Skip to main content
SpringerLink
Log in

Cellular Responses, Osmotic Adjustments, and Role of Osmolytes in Providing Salt Stress Resilience in Higher Plants: Polyamines and Nitric Oxide Crosstalk

  • Published:
Journal of Plant Growth Regulation Aims and scope Submit manuscript

Abstract

Salinity stress is a chief abiotic hindrance affecting crop productivity and yield particularly in arid and semi-arid regions across the globe. Plants have evolved a network of physiological and molecular mechanisms to cope with salinity stress. The complex and multi-faceted nature of salinity tolerance involve several mechanisms and a comprehensive approach on how plants employ tolerance to salinity at distinct levels and combining physiological measurements with new molecular technologies is an emerging area of crop research. Recent evidences from salinity tolerance mechanisms highlight osmolytes that play a key role in quenching free radicals, induce antioxidant machinery, and osmotic regulation. Polyamines (PAs) also exhibit a promising role in salt tolerance mechanism and adaptation strategies mainly by stabilization of membranes, neutralization of acids, and suppressing ROS synthesis. Interconnection of PAs and nitric oxide biosynthesis also raise hopes for better tolerance to plants under stressful environment. Based on recent findings, the present review highlights the protective role of ion pumps, osmolytes, and polyamines during salt stress. All these strategies have emerged as potential targets for researchers to confer salt stress tolerance in plants.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Acosta-Motos JR, Ortuño MF, Bernal-Vicente A, Diaz-Vivancos P, Sanchez-Blanco MJ, Hernandez JA (2017) Plant responses to salt stress: adaptive mechanisms. Agronomy 7(1):18

    Google Scholar 

  • Adem GD, Roy SJ, Huang Y, Chen Z-H, Wang F, Zhou M et al (2017) Expressing Arabidopsis thaliana V-ATPase subunit C in barley Hordeum vulgare improves plant performance under saline condition by enabling better osmotic adjustment. Funct Plant Biol 44:1147–1159. https://doi.org/10.1071/FP17133

    Article  CAS  PubMed  Google Scholar 

  • Ahmad R, Lim CJ, Kwon SY (2013) Glycine betaine: a versatile compound with great potential for gene pyramiding to improve crop plant performance against environmental stresses. Plant Biotechnol Rep 7(1):49–57

    Google Scholar 

  • Ahmad P, Abdel Latef AA, Abd_Allah EF, Hashem A, Sarwat M, Anjum NA, Gucel S (2016) Calcium and potassium supplementation enhanced growth, osmolyte secondary metabolite production, and enzymatic antioxidant machinery in cadmium-exposed chickpea (Cicer arietinum L.). Front Plant Sci 7:513

    PubMed  PubMed Central  Google Scholar 

  • Akram NA, Hafeez N, Farid-ul-Haq M, Ahmad A, Sadiq M, Ashraf M (2020) Foliage application and seed priming with nitric oxide causes mitigation of salinity-induced metabolic adversaries in broccoli (Brassica oleracea L.) plants. Acta Physiol Plant 42(10):1–9

    Google Scholar 

  • Alcázar R, Cuevas JC, Planas J, Zarza X, Bortolotti C, Carrasco P, Altabella T (2011) Integration of polyamines in the cold acclimation response. Plant Sci 180(1):31–38

    PubMed  Google Scholar 

  • Ali RM (2000) Role of putrescine in salt tolerance of Atropa belladonna plant. Plant Sci 152(2):173–179

    CAS  Google Scholar 

  • Al Hassan M, Fuertes MM, Sanchez FJR, Vicente O, Boscaiu M (2015) Effects of salt and water stress on plant growth and on accumulation of osmolytes and antioxidant compounds in cherry tomato. Not Bot Horti Agrobot ClujNapoca 43(1):1–11

    CAS  Google Scholar 

  • Asgher M, Per TS, Masood A, Fatma M, Freschi L, Corpas FJ, Khan NA (2017) Nitric oxide signaling and its crosstalk with other plant growth regulators in plant responses to abiotic stress. Environ Sci Pollut Res 24(3):2273–2285

    CAS  Google Scholar 

  • Ashraf MFMR, Foolad MR (2007) Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot 59(2):206–216

    CAS  Google Scholar 

  • Ashraf MPJC, Harris PJC (2004) Potential biochemical indicators of salinity tolerance in plants. Plant Sci 166(1):3–16

    CAS  Google Scholar 

  • Astier J, Gross I, Durner J (2018) Nitric oxide production in plants: an update. J Exp Bot 69(14):3401–3411

    CAS  PubMed  Google Scholar 

  • Bajguz A (2014) Nitric oxide: role in plants under abiotic stress. In: Physiological mechanisms and adaptation strategies in plants under changing environment. Springer, New York, pp 137–159

    Google Scholar 

  • Baniasadi F, Saffari VR, Moud AAM (2018) Physiological and growth responses of Calendula officinalis L. plants to the interaction effects of polyamines and salt stress. Sci Hortic 234:312–317

    CAS  Google Scholar 

  • Barragán V, Leidi EO, Andrés Z, Rubio L, De Luca A, Fernández JA, Pardo JM (2012) Ion exchangers NHX1 and NHX2 mediate active potassium uptake into vacuoles to regulate cell turgor and stomatal function in Arabidopsis. Plant Cell 24(3):1127–1142

    PubMed  PubMed Central  Google Scholar 

  • Benkő P, Jee S, Kaszler N, Fehér A, Gémes K (2020) Polyamines treatment during pollen germination and pollen tube elongation in tobacco modulate reactive oxygen species and nitric oxide homeostasis. J Plant Physiol 244:153085

    PubMed  Google Scholar 

  • Besson-Bard A, Pugin A, Wendehenne D (2008) New insights into nitric oxide signaling in plants. Annu Rev Plant Biol 59:21–39

    CAS  PubMed  Google Scholar 

  • Blumwald E (2000) Sodium transport and salt tolerance in plants. Curr Opin Cell Biol 12(4):431–434

    CAS  PubMed  Google Scholar 

  • Bohnert HJ, Nelson DE, Jensen RG (1995) Adaptations to environmental stresses. Plant Cell 7(7):1099

    CAS  PubMed  PubMed Central  Google Scholar 

  • Carillo P, Annunziata MG, Pontecorvo G, Fuggi A, Woodrow P (2011) Salinity stress and salt tolerance. Abiotic Stress Plants-Mech Adapt 1:21–38

    Google Scholar 

  • Corpas FJ, Palma JM, Del Río LA, Barroso JB (2009) Evidence supporting the existence of l-arginine-dependent nitric oxide synthase activity in plants. New Phytol 184(1):9–14

    CAS  PubMed  Google Scholar 

  • Chai YY, Jiang CD, Shi L, Shi TS, Gu WB (2010) Effects of exogenous spermine on sweet sorghum during germination under salinity. Biol Plant 54(1):145–148

    Google Scholar 

  • Chattopadhayay MK, Tiwari BS, Chattopadhyay G, Bose A, Sengupta DN, Ghosh B (2002) Protective role of exogenous polyamines on salinity-stressed rice (Oryza sativa) plants. Physiol Plant 116(2):192–199

    CAS  PubMed  Google Scholar 

  • Chaum S, Kirdmanee C (2010) Effect of glycine betaine on proline, water use, and photosynthetic efficiencies, and growth of rice seedlings under salt stress. Turk J Agric for 34(6):517–527

    CAS  Google Scholar 

  • Chen TH, Murata N (2002) Enhancement of tolerance of abiotic stress by metabolic engineering of betaines and other compatible solutes. Curr Opin Plant Biol 5(3):250–257

    CAS  PubMed  Google Scholar 

  • Chen S, Polle A (2010) Salinity tolerance of populus. Plant Biol 12(2):317–333

    CAS  PubMed  Google Scholar 

  • Cuin TA, Parsons D, Shabala S (2010) Wheat cultivars can be screened for NaCl salinity tolerance by measuring leaf chlorophyll content and shoot sap potassium. Funct Plant Biol 37(7):656–664

    CAS  Google Scholar 

  • Deinlein U, Stephan AB, Horie T, Luo W, Xu G, Schroeder JI (2014) Plant salt-tolerance mechanisms. Trends Plant Sci 19(6):371–379

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dietz KJ, Tavakoli N, Kluge C, Mimura T, Sharma SS, Harris GC, Golldack D (2001) Significance of the V-type ATPase for the adaptation to stressful growth conditions and its regulation on the molecular and biochemical level. J Exp Bot 52(363):1969–1980

    CAS  PubMed  Google Scholar 

  • Dong Y, Xu L, Wang Q, Fan Z, Kong J, Bai X (2014) Effects of exogenous nitric oxide on photosynthesis, antioxidative ability, and mineral element contents of perennial ryegrass under copper stress. J Plant Interact 9:402–411

    CAS  Google Scholar 

  • Duan J, Li J, Guo S, Kang Y (2008) Exogenous spermidine affects polyamine metabolism in salinity-stressed Cucumis sativus roots and enhances short-term salinity tolerance. J Plant Physiol 165(15):1620–1635

    CAS  PubMed  Google Scholar 

  • Farooq M, Hussain M, Wakeel A, Siddique KH (2015) Salt stress in maize: effects, resistance mechanisms, and management. A review. Agron Sustain Dev 35(2):461–481

    CAS  Google Scholar 

  • Farooq M, Gogoi N, Hussain M, Barthakur S, Paul S, Bharadwaj N, Siddique KH (2017) Effects, tolerance mechanisms and management of salt stress in grain legumes. Plant Physiol Biochem 118:199–217

    CAS  PubMed  Google Scholar 

  • Flowers TJ (2004) Improving crop salt tolerance. J Exp Bot 55(396):307–319

    CAS  PubMed  Google Scholar 

  • Flowers TJ, Troke PF, Yeo AR (1977) The mechanism of salt tolerance in halophytes. Annu Rev Plant Physiol 28(1):89–121

    CAS  Google Scholar 

  • Galston AW, Kaur-Sawhney R, Altabella T, Tiburcio AF (1997) Plant polyamines in reproductive activity and response to abiotic stress. Bot Acta 110(3):197–207

    CAS  Google Scholar 

  • Gálvez FJ, Baghour M, Hao G, Cagnac O, Rodríguez-Rosales MP, Venema K (2012) Expression of LeNHX isoforms in response to salt stress in salt sensitive and salt tolerant tomato species. Plant Physiol Biochem 51:109–115

    PubMed  Google Scholar 

  • Gao Z, Sagi M, Lips SH (1998) Carbohydrate metabolism in leaves and assimilate partitioning in fruits of tomato (Lycopersicon esculentum L.) as affected by salinity. Plant Sci 135(2):149–159

    CAS  Google Scholar 

  • Gill SS, Tuteja N (2010) Polyamines and abiotic stress tolerance in plants. Plant Signal Behav 5(1):26–33

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ghalati RE, Shamili M, Homaei A (2020) Effect of putrescine on biochemical and physiological characteristics of guava (Psidium guajava L.) seedlings under salt stress. Sci Hortic 261:108961

    Google Scholar 

  • Gong B, Li X, Bloszies S, Wen D, Sun S, Wei M, Wang X (2014) Sodic alkaline stress mitigation by interaction of nitric oxide and polyamines involves antioxidants and physiological strategies in Solanum lycopersicum. Free Radic Biol Med 71:36–48

    CAS  PubMed  Google Scholar 

  • Groppa MD, Benavides MP (2008) Polyamines and abiotic stress: recent advances. Amino Acids 34(1):35

    CAS  PubMed  Google Scholar 

  • Guo Y, Qiu QS, Quintero FJ, Pardo JM, Ohta M, Zhang C, Zhu JK (2004) Transgenic evaluation of activated mutant alleles of SOS2 reveals a critical requirement for its kinase activity and C-terminal regulatory domain for salt tolerance in Arabidopsis thaliana. Plant Cell 16(2):435–449

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gupta KJ, Fernie AR, Kaiser WM, Van Dongen JT (2011) On the origins of nitric oxide. Trends Plant Sci 16(3):160–168

    CAS  PubMed  Google Scholar 

  • Gupta K, Dey A, Gupta B (2013a) Plant polyamines in abiotic stress responses. Acta Physiol Plant 35(7):2015–2036

    CAS  Google Scholar 

  • Gupta K, Dey A, Gupta B (2013b) Polyamines and their role in plant osmotic stress tolerance. Climate change and plant abiotic stress tolerance. Wiley-VCH Verlag GmbH & Co, Weinheim, pp 1053–1072

    Google Scholar 

  • Hanson AD, Rathinasabapathi B, Rivoal J, Burnet M, Dillon MO, Gage DA (1994) Osmoprotective compounds in the Plumbaginaceae: a natural experiment in metabolic engineering of stress tolerance. Proc Natl Acad Sci 91(1):306–310

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hao F, Zhao S, Dong H, Zhang H, Sun L, Miao C (2010) Nia1 and Nia2 are involved in exogenous salicylic acid-induced nitric oxide generation and stomatal closure in Arabidopsis. J Integr Plant Biol 52(3):298–307

    CAS  PubMed  Google Scholar 

  • Hare PD, Cress WA, Van Staden J (1998) Dissecting the roles of osmolyte accumulation during stress. Plant Cell Environ 21(6):535–553

    CAS  Google Scholar 

  • Hasegawa PM (2013) Sodium (Na+) homeostasis and salt tolerance of plants. Environ Exp Bot 92:19–31

    CAS  Google Scholar 

  • Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annu Rev Plant Biol 51(1):463–499

    CAS  Google Scholar 

  • He X, Huang X, Shen Y, Huang Z (2014) Wheat V-H+-ATPase subunit genes significantly affect salt tolerance in Arabidopsis thaliana. PLoS ONE 9:e86982. https://doi.org/10.1371/journal.pone.0086982

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Heidari M (2009) Antioxidant activity and osmolyte concentration of sorghum (Sorghum bicolor) and wheat (Triticum aestivum) genotypes under salinity stress. Asian J Plant Sci 8(3):240

    CAS  Google Scholar 

  • Hernández JA, Ferrer MA, Jiménez A, Barceló AR, Sevilla F (2001) Antioxidant systems and O2.−/H2O2 production in the apoplast of pea leaves. Its relation with salt-induced necrotic lesions in minor veins. Plant Physiol 127(3):817–831

    PubMed  PubMed Central  Google Scholar 

  • Hu X, Zhang Y, Shi Y, Zhang Z, Zou Z, Zhang H, Zhao J (2012) Effect of exogenous spermidine on polyamine content and metabolism in tomato exposed to salinity–alkalinity mixed stress. Plant Physiol Biochem 57:200–209

    CAS  PubMed  Google Scholar 

  • Huo L, Guo Z, Wang P, Zhang Z, Jia X, Sun Y, Xun S, Xiaoqing G, Ma F (2020) MdATG8i functions positively in apple salt tolerance by maintaining photosynthetic ability and increasing the accumulation of arginine and polyamines. Environ Exp Bot 172:103989

    CAS  Google Scholar 

  • Hussain K, Nawaz K, Majeed A, Ilyas U, Lin F, Ali K, Nisar MF (2011a) Role of exogenous salicylic acid applications for salt tolerance in violet. Sarhad J Agric 27(2):171–175

    Google Scholar 

  • Hussain SS, Ali M, Ahmad M, Siddique KH (2011b) Polyamines: natural and engineered abiotic and biotic stress tolerance in plants. Biotechnol Adv 29(3):300–311

    CAS  PubMed  Google Scholar 

  • Islam MA, Pang JH, Meng FW, Li YW, Ning XU, Chao YANG, Jun LIU (2020) Putrescine, spermidine, and spermine play distinct roles in rice salt tolerance. J Integr Agric 19(3):643–655

    CAS  Google Scholar 

  • Isayenkov SV (2012) Physiological and molecular aspects of salt stress in plants. Cytol Genet 46(5):302–318

    Google Scholar 

  • Ishitani M, Liu J, Halfter U, Kim CS, Shi W, Zhu JK (2000) SOS3 function in plant salt tolerance requires N-myristoylation and calcium binding. Plant Cell 12(9):1667–1677

    CAS  PubMed  PubMed Central  Google Scholar 

  • James RA, Munns R, Von Caemmerer S, Trejo C, Miller C, Condon T (2006) Photosynthetic capacity is related to the cellular and subcellular partitioning of Na+, K+ and Cl-in salt-affected barley and durum wheat. Plant, Cell Environ 29(12):2185–2197

    CAS  PubMed  Google Scholar 

  • Jaarsma R, De Boer AH (2018) Salinity tolerance of two potato cultivars (Solanum tuberosum) correlates with differences in vacuolar transport activity. Front Plant Sci 9:737

    PubMed  PubMed Central  Google Scholar 

  • Kausar F, Shahbaz M (2013) Interactive effect of foliar application of nitric oxide (NO) and salinity on wheat (Triticum aestivum L.). Pak J Bot 45:67–73

    CAS  Google Scholar 

  • Kerepesi I, Galiba G (2000) Osmotic and salt stress-induced alteration in soluble carbohydrate content in wheat seedlings. Crop Sci 40(2):482–487

    CAS  Google Scholar 

  • Khan MA, Ungar IA, Showalter AM (2000) Effects of sodium chloride treatments on growth and ion accumulation of the halophyte Haloxylon recurvum. Commun Soil Sci Plant Anal 31(17–18):2763–2774

    CAS  Google Scholar 

  • Khare T, Srivastav A, Shaikh S, Kumar V (2018) Polyamines and their metabolic engineering for plant salinity stress tolerance. In: Salinity responses and tolerance in plants, vol 1. Springer, Cham, pp 339–358

    Google Scholar 

  • Knott JM, Römer P, Sumper M (2007) Putative spermine synthases from Thalassiosira pseudonana and Arabidopsis thaliana synthesize thermospermine rather than spermine. FEBS Lett 581(16):3081–3086

    CAS  PubMed  Google Scholar 

  • Kopyra M, Gwóźdź EA (2003) Nitric oxide stimulates seed germination and counteracts the inhibitory effect of heavy metals and salinity on root growth of Lupinus luteus. Plant Physiol Biochem 41(11–12):1011–1017

    CAS  Google Scholar 

  • Kovács Z, Simon-Sarkadi L, Szűcs A, Kocsy G (2010) Differential effects of cold, osmotic stress and abscisic acid on polyamine accumulation in wheat. Amino Acids 38(2):623–631

    PubMed  Google Scholar 

  • Läuchli A, Epstein E (1990) Plant responses to saline and sodic conditions. Agric Salin Assess Manage 71:113–137

    Google Scholar 

  • León J, Costa-Broseta Á (2020) Present knowledge and controversies, deficiencies, and misconceptions on nitric oxide synthesis, sensing, and signaling in plants. Plant Cell Environ 43(1):1–15

    Google Scholar 

  • Liu J, Ishitani M, Halfter U, Kim CS, Zhu JK (2000) The Arabidopsis thaliana SOS2 gene encodes a protein kinase that is required for salt tolerance. Proc Natl Acad Sci 97(7):3730–3734

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ma L, Zhang H, Sun L, Jiao Y, Zhang G, Miao C, Hao F (2012) NADPH oxidase AtrbohD and AtrbohF function in ROS-dependent regulation of Na+/K+ homeostasis in Arabidopsis under salt stress. J Exp Bot 63(1):305–317

    CAS  PubMed  Google Scholar 

  • Ma D-M, Xu W-R, Li H-W, Jin F-X, Guo L-N, Wang J, Dai H-J, Xu X (2014) Co-expression of the Arabidopsis SOS genes enhances salt tolerance in transgenic tall fescue (Festuca arundinacea Schreb.). Protoplasma 251:219–231

    CAS  PubMed  Google Scholar 

  • Martínez-Atienza J, Jiang X, Garciadeblas B, Mendoza I, Zhu JK, Pardo JM, Quintero FJ (2007) Conservation of the salt overly sensitive pathway in rice. Plant Physiol 143(2):1001–1012

    PubMed  PubMed Central  Google Scholar 

  • Matysik J, Alia, Bhalu B, Mohanty P (2002) Molecular mechanisms of quenching of reactive oxygen species by proline under stress in plants. Curr Sci 82:525–532

    CAS  Google Scholar 

  • Mishra S, Jha AB, Dubey RS (2011) Arsenite treatment induces oxidative stress, upregulates antioxidant system, and causes phytochelatin synthesis in rice seedlings. Protoplasma 248(3):565–577

    CAS  PubMed  Google Scholar 

  • Moschou PN, Paschalidis KA, Roubelakis-Angelakis KA (2008) Plant polyamine catabolism: the state of the art. Plant Signal Behav 3(12):1061–1066

    PubMed  PubMed Central  Google Scholar 

  • Moshaei MR, Nematzadeh GA, Askari H, Nejad ASM (2014) Quantitative gene expression analysis of some sodium ion transporters under salinity stress in Aeluropus littoralis. Saudi J Biol Sci 21:394–399

    Google Scholar 

  • Munns R (2002) Comparative physiology of salt and water stress. Plant Cell Environ 25:239–250

    CAS  PubMed  Google Scholar 

  • Munns R (2005) Genes and salt tolerance: bringing them together. New Phytol 167(3):645–663

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Munns R, Greenway H, Delane R, Gibbs J (1982) Ion concentration and carbohydrate status of the elongating leaf tissue 4 Hordeum vulgare growing at high external NaCl: II. CAUSE OF THE GROWTH REDUCTION. J Exp Bot 33(4):574–583

    CAS  Google Scholar 

  • Nahar K, Hasanuzzaman M, Alam MM, Rahman A, Suzuki T, Fujita M (2016) Polyamine and nitric oxide crosstalk: antagonistic effects on cadmium toxicity in mung bean plants through upregulating the metal detoxification, antioxidant defense and methylglyoxal detoxification systems. Ecotoxicol Environ Saf 126:245–255

    CAS  PubMed  Google Scholar 

  • Nalousi AM, Ahmadiyan S, Hatamzadeh A, Ghasemnezhad M (2012) Protective role of exogenous nitric oxide against oxidative stress induced by salt stress in bell-pepper (Capsicum annum L.). Am Eurasian J Agric Environ Sci 12:1085–1090

    CAS  Google Scholar 

  • Navakoudis E, Lütz C, Langebartels C, Lütz-Meindl U, Kotzabasis K (2003) Ozone impact on the photosynthetic apparatus and the protective role of polyamines. Biochimica Et Biophysica Acta (BBA)-General Subjects 1621(2):160–169

    CAS  PubMed  Google Scholar 

  • Nawaz K (2007) Alleviation of the adverse effects of salinity stress on maize (Zea mays L.) by exogenous application of glycine betaine (Doctoral dissertation, University of Agriculture Faisalabad, Pakistan)

  • Niu X, Bressan RA, Hasegawa PM, Pardo JM (1995) Ion homeostasis in NaCl stress environments. Plant Physiol 109(3):735

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nounjan N, Nghia PT, Theerakulpisut P (2012) Exogenous proline and trehalose promote recovery of rice seedlings from salt-stress and differentially modulate antioxidant enzymes and expression of related genes. J Plant Physiol 169(6):596–604

    CAS  PubMed  Google Scholar 

  • Oh DH, Lee SY, Bressan RA, Yun DJ, Bohnert HJ (2010) Intracellular consequences of SOS1 deficiency during salt stress. J Exp Bot 61(4):1205–1213

    CAS  PubMed  PubMed Central  Google Scholar 

  • Panicot M, Minguet EG, Ferrando A, Alcázar R, Blázquez MA, Carbonell J, Tiburcio AF (2002) A polyamine metabolon involving aminopropyl transferase complexes in Arabidopsis. Plant Cell 14(10):2539–2551

    CAS  PubMed  PubMed Central  Google Scholar 

  • Parida AK, Das AB (2005) Salt tolerance and salinity effects on plants: a review. Ecotoxicol Environ Saf 60(3):324–349

    CAS  PubMed  Google Scholar 

  • Parida AK, Das AB, Mohanty P (2004) Investigations on the antioxidative defence responses to NaCl stress in a mangrove, Bruguiera parviflora: differential regulations of isoforms of some antioxidative enzymes. Plant Growth Regul 42(3):213–226

    CAS  Google Scholar 

  • Qadir M, Quillérou E, Nangia V, Murtaza G, Singh M, Thomas RJ, Noble AD (2014) Economics of salt-induced land degradation and restoration. Nat Resour Forum 38(4):282–295

    Google Scholar 

  • Qian R, Ma X, Zhang X, Hu Q, Liu H, Zheng J (2020) Effect of exogenous spermidine on osmotic adjustment, antioxidant enzymes activity, and gene expression of Gladiolus gandavensis seedlings under salt stress. J Plant Growth Regul. https://doi.org/10.1007/s00344-020-10198-x

    Article  Google Scholar 

  • Quinet M, Ndayiragije A, Lefevre I, Lambillotte B, Dupont-Gillain CC, Lutts S (2010) Putrescine differently influences the effect of salt stress on polyamine metabolism and ethylene synthesis in rice cultivars differing in salt resistance. J Exp Bot 61(10):2719–2733

    CAS  PubMed  PubMed Central  Google Scholar 

  • Quintero FJ, Ohta M, Shi H, Zhu JK, Pardo JM (2002) Reconstitution in yeast of the Arabidopsis SOS signaling pathway for Na+ homeostasis. Proc Natl Acad Sci 99(13):9061–9066

    CAS  PubMed  PubMed Central  Google Scholar 

  • Quintero FJ, Martinez-Atienza J, Villalta I, Jiang X, Kim WY, Ali Z, Pardo JM (2011) Activation of the plasma membrane Na/H antiporter salt-overly-sensitive 1 (SOS1) by phosphorylation of an auto-inhibitory C-terminal domain. Proc Natl Acad Sci 108(6):2611–2616

    CAS  PubMed  PubMed Central  Google Scholar 

  • Qurashi AW, Sabri AN (2013) Osmolyte accumulation in moderately halophilic bacteria improves salt tolerance of chickpea. Pak J Bot 45(3):1011–1016

    CAS  Google Scholar 

  • Rahman MS, Miyake H, Takeoka Y (2002) Effects of exogenous glycine betaine on growth and ultrastructure of salt-stressed rice seedlings (Oryza sativa L.). Plant Prod Sci 5(1):33–44

    CAS  Google Scholar 

  • Ranganayakulu GS, Veeranagamallaiah G, Chinta S (2013) Effect of salt stress on osmolyte accumulation in two groundnut cultivars (Arachis hypogaea L.) with contrasting salt tolerance. Afr J Plant Sci 7(12):586–592

    CAS  Google Scholar 

  • Raven JA (1985) Tansley review no. 2. Regulation of pH and generation of osmolarity in vascular plants: a cost-benefit analysis in relation to efficiency of use of energy, nitrogen and water. New Phytol 101:25–77

    CAS  PubMed  Google Scholar 

  • Recalde L, Gómez Mansur NM, Cabrera AV, Matayoshi CL, Gallego SM, Groppa MD, Benavides MP (2021) Unravelling ties in the nitrogen network: polyamines and nitric oxide emerging as essential players in signalling roadway. Ann Appl Biol. https://doi.org/10.1111/aab.12642

    Article  Google Scholar 

  • Ren Y, Wang W, He J, Zhang L, Wei Y, Yang M (2020) Nitric oxide alleviates salt stress in seed germination and early seedling growth of pakchoi (Brassica chinensis L.) by enhancing physiological and biochemical parameters. Ecotoxicol Environ Saf 187:109785

    CAS  PubMed  Google Scholar 

  • Rengasamy P (2010) Soil processes affecting crop production in salt-affected soils. Funct Plant Biol 37(7):613–620

    Google Scholar 

  • Rhodes D, Nadolska-Orczyk A, Rich PJ (2002) Salinity, osmolytes and compatible solutes. In: Salinity: environment-plants-molecules. Springer, Dordrecht, pp 181–204

    Google Scholar 

  • Rolly NK, Imran QM, Lee IJ, Yun BW (2020) Salinity stress-mediated suppression of expression of salt overly sensitive signaling pathway genes suggests negative regulation by AtbZIP62 transcription factor in Arabidopsis thaliana. Int J Mol Sci 21(5):1726

    CAS  PubMed  PubMed Central  Google Scholar 

  • Roy M, Wu R (2002) Overexpression of S-adenosylmethionine decarboxylase gene in rice increases polyamine level and enhances sodium chloride-stress tolerance. Plant Sci 163(5):987–992

    CAS  Google Scholar 

  • Roychoudhury A, Basu S, Sengupta DN (2011) Amelioration of salinity stress by exogenously applied spermidine or spermine in three varieties of indica rice differing in their level of salt tolerance. J Plant Physiol 168(4):317–328

    CAS  PubMed  Google Scholar 

  • Siddiqui MH, Alamri SA, Al-Khaishany MY, Al-Qutami MA, Ali HM, Hala AR, Kalaji HM (2017) Exogenous application of nitric oxide and spermidine reduces the negative effects of salt stress on tomato. Hortic Environ Biotechnol 58(6):537–547

    CAS  Google Scholar 

  • Saha J, Brauer EK, Sengupta A, Popescu SC, Gupta K, Gupta B (2015) Polyamines as redox homeostasis regulators during salt stress in plants. Front Environ Sci 3:21

    Google Scholar 

  • Sairam RK, Tyagi A (2004) Physiology and molecular biology of salinity stress tolerance in plants. Curr Sci 86:407–421

    CAS  Google Scholar 

  • Sakihama Y, Murakami S, Yamasaki H (2003) Involvement of nitric oxide in the mechanism for stomatal opening in Vicia faba leaves. Biol Plant 46:117–119. https://doi.org/10.1023/A:1022378621030

    Article  CAS  Google Scholar 

  • Saxena SC, Kaur H, Verma P, Petla BP, Andugula VR, Majee M (2013) Osmoprotectants: potential for crop improvement under adverse conditions. In: Plant acclimation to environmental stress. Springer, New York, pp 197–232

    Google Scholar 

  • Schroeder JI, Delhaize E, Frommer WB, Guerinot ML, Harrison MJ, Herrera-Estrella L, Sanders D (2013) Using membrane transporters to improve crops for sustainable food production. Nature 497(7447):60–66

    CAS  PubMed  PubMed Central  Google Scholar 

  • Serrano R, Mulet JM, Rios G, Marquez JA, De Larrinoa IF, Leube MP, Montesinos C (1999) A glimpse of the mechanisms of ion homeostasis during salt stress. J Exp Bot 50:1023–1036

    CAS  Google Scholar 

  • Silini A, Cherif-Silini H, Yahiaoui B (2016) Growing varieties durum wheat (Triticum durum) in response to the effect of osmolytes and inoculation by Azotobacter chroococcum under salt stress. Afr J Microbiol Res 10(12):387–399

    CAS  Google Scholar 

  • Shabala S, Cuin TA (2008) Potassium transport and plant salt tolerance. Physiol Plant 133(4):651–669

    CAS  PubMed  Google Scholar 

  • Shabala SN, Lew RR (2002) Turgor regulation in osmotically stressed Arabidopsis epidermal root cells. Direct support for the role of inorganic ion uptake as revealed by concurrent flux and cell turgor measurements. Plant Physiol 129(1):290–299

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shabala S, Mackay A (2011) Ion transport in halophytes. Adv Bot Res 57:151–199. https://doi.org/10.1016/B978-0-12-387692-8.00005-9

    Article  CAS  Google Scholar 

  • Shabala S, Shabala L (2011) Ion transport and osmotic adjustment in plants and bacteria. BioMol Concept. https://doi.org/10.1515/BMC.2011.032

    Article  Google Scholar 

  • Shah SH, Islam S, Parrey ZA, Mohammad F (2021) Role of exogenously applied plant growth regulators in growth and development of edible oilseed crops under variable environmental conditions: a review. J Soil Sci Plant Nutr. https://doi.org/10.1007/s42729-021-00606-w

    Article  Google Scholar 

  • Shams M, Ekinci M, Ors S, Turan M, Agar G, Kul R, Yildirim E (2019) Nitric oxide mitigates salt stress effects of pepper seedlings by altering nutrient uptake, enzyme activity and osmolyte accumulation. Physiol Mol Biol Plants 25(5):1149–1161

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sheokand S, Kumari A, Sawhney V (2008) Effect of nitric oxide and putrescine on antioxidative responses under NaCl stress in chickpea plants. Physiol Mol Biol Plants 14:355–362

    CAS  PubMed  Google Scholar 

  • Shevyakova NI, Musatenko LI, Stetsenko LA, Vedenicheva NP, Voitenko LP, Sytnik KM, Kuznetsov VV (2013) Effects of abscisic acid on the contents of polyamines and proline in common bean plants under salt stress. Russ J Plant Physiol 60(2):200–211

    CAS  Google Scholar 

  • Shi H, Chan Z (2014) Improvement of plant abiotic stress tolerance through modulation of the polyamine pathway. J Integr Plant Biol 56(2):114–121

    CAS  PubMed  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 97(12):6896–6901

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shi H, Quintero FJ, Pardo JM, Zhu JK (2002) The putative plasma membrane Na+/H+ antiporter SOS1 controls long-distance Na+ transport in plants. Plant Cell 14(2):465–477

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shu S, Guo SR, Yuan LY (2012) A review: polyamines and photosynthesis. Advances in photosynthesis-fundamental aspects. InTech, London, pp 439–464

    Google Scholar 

  • Shu S, Yuan LY, Guo SR, Sun J, Yuan YH (2013) Effects of exogenous spermine on chlorophyll fluorescence, antioxidant system and ultrastructure of chloroplasts in Cucumis sativus L. under salt stress. Plant Physiol Biochem 63:209–216

    CAS  PubMed  Google Scholar 

  • Shu S, Yuan Y, Chen J, Sun J, Zhang W, Tang Y, Min Z, Guo S (2015) The role of putrescine in the regulation of proteins and fatty acids of thylakoid membranes under salt stress. Sci Rep 5(1):1–16

    Google Scholar 

  • Sickler CM, Edwards GE, Kiirats O, Gao Z, Loescher W (2007) Response of mannitol-producing Arabidopsis thaliana to abiotic stress. Funct Plant Biol 34(4):382–391

    CAS  PubMed  Google Scholar 

  • Sung CH, Hong JK (2010) Sodium nitroprusside mediates seedling development and attenuation of oxidative stresses in Chinese cabbage. Plant Biotechnol Rep 4(4):243–251

    Google Scholar 

  • Sushmita S, Priyanka D, Mamata R, Surendra CS (2010) Osmolyte modulated enhanced rice leaf catalase activity under salt-stress. Adv Biosci Biotechnol. https://doi.org/10.4236/abb.2010.11006

    Article  Google Scholar 

  • Taffouo VD, Nouck AE, Nyemene KP, Tonfack B, Meguekem TL, Youmbi E (2017) Effects of salt stress on plant growth, nutrient partitioning, chlorophyll content, leaf relative water content, accumulation of osmolytes and antioxidant compounds in pepper (Capsicum annuum L.) cultivars. Notulae Botanicae Horti Agrobotanici Cluj-Napoca 45(2):481–490

    Google Scholar 

  • Tahir MA, Aziz T, Farooq M, Sarwar G (2012) Silicon-induced changes in growth, ionic composition, water relations, chlorophyll contents and membrane permeability in two salt-stressed wheat genotypes. Arch Agron Soil Sci 58(3):247–256

    CAS  Google Scholar 

  • Tailor A, Tandon R, Bhatla SC (2019) Nitric oxide modulates polyamine homeostasis in sunflower seedling cotyledons under salt stress. Plant Signal Behav 14(11):1667730

    PubMed  PubMed Central  Google Scholar 

  • Tang H, Niu L, Wei J, Chen X, Chen Y (2019) Phosphorus limitation improved salt tolerance in maize through tissue mass density increase, osmolytes accumulation, and Na+ uptake inhibition. Front Plant Sci 10:856

    PubMed  PubMed Central  Google Scholar 

  • Tanou G, Ziogas V, Belghazi M, Christou A, Filippou P, Job D, Molassiotis A (2014) Polyamines reprogram oxidative and nitrosative status and the proteome of citrus plants exposed to salinity stress. Plant Cell Environ 37(4):864–885

    CAS  PubMed  Google Scholar 

  • Tanveer M, Shah AN (2017) An insight into salt stress tolerance mechanisms of Chenopodium album. Environ Sci Pollut Res 24(19):16531–16535

    CAS  Google Scholar 

  • Tester M, Davenport R (2003) Na+ tolerance and Na+ transport in higher plants. Ann Bot 91(5):503–527

    CAS  PubMed  PubMed Central  Google Scholar 

  • Thomas JC, Sepahi M, Arendall B, Bohnert HJ (1995) Enhancement of seed germination in high salinity by engineering mannitol expression in Arabidopsis thaliana. Plant Cell Environ 18(7):801–806

    CAS  Google Scholar 

  • Tisi A, Angelini R, Cona A (2008) Wound healing in plants: cooperation of copper amine oxidase and flavin-containing polyamine oxidase. Plant Signal Behav 3(3):204–206

    PubMed  PubMed Central  Google Scholar 

  • Volkmar KM, Hu Y, Steppuhn H (1998) Physiological responses of plants to salinity: a review. Can J Plant Sci 78(1):19–27

    CAS  Google Scholar 

  • Wang R, Guegler K, LaBrie ST, Crawford NM (2000) Genomic analysis of a nutrient response in Arabidopsis reveals diverse expression patterns and novel metabolic and potential regulatory genes induced by nitrate. Plant Cell 12(8):1491–1509

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang B, Lüttge U, Ratajczak R (2001) Effects of salt treatment and osmotic stress on V-ATPase and V-PPase in leaves of the halophyte Suaeda salsa. J Exp Bot 52(365):2355–2365

    CAS  PubMed  Google Scholar 

  • Wang X, Shi G, Xu Q, Hu J (2007) Exogenous polyamines enhance copper tolerance of Nymphoides peltatum. J Plant Physiol 164(8):1062–1070

    CAS  PubMed  Google Scholar 

  • Wani KI, Naeem M, Castroverde CDM, Kalaji HM, Albaqami M, Aftab T (2021) Molecular mechanisms of nitric oxide (NO) signaling and reactive oxygen species (ROS) homeostasis during abiotic stresses in plants. Int J Mol Sci 22(17):9656

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wong CE, Li Y, Labbe A, Guevara D, Nuin P, Whitty B, Moffatt BA (2006) Transcriptional profiling implicates novel interactions between abiotic stress and hormonal responses in Thellungiella, a close relative of Arabidopsis. Plant Physiol 140(4):1437–1450

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yamasaki H, Cohen MF (2006) NO signal at the crossroads: polyamine-induced nitric oxide synthesis in plants? Trends Plant Sci 11(11):522–524

    CAS  PubMed  Google Scholar 

  • Yamaguchi K, Takahashi Y, Berberich T, Imai A, Miyazaki A, Takahashi T, Kusano T (2006) The polyamine spermine protects against high salt stress in Arabidopsis thaliana. FEBS Lett 580(30):6783–6788

    CAS  PubMed  Google Scholar 

  • Yang Y, Guo Y (2018) Elucidating the molecular mechanisms mediating plant salt-stress responses. New Phytol 217(2):523–539

    CAS  PubMed  Google Scholar 

  • Yang J, Yen HE (2002) Early salt stress effects on the changes in chemical composition in leaves of ice plant and Arabidopsis. A Fourier transform infrared spectroscopy study. Plant Physiol 130(2):1032–1042

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yastreb TO, Kolupaev YE, Lugovaya AA, Dmitriev AP (2016) Content of osmolytes and flavonoids under salt stress in Arabidopsis thaliana plants defective in jasmonate signaling. Appl Biochem Microbiol 52(2):210–215

    CAS  Google Scholar 

  • Yiu JC, Juang LD, Fang DYT, Liu CW, Wu SJ (2009) Exogenous putrescine reduces flooding-induced oxidative damage by increasing the antioxidant properties of Welsh onion. Sci Hortic 120(3):306–314

    CAS  Google Scholar 

  • Zarza X, Atanasov KE, Marco F, Arbona V, Carrasco P, Kopka J, Alcázar R (2017) Polyamine oxidase 5 loss-of-function mutations in Arabidopsis thaliana trigger metabolic and transcriptional reprogramming and promote salt stress tolerance. Plant Cell Environ 40(4):527–542

    CAS  PubMed  Google Scholar 

  • Zelm E, Zhang Y, Testerink C (2020) Salt tolerance mechanisms of plants. Annu Rev Plant Biol 71:403–433

    PubMed  Google Scholar 

  • Zhang Y, Wang L, Liu Y, Zhang Q, Wei Q, Zhang W (2006) Nitric oxide enhances salt tolerance in maize seedlings through increasing activities of proton-pump and Na+/H+ antiport in the tonoplast. Planta 224(3):545–555

    CAS  PubMed  Google Scholar 

  • Zhang H, Kim MS, Sun Y, Dowd SE, Shi H, Paré PW (2008) Soil bacteria confer plant salt tolerance by tissue-specific regulation of the sodium transporter HKT1. Mol Plant Microbe Interact 21(6):737–744

    PubMed  Google Scholar 

  • Zhang M, Fang Y, Liang Z, Huang L (2012) Enhanced expression of vacuolar H sup sup-ATPase subunit E in the roots is associated with the adaptation of italic Broussonetia papyrifera italic to salt stress. PLoS ONE 7:e48183. https://doi.org/10.1371/journal.pone.0048183

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang Y, Yao Q, Shi Y, Li X, Hou L, Xing G, Ahammed GJ (2020) Elevated CO2 improves antioxidant capacity, ion homeostasis, and polyamine metabolism in tomato seedlings under Ca(NO3)2-induced salt stress. Sci Hortic 273:109644

    CAS  Google Scholar 

  • Zhao L, Zhang F, Guo J, Yang Y, Li B, Zhang L (2004) Nitric oxide functions as a signal in salt resistance in the calluses from two ecotypes of reed. Plant Physiol 134(2):849–857

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao F, Song CP, He J, Zhu H (2007) Polyamines improve K+/Na+ homeostasis in barley seedlings by regulating root ion channel activities. Plant Physiol 145(3):1061–1072

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

Ms. Sadaf Choudhary and Kaiser Iqbal Wani are thankful to the University Grants Commission (Government of India) for providing research fellowship.

Author information

Authors and Affiliations

  1. Department of Botany, Aligarh Muslim University, Aligarh, 202 002, India

    Sadaf Choudhary, Kaiser Iqbal Wani, M. Naeem, M. Masroor A. Khan & Tariq Aftab

Authors
  1. Sadaf Choudhary
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kaiser Iqbal Wani
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. M. Naeem
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. M. Masroor A. Khan
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Tariq Aftab
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

TA conceived and designed the first draft, contributed to the revisions, and was the advisor of this project. SC, MN, and TA wrote the first draft of the manuscript with support from MMAK. KIW helped in revision and prepared the table/figures. All authors read and approved final version of manuscript.

Corresponding author

Correspondence to Tariq Aftab.

Ethics declarations

Conflict of interest

The authors declare that the submitted work was not carried out in the presence of any personal, professional, or financial relationships that could potentially be constructed as a conflict of interest.

Additional information

Handling Editor: Parvaiz Ahmad.

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

Choudhary, S., Wani, K.I., Naeem, M. et al. Cellular Responses, Osmotic Adjustments, and Role of Osmolytes in Providing Salt Stress Resilience in Higher Plants: Polyamines and Nitric Oxide Crosstalk. J Plant Growth Regul 42, 539–553 (2023). https://doi.org/10.1007/s00344-022-10584-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00344-022-10584-7

Keywords

Search

Navigation