Skip to main content

Advertisement

Log in

Nitric Oxide: A Ubiquitous Signal Molecule for Enhancing Plant Tolerance to Salinity Stress and Their Molecular Mechanisms

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

Abstract

Salinity is a major constraint of agricultural productivity globally and is recognized to be severely elevated by alterations in the climatic conditions. High salinity levels cause osmotic pressure and ionic imbalance and adversely affects plant’s morphological, physiological and biochemical aspects, which subsequently hampers plant growth or death of the plant. Furthermore, as alterations in soil properties lead to an acceleration in salinity levels, our concern of how plants cope with salinity stress is becoming progressively meaningful. In this context, various signaling moieties and cross-talk between several sensors and signal transduction pathways, are required to increase plant tolerance against salinity stress. To protect from salinity, plants secrete different signaling moieties that trigger several stress-adaptation responses and cause either plant acclimation or programmed cell death. Among these signaling molecules, nitric oxide (NO) is a multifaceted, small gaseous reactive moiety that regulates numerous plant developmental progressions and provides endurance to different abiotic factors, including salinity stress. NO is known to be significant for plants exposed to salinity stress. It improves plant potential to cope with salinity by boosting plant growth, photosynthetic activity, stomatal conductance, accumulation of compatible solutes, maintains ion homeostasis, and reverse oxidative damage by stimulating anti-oxidant defense apparatus. It also alters the expression of defense-associated genes, thereby influence the phenotypic response of plant genotypes. Thus, it was concluded that NO is a crucial signaling molecule which remarkably mitigate salinity-induced adverse effects in plants by regulating various developmental aspects in plants. The aim of the present review is to provide an overall update on the NO mediated salinity stress tolerance in plants including NO metabolism, signal transduction via inducing various genes and post-translational modifications (PTMs), plant growth, photosynthetic activity, mineral nutrition, anti-oxidant defense system, gene expression and its cross-talk with phytohormones and with hydrogen sulfide.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Adamu TA, Mun BG, Lee SU, Hussain A, Yun BW (2018) Exogenously applied nitric oxide enhances salt tolerance in rice (Oryza sativa L.) at seedling stage. Agronomy 8(12):276

    CAS  Google Scholar 

  • Ahanger MA, Tittal M, Mir RA, Agarwal RM (2017a) Alleviation of water and osmotic stress-induced changes in nitrogen metabolizing enzymes in Triticum aestivum L. cultivars by potassium. Protoplasma 254:1953–1963

    CAS  PubMed  Google Scholar 

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

    PubMed  PubMed Central  Google Scholar 

  • Ahanger MA, Qin C, Maodong Q, Dong XX, Ahmad P, Abd Allah EF, Zhang L (2019) Spermine application alleviates salinity induced growth and photosynthetic inhibition in Solanum lycopersicum by modulating osmolyte and secondary metabolite accumulation and differentially regulating antioxidant metabolism. Plant Physiol Biochem 144:1–13

    CAS  PubMed  Google Scholar 

  • Ahanger MA, Aziz U, Alsahli AA, Alyemeni MN, Ahmad P (2020) Influence of exogenous salicylic acid and nitric oxide on growth, photosynthesis, and ascorbate-glutathione cycle in salt stressed Vigna angularis. Biomolecules 10(1):42

    CAS  Google Scholar 

  • Ahlfors R, Brosché M, Kollist H, Kangasjärvi J (2009) Nitric oxide modulates ozone-induced cell death, hormone biosynthesis and gene expression in Arabidopsis thaliana. Plant J 58(1):1–12

    CAS  PubMed  Google Scholar 

  • Ahmad P, Abdel Latef AA, Hashem A, Abd Allah EF, Gucel S, Tran LSP (2016) Nitric oxide mitigates salt stress by regulating levels of osmolytes and antioxidant enzymes in chickpea. Front Plant Sci 7:347

    PubMed  PubMed Central  Google Scholar 

  • Ahmad P, Abass Ahanger M, Nasser Alyemeni M, Wijaya L, Alam P, Ashraf M (2018) Mitigation of sodium chloride toxicity in Solanum lycopersicum L. by supplementation of jasmonic acid and nitric oxide. J Plant Interact 13(1):64–72

    CAS  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 

  • Ali Q, Daud MK, Haider MZ, Ali S, Rizwan M, Aslam N, Ali I (2017) Seed priming by sodium nitroprusside improves salt tolerance in wheat (Triticum aestivum L.) by enhancing physiological and biochemical parameters. Plant Physiol Biochem 119:50–58

    CAS  PubMed  Google Scholar 

  • Alsaeedi AH, El-Ramady H, Alshaal T, El-Garawani M, Elhawat N, Almohsen M (2017) Engineered silica nanoparticles alleviate the detrimental effects of Na+ stress on germination and growth of common bean (Phaseolus vulgaris). Environ Sci Pollut Res 24(27):21917–21928

    CAS  Google Scholar 

  • Arasimowicz M, Floryszak-Wieczorek J (2007) Nitric oxide as a bioactive signalling molecule in plant stress responses. Plant Sci 172(5):876–887

    CAS  Google Scholar 

  • Arora D, Jain P, Singh N, Kaur H, Bhatla SC (2016) Mechanisms of nitric oxide cross-talk with reactive oxygen species scavenging enzymes during abiotic stress tolerance in plants. Free Radic Res 50(3):291–303

    CAS  PubMed  Google Scholar 

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

    CAS  Google Scholar 

  • Assaha DV, Ueda A, Saneoka H, Al-Yahyai R, Yaish MW (2017) The role of Na+ and K+ transporters in salt stress adaptation in glycophytes. Front Physiol 8:509

    PubMed  PubMed Central  Google Scholar 

  • Badri DV, Loyola-Vargas VM, Du J, Stermitz FR, Broeckling CD, Iglesias-Andreu L, Vivanco JM (2008) Transcriptome analysis of Arabidopsis roots treated with signaling compounds: a focus on signal transduction, metabolic regulation and secretion. New Phytol 179(1):209–223

    CAS  PubMed  Google Scholar 

  • Barroso JB, Corpas FJ, Carreras A, Sandalio LM, Valderrama R, Palma J, Del Río LA (1999) Localization of nitric-oxide synthase in plant peroxisomes. J Biol Chem 274(51):36729–36733

    CAS  PubMed  Google Scholar 

  • Begara-Morales JC, Chaki M, Valderrama R, Sánchez-Calvo B, Mata-Pérez C, Padilla MN, Barroso JB (2018) Nitric oxide buffering and conditional nitric oxide release in stress response. J Exp Bot 69(14):3425–3438

    CAS  PubMed  Google Scholar 

  • Beligni MV, Lamattina L (2001) Nitric oxide in plants: the history is just beginning. Plant Cell Environ 24(3):267–278

    CAS  Google Scholar 

  • Besson-Bard A, Gravot A, Richaud P, Auroy P, Duc C, Gaymard F, Wendehenne D (2009) Nitric oxide contributes to cadmium toxicity in Arabidopsis by promoting cadmium accumulation in roots and by up-regulating genes related to iron uptake. Plant Physiol 149(3):1302–1315

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bethke PC, Badger MR, Jones RL (2004) Apoplastic synthesis of nitric oxide by plant tissues. Plant Cell 16(2):332–341

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bhuyan MB, Hasanuzzaman M, Parvin K, Mohsin SM, Al Mahmud J, Nahar K, Fujita M (2020) Nitric oxide and hydrogen sulfide: two intimate collaborators regulating plant defense against abiotic stress. Plant Growth Regul 90(3):409–424

    CAS  Google Scholar 

  • Campos FV, Oliveira JA, Pereira MG, Farnese FS (2019) Nitric oxide and phytohormone interactions in the response of Lactuca sativa to salinity stress. Planta 250(5):1475–1489

    CAS  PubMed  Google Scholar 

  • Chakraborty N, Acharya K (2017) “NO way”! Says the plant to abiotic stress. Plant Gene 11:99–105

    CAS  Google Scholar 

  • Chen J, Wang WH, Wu FH, He EM, Liu X, Shangguan ZP, Zheng HL (2015) Hydrogen sulfide enhances salt tolerance through nitric oxide-mediated maintenance of ion homeostasis in barley seedling roots. Sci Rep 5:12516

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cooney RV, Harwood PJ, Custer LJ, Franke AA (1994) Light-mediated conversion of nitrogen dioxide to nitric oxide by carotenoids. Environ Health Perspect 102(5):460–462

    CAS  PubMed  PubMed Central  Google Scholar 

  • Corpas FJ, Palma JM (2018) Nitric oxide on/off in fruit ripening. Plant Biol 20(5):805–807

    CAS  PubMed  Google Scholar 

  • Corpas FJ, Leterrier M, Valderrama R, Airaki M, Chaki M, Palma JM, Barroso JB (2011) Nitric oxide imbalance provokes a nitrosative response in plants under abiotic stress. Plant Sci 181(5):604–611

    CAS  PubMed  Google Scholar 

  • Correa-Aragunde N, Graziano M, Lamattina L (2004) Nitric oxide plays a central role in determining lateral root development in tomato. Planta 218(6):900–905

    CAS  PubMed  Google Scholar 

  • Crawford NM (2006) Mechanisms for nitric oxide synthesis in plants. J Exp Bot 57(3):471–478

    CAS  PubMed  Google Scholar 

  • Culotta E, Koshland DE Jr (1992) NO news is good news. Science 258(5090):1862–1866

    CAS  PubMed  Google Scholar 

  • Da Silva CJ, Modolo LV (2018) Hydrogen sulfide: a new endogenous player in an old mechanism of plant tolerance to high salinity. Acta Botanica Brasilica 32(1):150–160

    Google Scholar 

  • Da Silva CJ, Fontes EPB, Modolo LV (2017) Salinity-induced accumulation of endogenous H2S and NO is associated with modulation of the antioxidant and redox defense systems in Nicotiana tabacum L. cv Havana. Plant Sci 256:148–159

    PubMed  Google Scholar 

  • Da Silva CJ, Mollica DC, Vicente MH, Peres LE, Modolo LV (2018) NO, hydrogen sulfide does not come first during tomato response to high salinity. Nitric Oxide 76:164–173

    Google Scholar 

  • David A, Yadav S, Bhatla SC (2010) Sodium chloride stress induces nitric oxide accumulation in root tips and oil body surface accompanying slower oleosin degradation in sunflower seedlings. Physiol Plant 140(4):342–354

    CAS  PubMed  Google Scholar 

  • Dean JV, Harper JE (1986) Nitric oxide and nitrous oxide production by soybean and winged bean during the in vivo nitrate reductase assay. Plant Physiol 82(3):718–723

    CAS  PubMed  PubMed Central  Google Scholar 

  • del Carmen Martínez-Ballesta M, Bastías E, Carvajal M (2008) Combined effect of boron and salinity on water transport: the role of aquaporins. Plant Signal Behav 3(10):844

    PubMed  PubMed Central  Google Scholar 

  • Dinler BS, Antoniou C, Fotopoulos V (2014) Interplay between GST and nitric oxide in the early response of soybean (Glycine max L.) plants to salinity stress. J Plant Physiol 171(18):1740–1747

    CAS  PubMed  Google Scholar 

  • Domingos P, Prado AM, Wong A, Gehring C, Feijo JA (2015) Nitric oxide: a multitasked signaling gas in plants. Mol Plant 8(4):506–520

    CAS  PubMed  Google Scholar 

  • Dong F, Simon J, Rienks M, Lindermayr C, Rennenberg H (2015) Effects of rhizopheric nitric oxide (NO) on N uptake in Fagus sylvatica seedlings depend on soil CO2 concentration, soil N availability and N source. Tree Physiol 35(8):910–920

    CAS  PubMed  Google Scholar 

  • Duan P, Ding F, Wang F, Wang BS (2007) Priming of seeds with nitric oxide donor sodium nitroprusside (SNP) alleviates the inhibition on wheat seed germination by salt stress. Zhi wu sheng li yu fen zi sheng wu xue xue bao. J Plant Physiol Mole Biol 33(3):244

    CAS  Google Scholar 

  • Egbichi I, Keyster M, Ludidi N (2014) Effect of exogenous application of nitric oxide on salt stress responses of soybean. S Afr J Bot 90:131–136

    CAS  Google Scholar 

  • Elkelish AA, Soliman MH, Alhaithloul HA, El-Esawi MA (2019) Selenium protects wheat seedlings against salt stress-mediated oxidative damage by up-regulating antioxidants and osmolytes metabolism. Plant Physiol Biochem 137:144–153

    CAS  PubMed  Google Scholar 

  • Fallah F, Nokhasi F, Ghaheri M, Kahrizi D, Beheshti Ale AA, Ghorbani T, Ansarypour Z (2017) Effect of salinity on gene expression, morphological and biochemical characteristics of Stevia rebaudiana Bertoni under in vitro conditions. Cell Mol Biol 63:102–106

    CAS  PubMed  Google Scholar 

  • Fan HF, Du CX, Ding L, Xu YL (2013) Effects of nitric oxide on the germination of cucumber seeds and antioxidant enzymes under salinity stress. Acta Physiol Plant 35(9):2707–2719

    CAS  Google Scholar 

  • Fang Y, Li J, Jiang J, Geng Y, Wang J, Wang Y (2017) Physiological and epigenetic analyses of Brassica napus seed germination in response to salt stress. Acta Physiol Plant 39(6):128

    Google Scholar 

  • Farhangi-Abriz S, Ghassemi-Golezani K (2018) How can salicylic acid and jasmonic acid mitigate salt toxicity in soybean plants? Ecotoxicol Environ Saf 147:1010–1016

    CAS  PubMed  Google Scholar 

  • Farnese FS, Menezes-Silva PE, Gusman GS, Oliveira JA (2016) When bad guys become good ones: the key role of reactive oxygen species and nitric oxide in the plant responses to abiotic stress. Front Plant Sci 7:471

    PubMed  PubMed Central  Google Scholar 

  • Fatma M, Khan NA (2014) Nitric oxide protects photosynthetic capacity inhibition by salinity in Indian mustard. J Funct Environ Bot 4(2):106–116

    Google Scholar 

  • Fatma M, Masood A, Per TS, Khan NA (2016a) Nitric oxide alleviates salt stress inhibited photosynthetic performance by interacting with sulfur assimilation in mustard. Front Plant Sci 7:521

    PubMed  PubMed Central  Google Scholar 

  • Fatma M, Masood A, Per TS, Rasheed F, Khan NA (2016b) Interplay between nitric oxide and sulfur assimilation in salt tolerance in plants. Crop J 4(3):153–161

    Google Scholar 

  • Foresi N, Correa-Aragunde N, Parisi G, Caló G, Salerno G, Lamattina L (2010) Characterization of a nitric oxide synthase from the plant kingdom: NO generation from the green alga Ostreococcus tauri is light irradiance and growth phase dependent. Plant Cell 22(11):3816–3830

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gadelha CG, de Souza Miranda R, Alencar NLM, Costa JH, Prisco JT, Gomes-Filho E (2017) Exogenous nitric oxide improves salt tolerance during establishment of Jatropha curcas seedlings by ameliorating oxidative damage and toxic ion accumulation. J Plant Physiol 212:69–79

    CAS  PubMed  Google Scholar 

  • Ghaly AE, Ramakrishnan VV (2015) Nitrogen sources and cycling in the ecosystem and its role in air, water and soil pollution: a critical review. J Pollut Eff Control. https://doi.org/10.4172/2375-4397.1000136

    Article  Google Scholar 

  • Gill SS, Hasanuzzaman M, Nahar K, Macovei A, Tuteja N (2013) Importance of nitric oxide in cadmium stress tolerance in crop plants. Plant Physiol Biochem 63:254–261

    CAS  PubMed  Google Scholar 

  • Grün S, Lindermayr C, Sell S, Durner J (2006) Nitric oxide and gene regulation in plants. J Exp Bot 57(3):507–516

    PubMed  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 P, Srivastava S, Seth CS (2017) 24-Epibrassinolide and sodium nitroprusside alleviate the salinity stress in Brassica juncea L. cv. Varuna through cross talk among proline, nitrogen metabolism and abscisic acid. Plant Soil 411(1–2):483–498

    CAS  Google Scholar 

  • Habib N, Ashraf M, Ahmad MSA (2010) Enhancement in seed germinability of rice (Oryza sativa L.) by pre-sowing seed treatment with nitric oxide (NO) under salt stress. Pak J Bot 42(6):4071–4078

    Google Scholar 

  • Habib M, Ashraf M, Shahbaz M (2013) Effect of exogenously applied nitric oxide on some key physiological attributes of rice (Oryza sativa L.) plants under salt stress. Pak J Bot 45(5):1563–1569

    CAS  Google Scholar 

  • Habib N, Akram MS, Javed MT, Azeem M, Ali Q, Shaheen HL, Ashraf M (2016) Nitric oxide regulated improvement in growth and yield of rice plants grown under salinity stress: antioxidant defense system. Appl Ecol Environ Res 14(5):91–105

    Google Scholar 

  • Hasanuzzaman M, Gill SS, Fujita M (2013a) Physiological role of nitric oxide in plants grown under adverse environmental conditions. In: Tuteja N, Gill SS (eds) Plant acclimation to environmental stress. Springer, New York, pp 269–322

    Google Scholar 

  • Hasanuzzaman M, Nahar K, Fujita M (2013b) Plant response to salt stress and role of exogenous protectants to mitigate salt-induced damages. In: Ahmad P, Azooz MM, Prasad MNV (eds) Ecophysiology and responses of plants under salt stress. Springer, New York, pp 25–87

    Google Scholar 

  • Hasanuzzaman M, Oku H, Nahar K, Bhuyan MB, Al Mahmud J, Baluska F, Fujita M (2018) Nitric oxide-induced salt stress tolerance in plants: ROS metabolism, signaling, and molecular interactions. Plant Biotechnol Rep 12(2):77–92

    Google Scholar 

  • Hayat S, Yadav S, Nasser Alyemeni M, Irfan M, Wani AS, Ahmad A (2013) Alleviation of salinity stress with sodium nitroprusside in tomato. Int J Veg Sci 19(2):164–176

    Google Scholar 

  • He Y, Tang RH, Hao Y, Stevens RD, Cook CW, Ahn SM, Pei ZM (2004) Nitric oxide represses the Arabidopsis floral transition. Science 305(5692):1968–1971

    CAS  PubMed  Google Scholar 

  • Hess DT, Matsumoto A, Kim SO, Marshall HE, Stamler JS (2005) Protein S-nitrosylation: purview and parameters. Nat Rev Mol Cell Biol 6(2):150–166

    CAS  PubMed  Google Scholar 

  • Huang X, von Rad U, Durner J (2002) Nitric oxide induces transcriptional activation of the nitric oxide-tolerant alternative oxidase in Arabidopsis suspension cells. Planta 215(6):914–923

    CAS  PubMed  Google Scholar 

  • Huang X, Stettmaier K, Michel C, Hutzler P, Mueller MJ, Durner J (2004) Nitric oxide is induced by wounding and influences jasmonic acid signaling in Arabidopsis thaliana. Planta 218(6):938–946

    CAS  PubMed  Google Scholar 

  • Jamali B, Eshghi S, Tafazoli E (2015) Mineral composition of ‘Selva’strawberry as affected by time of application of nitric oxide under saline conditions. Hortic Environ Biotechnol 56(3):273–279

    CAS  Google Scholar 

  • Jasid S, Galatro A, Villordo JJ, Puntarulo S, Simontacchi M (2009) Role of nitric oxide in soybean cotyledon senescence. Plant Sci 176(5):662–668

    CAS  Google Scholar 

  • Jayakannan M, Bose J, Babourina O, Rengel Z, Shabala S (2015) Salicylic acid in plant salinity stress signalling and tolerance. Plant Growth Regul 76:25–40

    CAS  Google Scholar 

  • Kataria S, Baghel L, Guruprasad KN (2017) Pre-treatment of seeds with static magnetic field improves germination and early growth characteristics under salt stress in maize and soybean. Biocatal Agric Biotechnol 10:83–90

    Google Scholar 

  • Kausar F, Shahbaz M, Ashraf M (2013) Protective role of foliar-applied nitric oxide in Triticum aestivum under saline stress. Turk J Bot 37(6):1155–1165

    CAS  Google Scholar 

  • Kaya C, Ashraf M, Sönmez O, Tuna AL, Aydemir S (2015) Exogenously applied nitric oxide confers tolerance to salinity-induced oxidative stress in two maize (Zea mays L.) cultivars differing in salinity tolerance. Turk J Agric for 39(6):909–919

    CAS  Google Scholar 

  • Ke X, Cheng Z, Ma W, Gong M (2013) Nitric oxide enhances osmoregulation of tobacco (Nicotiana tobacam L.) cultured cells under phenylethanoid glycosides (PEG) 6000 stress by regulating proline metabolism. Afr J Biotechnol 12(11):1257–1266

    CAS  Google Scholar 

  • Khan MN, Siddiqui MH, Mohammad F, Naeem M (2012) Interactive role of nitric oxide and calcium chloride in enhancing tolerance to salt stress. Nitric Oxide 27(4):210–218

    CAS  PubMed  Google Scholar 

  • Khan MIR, Asgher M, Khan NA (2014) Alleviation of salt-induced photosynthesis and growth inhibition by salicylic acid involves glycinebetaine and ethylene in mungbean (Vigna radiata L.). Plant Physiol Biochem 80:67–74

    CAS  PubMed  Google Scholar 

  • Khan MIR, Nazir F, Asgher M, Per TS, Khan NA (2015) Selenium and sulfur influence ethylene formation and alleviate cadmium-induced oxidative stress by improving proline and glutathione production in wheat. J Plant Physiol 173:9–18

    CAS  PubMed  Google Scholar 

  • Khator K, Shekhawat GS (2020) Nitric oxide mitigates salt-induced oxidative stress in Brassica juncea seedlings by regulating ROS metabolism and antioxidant defense system. 3Biotech 10(11):1–12

    Google Scholar 

  • Khoshbakht D, Asghari MR, Haghighi M (2018) Effects of foliar applications of nitric oxide and spermidine on chlorophyll fluorescence, photosynthesis and antioxidant enzyme activities of citrus seedlings under salinity stress. Photosynthetica 56(4):1313–1325

    CAS  Google Scholar 

  • Kong J, Dong Y, Xu L, Liu S, Bai X (2014) Effects of foliar application of salicylic acid and nitric oxide in alleviating iron deficiency induced chlorosis of Arachis hypogaea L. Bot Stud 55(1):9

    PubMed  PubMed Central  Google Scholar 

  • Kong X, Wang T, Li W, Tang W, Zhang D, Dong H (2016) Exogenous nitric oxide delays salt-induced leaf senescence in cotton (Gossypium hirsutum L.). Acta Physiol Plant 38(3):61

    Google Scholar 

  • Lin Y, Yang L, Paul M, Zu Y, Tang Z (2013) Ethylene promotes germination of Arabidopsis seed under salinity by decreasing reactive oxygen species: evidence for the involvement of nitric oxide simulated by sodium nitroprusside. Plant Physiol Biochem 73:211–218

    CAS  PubMed  Google Scholar 

  • Lindermayr C, Saalbach G, Durner J (2005) Proteomic identification of S-nitrosylated proteins in Arabidopsis. Plant Physiol 137(3):921–930

    CAS  PubMed  PubMed Central  Google Scholar 

  • Liu L, Hausladen A, Zeng M, Que L, Heitman J, Stamler JS (2001) A metabolic enzyme for S-nitrosothiol conserved from bacteria to humans. Nature 410(6827):490–494

    CAS  PubMed  Google Scholar 

  • Liu S, Dong Y, Xu L, Kong J (2014) Effects of foliar applications of nitric oxide and salicylic acid on salt-induced changes in photosynthesis and antioxidative metabolism of cotton seedlings. Plant Growth Regul 73(1):67–78

    CAS  Google Scholar 

  • Liu W, Li RJ, Han TT, Cai W, Fu ZW, Lu YT (2015) Salt stress reduces root meristem size by nitric oxide-mediated modulation of auxin accumulation and signaling in Arabidopsis. Plant Physiol 168(1):343–356

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ma NL, Lah WAC, Kadir NA, Mustaqim M, Rahmat Z, Ahmad A, Ismail MR (2018) Susceptibility and tolerance of rice crop to salt threat: physiological and metabolic inspections. PLoS ONE 13:e0192732

    PubMed  PubMed Central  Google Scholar 

  • Manai J, Kalai T, Gouia H, Corpas FJ (2014) Exogenous nitric oxide (NO) ameliorates salinity-induced oxidative stress in tomato (Solanum lycopersicum) plants. J Soil Sci Plant Nutr 14(2):433–446

    Google Scholar 

  • Marvasi M (2017) Potential use and perspectives of nitric oxide donors in agriculture. J Sci Food Agric 97(4):1065–1072

    CAS  PubMed  Google Scholar 

  • Misra AN, Misra M, Singh R (2011) Nitric oxide: a ubiquitous signaling molecule with diverse role in plants. Afr J Plant Sci 5(2):57–74

    CAS  Google Scholar 

  • Mur LA, Sivakumaran A, Mandon J, Cristescu SM, Harren FJ, Hebelstrup KH (2012) Haemoglobin modulates salicylate and jasmonate/ethylene-mediated resistance mechanisms against pathogens. J Exp Bot 63(12):4375–4387

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mur LA, Prats E, Pierre S, Hall MA, Hebelstrup KH (2013) Integrating nitric oxide into salicylic acid and jasmonic acid/ethylene plant defense pathways. Front Plant Sci 4:215

    PubMed  PubMed Central  Google Scholar 

  • Nabi RBS, Tayade R, Hussain A, Kulkarni KP, Imran QM, Mun BG, Yun BW (2019) Nitric oxide regulates plant responses to drought, salinity, and heavy metal stress. Environ Exp Bot 161:120–133

    CAS  Google Scholar 

  • Neill S, Barros R, Bright J, Desikan R, Hancock J, Harrison J, Wilson I (2008) Nitric oxide, stomatal closure, and abiotic stress. J Exp Bot 59(2):165–176

    CAS  PubMed  Google Scholar 

  • Pagnussat GC, Lanteri ML, Lamattina L (2003) Nitric oxide and cyclic GMP are messengers in the indole acetic acid-induced adventitious rooting process. Plant Physiol 132(3):1241–1248

    CAS  PubMed  PubMed Central  Google Scholar 

  • Palmieri MC, Sell S, Huang X, Scherf M, Werner T, Durner J, Lindermayr C (2008) Nitric oxide-responsive genes and promoters in Arabidopsis thaliana: a bioinformatics approach. J Exp Bot 59(2):177–186

    CAS  PubMed  Google Scholar 

  • Parani M, Rudrabhatla S, Myers R, Weirich H, Smith B, Leaman DW, Goldman SL (2004) Microarray analysis of nitric oxide responsive transcripts in Arabidopsis. Plant Biotechnol J 2(4):359–366

    CAS  PubMed  Google Scholar 

  • Perazzolli M, Dominici P, Romero-Puertas MC, Zago E, Zeier J, Sonoda M, Delledonne M (2004) Arabidopsis non-symbiotic hemoglobin AHb1 modulates nitric oxide bioactivity. Plant Cell 16(10):2785–2794

    CAS  PubMed  PubMed Central  Google Scholar 

  • Polverari A, Molesini B, Pezzotti M, Buonaurio R, Marte M, Delledonne M (2003) Nitric oxide-mediated transcriptional changes in Arabidopsis thaliana. Mol Plant Microbe Interact 16(12):1094–1105

    CAS  PubMed  Google Scholar 

  • Qiao W, Li C, Fan LM (2014) Cross-talk between nitric oxide and hydrogen peroxide in plant responses to abiotic stresses. Environ Exp Bot 100:84–93

    CAS  Google Scholar 

  • Ramadan AA, Abd Elhamid EM, Sadak MS (2019) Comparative study for the effect of arginine and sodium nitroprusside on sunflower plants grown under salinity stress conditions. Bull Natl Res Cent 43(1):118

    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 

  • Richards SL, Wilkins KA, Swarbreck SM, Anderson AA, Habib N, Smith AG, Davies JM (2015) The hydroxyl radical in plants: from seed to seed. J Exp Bot 66(1):37–46

    CAS  PubMed  Google Scholar 

  • Romero-Puertas MC, Campostrini N, Mattè A, Righetti PG, Perazzolli M, Zolla L, Delledonne M (2008) Proteomic analysis of S-nitrosylated proteins in Arabidopsis thaliana undergoing hypersensitive response. Proteomics 8(7):1459–1469

    CAS  PubMed  Google Scholar 

  • Rümer S, Gupta KJ, Kaiser WM (2009) Plant cells oxidize hydroxylamines to NO. J Exp Bot 60(7):2065–2072

    PubMed  PubMed Central  Google Scholar 

  • Saddhe AA, Malvankar MR, Karle SB, Kumar K (2019) Reactive nitrogen species: paradigms of cellular signaling and regulation of salt stress in plants. Environ Exp Bot 161:86–97

    CAS  Google Scholar 

  • Salahuddin M, Nawaz F, Shahbaz M, Naeem M, Zulfiqar B, Shabbir RN, Hussain RA (2017) Effect of exogenous nitric oxide (NO) supply on germination and seedling growth of mungbean (cv. Nm-54) under salinity stress. Legume Res 40(5):846–852

    Google Scholar 

  • Sami F, Faizan M, Faraz A, Siddiqui H, Yusuf M, Hayat S (2018) Nitric oxide-mediated integrative alterations in plant metabolism to confer abiotic stress tolerance, NO cross-talk with phytohormones and NO-mediated post translational modifications in modulating diverse plant stress. Nitric Oxide 73:22–38

    CAS  PubMed  Google Scholar 

  • Sanz-Luque E, Ocaña-Calahorro F, de Montaigu A, Chamizo-Ampudia A, Llamas Á, Galván A, Fernández E (2015) THB 1, a truncated hemoglobin, modulates nitric oxide levels and nitrate reductase activity. Plant J 81(3):467–479

    CAS  PubMed  Google Scholar 

  • Sehar Z, Masood A, Khan NA (2019) Nitric oxide reverses glucose-mediated photosynthetic repression in wheat (Triticum aestivum L.) under salt stress. Environ Exp Bot 161:277–289

    CAS  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 

  • Shiraz M, Sami F, Siddiqui H, Yusuf M, Hayat S (2020) Interaction of auxin and nitric oxide improved photosynthetic efficiency and antioxidant system of Brassica juncea plants under salt stress. J Plant Growth Regul. https://doi.org/10.1007/s00344-020-10268-0

    Article  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 

  • Singh R, Parihar P, Singh S, Singh MPVVB, Singh VP, Prasad SM (2017) Micro RNAs and nitric oxide cross talk in stress tolerance in plants. Plant Growth Regul 83(2):199–205

    CAS  Google Scholar 

  • Talaat NB, Ghoniem AE, Abdelhamid MT, Shawky BT (2015) Effective microorganisms improve growth performance, alter nutrients acquisition and induce compatible solutes accumulation in common bean (Phaseolus vulgaris L.) plants subjected to salinity stress. Plant Growth Regul 75:281–295

    CAS  Google Scholar 

  • Terrile MC, París R, Calderón-Villalobos LI, Iglesias MJ, Lamattina L, Estelle M, Casalongué CA (2012) Nitric oxide influences auxin signaling through S-nitrosylation of the Arabidopsis TRANSPORT INHIBITOR RESPONSE 1 auxin receptor. Plant J 70(3):492–500

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tiwari S, Verma N, Singh VP, Prasad SM (2019) Nitric oxide ameliorates aluminium toxicity in Anabaena PCC 7120: regulation of aluminium accumulation, exopolysaccharides secretion, photosynthesis and oxidative stress markers. Environ Exp Bot 161:218–227

    CAS  Google Scholar 

  • Tun NN, Santa-Catarina C, Begum T, Silveira V, Handro W, Floh EIS, Scherer GF (2006) Polyamines induce rapid biosynthesis of nitric oxide (NO) in Arabidopsis thaliana seedlings. Plant Cell Physiol 47(3):346–354

    CAS  PubMed  Google Scholar 

  • Wang Y, Li L, Cui W, Xu S, Shen W, Wang R (2012) Hydrogen sulfide enhances alfalfa (Medicago sativa) tolerance against salinity during seed germination by nitric oxide pathway. Plant Soil 351(1–2):107–119

    CAS  Google Scholar 

  • Wang X, Hou C, Liu J, He W, Nan W, Gong H, Bi Y (2013) Hydrogen peroxide is involved in the regulation of rice (Oryza sativa L.) tolerance to salt stress. Acta Physiol Plant 35(3):891–900

    CAS  Google Scholar 

  • Wu X, Zhu W, Zhang H, Ding H, Zhang HJ (2011) Exogenous nitric oxide protects against salt-induced oxidative stress in the leaves from two genotypes of tomato (Lycopersicom esculentum Mill.). Acta Physiol Plant 33(4):1199–1209

    CAS  Google Scholar 

  • Wulff A, Oliveira HC, Saviani EE, Salgado I (2009) Nitrite reduction and superoxide-dependent nitric oxide degradation by Arabidopsis mitochondria: influence of external NAD (P) H dehydrogenases and alternative oxidase in the control of nitric oxide levels. Nitric Oxide 21(2):132–139

    CAS  PubMed  Google Scholar 

  • Yadu S, Dewangan TL, Chandrakar V, Keshavkant S (2017) Imperative roles of salicylic acid and nitric oxide in improving salinity tolerance in Pisum sativum L. Physiol Mol Biol Plants 23(1):43–58

    CAS  PubMed  Google Scholar 

  • Yamasaki H, Sakihama Y (2000) Simultaneous production of nitric oxide and peroxynitrite by plant nitrate reductase: in vitro evidence for the NR-dependent formation of active nitrogen species. FEBS Lett 468(1):89–92

    CAS  PubMed  Google Scholar 

  • Yamasaki H, Sakihama Y, Takahashi S (1999) An alternative pathway for nitric oxide production in plants: new features of an old enzyme. Trends Plant Sci 4(4):128–129

    CAS  PubMed  Google Scholar 

  • Zago E, Morsa S, Dat JF, Alard P, Ferrarini A, Inzé D, Van Breusegem F (2006) Nitric oxide-and hydrogen peroxide-responsive gene regulation during cell death induction in tobacco. Plant Physiol 141(2):404–411

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang L, Wang Y, Zhao L, Shi S, Zhang L (2006) Involvement of nitric oxide in light-mediated greening of barley seedlings. J Plant Physiol 163(8):818–826

    CAS  PubMed  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 

  • Zheng C, Jiang D, Liu F, Dai T, Liu W, Jing Q, Cao W (2009) Exogenous nitric oxide improves seed germination in wheat against mitochondrial oxidative damage induced by high salinity. Environ Exp Bot 67(1):222–227

    CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Contributions

Conceived and designed the article: JS, PCR, RP, and DK; wrote the draft manuscript: SB, SS, VG, DSD, and SJ; and reviewed and edited the manuscript: JS, RP, PCR, RP and DSD. All authors have read and approved the manuscript.

Corresponding authors

Correspondence to Ram Prasad or Joginder Singh.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Handling editor: Rhonda Peavy.

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

Bhardwaj, S., Kapoor, D., Singh, S. et al. Nitric Oxide: A Ubiquitous Signal Molecule for Enhancing Plant Tolerance to Salinity Stress and Their Molecular Mechanisms. J Plant Growth Regul 40, 2329–2341 (2021). https://doi.org/10.1007/s00344-021-10394-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00344-021-10394-3

Keywords

Navigation