Skip to main content
Log in

Cytokinins as central regulators during plant growth and stress response

  • Review
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

Key message

Cytokinins are a class of phytohormone that participate in the regulation of the plant growth, development, and stress response. In this review, the potential regulating mechanism during plant growth and stress response are discussed.

Abstract

Cytokinins are a class of phytohormone that participate in the regulation of plant growth, physiological activities, and yield. Cytokinins also play a key role in response to abiotic stresses, such as drought, salt and high or low temperature. Through the signal transduction pathway, cytokinins interact with various transcription factors via a series of phosphorylation cascades to regulate cytokinin-target gene expression. In this review, we systematically summarize the biosynthesis and metabolism of cytokinins, cytokinin signaling, and associated gene regulation, and highlight the function of cytokinins during plant development and resistance to abiotic stress. We also focus on the importance of crosstalk between cytokinins and other classes of phytohormones, including auxin, ethylene, strigolactone, and gibberellin. Our aim is to provide a comprehensive overview of recent findings on the mechanisms by which cytokinins act as central regulators of plant development and stress reactions, and highlight topics for future research.

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.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Aki SS, Mikami T, Naramoto S, Nishihama R, Ishizaki K, Kojima M, Takebayashi Y, Sakakibara H, Kyozuka J, Kohchi T, Umeda M (2019) Cytokinin signaling is essential for organ formation in Marchantia polymorpha. Plant Cell Physiol 60:1842–1854

    CAS  PubMed  Google Scholar 

  • Aloni R (1995) The induction of vascular tissues by auxin and cytokinin. In: Davies PJ (eds) Plant hormones. Springer, Dordrecht, pp 531–546

    Google Scholar 

  • An J, Yao J, Xu R, You C, Wang X, Hao Y (2018) An apple NAC transcription factor enhances salt stress tolerance by modulating the ethylene response. Physiol Plant 164:279–289

    CAS  PubMed  Google Scholar 

  • Argueso CT, Ferreira FJ, Kieber JJ (2009) Environmental perception avenues: the interaction of cytokinin and environmental response pathways. Plant Cell Environ 32:1147–1160

    CAS  PubMed  Google Scholar 

  • Argueso CT, Raines T, Kieber JJ (2010) Cytokinin signaling and transcriptional networks. Curr Opin Plant Biol 13:533–539

    CAS  PubMed  Google Scholar 

  • Arkhipov DV, Lomin SN, Myakushina YA, Savelieva EM, Osolodkin DI, Romanov GA (2019) Modeling of protein–protein interactions in cytokinin signal transduction. Int J Mol Sci 20:2096–2118

    CAS  PubMed Central  Google Scholar 

  • Artner C, Benkova E (2019) Ethylene and cytokinin: partners in root growth regulation. Mol Plant 12:1312–1314

    CAS  PubMed  Google Scholar 

  • Astot C, Dolezal K, Nordstrom A, Wang Q, Kunkel T, Moritz T, Chua NH, Sandberg G (2000) An alternative cytokinin biosynthesis pathway. Proc Natl Acad Sci USA 97:14778–14783

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bhargava A, Clabaugh I, To JP, Maxwell BB, Chiang YH, Schaller GE, Loraine A, Kieber JJ (2013) Identification of cytokinin-responsive genes using microarray meta-analysis and RNA-Seq in Arabidopsis. Plant Physiol 162:272–294

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bolle C (2004) The role of GRAS proteins in plant signal transduction and development. Planta 218:683–692

    CAS  PubMed  Google Scholar 

  • Caers M, Rudelsheim P, Van Onckelen H, Horemans S (1985) Effect of heat stress on photosynthetic activity and chloroplast ultrastructure in correlation with endogenous cytokinin concentration in maize seedlings. Plant Cell Physiol 26:47–52

    CAS  Google Scholar 

  • Cai B, Li Q, Liu F, Bi H, Ai X (2018) Decreasing fructose-1,6-bisphosphate aldolase activity reduces plant growth and tolerance to chilling stress in tomato seedlings. Physiol Plant 163:247–258

    CAS  PubMed  Google Scholar 

  • Chen B, Yang H (2013) 6-Benzylaminopurine alleviates chilling injury of postharvest cucumber fruit through modulating antioxidant system and energy status. J Sci Food Agric 93:1915–1921

    CAS  PubMed  Google Scholar 

  • Chen Y, Han Y, Kong X, Kang H, Ren Y, Wang W (2017) Ectopic expression of wheat expansin gene TaEXPA2 improved the salt tolerance of transgenic tobacco by regulating Na+/K+ and antioxidant competence. Physiol Plant 159:161–177

    CAS  PubMed  Google Scholar 

  • Cheng X, Jiang H, Zhang J, Qian Y, Zhu S, Cheng B (2010) Overexpression of type-A rice response regulators, OsRR3 and OsRR5, results in lower sensitivity to cytokinins. Genet Mol Res 9:348–359

    CAS  PubMed  Google Scholar 

  • Cheng Z, Wang L, Sun W, Zhang Y, Zhou C, Su Y, Li W, Sun T, Zhao X, Li X, Cheng Y, Zhao Y, Xie Q, Zhang X (2013) Pattern of auxin and cytokinin responses for shoot meristem induction results from the regulation of cytokinin biosynthesis by AUXIN RESPONSE FACTOR3. Plant Physiol 161:240–251

    CAS  PubMed  Google Scholar 

  • Coenen C, Lomax TL (1997) Auxin-cytokinin interactions in higher plants: old problems and new tools. Trends Plant Sci 2:351–356

    CAS  PubMed  Google Scholar 

  • Corot A, Roman H, Douillet O, Autret H, Perez-Garcia MD, Citerne S, Bertheloot J, Sakr S, Leduc N, Demotes-Mainard S (2017) Cytokinins and abscisic acid act antagonistically in the regulation of the bud outgrowth pattern by light intensity. Front Plant Sci 8:1724–1739

    PubMed  PubMed Central  Google Scholar 

  • Cortleven A, Ehret S, Schmulling T, Johansson H (2019a) Ethylene-independent promotion of photomorphogenesis in the dark by cytokinin requires COP1 and the CDD complex. J Exp Bot 70:165–178

    CAS  PubMed  Google Scholar 

  • Cortleven A, Leuendorf JE, Frank M, Pezzetta D, Bolt S, Schmulling T (2019b) Cytokinin action in response to abiotic and biotic stresses in plants. Plant Cell Environ 42:998–1018

    CAS  PubMed  Google Scholar 

  • Davies WJ, Kudoyarova G, Hartung W (2005) Long-distance ABA Signaling and its relation to other signaling pathways in the detection of soil drying and the mediation of the Plant’s response to drought. J Plant Growth Regul 24:285–295

    CAS  Google Scholar 

  • Di Mambro R, De Ruvo M, Pacifici E, Salvi E, Sozzani R, Benfey PN, Busch W, Novak O, Ljung K, Di Paola L, Maree AFM, Costantino P, Grieneisen VA, Sabatini S (2017) Auxin minimum triggers the developmental switch from cell division to cell differentiation in the Arabidopsis root. Proc Natl Acad Sci USA 114:E7641–E7649

    PubMed  PubMed Central  Google Scholar 

  • Dolgikh AV, Kirienko AN, Tikhonovich IA, Foo E, Dolgikh EA (2019) The DELLA proteins influence the expression of cytokinin biosynthesis and response genes during nodulation. Front Plant Sci 10:432

  • Duan J, Yu H, Yuan K, Liao Z, Meng X, Jing Y, Liu G, Chu J, Li J (2019) Strigolactone promotes cytokinin degradation through transcriptional activation of CYTOKININ OXIDASE/DEHYDROGENASE 9 in rice. Proc Natl Acad Sci USA 116:14319–14324

    CAS  PubMed  PubMed Central  Google Scholar 

  • Durbak A, Yao H, McSteen P (2012) Hormone signaling in plant development. Curr Opin Plant Biol 15:92–96

    CAS  PubMed  Google Scholar 

  • Elena P, Riccardo DM, Raffaele DI, Paolo C, Sabrina S (2018) Acidic cell elongation drives cell differentiation in the Arabidopsis root. EMBO J 37:e99134

    Google Scholar 

  • Feng Z, Deng Y, Fan H, Sun Q, Sui N, Wang B (2014) Effects of NaCl stress on the growth and photosynthetic characteristics of Ulmus pumila L. seedlings in sand culture. Photosynthetica 52:313–320

    CAS  Google Scholar 

  • Feng Z, Deng Y, Zhang S, Liang X, Yuan F, Hao J, Zhang J, Sun S, Wang B (2015) K+ accumulation in the cytoplasm and nucleus of the salt gland cells of Limonium bicolor accompanies increased rates of salt secretion under NaCl treatment using NanoSIMS. Plant Sci 238:286–296

    CAS  PubMed  Google Scholar 

  • Forst S, Kim DJ (2001) Genomic analysis of the histidine kinase family in bacteria and archaea. Microbiology 147:1197–1212

    PubMed  Google Scholar 

  • Gordon SP, Heisler MG, Reddy GV, Ohno C, Das P, Meyerowitz EM (2007) Pattern formation during de novo assembly of the Arabidopsis shoot meristem. Development 134:3539–3548

    CAS  PubMed  Google Scholar 

  • Guo Y, Jia W, Song J, Wang D, Chen M, Wang B (2012) Thellungilla halophilais more adaptive to salinity than Arabidopsis thaliana at stages of seed germination and seedling establishment. Acta Physiol Plant 34:1287–1294

    CAS  Google Scholar 

  • Guo J, Suo S, Wang B (2015) Sodium chloride improves seed vigour of the euhalophyte Suaeda salsa. Seed Sci Res 25:335–344

    CAS  Google Scholar 

  • Guo Y, Tian S, Liu S, Wang W, Sui N (2018) Energy dissipation and antioxidant enzyme system protect photosystem II of sweet sorghum under drought stress. Photosynthetica 56:861–872

    CAS  Google Scholar 

  • Hansen M, Chae HS, Kieber JJ (2009) Regulation of ACS protein stability by cytokinin and brassinosteroid. Plant J 57:606–614

    CAS  PubMed  Google Scholar 

  • Hare PD, Cress WA, Staden JV (1997) The involvement of cytokinins in plant responses to environmental stress. Plant Growth Regul 23:79–103

    CAS  Google Scholar 

  • Hu D, Ma Q, Sun C, Sun M, You C, Hao Y (2016) Overexpression of MdSOS2L1, a CIPK protein kinase, increases the antioxidant metabolites to enhance salt tolerance in apple and tomato. Physiol Plant 156:201–214

    CAS  PubMed  Google Scholar 

  • Huang X, Hou L, Meng J, You H, Li Z, Gong Z, Yang S, Shi Y (2018) The antagonistic action of abscisic acid and cytokinin signaling mediates drought stress response in Arabidopsis. Mol Plant 11:970–982

    CAS  PubMed  Google Scholar 

  • Hutchison CE, Li J, Argueso C, Gonzalez M, Lee E, Lewis MW, Maxwell BB, Perdue TD, Schaller GE, Alonso JM (2006) The Arabidopsis histidine phosphotransfer proteins are redundant positive regulators of cytokinin signaling. Plant Cell 18:3073–3087

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hwang I, Sheen J (2001) Two-component circuitry in Arabidopsis cytokinin signal transduction. Nature 413:383–389

    CAS  PubMed  Google Scholar 

  • Hwang I, Sheen J, Müller B (2012) Cytokinin signaling networks. Annu Rev Plant Biol 63:353–380

    CAS  PubMed  Google Scholar 

  • Hyoung SJ, Cho SH, Chung JH, So WM, Cui MH, Shin JS (2020) Cytokinin oxidase PpCKX1 plays regulatory roles in development and enhances dehydration and salt tolerance in Physcomitrella patens. Plant Cell Rep 39:419–430

    CAS  PubMed  Google Scholar 

  • Ioio RD, Linhares FS, Scacchi E, Casamitjanamartinez E, Heidstra R, Costantino P, Sabatini S (2007) Cytokinins determine arabidopsis root-meristem size by controlling cell differentiation. Curr Biol 17:678–682

    Google Scholar 

  • Ioio RD, Nakamura K, Moubayidin L, Perilli S, Taniguchi M, Morita MT, Aoyama T, Costantino P, Sabatini S (2008) A genetic framework for the control of cell division and differentiation in the root meristem. Science 322:1380–1384

    Google Scholar 

  • Jeon J, Kim J (2013) Arabidopsis response regulator1 and Arabidopsis histidine phosphotransfer protein2 (AHP2), AHP3, and AHP5 function in cold signaling. Plant Physiol 161:408–424

    CAS  PubMed  Google Scholar 

  • Jeon J, Kim NY, Kim S, Kang NY, Novák O, Ku S, Cho C, Lee DJ, Lee E, Strnad M (2010) A subset of cytokinin two-component signaling system plays a role in cold temperature stress response in Arabidopsis. J Biol Chem 285:23371–23386

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jeon J, Cho C, Lee MR, Van BN, Kim J (2016) CYTOKININ RESPONSE FACTOR2 (CRF2) and CRF3 regulate lateral root development in response to cold stress in Arabidopsis. Plant Cell 28:1828–1843

    CAS  PubMed  PubMed Central  Google Scholar 

  • Joshi R, Wani SH, Singh B, Bohra A, Dar ZA, Lone AA, Pareek A, Singla-Pareek SL (2016) Transcription factors and plants response to drought stress: current understanding and future directions. Front Plant Sci 7:1029

    PubMed  PubMed Central  Google Scholar 

  • Kakimoto T (2001) Identification of plant cytokinin biosynthetic enzymes as dimethylallyl diphosphate: ATP/ADP isopentenyltransferases. Plant Cell Physiol 42:677–685

    CAS  PubMed  Google Scholar 

  • Kang NY, Cho C, Kim NY, Kim J (2012) Cytokinin receptor-dependent and receptor-independent pathways in the dehydration response of Arabidopsis thaliana. J Plant Physiol 169:1382–1391

    CAS  PubMed  Google Scholar 

  • Kong F, Deng Y, Wang G, Wang J, Liang X, Meng Q (2014a) LeCDJ1, a chloroplast DnaJ protein, facilitates heat tolerance in transgenic tomatoes. J Integr Plant Biol 56:63–74

    CAS  PubMed  Google Scholar 

  • Kong F, Deng Y, Zhou B, Wang G, Wang Y, Meng Q (2014b) A chloroplast-targeted DnaJ protein contributes to maintenance of photosystem II under chilling stress. J Exp Bot 65:143–158

    CAS  PubMed  Google Scholar 

  • Krall L, Raschke M, Zenk MH, Baron C (2002) The Tzs protein from Agrobacterium tumefaciens C58 produces zeatin riboside 5'-phosphate from 4-hydroxy-3-methyl-2-(E)-butenyl diphosphate and AMP. FEBS Lett 527:315–318

    CAS  PubMed  Google Scholar 

  • Kurakawa T, Ueda N, Maekawa M, Kobayashi K, Kojima M, Nagato Y, Sakakibara H, Kyozuka J (2007) Direct control of shoot meristem activity by a cytokinin-activating enzyme. Nature 445:652–655

    CAS  PubMed  Google Scholar 

  • Kurepa J, Shull TE, Smalle JA (2019) Antagonistic activity of auxin and cytokinin in shoot and root organs. Plant Direct 3:1–9

    Google Scholar 

  • Lakehal A, Dob A, Rahneshan Z, Novák O, Escamez S, Alallaq S, Strnad M, Tuominen H, Bellini C (2020) ETHYLENE RESPONSE FACTOR 115 integrates jasmonate and cytokinin signaling machineries to repress adventitious rooting in Arabidopsis. New Phytol. https://doi.org/10.1111/nph.16794

    Article  PubMed  Google Scholar 

  • Letham DS (1963) Zeatin, a factor inducing cell division isolated from Zea mays. Life Sci 2:569–573

    CAS  Google Scholar 

  • Li X, Liu Y, Chen M, Song Y, Song J, Wang B, Feng G (2012) Relationships between ion and chlorophyll accumulation in seeds and adaptation to saline environments in Suaeda salsa populations. Plant Biosyst 146:142–149

    Google Scholar 

  • Li M, Guo S, Xu Y, Meng Q, Li G, Yang X (2014) Glycine betaine-mediated potentiation of HSP gene expression involves calcium signaling pathways in tobacco exposed to NaCl stress. Physiol Plant 150:63–75

    CAS  PubMed  Google Scholar 

  • Li M, Sui N, Lin L, Yang Z, Zhang Y (2019) Transcriptomic profiling revealed genes involved in response to cold stress in maize. Funct Plant Biol 46:830–844

    CAS  PubMed  Google Scholar 

  • Liu X, Huang B (2002) Cytokinin effects on creeping bentgrass response to heat stress: II. Leaf senescence and antioxidant metabolism. Crop Sci 42:466–472

    CAS  Google Scholar 

  • Liu S, Zhu D, Chen G, Gao X, Zhang X (2012) Disrupted actin dynamics trigger an increment in the reactive oxygen species levels in the Arabidopsis root under salt stress. Plant Cell Rep 31:1219–1226

    CAS  PubMed  Google Scholar 

  • Liu Y, Wang L, Xing X, Sun L, Pan J, Kong X, Zhang M, Li D (2013) ZmLEA3, a multifunctional group 3 LEA protein from maize (Zea mays L.), is involved in biotic and abiotic stresses. Plant Cell Physiol 54:944–959

    CAS  PubMed  Google Scholar 

  • Liu S, Wang W, Li M, Wan S, Sui N (2017) Antioxidants and unsaturated fatty acids are involved in salt tolerance in peanut. Acta Physiol Plant 39:207–216

    CAS  Google Scholar 

  • Liu H, Zhang H, Dong Y, Hao Y, Zhang X (2018) DNA METHYLTRANSFERASE1-mediated shoot regeneration is regulated by cytokinin-induced cell cycle in Arabidopsis. New Phytol 217:219–232

    CAS  PubMed  Google Scholar 

  • Lu C, Chen M, Liu R, Zhang L, Hou X, Liu S, Ding X, Jiang Y, Xu J, Zhang J, Zhao X, Liu Y (2019) Abscisic acid regulates auxin distribution to mediate maize lateral root development under salt stress. Front Plant Sci 10:716

    PubMed  PubMed Central  Google Scholar 

  • Ma N, Zuo Y, Liang X, Yin B, Wang G, Meng Q (2013) The multiple stress-responsive transcription factor SlNAC1 improves the chilling tolerance of tomato. Physiol Plant 149:474–486

    CAS  PubMed  Google Scholar 

  • Ma X, Chen C, Yang M, Dong X, Lv W, Meng Q (2018) Cold-regulated protein (SlCOR413IM1) confers chilling stress tolerance in tomato plants. Plant Physiol Biochem 124:29–39

    CAS  PubMed  Google Scholar 

  • Ma Q, Sun M, Kang H, Lu J, You C, Hao Y (2019) A CIPK protein kinase targets sucrose transporter MdSUT2.2 at Ser254 for phosphorylation to enhance salt tolerance. Plant Cell Environ 42:918–930

    CAS  PubMed  Google Scholar 

  • Mao C, He J, Liu L, Deng Q, Yao X, Liu C, Qiao Y, Li P, Ming F (2019) OsNAC2 integrates auxin and cytokinin pathways to modulate rice root development. Plant Biotechnol J 18:429–442

    PubMed  PubMed Central  Google Scholar 

  • Marhavý P, Bielach A, Abas L, Abuzeineh A, Duclercq J, Tanaka H, Pařezova M, Petrasek J, Friml J, Kleinevehn J (2011) Cytokinin modulates endocytic trafficking of PIN1 auxin efflux carrier to control plant organogenesis. Dev Cell 21:796–804

    PubMed  Google Scholar 

  • Marhavý P, Duclercq J, Weller B, Feraru E, Bielach A, Offringa R, Friml J, Schwechheimer C, Murphy AS, Benkova E (2014) Cytokinin controls polarity of PIN1-dependent auxin transport during lateral root organogenesis. Curr Biol 24:1031–1037

    PubMed  Google Scholar 

  • Mason MG, Jha D, Salt DE, Tester M, Hill K, Kieber JJ, Schaller GE (2010) Type-B response regulators ARR1 and ARR12 regulate expression of AtHKT1;1 and accumulation of sodium in Arabidopsis shoots. Plant J 64:753–763

    CAS  PubMed  Google Scholar 

  • Matsumoto-Kitano M, Kusumoto T, Tarkowski P, Kinoshita-Tsujimura K, Vaclavikova K, Miyawaki K, Kakimoto T (2008) Cytokinins are central regulators of cambial activity. Proc Natl Acad Sci USA 105:20027–20031

    CAS  PubMed  PubMed Central  Google Scholar 

  • Meng X, Yin B, Feng H, Zhang S, Liang X, Meng Q (2014) Overexpression of R2R3-MYB gene leads to accumulation of anthocyanin and enhanced resistance to chilling and oxidative stress. Biol Plant 58:121–130

    CAS  Google Scholar 

  • Meng W, Cheng Z, Sang Y, Zhang M, Rong X, Wang Z, Tang Y, Zhang X (2017) Type-B ARABIDOPSIS RESPONSE REGULATORs specify the shoot stem cell niche by dual regulation of WUSCHEL. Plant Cell 29:1357–1372

    CAS  PubMed  PubMed Central  Google Scholar 

  • Miller CO, Skoog F, Von Saltza MH, Strong FM (1955) Kinetin, a cell division factor from deoxyribonucleic Acid1. J Am Chem Soc 77:1392–1392

    CAS  Google Scholar 

  • Miyawaki K, Tarkowski P, Matsumoto-Kitano M, Kato T, Sato S, Tarkowska D, Tabata S, Sandberg G, Kakimoto T (2006) Roles of Arabidopsis ATP/ADP isopentenyltransferases and tRNA isopentenyltransferases in cytokinin biosynthesis. Proc Natl Acad Sci USA 103:16598–16603

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mok DW, Mok MC (2001) Cytokinin metabolism and action. Annu Rev Plant Biol 52:89–118

    CAS  Google Scholar 

  • Müller B, Sheen J (2007) Advances in cytokinin signaling. Science 318:68–69

    PubMed  Google Scholar 

  • Nguyen KH, Ha CV, Nishiyama R, Watanabe Y, Leyva-Gonzalez MA, Fujita Y, Tran UT, Li W, Tanaka M, Seki M, Schaller GE, Herrera-Estrella L, Tran LS (2016) Arabidopsis type B cytokinin response regulators ARR1, ARR10, and ARR12 negatively regulate plant responses to drought. Proc Natl Acad Sci USA 113:3090–3095

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nieminen K, Lmmanen J, Laxell M, Kauppinen L, Tarkowski P, Dolezal K, Taehtiharju S, Elo A, Decourteix M, Ljung K (2009) Cytokinin signaling regulates cambial development in poplar. Proc Natl Acad Sci USA. 105:20032–20037

    Google Scholar 

  • Nishiyama R, Watanabe Y, Fujita Y, Le DT, Kojima M, Werner T, Vankova R, Yamaguchi-Shinozaki K, Shinozaki K, Kakimoto T, Sakakibara H, Schmülling T, Tran L-SP (2011) Analysis of cytokinin mutants and regulation of cytokinin metabolic genes reveals important regulatory roles of cytokinins in drought, salt and abscisic acid responses, and abscisic acid biosynthesis. Plant Cell 23:2169–2183

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nishiyama R, Watanabe Y, Leyva-Gonzalez MA, Van Ha C, Fujita Y, Tanaka M, Seki M, Yamaguchi-Shinozaki K, Shinozaki K, Herrera-Estrella L, Tran LSP (2013) Arabidopsis AHP2, AHP3, and AHP5 histidine phosphotransfer proteins function as redundant negative regulators of drought stress response. Proc Natl Acad Sci USA 110:4840–4845

    CAS  PubMed  PubMed Central  Google Scholar 

  • O'Brien JA, Benková E (2013) Cytokinin Cross-talking during biotic and abiotic stress responses. Front Plant Sci 4:451

    PubMed  PubMed Central  Google Scholar 

  • Qin L, Li L, Bi C, Zhang Y, Wan S, Meng J, Meng Q, Li X (2011) Damaging mechanisms of chilling- and salt stress to Arachis hypogaea L. leaves. Photosynthetica 49:37–42

    CAS  Google Scholar 

  • Ren B, Liang Y, Deng Y, Chen Q, Zhang J, Yang X, Zuo J (2009) Genome-wide comparative analysis of type-A Arabidopsis response regulator genes by overexpression studies reveals their diverse roles and regulatory mechanisms in cytokinin signaling. Cell Res 19:1178–1190

    CAS  PubMed  Google Scholar 

  • Rong X, Sang Y, Wang L, Meng W, Zou C, Dong Y, Bie X, Cheng Z, Zhang X (2018) Type-B ARRs control carpel regeneration through mediating AGAMOUS expression in Arabidopsis. Plant Cell Physiol 59:761–769

    CAS  Google Scholar 

  • Sakai H, Honma T, Aoyama T, Sato S, Kato T, Tabata S, Oka A (2001) ARR1, a transcription factor for genes immediately responsive to cytokinins. Science 294:1519–1521

    CAS  PubMed  Google Scholar 

  • Sakamoto T, Sakakibara H, Kojima M, Yamamoto Y, Nagasaki H, Inukai Y, Sato Y, Matsuoka M (2006) Ectopic expression of KNOTTED1-like homeobox protein induces expression of cytokinin biosynthesis genes in rice. Plant Physiol 142:54–62

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sang Y, Cheng Z, Zhang X (2018) Plant stem cells and de novo organogenesis. New Phytol 218:1334–1339

    PubMed  Google Scholar 

  • Schaller GE, Bishopp A, Kieber JJ (2015) The Yin-Yang of hormones: cytokinin and auxin interactions in plant development. Plant Cell 27:44–63

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shi X, Ren J, Yu Q, Zhou S, Ren Q, Kong L, Wang X (2018) Overexpression of SDH confers tolerance to salt and osmotic stress, but decreases ABA sensitivity in Arabidopsis. Plant Biol 20:327–337

    CAS  PubMed  Google Scholar 

  • Skoog F, Armstrong DJ (1970) Cytokinins. Annu Rev Plant Physiol 21:359–384

    CAS  Google Scholar 

  • Skoog F, Miller CO (1957) Chemical regulation of growth and organ formation in plant tissues cultured in vitro. Symp Soc Exp Biol 11:118–130

    CAS  PubMed  Google Scholar 

  • Skoog F, Hamzi HQ, Szweykowska AM, Leonard NJ, Carraway KL, Fujii T, Helgeson JP, Loeppky RN (1967) Cytokinins: structure/activity relationships. Phytochemistry 6:1169–1192

    CAS  Google Scholar 

  • Song J, Wang B (2015) Using euhalophytes to understand salt tolerance and to develop saline agriculture: Suaeda salsa as a promising model. Ann Bot 115:541–553

    CAS  PubMed  Google Scholar 

  • Song J, Shi W, Liu R, Xu Y, Sui N, Zhou J, Feng G (2017) The role of the seed coat in adaptation of dimorphic seeds of the euhalophyte Suaeda salsa to salinity. Plant Spec Biol 32:107–114

    Google Scholar 

  • Song Y, Li J, Liu M, Meng Z, Liu K, Sui N (2019) Nitrogen increases drought tolerance in maize seedlings. Funct Plant Biol 46:350–359

    CAS  PubMed  Google Scholar 

  • Stock J (1999) Signal transduction: gyrating protein kinases. Curr Biol 9:R364–R367

    CAS  PubMed  Google Scholar 

  • Stock AM, Robinson VL, Goudreau PN (2000) Two-component signal transduction. Annu Rev Biochem 69:183–215

    CAS  PubMed  Google Scholar 

  • Su Y, Su Y, Liu Y, Zhang X (2013) Abscisic acid is required for somatic embryo initiation through mediating spatial auxin response in Arabidopsis. Plant Growth Regul 69:167–176

    CAS  Google Scholar 

  • Su Y, Liu Y, Bai B, Zhang X (2015) Establishment of embryonic shoot–root axis is involved in auxin and cytokinin response during Arabidopsis somatic embryogenesis. Front Plant Sci 5:792

    PubMed  PubMed Central  Google Scholar 

  • Sui N (2015) Photoinhibition of Suaeda salsa to chilling stress is related to energy dissipation and water–water cycle. Photosynthetica 53:207–212

    CAS  Google Scholar 

  • Sui N, Han G (2014) Salt-induced photoinhibition of PSII is alleviated in halophyte Thellungiella halophila by increases of unsaturated fatty acids in membrane lipids. Acta Physiol Plant 36:983–992

    CAS  Google Scholar 

  • Sui N, Tian S, Wang W, Wang M, Fan H (2017) Overexpression of glycerol-3-phosphate acyltransferase from Suaeda salsa improves salt tolerance in Arabidopsis. Front Plant Sci 8:1337

    PubMed  PubMed Central  Google Scholar 

  • Sun T (2010) Gibberellin-GID1-DELLA: a pivotal regulatory module for plant growth and development. Plant Physiol 154:567–570

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sun J, Niu Q, Tarkowski P, Zheng B, Tarkowska D, Sandberg G, Chua N, Zuo J (2003) The Arabidopsis AtIPT8/PGA22 gene encodes an isopentenyl transferase that is involved in de novo cytokinin biosynthesis. Plant Physiol 131:167–176

    CAS  PubMed  PubMed Central  Google Scholar 

  • Takei K, Sakakibara H, Sugiyama T (2001a) Identification of genes encoding adenylate isopentenyltransferase, a cytokinin biosynthesis enzyme, in Arabidopsis thaliana. J Biol Chem 276:26405–26410

    CAS  PubMed  Google Scholar 

  • Takei K, Sakakibara H, Taniguchi M, Sugiyama T (2001b) Nitrogen-dependent accumulation of cytokinins in root and the translocation to leaf: implication of cytokinin species that induces gene expression of maize response regulator. Plant Cell Physiol 42:85–93

    CAS  PubMed  Google Scholar 

  • Tang L, Zhou C, Wang S, Yuan J, Zhang X, Su Y (2017) FUSCA3 interacting with LEAFY COTYLEDON2 controls lateral root formation through regulating YUCCA4 gene expression in Arabidopsis thaliana. New Phytol 213:1740–1754

    CAS  PubMed  Google Scholar 

  • Tian F, Gong J, Zhang J, Zhang M, Wang G, Li A, Wang W (2013) Enhanced stability of thylakoid membrane proteins and antioxidant competence contribute to drought stress resistance in the tasg1 wheat stay-green mutant. J Exp Bot 64:1509–1520

    CAS  PubMed  PubMed Central  Google Scholar 

  • To JPC, Kieber JJ (2008) Cytokinin signaling: two-components and more. Trends Plant Sci 13:85–92

    CAS  PubMed  Google Scholar 

  • Wang F, Xu Y, Wang S, Shi W, Liu R, Feng G, Song J (2015a) Salinity affects production and salt tolerance of dimorphic seeds of Suaeda salsa. Plant Physiol Biochem 95:41–48

    CAS  PubMed  Google Scholar 

  • Wang G, Kong F, Zhang S, Meng X, Wang Y, Meng Q (2015b) A tomato chloroplast-targeted DnaJ protein protects Rubisco activity under heat stress. J Exp Bot 66:3027–3040

    CAS  PubMed  Google Scholar 

  • Wang G, Zhang S, Ma X, Wang Y, Kong F, Meng Q (2016a) A stress-associated NAC transcription factor (SlNAC35) from tomato plays a positive role in biotic and abiotic stresses. Physiol Plant 158:45–64

    CAS  PubMed  Google Scholar 

  • Wang Q, Sun H, Dong Q, Sun T, Jin Z, Hao Y, Yao Y (2016b) The enhancement of tolerance to salt and cold stresses by modifying the redox state and salicylic acid content via the cytosolic malate dehydrogenase gene in transgenic apple plants. Plant Biotechnol J 14:1986–1997

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang C, Lu W, He X, Wang F, Zhou Y, Guo X, Guo X (2016c) The cotton mitogen-activated protein kinase kinase 3 functions in drought tolerance by regulating stomatal responses and root growth. Plant Cell Physiol 57:1629–1642

    CAS  PubMed  Google Scholar 

  • Wang J, Tian C, Zhang C, Shi B, Cao X, Zhang T, Zhao Z, Wang J, Jiao Y (2017) Cytokinin signaling activates WUSCHEL expression during axillary meristem initiation. Plant Cell 29:1373–1387

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang W, Hao Q, Wang W, Li Q, Chen F, Ni WY, Fu D, Wu J, Wang W (2019) The involvement of cytokinin and nitrogen metabolism in delayed flag leaf senescence in a wheat stay-green mutant, tasg1. Plant Sci 278:70–79

    CAS  PubMed  Google Scholar 

  • Wei D, Zhang W, Wang C, Meng Q, Li G, Chen T, Yang X (2017) Genetic engineering of the biosynthesis of glycinebetaine leads to alleviate salt-induced potassium efflux and enhances salt tolerance in tomato plants. Plant Sci 257:74–83

    CAS  PubMed  Google Scholar 

  • Werner T, Schmülling T (2009) Cytokinin action in plant development. Curr Opin Plant Biol 12:527–538

    CAS  PubMed  Google Scholar 

  • Werner T, Motyka V, Strnad M, Schmülling T (2001) Regulation of plant growth by cytokinin. Proc Natl Acad Sci USA 98:10487–10492

    CAS  PubMed  PubMed Central  Google Scholar 

  • Werner T, Motyka V, Laucou V, Smets R, Onckelen HV, Schmülling T (2003) Cytokinin-Deficient transgenic Arabidopsis plants show multiple developmental alterations indicating opposite functions of cytokinins in the regulation of shoot and root meristem activity. Plant Cell 15:2532–2550

    CAS  PubMed  PubMed Central  Google Scholar 

  • Werner T, Nehnevajova E, Köllmer I, Novák O, Strnad M, Krämer U, Schmülling T (2010) Root-specific reduction of cytokinin causes enhanced root growth, drought tolerance, and leaf mineral enrichment in Arabidopsis and tobacco. Plant Cell 22:3905–3920

    PubMed  PubMed Central  Google Scholar 

  • Wu J, Jin Y, Liu C, Vonapartis E, Liang J, Wu W, Gazzarrini S, He J, Yi MF (2019) GhNAC83 inhibits corm dormancy release by regulating ABA signaling and cytokinin biosynthesis in Gladiolus hybridus. J Exp Bot 70:1221–1237

    CAS  PubMed  Google Scholar 

  • Xie M, Chen H, Huang L, O’Neil RC, Shokhirev MN, Ecker JR (2018) A B-ARR-mediated cytokinin transcriptional network directs hormone cross-regulation and shoot development. Nat Commun 9:1604

    PubMed  PubMed Central  Google Scholar 

  • Xu YG, Liu R, Sui N, Shi W, Wang L, Tian C, Song J (2016) Changes in endogenous hormones and seed-coat phenolics during seed storage of two Suaeda salsa populations. Aust J Bot 64:325–332

    CAS  Google Scholar 

  • Yan H, Jia H, Chen X, Hao L, An H, Guo X (2014) The cotton WRKY transcription factor GhWRKY17 Functions in Drought and salt stress in transgenic Nicotiana benthamiana through ABA signaling and the modulation of reactive oxygen species production. Plant Cell Physiol 55:2060–2076

    CAS  PubMed  Google Scholar 

  • Yang Z, Liu G, Liu J, Zhang B, Meng W, Müller B, Hayashi KI, Zhang X, Zhao Z, De Smet I (2017) Synergistic action of auxin and cytokinin mediates aluminum-induced root growth inhibition in Arabidopsis. EMBO Rep 18:1213–1230

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yuan F, Leng B, Wang B (2016) Progress in studying salt secretion from the salt glands in recretohalophytes: how do plants secrete salt? Front Plant Sci 7:977

    PubMed  PubMed Central  Google Scholar 

  • Zhang P, Wang W, Zhang G, Kaminek M, Dobrev P, Xu J, Gruissem W (2010) Senescence-inducible expression of isopentenyl transferase extends leaf life, increases drought stress resistance and alters cytokinin metabolism in Cassava. J Integr Plant Biol 52:653–669

    CAS  PubMed  Google Scholar 

  • Zhang L, Li Y, Lu W, Meng F, Wu C, Guo X (2012) Cotton GhMKK5 affects disease resistance, induces HR-like cell death, and reduces the tolerance to salt and drought stress in transgenic Nicotiana benthamiana. J Exp Bot 63:3935–3951

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang Q, Wang L, Kong F, Deng Y, Li B, Meng Q (2012) Constitutive accumulation of zeaxanthin in tomato alleviates salt stress-induced photoinhibition and photooxidation. Physiol Plant 146:363–373

    CAS  PubMed  Google Scholar 

  • Zhang D, Zhang M, Zhou Y, Wang Y, Liang J (2019) The rice G protein γ subunit DEP1/qPE9-1 positively regulates grain-filling process by increasing auxin and cytokinin content in rice grains. Rice 12:91

    PubMed  PubMed Central  Google Scholar 

  • Zhao Y, Cheng S, Song Y, Huang Y, Zhou S, Liu X, Zhou D (2015) The interaction between rice ERF3 and WOX11 promotes crown root development by regulating gene expression involved in cytokinin signaling. Plant Cell 27:2469–2483

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou J, Fu T, Sui N, Guo J, Feng G, Fan J, Song J (2016) The role of salinity in seed maturation of the euhalophyte Suaeda salsa. Plant Biosyst 150:83–90

    Google Scholar 

  • Zhou MX, Ghnaya T, Dailly H, Cui GL, Vanpee B, Han RM, Lutts S (2019) The cytokinin trans-zeatine riboside increased resistance to heavy metals in the halophyte plant species Kosteletzkya pentacarpos in the absence but not in the presence of NaCl. Chemosphere 233:954–965

    CAS  PubMed  Google Scholar 

  • Zhu J, Zhang K, Wang W, Gong W, Liu W, Chen H, Xu H, Lu Y (2015) Low temperature inhibits root growth by reducing auxin accumulation via ARR1/12. Plant Cell Physiol 56:727–736

    CAS  PubMed  Google Scholar 

  • Zhuang K, Kong F, Zhang S, Meng C, Yang M, Liu Z, Wang Y, Ma N, Meng Q (2019) Whirly1 enhances tolerance to chilling stress in tomato via protection of photosystem II and regulation of starch degradation. New Phytol 221:1998–2012

    CAS  PubMed  Google Scholar 

  • Zhuang K, Gao Y, Liu Z, Diao P, Sui N, Meng Q, Meng C, Kong F (2020) WHIRLY1 regulates HSP21.5A expression to promote thermotolerance in tomato. Plant Cell Physiol 61:169–177

    CAS  PubMed  Google Scholar 

  • Zou X, Shao J, Wang Q, Chen P, Zhu Y, Yin C (2018) Supraoptimal cytokinin content inhibits rice seminal root growth by reducing root meristem size and cell length via increased ethylene content. Int J Mol Sci 19:4051

    PubMed Central  Google Scholar 

  • Zubo YO, Blakley IC, Yamburenko MV, Worthen JM, Street IH, Franco-Zorrilla JM, Zhang WJ, Hill K, Raines T, Solano R, Kieber JJ, Loraine AE, Schaller GE (2017) Cytokinin induces genome-wide binding of the type-B response regulator ARR10 to regulate growth and development in Arabidopsis. Proc Natl Acad Sci USA 114:E5995–E6004

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We are grateful for financial support from the National Natural Science Research Foundation of China (U1906204, 31871538), the National Key R&D Program of China (2018YFD1000700, 2018YFD1000704), Shandong Province Key Research and Development Program (2019GSF107079), the Development Plan for Youth Innovation Team of Shandong Provincial (2019KJE012), the Science and Technology Demonstration Project of "Bohai Granary" of Shandong Province (2019BHLC002).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Na Sui.

Ethics declarations

Conflict of interest

The authors declare that they have no competing interests.

Additional information

Communicated by Neal Stewart.

Publisher's Note

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Li, SM., Zheng, HX., Zhang, XS. et al. Cytokinins as central regulators during plant growth and stress response. Plant Cell Rep 40, 271–282 (2021). https://doi.org/10.1007/s00299-020-02612-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-020-02612-1

Keywords

Navigation