Cytokinin Signaling in Plants Under Salt Stress

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Auxins, Cytokinins and Gibberellins Signaling in Plants

Part of the book series: Signaling and Communication in Plants ((SIGCOMM))

Abstract

Salt stress negatively affects plant growth by impairing biochemical and physiological processes. Appropriate modulation of cytokinin (CK) metabolism and signaling can improve salt tolerance in plants. Protection of the photosynthetic apparatus, promotion of antioxidant systems, improvement of plant growth and differentiation, and crosstalk with stress-related phytohormones are important mechanisms that may contribute to cytokinin-mediated enhancement of salt tolerance. CKs mainly trigger plant environmental stress responses through the regulation of gene expression. A two-component system is employed to transduce the cytokinin signal to the target genes. CKs are perceived by membrane-localized histidine kinase receptors. The signal is transduced through a His-Asp phosphorelay (Histidine-aspartate phosphorelays) to activate a family of transcription factors in the nucleus. CKs cause organ specific responses in plants. This hormone is a negative regulator of root growth. Root-specific overexpression of CKX (cytokinin oxidase/dehydrogenase) gene can enhance root growth, nutrient uptake and salt tolerance. In contrast, increasing cytokinin level (by overexpression of IPT genes) promotes shoot growth of salt stressed plants, by inducing the expression of genes that are involved in photosynthesis, chlorophyll levels, photochemical quenching, photochemical efficiency, electron transport rates and CO2 assimilation. This chapter focuses on the cytokinin metabolism, transport and signaling, and discusses the role of this phytohormone in regulating changes in gene expression and physiological processes to mediate salt tolerance in plants.

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References

  • Abdel Latef AAH, Akter A, Tahjib-Ul-Arif M (2021) Foliar application of auxin or cytokinin can confer salinity stress tolerance in (Vicia faba L.). Agronomy 11, 790

    Google Scholar 

  • Ahanger MA, Alyemeni MN, Wijaya L, Alamri SA, Alam P, Ashraf M et al (2018) Potential of exogenously sourced kinetin in protecting Solanum lycopersicum from NaCl-induced oxidative stress through up-regulation of the antioxidant system, ascorbate-glutathione cycle and glyoxalase system. PLoS ONE 13(9):e0202175

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ahanger MA, Tomar NS, Tittal M, Argal S, Agarwal RM (2017) Plant growth under water/salt stress: ROS production; antioxidants and significance of added potassium under such conditions. Physiol Mol Biol Plants 23:731–744

    Article  PubMed  PubMed Central  Google Scholar 

  • Aldesuquy HS, Mickky BM (2014) Interactive effects of kinetin and spermine on anatomical adaptations and productivity to seawater salinity in wheat. Int J Bioassays 3(11):3499–3508

    Google Scholar 

  • Aloni R (1993) The role of cytokinin in organized differentiation of vascular tissues. Funct Plant Biol 20:601–608

    Article  CAS  Google Scholar 

  • Aremu AO, Masondo NA, Sunmonu TO, Kulkarni MG, Zatloukal M, Spichal L (2014) A novel inhibitor of cytokinin degradation (INCYDE) influences the biochemical parameters and photosynthetic apparatus in NaCl-stressed tomato plants. Planta 240:877–889

    Article  CAS  PubMed  Google Scholar 

  • Arghavani M, Kafi M, Babalar M, Naderi R, Hoque MA, Murata Y (2012) Improvement of salt tolerance in kentucky bluegrass by trinexapac-ethyl. HortScience 47:1163–1170

    Article  Google Scholar 

  • Avalbaev A, Allagulova C, Maslennikova D, Fedorova K, Shakirova F (2020) Methyl jasmonate and cytokinin mitigate the salinity-induced oxidative injury in wheat seedlings. J Plant Growth Regul 40(4):1741–1752

    Article  CAS  Google Scholar 

  • Avalbaev A, Yuldashev RA, Fedorova KA, Somov K, Vysotskaya LB, Allagulova C et al (2016) Exogenous methyl jasmonate regulates cytokinin content by modulating cytokinin oxidase activity in wheat seedlings under salinity. J Plant Physiol 191:101–110

    Article  CAS  PubMed  Google Scholar 

  • Beveridge CA, Murfet IC, Kerhoas L, Sotta B, Miginiac E, Rameau C (1997) The shoot controls zeatin riboside export from pea roots. Evidence from the branching mutant rms4. Plant J 11:339–345

    Article  CAS  Google Scholar 

  • Bhagyawant SS, Narvekar DT, Gupta N, Bhadkaria A, Koul KK, Srivastava N (2019) Variations in the antioxidant and free radical scavenging under induced heavy metal stress expressed as proline content in chickpea. Physiol Mol Biol Plants 25:683–696

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bhattacharya A, Sood P, Citovsky V (2010) The roles of plant phenolics in defense and communication during Agrobacterium and Rhizobium infection. Mol Plant Pathol 11:705–719

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bielach A, Hrtyan M, Tognetti VB (2017) Plants under stress: involvement of auxin and cytokinin. Int J Mol Sci 18:1427

    Article  PubMed Central  CAS  Google Scholar 

  • Bishopp A, Help H, El- S, Weijers D, Scheres B, Friml J et al (2011) A mutually inhibitory interaction between auxin and cytokinin specifies vascular pattern in roots. Curr Biol 21:917–926

    Google Scholar 

  • Blum A (2010) Drought resistance and its improvement. In: Blum A (eds) Plant breeding for water-limited environments. Springer, New York, USA, pp 53–152

    Google Scholar 

  • Campbell L, Turner S (2017) Regulation of vascular cell division. J Exp Bot 68(1):27–43

    Article  CAS  PubMed  Google Scholar 

  • Chen JJ, Wang LY, Immanen J, Nieminen K, Spicer R, Helariutta Y et al (2019) New Phytol 224:188–201

    Article  CAS  PubMed  Google Scholar 

  • Chen M, Zhao Y, Zhuo C, Lu S, Guo Z (2015) Overexpression of a NFYC transcription factor from bermudagrass confers tolerance to drought and salinity in transgenic rice. Plant Biotechnol J 13:482–491

    Google Scholar 

  • Chernyad’ev (2009) The protective action of cytokinins on the photosynthetic machinery and productivity of plants under stress. Appl Biochem Microbiol 45(4):351–362

    Google Scholar 

  • Corbesier L, Prinsen E, Jacqmard A, Lejeune P, Van Onckelen H, Perilleux C et al (2003) Cytokinin levels in leaves, leaf exudate and shoot apical meristem of Arabidopsis thaliana during floral transition. J Exp Bot 54:2511–2517

    Google Scholar 

  • Cortleven A, Valcke R (2012) Evaluation of the photosynthetic activity in transgenic tobacco plants with altered endogenous cytokinin content: lessons from cytokinin. Physiol Plant 144:394–408

    Article  CAS  PubMed  Google Scholar 

  • Cortleven A, Nitschke S, Klaumunzer M, AbdElgawad H, Asard H, Grimm B et al (2014) A novel protective function for cytokinin in the light stress response is mediated by the ARABIDOPSIS HISTIDINE KINASE2 and ARABIDOPSIS HISTIDINE KINASE3 receptors. Plant Physiol 164:1470–1483

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cortleven A, Noben JP, Valcke R (2011) Analysis of the photosynthetic apparatus in transgenic tobacco plants with altered endogenous cytokinin content: a proteomic study. Proteome Sci 9:1

    Article  CAS  Google Scholar 

  • Cui F, Sui N, Duan G, Liu Y, Han Y, Liu S et al (2018) Identification of metabolites and transcripts involved in salt stress and recovery in peanut. Front Plant Sci 9:217

    Article  PubMed  PubMed Central  Google Scholar 

  • Díaz-Mendoza M, Velasco-Arroyo B, González P, Martínez M, Díaz I (2014) C1A cysteine protease–cystatin interactions in leaf senescence. J Exp Bot 65:3825–3833

    Google Scholar 

  • Escalante-Pérez M, Lautner S, Nehls U, Selle A, Teuber M, Schnitzler JP et al (2009) Salt stress affects xylem differentiation of grey poplar (Populus x canescens). Planta 229:299–309

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Foyer CH, Noctor G (2000) Oxygen processing in photosynthesis: regulation and signalling. New Phytol 146:359–388

    Article  CAS  Google Scholar 

  • GajdoÅ¡ová S, Spıchal L, Kamınek M, Hoyerova K, Novák O, Dobrev PI et al (2011) Distribution, biological activities, metabolism, and the conceivable function of cis-zeatin-type cytokinins in plants. J Exp Bot 62:2827–2840

    Article  PubMed  CAS  Google Scholar 

  • Galuszka P, Popelkova H, Werner T, Frebortova J, Pospisilova H, Mik V et al (2007) Biochemical characterization of cytokinin oxidases/dehydrogenases from Arabidopsis thaliana expressed in Nicotiana tabacum L. J Plant Growth Regul 26:255–267

    Article  CAS  Google Scholar 

  • Gao S, Fang J, Xu F, Wang W, Sun X, Chu J et al (2014) A cytokinin oxidase/dehydrogenase gene OsCKX4 integrates cytokinin and auxin signaling to control rice crown root formation. Plant Physiol 165:1035–1046

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ghanem ME, Albacete A, Martinezandujar C, Acosta M, Romeroaranda MR, Dodd IC et al (2008) Hormonal changes during salinity-induced leaf senescence in tomato (Solanum lycopersicum L.). J Exp Bot 59:3039–3050

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ghanem ME, Albacete A, Smigocki AC, Frebort I, Pospısilova H, Martınez C et al (2011) Root-synthesized cytokinins improve shoot growth and fruit yield in salinized tomato (Solanum lycopersicum L.). J Exp Bot 62:125–140

    Google Scholar 

  • Ghassemi-Golezani K, Samea-Andabjadid S (2022) Exogenous cytokinin and salicylic acid improve amino acid content and composition of faba bean seeds under salt stress. Gesunde Pflanzen. https://doi.org/10.1007/s10343-022-00673-8

  • Gomez-Cadenas A, Vives V, Zandalinas SI, Manzi M, SanchezPerez AM, Perez- et al (2015) Abscisic acid: a versatile phytohormone in plant signaling and beyond. Curr Protein Pept Sci 16:413–434

    Google Scholar 

  • Guan C, Huang YH, Cui X, Liu SJ, Zhou YZ, Zhang YW (2018) Overexpression of gene encoding the key enzyme involved in proline biosynthesis (PuP5CS) to improve salt tolerance in switchgrass (Panicum virgatum L.). Plant Cell Rep 37:1187–1199

    Article  CAS  PubMed  Google Scholar 

  • Guan C, Wang X, Feng J, Hong S, Liang Y, Ren B et al (2014) Cytokinin antagonizes abscisic acid-mediated inhibition of cotyledon greening by promoting the degradation of abscisic acid insensitive 5 protein in Arabidopsis. Plant Physiol 164:1515–1526

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gupta BK, Sahoo KK, Ghosh A, Tripathi AK, Anwar K, Das P et al (2017) Manipulation of glyoxalase pathway confers tolerance to multiple stresses in rice. Plant, Cell Environ 41:1186–1200

    Article  CAS  Google Scholar 

  • Hajiboland R, Radpour E, Pasbani B (2014) Effect of phosphorus deficiency on drought stress tolerance in two tomato (Solanum lycopersum L.) cultivars. Iran J Biol 27:788–803

    Google Scholar 

  • Hanin M, Brini F, Ebel C, Toda Y, Takeda S, Masmoudi K (2011) Plant dehydrins and stress tolerance: versatile proteins for complex mechanisms. Plant Signal Behav 6:1503–1509

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Harinasut P, Srisunak S, Pitukchaisopol S, Charoensataporn R (2000) Mechanisms of adaptation to increasing salinity of mulberry: Proline content and ascorbate peroxidase activity in leaves of multiple shoots. Sci Asia 26:207–211

    Article  CAS  Google Scholar 

  • Heyl A, Ramireddy E, Brenner WG, Riefler M, Allemeersch J, Schmülling T (2008) The transcriptional silencer ARR1-SRDX suppresses pleiotropic cytokinin activities in Arabidopsis. Plant Physiol 147:1380–1395

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hirose N, Takei K, Kuroha T, Kamada T, Hayashi H, Sakakibara H (2008) Regulation of cytokinin biosynthesis, compartmentalization and translocation. J Exp Bot 59:75–83

    Google Scholar 

  • Hu CA, Delauney AJ, Verma DP (1992) A bifunctional enzyme (delta 1-pyrroline-5-carboxylate synthetase) catalyzes the first two steps in proline biosynthesis in plants. Proc Natl Acad Sci USA 89:9354–9358

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang H, Liu B, Liu L, Song S (2017a) Jasmonate action in plant growth and development. J Exp Bot 68:1349–1359

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Huang Y, Sun MM, Ye Q, Wu XQ, Wu WH, Chen YF (2017b) Abscisic acid modulates seed germination via ABA INSENSITIVE5-Mediated PHOSPHATE1. Plant Physiol 175:1661–1668

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Iqbal N, Umar S, Khan NA (2015) Nitrogen availability regulates proline and ethylene production and alleviates salinity stress in mustard (Brassica juncea). J Plant Physiol 178:84–91

    Article  CAS  PubMed  Google Scholar 

  • Jang G, Choi YD (2018) Drought stress promotes xylem differentiation by modulating the interaction between cytokinin and jasmonic acid. Plant Signal Behav 13(3):e1451707

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jang G, Chang SH, Um TY, Lee S, Kim JK, Choi Y (2017) Antagonistic interaction between jasmonic acid and cytokinin in xylem development. Sci Rep 7:10212

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jang G, Yoon Y, Choi YD (2020) Crosstalk with jasmonic acid integrates multiple responses in plant development. Int J Mol Sci 21:305

    Article  CAS  PubMed Central  Google Scholar 

  • Janz D, Lautner S, Wildhagen H, Behnke K, Schnitzler JP, Rennenberg H et al (2012) Salt stress induces the formation of a novel type of ‘pressure wood’ in two Populus species. New Phytol 194:129–141

    Article  CAS  PubMed  Google Scholar 

  • Joshi R, Sahoo KK, Tripathi AK, Kumar R, Gupta BK, Pareek A et al (2018) Knockdown of an inflorescence meristem-specific cytokinin oxidase—OsCKX2 in rice reduces yield penalty under salinity stress condition. Plant, Cell Environ 41:936–946

    Article  CAS  Google Scholar 

  • Junghans U, Polle A, Düchting P, Weiler E, Kuhlman B, Gruber F et al (2006) Adaptation to high salinity in poplar involves changes in xylem anatomy and auxin physiology. Plant, Cell Environ 29:1519–1531

    Article  CAS  Google Scholar 

  • Kang J, Li J, Gao S, Tian C, Zha X (2017) Overexpression of the leucine rich receptor-like kinase gene LRK2 increases drought tolerance and tiller number in rice. Plant Biotechnol J 15:1175–1185

    Article  CAS  PubMed  PubMed Central  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

    Article  CAS  PubMed  Google Scholar 

  • Kiba T, Aoki K, Sakakibara H, Mizuno T (2004) Arabidopsis response regulator, ARR22, ectopic expression of which results in phenotypes similar to the wol cytokinin-receptor mutant. Plant Cell Physiol 45:1063–1077

    Article  CAS  PubMed  Google Scholar 

  • Kiba T, Yamada H, Sato S, Kato T, Tabata S, Yamashino T et al (2003) The type-A response regulator, ARR15, acts as a negative regulator in the cytokinin-mediated signal transduction in Arabidopsis thaliana. Plant Cell Physiol 44:868–874

    Google Scholar 

  • Kieber JJ, Schaller GE (2014) Cytokinins. In: The arabidopsis book. American Society of Plant Biologists, p 12

    Google Scholar 

  • Kieber JJ, Schaller GE (2018) Cytokinin signaling in plant development. Development 145

    Google Scholar 

  • Klein A, Keyster M, Ludidi N (2015) Response of soybean nodules to exogenously applied caffeic acid during NaCl-induced salinity. S Afr J Bot 96:13–18

    Article  CAS  Google Scholar 

  • Ko D, Kang J, Kiba T, Park J, Kojima M, Do J et al (2014) Arabidopsis ABCG14 is essential for the root-to-shoot translocation of cytokinin. Proc Natl Acad Sci USA 111:7150–7155

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kobayashi K, Baba S, Obayashi T, Sato M, Toyooka K, Keränen M et al (2012) Regulation of root greening by light and auxin/cytokinin signaling in Arabidopsis. Plant Cell 24:1081–1095

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kollmer I, Novak O, Strnad M, Schmulling T, Werner T (2014) Overexpression of the cytosolic cytokinin oxidase/dehydrogenase (CKX7) from Arabidopsis causes specific changes in root growth and xylem differentiation. Plant J 78:359–371

    Article  PubMed  CAS  Google Scholar 

  • Krupinska K, Mulisch M, Hollmann J, Tokarz K, Zschiesche W, Kage H et al (2012) An alternative strategy of dismantling of the chloroplasts during leaf senescence observed in a high-yield variety of barley. Physiol Plant 144:189–200

    Article  CAS  PubMed  Google Scholar 

  • Kumar M, Lee SC, Kim JY, Kim SJ, Aye SS, Kim SR (2014) Over-expression of dehydrin gene, OsDhn1, improves drought and salt stress tolerance through scavenging of reactive oxygen species in rice (Oryza sativa L.). J Plant Biol 57:383–393

    Article  CAS  Google Scholar 

  • Kumari S, Kumar S, Prakash P (2018) Exogenous application of cytokinin (6-BAP) ameliorates the adverse effect of combined drought and high temperature stress in wheat seedling. J Pharmaco Phytochem 7:1176–1180

    CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Kuroha T, Tokunaga H, Kojima M, Ueda N, Ishida T, Nagawa S et al (2009) Functional analyses of LONELY GUY cytokinin-activating enzymes reveal the importance of the direct activation pathway in Arabidopsis. Plant Cell 21:3152–3169

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lautner S (2013) Wood formation under drought stress and salinity. In: Fromm J (ed.) Cellular aspects of wood formation, vol 20, pp 187–202. Springer, Berlin, Germany

    Google Scholar 

  • Leta TB, Miccah SS, Steven MR, Wondyifraw T, Francis W (2016) Drought tolerant tropical maize (Zea mays L.) developed through genetic transformation with isopentenyltransferase gene. Afr J Biotech 15:2447–2464

    Article  Google Scholar 

  • Li S, An Y, Hailati S, Zhang J, Cao Y, Liu Y et al (2019) Overexpression of the cytokinin oxidase/dehydrogenase (CKX) from Medicago sativa enhanced salt stress tolerance of Arabidopsis. J Plant Biol 62:374–386

    Article  CAS  Google Scholar 

  • Li Y, Liu F, Li P, Wang T, Zheng C, Hou B (2020) An Arabidopsis cytokinin-modifying glycosyltransferase UGT76C2 improves drought and salt tolerance in rice. Front Plant Sci 11:560696

    Article  PubMed  PubMed Central  Google Scholar 

  • Liang W, Ma X, Wan P, Liu L (2017) Plant salt-tolerance mechanism: a review. Biochem Biophys Res Commun 495:286–291

    Article  PubMed  CAS  Google Scholar 

  • Liao X, Guo X, Wang Q, Wang Y, Zhao D, Yao L et al (2017) Overexpression of MsDREB6.2 results in cytokinin-deficient developmental phenotypes and enhances drought tolerance in transgenic apple plants. Plant J 89:510–526

    Google Scholar 

  • Liu CJ, Zhao Y, Zhang K (2019) Cytokinin transporters: multisite players in cytokinin homeostasis and signal distribution. Front Plant Sci 10:693

    Google Scholar 

  • Liu L, Li H, Zeng H, Cai Q, Zhou X, Yin C (2016) Exogenous jasmonic acid and cytokinin antagonistically regulate rice flag leaf senescence by mediating chlorophyll degradation, membrane deterioration, and senescence-associated genes expression. J Plant Growth Regul 35:366–376

    Google Scholar 

  • Liu Y, Zhang M, Meng Z, Wang B, Chen M (2020) Research progress on the roles of cytokinin in plant response to stress. Int J Mol Sci 21:6574

    Google Scholar 

  • Ma Q, Yue LJ, Zhang JL, Wu GQ, Bao AK, Wang SM (2012) Sodium chloride improves photosynthesis and water status in the succulent xerophyte Zygophyllum xanthoxylum. Tree Physiol 32:4–13

    Google Scholar 

  • Macková H, Hronková M, Dobrá J, Turecková V, Novák O, Lubovská Z et al (2013) Enhanced drought and heat stress tolerance of tobacco plants with ectopically enhanced cytokinin oxidase/dehydrogenase gene expression. J Exp Bot 64:2805–2815

    Google Scholar 

  • Mähönen AP, Bishopp A, Higuchi M, Nieminen KM, Kinoshita K, Törmäkangas K et al (2006) Cytokinin signaling and its inhibitor AHP6 regulate cell fate during vascular development. Science 311:94–98

    Google Scholar 

  • Mason MG, Jha D, Salt DE, Tester M, Hill K, Kieber JJ et al (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

    Google Scholar 

  • Merewitz EB, Gianfagna T, Huang B (2011) Protein accumulation in leaves and roots associated with improved drought tolerance in cree** bentgrass expressing an ipt gene for cytokinin synthesis. J Exp Bot 62:5311–5333

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mhamdi A, Queval G, Chaouch S, Vanderauwera S, Van Breusegem F, Noctor G (2010) Catalase function in plants: a focus on Arabidopsis mutants as stress-mimic models. J Exp Bot 61:4197–4220

    Article  CAS  PubMed  Google Scholar 

  • Mrızova K, Jiskrova E, Vyroubalova S, Novak O, Ohnoutkova L, Pospısilova H et al (2013) Overexpression of cytokinin dehydrogenase genes in barley (Hordeum vulgare cv. Golden Promise) fundamentally affects morphology and fertility. PLoS One 8, e79029

    Google Scholar 

  • Mukherjee I, Reid D, Naik G (2002) Influence of cytokinins on the methyl jasmonate-promoted senescence in Helianthus annuus cotyledons. Plant Growth Regul 38:61–68

    Google Scholar 

  • Mundree SG, Baker B, Sh, Mowla, Sh, Peters, Marais S, Willigen CV et al (2002) Physiological and molecular insights into drought tolerance. Afr J Biotech 1:28–38

    Google Scholar 

  • Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681

    Google Scholar 

  • Nieminen K, Immanen J, Laxell M, Kauppinen L, Tarkowski P, Dolezal K et al (2008) Cytokinin signaling regulates cambial development in poplar. Proc Natl Acad Sci USA 105:20032–20037

    Google Scholar 

  • Nishiyama R, Le DT, Watanabe Y, Matsui A, Tanaka M, Seki M et al (2012) Transcriptome analyses of a salt-tolerant cytokinin-deficient mutant reveal differential regulation of salt stress response by cytokinin deficiency. PLoS ONE 7:e32124

    Google Scholar 

  • Nishiyama R, Watanabe Y, Fujita Y, Le DT, Kojima M, Werner T et al (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

    Google Scholar 

  • Nishiyama R, Watanabe Y, Leyva-Gonzalez MA, Ha CV, Fujita Y, Tanaka M et al (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

    Google Scholar 

  • Noctor G, Veljovic-Jovanovic S, Driscoll S, Novitskaya L, Foyer CH (2002) Drought and oxidative load in the leaves of C-3 plants: a predominant role for photorespiration? Annals Botany (London) 89:841–850

    Google Scholar 

  • Osugi A, Sakakibara H (2015) Q&A: how do plants respond to cytokinins and what is their importance? BMC Biol 13:102

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Osugi A, Kojima M, Takebayashi Y, Ueda N, Kiba T, Sakakibara H (2017) Systemic transport of trans-zeatin and its precursor have differing roles in Arabidopsis shoots. Nat Plants 3:17112

    Article  CAS  PubMed  Google Scholar 

  • Oteiza PI, Erlejman AG, Verstraeten SV, Keen CL, Fraga CG (2005) Flavonoid membrane Interactions: a protective role of flavonoids at the membrane surface? Clin Dev Immunol 12:19–25

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pavlu J, Novak J, Koukalová V, Luklova M, Brzobohatý B, Cerný M (2018) Cytokinin at the crossroads of abiotic stress signaling pathways. Int J Mol Sci 19:2450

    Article  PubMed Central  CAS  Google Scholar 

  • Pospisilova H, Jiskrova E, Vojta P, Mrizova K, Kokas F, Cudejkova MM et al (2016) Transgenic barley overexpressing a cytokinin dehydrogenase gene shows greater tolerance to drought stress. New Biotechnol 33:692–705

    Article  CAS  Google Scholar 

  • Pospisilova J, Vagner M, Malbeck J, Travniakova A, Batkova P (2005) Interactions between abscisic acid and cytokinins during water stress and subsequent rehydration. Biol Plant 49:533–540

    Article  CAS  Google Scholar 

  • Qin H, He L, Huang R (2019) The coordination of ethylene and other hormones in primary root development. Front Plant Sci 10:874

    Article  PubMed  PubMed Central  Google Scholar 

  • Rahman MM, Mostofa MG, Rahman MA, Islam MR, Keya SS, Das AK et al (2019) Acetic acid: a cost-effective agent for mitigation of seawater-induced salt toxicity in Mung Bean. Sci Rep 9:15186

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rai MI, Wang X, Thibault DM, Kim HJ, Bombyk MM, Binder BM et al (2015) The ARGOS gene family functions in a negative feedback loop to desensitize plants to ethylene. BMC Plant Biol 15:157

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ramireddy E, Hosseini SA, Eggert K, Gillandt S, Gnad H, von Wirén N et al (2018) Root Engineering in Barley: increasing cytokinin degradation produces a larger root system, mineral enrichment in the shoot and improved drought tolerance. Plant Physiol 177:1078–1095

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reguera M, Peleg Z, Abdel-Tawab YM, Tumimbang E, Delatorre CA, Blumwald E (2013) Stress-induced CK synthesis increases drought tolerance through the coordinated regulation of carbon and nitrogen assimilation in rice. Plant Physiol 163:1609–1622

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rivero RM, Gimeno J, Van Deynze A, Walia H, Blumwald E (2010) Enhanced cytokinin synthesis in tobacco plants expressing p(SARK)::IPT prevents the degradation of photosynthetic protein complexes during drought. Plant Cell Physiol 51:1929–1941

    Article  CAS  PubMed  Google Scholar 

  • Rivero RM, Shulaev V, Blumwald E (2009) Cytokinin-dependent photorespiration and the protection of photosynthesis during water deficit. Plant Physiol 150:1530–1540

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Riyazuddin R, Verma R, Singh K, Nisha N, Keisham M, Bhati KK et al (2020) Ethylene: a master regulator of salinity stress tolerance in plants. Biomolecules 10:959

    Article  CAS  PubMed Central  Google Scholar 

  • Sakakibara H (2006) Cytokinins: activity, biosynthesis, and translocation. Annu Rev Plant Biol 57:431–449

    Article  CAS  PubMed  Google Scholar 

  • Samea S, Ghassemi-Golezani K, Nasrollahzadeh S, Najafi N (2018) Exogenous salicylic acid and cytokinin alter sugar accumulation, antioxidants and membrane stability of faba bean. Acta Biol Hung 69:86–96

    Google Scholar 

  • Sasaki T, Suzaki T, Soyano T, Kojima M, Sakakibara H, Kawaguchi M (2014) Shoot-derived cytokinins systemically regulate root nodulation. Nat Commun 5:4983

    Article  CAS  PubMed  Google Scholar 

  • Schmulling T, Werner T, Riefler M, Krupkova E, Bartrina (2003) Structure and function of cytokinin oxidase/dehydrogenase genes of maize, rice, Arabidopsis and other species. J Plant Res 116:241–252

    Google Scholar 

  • Sebastian J, Ryu KH, Zhou J, Tarkowská D, Tarkowski P, Cho YH et al (2015) PHABULOSA controls the quiescent center-independent root meristem activities in Arabidopsis thaliana. PLoS Genet 11:e1004973

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sharma A, Shahzad B, Kumar V, Kohli SK, Sidhu GPS, Bali AS et al (2019) Phytohormones regulate accumulation of osmolytes under abiotic stress. Biomolecules 9:285

    Article  CAS  PubMed Central  Google Scholar 

  • Shi H, Ishitani M, Kim C, Zhu JK (2000) The Arabidopsis thaliana salt tolerance gene SOS1 encodes a putative Na+/H+ antiporter. Proc Natl Acad Sci USA 97:6896–6901

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sidari M, Santonoceto C, Anastasi U, Preiti G, Muscolo A (2008) Variations in four genotypes of lentil under NaCl-salinity stress. Am J Agric Biol Sci 3:410–416

    Article  Google Scholar 

  • Siddiqui MW, Singh JP, Nayyer MA, Barman K, Ahmad MS, Kumar V (2015) 6-Benzylaminopurine affects lipid peroxidation and membrane permeability and thereby preserves curd quality and antioxidants during storage of cauliflower. Acta Physiol Plant 37:96

    Article  CAS  Google Scholar 

  • Song J, Zhou J, Zhao W, Xu H, Wang F, Xu Y et al (2016) Effects of salinity and nitrate on production and germination of dimorphic seeds applied both through the mother plant and exogenously during germination in Suaeda salsa. Plant Species Biol 31:19–28

    Article  Google Scholar 

  • Spichal L, Rakova NY, Riefler M, Mizuno T, Romanov GA, Strnad M et al (2004) Two cytokinin receptors of Arabidopsis thaliana, CRE1/AHK4 and AHK3, differ in their ligand specificity in a bacterial assay. Plant Cell Physiol 45:1299–1305

    Article  CAS  PubMed  Google Scholar 

  • Sripinyowanich S, Klomsakul P, Boonburapong B, Bangyeekhun T, Asami T, Gu H et al (2013) Exogenous ABA induces salt tolerance in indica rice (Oryza sativa L.): the role of OsP5CS1 and OsP5CR gene expression during salt stress. Environ Exp Bot 86:94–105

    Article  CAS  Google Scholar 

  • Sui N, Wang Y, Liu S, Yang Z, Wang F, Wan S (2018) Transcriptomic and physiological evidence for the relationship between unsaturated fatty acid and salt stress in peanut. Front Plant Sci 9:7

    Article  PubMed  PubMed Central  Google Scholar 

  • Sui N, Yang Z, Liu M, Wang B (2015) Identification and transcriptomic profiling of genes involved in increasing sugar content during salt stress in sweet sorghum leaves. BMC Genomics 16:534

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Szabados L, Savouré A (2010) Proline: a multifunctional amino acid. Trends Plant Sci 15:89–97

    Article  CAS  PubMed  Google Scholar 

  • Takei K, Yamaya T, Sakakibara H (2004) Arabidopsis CYP735A1 and CYP735A2 encode cytokinin hydroxylases that catalyze the biosynthesis of trans-zeatin. J Biol Chem 279:41866–41872

    Article  CAS  PubMed  Google Scholar 

  • Tran LS, Shinozaki K, Yamaguchi-Shinozaki K (2010) Role of cytokinin responsive two-component system in ABA and osmotic stress signaling. Plant Signal Behav 5(2):148–150

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tran LS, Urao T, Qin F, Maruyama K, Kakimoto T, Shinozaki K et al (2007) Functional analysis of AHK1/ATHK1 and cytokinin receptor histidine kinases in response to abscisic acid, drought, and salt stress in Arabidopsis. Proc Natl Acad Sci USA 104:20623–20628

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tsai YC, Weir NR, Hill K, Zhang W, Kim HJ, Shiu SH et al (2012) Characterization of genes involved in cytokinin signaling and metabolism from rice. Plant Physiol 158:1666–1684

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tuteja N (2007) Abscisic acid and abiotic stress signaling. Plant Signal Behav 2:135–138

    Article  PubMed  PubMed Central  Google Scholar 

  • Ueda J, Kato J (1982) Inhibition of cytokinin-induced plant growth by jasmonic acid and its methyl ester. Physiol Plant 54:249–252

    Article  CAS  Google Scholar 

  • Ursache R, Miyashima S, Chen Q, Vatén A, Nakajima K, Carlsbecker A et al (2014) Tryptophan-dependent auxin biosynthesis is required for HD-ZIP III-mediated xylem patterning. Development 141:1250–1259

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Verma D, Lakhanpal N, Singh K (2019) Genome-wide identification and characterization of abiotic-stress responsive SOD (superoxide dismutase) gene family in Brassica juncea and B. rapa. BMC Genomics 20, 227

    Google Scholar 

  • Veselova SV, Farkhutdinov RG, Veselov DS, Kudoyarova GR (2006) Role of cytokinins in the regulation of stomatal conductance of wheat seedlings under conditions of rapidly changing local temperature. Russ J Plant Physiol 53:756–761

    Article  CAS  Google Scholar 

  • Vojta P, Kokáš F, Husicková A, Grúz J, Bergougnoux V, Marchetti CF et al (2016) Whole transcriptome analysis of transgenic barley with altered cytokinin homeostasis and increased tolerance to drought stress. New Biotechnol 33:676–691

    Article  CAS  Google Scholar 

  • Wakeel A, Xu M, Gan Y (2020) Chromium-induced reactive oxygen species accumulation by altering the enzymatic antioxidant system and associated cytotoxic, genotoxic, ultrastructural, and photosynthetic changes in plants. Int J Mol Sci 21:728

    Article  CAS  PubMed Central  Google Scholar 

  • Wang H (2019) Regulation of vascular cambium activity. Plant Sci 291:110322

    Google Scholar 

  • Wang WC, Lin TC, Kieber J, Tsai YC (2019) Response regulators 9 and 10 negatively regulate salinity tolerance in Rice. Plant Cell Physiol 60(11):2549–2563

    Google Scholar 

  • Wang Y, Shen W, Chan Z, Wu Y (2015) Endogenous cytokinin overproduction modulates ROS homeostasis and decreases salt stress resistance in Arabidopsis Thaliana. Front Plant Sci 6:1004

    Google Scholar 

  • Wang Z, Pote J, Huang B (2003) Responses of cytokinins, antioxidant enzymes, and lipid peroxidation in shoots of cree** bentgrass to high root-zone temperatures. J Am Soc Hortic Sci 128:648–655

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Werner T, Köllmer I, Bartrina I, Holst K, Schmülling T (2006) New insights into the biology of cytokinin degradation. Plant Biol 8:371–381

    Article  CAS  PubMed  Google Scholar 

  • Werner T, Motyka V, Laucou V, Smets R, Van Onckelen H, Schmulling 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

    Google Scholar 

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

    Google Scholar 

  • Werner T, Nehnevajova E, Kollmer I, Novak O, Strnad M, Kramer U et al (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

    Article  PubMed  PubMed Central  Google Scholar 

  • Wingler A, Lea PJ, Quick WP, Leegood RC (2000) Photorespiration: metabolic pathways and their role in stress protection. Philos Trans R Soc Lond B Biol Sci 355:1517–1529

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wohlbach DJ, Quirino BF, Sussman MR (2008) Analysis of the Arabidopsis histidine kinase ATHK1 reveals a connection between vegetative osmotic stress sensing and seed maturation. Plant Cell 20:1101–1117

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu X, Zhu Z, Li X, Zha D (2012) Effects of cytokinin on photosynthetic gas exchange, chlorophyll fluorescence parameters and antioxidative system in seedlings of eggplant (Solanum melongena L.) under salinity stress. Acta Physiol Plant 34:2105–2114

    Article  CAS  Google Scholar 

  • **ao XO, Zeng YM, Cao BH, Lei JJ, Cheng YJ (2017) PSAG12-IPT overexpression in eggplant delays leaf senescence and induces abiotic stress tolerance. J Hortic Sci Biotechnol 92:1–9

    Article  CAS  Google Scholar 

  • **ong H, Li J, Liu P, Duan J, Zhao Y, Guo X et al (2014) Overexpression of OsMYB48-1, a novel MYB-related transcription factor, enhances drought and salinity tolerance in rice. PLoS ONE 9:e92913

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Xu YH, Liu R, Yan L, Liu ZQ, Jiang SC, Shen YY et al (2012) Light-harvesting chlorophyll a/b-binding proteins are required for stomatal response to abscisic acid in Arabidopsis. J Exp Bot 63:1095–1106

    Article  PubMed  CAS  Google Scholar 

  • Xu Y, Burgess P, Zhang X, Huang B (2016) Enhancing cytokinin synthesis by overexpressing ipt alleviated drought inhibition of root growth through activating ROS-scavenging systems in Agrostis stolonifera. J Exp Bot 67:1979–1992

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang Z, Li JL, Liu LN, **e Q, Sui N (2020) Photosynthetic regulation under salt stress and salt-tolerance mechanism of sweet sorghum. Front Plant Sci 10:1722

    Article  PubMed  PubMed Central  Google Scholar 

  • Yaronskaya E, Vershilovskaya I, Poers Y, Alawady AE, Averina N, Grimm B (2006) Cytokinin effects on tetrapyrrole biosynthesis and photosynthetic activity in barley seedlings. Planta 224:700–709

    Article  CAS  PubMed  Google Scholar 

  • Yi X, Hargett SR, Frankel LK, Bricker TM (2008) The effects of simultaneous RNAi suppression of PsbO and PsbP protein expression in photosystem II of Arabidopsis. Photosynth Res 98:439–448

    Article  CAS  PubMed  Google Scholar 

  • Yin W, **ao Y, Niu M, Meng W, Li L, Zhang X et al (2020) ARGONAUTE2 enhances grain length and salt tolerance by activating BIG GRAIN3 to modulate cytokinin distribution in Rice. Plant Cell 32:2292–2306

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yokoyama A, Yamashino T, Amano YI, Tajima Y, Imamura A, Sakakibara H et al (2007) Type-B ARR transcription factors, ARR10 and ARR12, are implicated in cytokinin-mediated regulation of protoxylem differentiation in roots of Arabidopsis thaliana. Plant Cell Physiol 48:84–96

    Article  CAS  PubMed  Google Scholar 

  • Zalabák D, Galuszka P, Mrızova K, Podlešáková K, Gu R, Frébortová J (2014) Biochemical characterization of the maize cytokinin dehydrogenase family and cytokinin profiling in develo** maize plantlets in relation to the expression of cytokinin dehydrogenase genes. Plant Physiol Biochem 74:283–293

    Article  PubMed  CAS  Google Scholar 

  • Zdarska M, Cuyacot AR, Tarr PT, Yamoune A, Szmitkowska A, Hrdinova V et al (2019) ETR1 integrates response to ethylene and cytokinins into a single multistep phosphorelay pathway to control root growth. Mol Plant 12:1338–1352

    Google Scholar 

  • Zdarska M, Dobisova T, Gelova Z, Pernisova M, Dabravolski S, Hejatko J (2015) Illuminating light, cytokinin, and ethylene signaling crosstalk in plant development. J Exp Bot 66:4913–4931

    Google Scholar 

  • Zhang H, Zheng J, Su H, **a K, Jian S, Zhang M (2018) Molecular cloning and functional characterization of the dehydrin (IpDHN) gene from Ipomoea pes-caprae. Front Plant Sci 9:1454

    Google Scholar 

  • Zhang K, Novak O, Wei Z, Gou M, Zhang X, Yu Y et al (2014) Arabidopsis ABCG14 protein controls the acropetal translocation of root-synthesized cytokinins. Nat Commun 5:3274

    Google Scholar 

  • Zhu JK (2001) Plant salt tolerance. Trends Plant Sci 6(2):66–71

    Google Scholar 

  • Žižková E, Dobrev PI, Muhovski Y, HoÅ¡ek P, Hoyerová K, Haisel D et al (2015) Tomato (Solanum lycopersicum L.) SlIPT3 and SlIPT4 isopentenyltransferases mediate salt stress response in tomato. BMC Plant Biol 15(1), 1–20

    Google Scholar 

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Ghassemi-Golezani, K., Samea-Andabjadid, S. (2022). Cytokinin Signaling in Plants Under Salt Stress. In: Aftab, T. (eds) Auxins, Cytokinins and Gibberellins Signaling in Plants. Signaling and Communication in Plants. Springer, Cham. https://doi.org/10.1007/978-3-031-05427-3_8

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