transcription in Arabidopsis thaliana

  • Hetherington AM, Woodward FI (2003) The role of stomata in sensing and driving environmental change. Nature 424(6951):901–908

    Article  CAS  PubMed  Google Scholar 

  • Hill CS, Treisman R (1995) Transcriptional regulation by extracellular signals: mechanisms and specificity. Cell 80(2):199–211

    Article  CAS  PubMed  Google Scholar 

  • Hoang MHT, Nguyen XC, Lee K, Kwon YS, Pham HTT, Park HC, Yun D-J, Lim CO, Chung WS (2012) Phosphorylation by AtMPK6 is required for the biological function of AtMYB41 in Arabidopsis. Biochem Biophys Res Commun 422(1):181–186

    Article  CAS  PubMed  Google Scholar 

  • Hu L, Ye M, Li R, Zhang T, Zhou G, Wang Q, Lu J, Lou Y (2015) The rice transcription factor WRKY53 suppresses herbivore-induced defenses by acting as a negative feedback modulator of mitogen-activated protein kinase activity. Plant Physiol 169(4):2907–2921

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hunter T, Karin M (1992) The regulation of transcription by phosphorylation. Cell 70(3):375–387

    Article  CAS  PubMed  Google Scholar 

  • Inukai S, Kock KH, Bulyk ML (2017) Transcription factor–DNA binding: beyond binding site motifs. Curr Opin Genet Dev 43:110–119

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jacobs D, Glossip D, Xing H, Muslin AJ, Kornfeld K (1999) Multiple docking sites on substrate proteins form a modular system that mediates recognition by ERK MAP kinase. Genes Dev 13(2):163–175

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jakoby M, Weisshaar B, Dröge-Laser W, Vicente-Carbajosa J, Tiedemann J, Kroj T, Parcy F (2002) bZIP transcription factors in Arabidopsis. Trends Plant Sci 7(3):106–111

    Article  CAS  PubMed  Google Scholar 

  • Javed T, Shabbir R, Ali A, Afzal I, Zaheer U, Gao S-J (2020) Transcription factors in plant stress responses: challenges and potential for sugarcane improvement. Plants 9(4):491

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jensen MK, Kjaersgaard T, Nielsen MM, Galberg P, Petersen K, O’shea C, Skriver K (2010) The Arabidopsis thaliana NAC transcription factor family: structure–function relationships and determinants of ANAC019 stress signalling. Biochem J 426(2):183–196

    Article  CAS  PubMed  Google Scholar 

  • Jeong JS, Kim YS, Baek KH, Jung H, Ha S-H, Do Choi Y, Kim M, Reuzeau C, Kim J-K (2010) Root-specific expression of OsNAC10 improves drought tolerance and grain yield in rice under field drought conditions. Plant Physiol 153(1):185–197

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jiang Y, Deyholos MK (2006) Comprehensive transcriptional profiling of NaCl-stressed Arabidopsis roots reveals novel classes of responsive genes. BMC Plant Biol 6(1):1–20

    Article  Google Scholar 

  • Jiang Y, Zeng B, Zhao H, Zhang M, Xie S, Lai J (2012) Genome-wide transcription factor gene prediction and their expressional tissue-specificities in maize F. J Integr Plant Biol 54(9):616–630

    Article  CAS  PubMed  Google Scholar 

  • Jiang J, Ma S, Ye N, Jiang M, Cao J, Zhang J (2017) WRKY transcription factors in plant responses to stresses. J Integr Plant Biol 59(2):86–101

    Article  CAS  PubMed  Google Scholar 

  • Jin H, Martin C (1999) Multifunctionality and diversity within the plant MYB-gene family. Plant Mol Biol 41(5):577–585

    Article  CAS  PubMed  Google Scholar 

  • Julkowska MM, Testerink C (2015) Tuning plant signaling and growth to survive salt. Trends Plant Sci 20(9):586–594

    Article  CAS  PubMed  Google Scholar 

  • Kagaya Y, Hobo T, Murata M, Ban A, Hattori T (2002) Abscisic acid–induced transcription is mediated by phosphorylation of an abscisic acid response element binding factor, TRAB1. Plant Cell 14(12):3177–3189

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kang J-y, Choi H-i, Im M-y, Kim SY (2002) Arabidopsis basic leucine zipper proteins that mediate stress-responsive abscisic acid signaling. Plant Cell 14(2):343–357

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim S, Jy K, Cho DI, Park JH, Kim SY (2004) ABF2, an ABRE-binding bZIP factor, is an essential component of glucose signaling and its overexpression affects multiple stress tolerance. Plant J 40(1):75–87

    Article  CAS  PubMed  Google Scholar 

  • Kim J-S, Mizoi J, Yoshida T, Fujita Y, Nakajima J, Ohori T, Todaka D, Nakashima K, Hirayama T, Shinozaki K (2011) An ABRE promoter sequence is involved in osmotic stress-responsive expression of the DREB2A gene, which encodes a transcription factor regulating drought-inducible genes in Arabidopsis. Plant Cell Physiol 52(12):2136–2146

    Article  CAS  PubMed  Google Scholar 

  • Kim MJ, Park M-J, Seo PJ, Song J-S, Kim H-J, Park C-M (2012) Controlled nuclear import of the transcription factor NTL6 reveals a cytoplasmic role of SnRK2. 8 in the drought-stress response. Biochem J 448(3):353–363

    Article  CAS  PubMed  Google Scholar 

  • Kim SH, Kim HS, Bahk S, An J, Yoo Y, Kim J-Y, Chung WS (2017) Phosphorylation of the transcriptional repressor MYB15 by mitogen-activated protein kinase 6 is required for freezing tolerance in Arabidopsis. Nucleic Acids Res 45(11):6613–6627

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kizis D, Pagès M (2002) Maize DRE-binding proteins DBF1 and DBF2 are involved in rab17 regulation through the drought-responsive element in an ABA-dependent pathway. Plant J 30(6):679–689

    Article  CAS  PubMed  Google Scholar 

  • Klimczak LJ, Collinge MA, Farini D, Giuliano G, Walker JC, Cashmore AR (1995) Reconstitution of Arabidopsis casein kinase II from recombinant subunits and phosphorylation of transcription factor GBF1. Plant Cell 7(1):105–115

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kobayashi Y, Murata M, Minami H, Yamamoto S, Kagaya Y, Hobo T, Yamamoto A, Hattori T (2005) Abscisic acid-activated SNRK2 protein kinases function in the gene-regulation pathway of ABA signal transduction by phosphorylating ABA response element-binding factors. Plant J 44(6):939–949

    Article  CAS  PubMed  Google Scholar 

  • Kobayashi F, Maeta E, Terashima A, Kawaura K, Ogihara Y, Takumi S (2008a) Development of abiotic stress tolerance via bZIP-type transcription factor LIP19 in common wheat. J Exp Bot 59(4):891–905

    Article  CAS  PubMed  Google Scholar 

  • Kobayashi F, Maeta E, Terashima A, Takumi S (2008b) Positive role of a wheat HvABI5 ortholog in abiotic stress response of seedlings. Physiol Plant 134(1):74–86

    Article  CAS  PubMed  Google Scholar 

  • Lampard GR, MacAlister CA, Bergmann DC (2008) Arabidopsis stomatal initiation is controlled by MAPK-mediated regulation of the bHLH SPEECHLESS. Science 322(5904):1113–1116

    Article  CAS  PubMed  Google Scholar 

  • Lan Thi Hoang X, Du Nhi NH, Binh Anh Thu N, Phuong Thao N, Phan Tran L-S (2017) Transcription factors and their roles in signal transduction in plants under abiotic stresses. Curr Genom 18(6):483–497

    Google Scholar 

  • Le DT, Nishiyama R, Watanabe Y, Mochida K, Yamaguchi-Shinozaki K, Shinozaki K, Tran L-SP (2011) Genome-wide survey and expression analysis of the plant-specific NAC transcription factor family in soybean during development and dehydration stress. DNA Res 18(4):263–276

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee SC, Luan S (2012) ABA signal transduction at the crossroad of biotic and abiotic stress responses. Plant, Cell Environ 35(1):53–60

    Article  CAS  PubMed  Google Scholar 

  • Li Jb, Luan Ys, Liu Z (2015) Overexpression of SpWRKY1 promotes resistance to Phytophthora nicotianae and tolerance to salt and drought stress in transgenic tobacco. Physiol Plant 155(3):248–266

    Article  CAS  PubMed  Google Scholar 

  • Liao Y, Zou H-F, Wei W, Hao Y-J, Tian A-G, Huang J, Liu Y-F, Zhang J-S, Chen S-Y (2008) Soybean GmbZIP44, GmbZIP62 and GmbZIP78 genes function as negative regulator of ABA signaling and confer salt and freezing tolerance in transgenic Arabidopsis. Planta 228(2):225–240

    Article  CAS  PubMed  Google Scholar 

  • Lim CW, Baek W, Jung J, Kim J-H, Lee SC (2015) Function of ABA in stomatal defense against biotic and drought stresses. Int J Mol Sci 16(7):15251–15270

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu Y, Zhang S (2004) Phosphorylation of 1-aminocyclopropane-1-carboxylic acid synthase by MPK6, a stress-responsive mitogen-activated protein kinase, induces ethylene biosynthesis in Arabidopsis. Plant Cell 16(12):3386–3399

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu Q, Kasuga M, Sakuma Y, Abe H, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (1998) Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought-and low-temperature-responsive gene expression, respectively. Arabidopsis Plant Cell 10(8):1391–1406

    Article  CAS  PubMed  Google Scholar 

  • Liu Jx, Srivastava R, Howell SH (2008) Stress-induced expression of an activated form of AtbZIP17 provides protection from salt stress in Arabidopsis. Plant Cell Environ 31(12):1735–1743

    Article  CAS  PubMed  Google Scholar 

  • Liu Q-L, Xu K-D, Zhao L-J, Pan Y-Z, Jiang B-B, Zhang H-Q, Liu G-L (2011) Overexpression of a novel chrysanthemum NAC transcription factor gene enhances salt tolerance in tobacco. Biotech Lett 33(10):2073–2082

    Article  CAS  Google Scholar 

  • Lobell DB, Schlenker W, Costa-Roberts J (2011) Climate trends and global crop production since 1980. Science 333(6042):616–620

    Article  CAS  PubMed  Google Scholar 

  • Lu M, Ying S, Zhang D-F, Shi Y-S, Song Y-C, Wang T-Y, Li Y (2012) A maize stress-responsive NAC transcription factor, ZmSNAC1, confers enhanced tolerance to dehydration in transgenic Arabidopsis. Plant Cell Rep 31(9):1701–1711

    Article  CAS  PubMed  Google Scholar 

  • Mallory AC, Dugas DV, Bartel DP, Bartel B (2004) MicroRNA regulation of NAC-domain targets is required for proper formation and separation of adjacent embryonic, vegetative, and floral organs. Curr Biol 14(12):1035–1046

    Article  CAS  PubMed  Google Scholar 

  • Mao G, Meng X, Liu Y, Zheng Z, Chen Z, Zhang S (2011) Phosphorylation of a WRKY transcription factor by two pathogen-responsive MAPKs drives phytoalexin biosynthesis in Arabidopsis. Plant Cell 23(4):1639–1653

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meng X, Xu J, He Y, Yang K-Y, Mordorski B, Liu Y, Zhang S (2013) Phosphorylation of an ERF transcription factor by Arabidopsis MPK3/MPK6 regulates plant defense gene induction and fungal resistance. Plant Cell 25(3):1126–1142

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miao Y, Laun TM, Smykowski A, Zentgraf U (2007) Arabidopsis MEKK1 can take a short cut: it can directly interact with senescence-related WRKY53 transcription factor on the protein level and can bind to its promoter. Plant Mol Biol 65(1):63–76

    Article  CAS  PubMed  Google Scholar 

  • Mishra S, Triptahi V, Singh S, Phukan UJ, Gupta M, Shanker K, Shukla RK (2013) Wound induced tanscriptional regulation of benzylisoquinoline pathway and characterization of wound inducible PsWRKY transcription factor from Papaver somniferum. PLoS ONE 8(1):e52784

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mitula F, Tajdel M, Cieśla A, Kasprowicz-Maluśki A, Kulik A, Babula-Skowrońska D, Michalak M, Dobrowolska G, Sadowski J, Ludwików A (2015) Arabidopsis ABA-activated kinase MAPKKK18 is regulated by protein phosphatase 2C ABI1 and the ubiquitin–proteasome pathway. Plant Cell Physiol 56(12):2351–2367

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mizoi J, Shinozaki K (1819) Yamaguchi-Shinozaki K (2012) AP2/ERF family transcription factors in plant abiotic stress responses. Biochim Biophys Acta (BBA)-Gene Regul Mech 2:86–96

    Google Scholar 

  • Mizoi J, Kanazawa N, Kidokoro S, Takahashi F, Qin F, Morimoto K, Shinozaki K, Yamaguchi-Shinozaki K (2019) Heat-induced inhibition of phosphorylation of the stress-protective transcription factor DREB2A promotes thermotolerance of Arabidopsis thaliana. J Biol Chem 294(3):902–917

    Article  CAS  PubMed  Google Scholar 

  • Muñiz García MN, Giammaria V, Grandellis C, Téllez-Iñón MT, Ulloa RM, Capiati DA (2012) Characterization of StABF1, a stress-responsive bZIP transcription factor from Solanum tuberosum L. that is phosphorylated by StCDPK2 in vitro. Planta 235(4):761–778

    Article  PubMed  Google Scholar 

  • Nakabayashi R, Yonekura-Sakakibara K, Urano K, Suzuki M, Yamada Y, Nishizawa T, Matsuda F, Kojima M, Sakakibara H, Shinozaki K (2014) Enhancement of oxidative and drought tolerance in Arabidopsis by overaccumulation of antioxidant flavonoids. Plant J 77(3):367–379

    Article  CAS  PubMed  Google Scholar 

  • Nakagami H, Sugiyama N, Mochida K, Daudi A, Yoshida Y, Toyoda T, Tomita M, Ishihama Y, Shirasu K (2010) Large-scale comparative phosphoproteomics identifies conserved phosphorylation sites in plants. Plant Physiol 153(3):1161–1174

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nakashima K, Ito Y, Yamaguchi-Shinozaki K (2009) Transcriptional regulatory networks in response to abiotic stresses in Arabidopsis and grasses. Plant Physiol 149(1):88–95

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nakashima K, Yamaguchi-Shinozaki K, Shinozaki K (2014) The transcriptional regulatory network in the drought response and its crosstalk in abiotic stress responses including drought, cold, and heat. Front Plant Sci 5:170

    Article  PubMed  PubMed Central  Google Scholar 

  • Nguyen XC, Hoang MHT, Kim HS, Lee K, Liu X-M, Kim SH, Bahk S, Park HC, Chung WS (2012a) Phosphorylation of the transcriptional regulator MYB44 by mitogen activated protein kinase regulates Arabidopsis seed germination. Biochem Biophys Res Commun 423(4):703–708

    Article  CAS  PubMed  Google Scholar 

  • Nguyen XC, Kim SH, Lee K, Kim KE, Liu X-M, Han HJ, Hoang MHT, Lee S-W, Hong JC, Moon Y-H (2012b) Identification of a C2H2-type zinc finger transcription factor (ZAT10) from Arabidopsis as a substrate of MAP kinase. Plant Cell Rep 31(4):737–745

    Article  CAS  PubMed  Google Scholar 

  • Nguyen XC, Kim SH, Hussain S, An J, Yoo Y, Han HJ, Yoo JS, Lim CO, Yun D-J, Chung WS (2016) A positive transcription factor in osmotic stress tolerance, ZAT10, is regulated by MAP kinases in Arabidopsis. J Plant Biol 59(1):55–61

    Article  CAS  Google Scholar 

  • Nuruzzaman M, Manimekalai R, Sharoni AM, Satoh K, Kondoh H, Ooka H, Kikuchi S (2010) Genome-wide analysis of NAC transcription factor family in rice. Gene 465(1–2):30–44

    Article  CAS  PubMed  Google Scholar 

  • Oh JE, Kwon Y, Kim JH, Noh H, Hong S-W, Lee H (2011) A dual role for MYB60 in stomatal regulation and root growth of Arabidopsis thaliana under drought stress. Plant Mol Biol 77(1):91–103

    Article  CAS  PubMed  Google Scholar 

  • Olsen AN, Ernst HA, Leggio LL, Skriver K (2005) NAC transcription factors: structurally distinct, functionally diverse. Trends Plant Sci 10(2):79–87

    Article  CAS  PubMed  Google Scholar 

  • Olsen JV, Blagoev B, Gnad F, Macek B, Kumar C, Mortensen P, Mann M (2006) Global, in vivo, and site-specific phosphorylation dynamics in signaling networks. Cell 127(3):635–648

    Article  CAS  PubMed  Google Scholar 

  • Ooka H, Satoh K, Doi K, Nagata T, Otomo Y, Murakami K, Matsubara K, Osato N, Kawai J, Carninci P (2003) Comprehensive analysis of NAC family genes in Oryza sativa and Arabidopsis thaliana. DNA Res 10(6):239–247

    Article  CAS  PubMed  Google Scholar 

  • Popescu SC, Popescu GV, Bachan S, Zhang Z, Gerstein M, Snyder M, Dinesh-Kumar SP (2009) MAPK target networks in Arabidopsis thaliana revealed using functional protein microarrays. Genes Dev 23(1):80–92

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Puranik S, Bahadur RP, Srivastava PS, Prasad M (2011) Molecular cloning and characterization of a membrane associated NAC family gene, SiNAC from foxtail millet [Setaria italica (L.) P. Beauv]. Mol Biotechnol 49(2):138–150

    Article  CAS  PubMed  Google Scholar 

  • Puranik S, Sahu PP, Srivastava PS, Prasad M (2012) NAC proteins: regulation and role in stress tolerance. Trends Plant Sci 17(6):369–381

    Article  CAS  PubMed  Google Scholar 

  • Qiu JL, Fiil BK, Petersen K, Nielsen HB, Botanga CJ, Thorgrimsen S, Palma K, Suarez-Rodriguez MC, Sandbech-Clausen S, Lichota J (2008) Arabidopsis MAP kinase 4 regulates gene expression through transcription factor release in the nucleus. EMBO J 27(16):2214–2221

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Raineri J, Ribichich KF, Chan RL (2015) The sunflower transcription factor HaWRKY76 confers drought and flood tolerance to Arabidopsis thaliana plants without yield penalty. Plant Cell Rep 34(12):2065–2080

    Article  CAS  PubMed  Google Scholar 

  • Ramegowda V, Senthil-Kumar M, Nataraja KN, Reddy MK, Mysore KS, Udayakumar M (2012) Expression of a finger millet transcription factor, EcNAC1, in tobacco confers abiotic stress-tolerance. PLoS ONE 7(7):e40397

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rodriguez-Uribe L, O’Connell MA (2006) A root-specific bZIP transcription factor is responsive to water deficit stress in tepary bean (Phaseolus acutifolius) and common bean (P. vulgaris). J Exp Bot 57(6):1391–1398

    Article  CAS  PubMed  Google Scholar 

  • Saibo NJ, Lourenço T, Oliveira MM (2009) Transcription factors and regulation of photosynthetic and related metabolism under environmental stresses. Ann Bot 103(4):609–623

    Article  CAS  PubMed  Google Scholar 

  • Sakuma Y, Liu Q, Dubouzet JG, Abe H, Shinozaki K, Yamaguchi-Shinozaki K (2002) DNA-binding specificity of the ERF/AP2 domain of Arabidopsis DREBs, transcription factors involved in dehydration-and cold-inducible gene expression. Biochem Biophys Res Commun 290(3):998–1009

    Article  CAS  PubMed  Google Scholar 

  • Sakuma Y, Maruyama K, Osakabe Y, Qin F, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2006a) Functional analysis of an Arabidopsis transcription factor, DREB2A, involved in drought-responsive gene expression. Plant Cell 18(5):1292–1309

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sakuma Y, Maruyama K, Qin F, Osakabe Y, Shinozaki K, Yamaguchi-Shinozaki K (2006b) Dual function of an Arabidopsis transcription factor DREB2A in water-stress-responsive and heat-stress-responsive gene expression. Proc Natl Acad Sci 103(49):18822–18827

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Seger R, Krebs EG (1995) The MAPK signaling cascade. FASEB J 9(9):726–735

    Article  CAS  PubMed  Google Scholar 

  • Shahnejat-Bushehri S, Mueller-Roeber B, Balazadeh S (2012) Arabidopsis NAC transcription factor JUNGBRUNNEN1 affects thermomemory-associated genes and enhances heat stress tolerance in primed and unprimed conditions. Plant Signal Behav 7(12):1518–1521

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shan W, Kuang JF, Lu WJ, Chen JY (2014) Banana fruit NAC transcription factor MaNAC 1 is a direct target of MaICE 1 and involved in cold stress through interacting with MaCBF 1. Plant Cell Environ 37(9):2116–2127

    Article  CAS  PubMed  Google Scholar 

  • Shao H-B, Chu L-Y, Jaleel CA, Manivannan P, Panneerselvam R, Shao M-A (2009) Understanding water deficit stress-induced changes in the basic metabolism of higher plants–biotechnologically and sustainably improving agriculture and the ecoenvironment in arid regions of the globe. Crit Rev Biotechnol 29(2):131–151

    Article  CAS  PubMed  Google Scholar 

  • Shiu S-H, Bleecker AB (2003) Expansion of the receptor-like kinase/Pelle gene family and receptor-like proteins in Arabidopsis. Plant Physiol 132(2):530–543

    Article  CAS  PubMed  Google Scholar 

  • Solomon S, Manning M, Marquis M, Qin D (2007a) Climate change 2007-the physical science basis: Working group I contribution to the fourth assessment report of the IPCC, vol 4. Cambridge University Press

    Google Scholar 

  • Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt K, Tignor M, Miller HL (2007b) IPCC, 2007b: Climate change 2007b: The physical science basis. Contribution of Working Group I to the fourth assessment report of the Intergovernmental Panel on Climate Change. SD Solomon (Ed)

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stracke R, Werber M, Weisshaar B (2001) The R2R3-MYB gene family in Arabidopsis thaliana. Curr Opin Plant Biol 4(5):447–456

    Article  CAS  PubMed  Google Scholar 

  • Sugiyama N, Nakagami H, Mochida K, Daudi A, Tomita M, Shirasu K, Ishihama Y (2008) Large-scale phosphorylation mapping reveals the extent of tyrosine phosphorylation in Arabidopsis. Mol Syst Biol 4(1):193

    Article  PubMed  PubMed Central  Google Scholar 

  • Sun Y, Zhao J, Li X, Li Y (2020) E2 conjugases UBC1 and UBC2 regulate MYB42-mediated SOS pathway in response to salt stress in Arabidopsis. New Phytol 227(2):455–472

    Article  CAS  PubMed  Google Scholar 

  • Takasaki H, Maruyama K, Kidokoro S, Ito Y, Fujita Y, Shinozaki K, Yamaguchi-Shinozaki K, Nakashima K (2010) The abiotic stress-responsive NAC-type transcription factor OsNAC5 regulates stress-inducible genes and stress tolerance in rice. Mol Genet Genom 284(3):173–183

    Article  CAS  Google Scholar 

  • Tang Y, Liu M, Gao S, Zhang Z, Zhao X, Zhao C, Zhang F, Chen X (2012) Molecular characterization of novel TaNAC genes in wheat and overexpression of TaNAC2a confers drought tolerance in tobacco. Physiol Plant 144(3):210–224

    Article  CAS  PubMed  Google Scholar 

  • Thurow C, Schiermeyer A, Krawczyk S, Butterbrodt T, Nickolov K, Gatz C (2005) Tobacco bZIP transcription factor TGA2. 2 and related factor TGA2. 1 have distinct roles in plant defense responses and plant development. Plant J 44(1):100–113

    Article  CAS  PubMed  Google Scholar 

  • Todaka D, Shinozaki K, Yamaguchi-Shinozaki K (2015) Recent advances in the dissection of drought-stress regulatory networks and strategies for development of drought-tolerant transgenic rice plants. Front Plant Sci 6:84

    Article  PubMed  PubMed Central  Google Scholar 

  • Tripathi P, Rabara RC, Rushton PJ (2014) A systems biology perspective on the role of WRKY transcription factors in drought responses in plants. Planta 239(2):255–266

    Article  CAS  PubMed  Google Scholar 

  • van Bentem SdlF, Hirt H H (2009) Protein tyrosine phosphorylation in plants: more abundant than expected? Trends Plant Sci 14(2):71–76

    Article  Google Scholar 

  • Wang H, Ngwenyama N, Liu Y, Walker JC, Zhang S (2007) Stomatal development and patterning are regulated by environmentally responsive mitogen-activated protein kinases in Arabidopsis. Plant Cell 19(1):63–73

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang Z, Zhu Y, Wang L, Liu X, Liu Y, Phillips J, Deng X (2009) A WRKY transcription factor participates in dehydration tolerance in Boea hygrometrica by binding to the W-box elements of the galactinol synthase (BhGolS1) promoter. Planta 230(6):1155–1166

    Article  CAS  PubMed  Google Scholar 

  • Wang Z, Casas-Mollano JA, Xu J, Riethoven J-JM, Zhang C, Cerutti H (2015) Osmotic stress induces phosphorylation of histone H3 at threonine 3 in pericentromeric regions of Arabidopsis thaliana. Proc Natl Acad Sci 112(27):8487–8492

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang F, Kong W, Wong G, Fu L, Peng R, Li Z, Yao Q (2016a) AtMYB12 regulates flavonoids accumulation and abiotic stress tolerance in transgenic Arabidopsis thaliana. Mol Genet Genom 291(4):1545–1559

    Article  CAS  Google Scholar 

  • Wang H, Wang H, Shao H, Tang X (2016b) Recent advances in utilizing transcription factors to improve plant abiotic stress tolerance by transgenic technology. Front Plant Sci 7:67

    PubMed  PubMed Central  Google Scholar 

  • Wu S, Bates B, Zbigniew Kundzewicz A, Palutikof J (2008) Climate change and water. Technical Paper of the Intergovernmental Panel on Climate Change Geneva

  • Xie C, Zhou X, Deng X, Guo Y (2010) PKS5, a SNF1-related kinase, interacts with and phosphorylates NPR1, and modulates expression of WRKY38 and WRKY62. J Genet Genomics 37(6):359–369

    Article  CAS  PubMed  Google Scholar 

  • Xu Q, Feng W, Peng H, Ni Z, Sun Q (2014) TaWRKY71, a WRKY transcription factor from wheat, enhances tolerance to abiotic stress in transgenic Arabidopsis thaliana. Cereal Res Commun 42(1):47–57

    Article  CAS  Google Scholar 

  • Yamaguchi-Shinozaki K, 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(2):251–264

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yang Y, Guo Y (2018) Unraveling salt stress signaling in plants. J Integr Plant Biol 60(9):796–804

    Article  CAS  PubMed  Google Scholar 

  • Yang S-H, Sharrocks AD, Whitmarsh AJ (2003) Transcriptional regulation by the MAP kinase signaling cascades. Gene 320:3–21

    Article  CAS  PubMed  Google Scholar 

  • Yang W, Zhang W, Wang X (2017) Post-translational control of ABA signalling: the roles of protein phosphorylation and ubiquitination. Plant Biotechnol J 15(1):4–14

    Article  CAS  PubMed  Google Scholar 

  • Yokotani N, Ichikawa T, Kondou Y, Matsui M, Hirochika H, Iwabuchi M, Oda K (2009) Tolerance to various environmental stresses conferred by the salt-responsive rice gene ONAC063 in transgenic Arabidopsis. Planta 229(5):1065–1075

    Article  CAS  PubMed  Google Scholar 

  • Yoshida T, Ohama N, Nakajima J, Kidokoro S, Mizoi J, Nakashima K, Maruyama K, Kim J-M, Seki M, Todaka D (2011) Arabidopsis HsfA1 transcription factors function as the main positive regulators in heat shock-responsive gene expression. Mol Genet Genom 286:321–332

    Article  CAS  Google Scholar 

  • You J, Zong W, Li X, Ning J, Hu H, Li X, Xiao J, Xiong L (2013) The SNAC1-targeted gene OsSRO1c modulates stomatal closure and oxidative stress tolerance by regulating hydrogen peroxide in rice. J Exp Bot 64(2):569–583

    Article  CAS  PubMed  Google Scholar 

  • Zhang L, Zhang L, Xia C, Zhao G, Liu J, Jia J, Kong X (2015) A novel wheat bZIP transcription factor, TabZIP60, confers multiple abiotic stress tolerances in transgenic Arabidopsis. Physiol Plant 153(4):538–554

    Article  CAS  PubMed  Google Scholar 

  • Zhao R, Sun HL, Mei C, Wang XJ, Yan L, Liu R, Zhang XF, Wang XF, Zhang DP (2011) The Arabidopsis Ca2+-dependent protein kinase CPK12 negatively regulates abscisic acid signaling in seed germination and post-germination growth. New Phytol 192(1):61–73

    Article  CAS  PubMed  Google Scholar 

  • Zhou QY, Tian AG, Zou HF, Xie ZM, Lei G, Huang J, Wang CM, Wang HW, Zhang JS, Chen SY (2008) Soybean WRKY-type transcription factor genes, GmWRKY13, GmWRKY21, and GmWRKY54, confer differential tolerance to abiotic stresses in transgenic Arabidopsis plants. Plant Biotechnol J 6(5):486–503

    Article  CAS  PubMed  Google Scholar 

  • Zhu S-Y, Yu X-C, Wang X-J, Zhao R, Li Y, Fan R-C, Shang Y, Du S-Y, Wang X-F, Wu F-Q (2007) Two calcium-dependent protein kinases, CPK4 and CPK11, regulate abscisic acid signal transduction in Arabidopsis. Plant Cell 19(10):3019–3036

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu X, Liu S, Meng C, Qin L, Kong L, Xia G (2013) WRKY transcription factors in wheat and their induction by biotic and abiotic stress. Plant Mol Biol Report 31(5):1053–1067

    Article  CAS  Google Scholar 

  • Zhu Y, Yan J, Liu W, Liu L, Sheng Y, Sun Y, Li Y, Scheller HV, Jiang M, Hou X (2016) Phosphorylation of a NAC transcription factor by a calcium/calmodulin-dependent protein kinase regulates abscisic acid-induced antioxidant defense in maize. Plant Physiol 171(3):1651–1664

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zou M, Guan Y, Ren H, Zhang F, Chen F (2008) A bZIP transcription factor, OsABI5, is involved in rice fertility and stress tolerance. Plant Mol Biol 66(6):675–683

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

This work was supported by the earmarked funds for China Agricultural Research System (Grant No. CARS-01–61), National Science and Technology Support Program of China (Grant No. 2015BAD01B01), Science and Technology Support Program of Jiangsu Province, China (Grant Nos. BE2016370-3 and BE2017323), Natural Science Foundation of Jiangsu Province of China (BK20201214), the Natural Science Foundation of Jiangsu Province, China (Grant No. BK20161299), and the Financial Grant Support Program of Lianyungang City, Jiangsu Province, China (Grant Nos. QNJJ1704, QNJJ2102, QNJJ2107 and QNJJ2211).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Xu Dayong or Babatunde Kazeem Bello.

Ethics declarations

Conflict of interest

All the authors affirm that they have no financial or personal relationships that would create a conflict of interest.

Additional information

Communicated by Gerhard Leubner.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Baoxiang, W., Zhiguang, S., Yan, L. et al. A pervasive phosphorylation cascade modulation of plant transcription factors in response to abiotic stress. Planta 258, 73 (2023). https://doi.org/10.1007/s00425-023-04232-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00425-023-04232-x

Keywords

Navigation