Abstract
It is a well-established fact that nitric oxide (NO) is a multifaceted signaling molecule, which plays diverse role in organisms. In the past two decades, various pieces of evidence have been documented to address its involvement under various abiotic and biotic stress responses in plant systems. One of the prime consequences of abiotic stress is an increase in the cellular concentration of reactive oxygen species (ROS) and reactive nitrogen species such as nitric oxide (NO) peroxynitrite (ONOO), and nitrogen dioxide (NO2). But how the pathways of these reactive oxygen species (ROS) and hormones are integrated with NO and how the signals are relayed in biological systems remain incoherent and scanty in the literature. Thus, this review attempts to address NO-mediated ROS metabolism, defense responses, and its interactions with other bioactive molecules.
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Abbreviations
- NaCl:
-
Sodium chloride
- NO:
-
Nitric oxide
- SNP:
-
Sodium nitroprusside
- cPTIO:
-
2-Phenyl-4,4,5,5,-tetramethylimidazoline 1-oxyl 3-oxide
- LNAME:
-
Nω-Nitro-L-arginine methyl ester hydrochloride (inhibitor of mammalian nitric oxide synthase)
- ST:
-
Sodium tungstate (inhibitor of nitrate reductase)
- ROS:
-
Reactive oxygen species
- ABA:
-
Abscisic acid
- AUX:
-
Auxin
- SA:
-
Salicylic acid
- GA:
-
Gibberellic acid
- CYT:
-
Cytokinin
- ETH:
-
Ethylene
- JA:
-
Jasmonic acid
- MAPKs:
-
Mitogen-activated protein kinases
- NADH:
-
Nicotinamide adenine dinucleotide hydrogen
- NADPH:
-
Nicotinamide adenine dinucleotide phosphate hydrogen
- FAD:
-
Flavin adenine dinucleotide
- FMN:
-
Flavin mono nucleotide
- ATP:
-
Adenosine triphosphate
- cADPR:
-
Cyclic adenosine 5′-diphosphate ribose
- CaM:
-
Calmodulin
- CMLs:
-
Calmodulin-like proteins
References
Abogadallah GM (2010) Antioxidative defense under salt stress. Plant Signal Behav 5(4):369–374
Acosta-Motos JR, Ortuño MF, Bernal-Vicente A, Diaz-Vivancos P, Sanchez-Blanco MJ, Hernandez JA (2017) Responses to salt stress: Adaptive mechanisms. Agronomy 7:18. https://doi.org/10.3390/agronomy7010018
Ahammed GI, Li Y, Li X et al (2018) Epigallocatechin-3-Gallate alleviates salinity-retarded seed germination and oxidative stress in tomato. J Plant Growth Regul 37:1349–1356
Ahmad P, Abdel Latef AA, Hashem A, Abd Allah EF, Gucel S, Tran LS (2016) Nitric oxide mitigates salt stress by regulating levels of osmolytes and antioxidant enzymes in chickpea. Front Plant Sci 7:347
Ahmad P, Ahanger MA, Alyemenia MN, Wijayaa 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
Ashraf MA, Rasheed R, Hussain I, Iqbal M, Haider MQ, Parveen S, Sajid MA (2015) Hydrogen peroxide modulates antioxidant system and nutrient relation in maize. Zea mays L. https://doi.org/10.1080/03650340.2014.938644
Ávila AC, Ochoa J, Proaño K, Martínez MC (2019) Jasmonic acid and nitric oxide protects naranjilla Solanum quitoense against infection by Fusarium oxysporum f sp quitoense by eliciting plant defense responses. Physiol Mol Plant P 106: 129–136
Begara-Morales JC, Chaki M, Valderrama R, Sánchez-Calvo B, Mata-Pérez C, Padilla MN, Corpas FJ, Barroso JB (2018) Nitric oxide buffering and conditional nitric oxide release in stress response. J Exp Bot 69:3425–3438
Besson-Bard A, Pugin A, Wendehenne D (2008) New insights into nitric oxide signaling in plants. Ann Rev Plant Biol 59:21–39
Besson-Bard A, Astier J, Rasul S, Wawer I, Dubreuil-Maurizi C, Jeandroz S, Wendehenne D (2009) Current view of nitric oxide-responsive genes in plants. Plant Sci 177:302–309
Bethke PC, Badger MR, Jones RL (2004) Apoplastic synthesis of nitric oxide by plant tissues. Plant Cell 16:332–341
Bray EA (2002) Abscisic acid regulation of gene expression during water-deficit stress in the era of the Arabidopsis genome. Plant Cell Environ 25:153–161
Campbell MG, Smith BC, Potter CS, Carragher B, Marletta MA (2014) Molecular architecture of mammalian nitric oxide synthases. PNAS 111(35):3614–3623
Castello FD, Nejamkin A, Cassia R, Correa-Aragunde N, Fernández H, Foresi N, Lombardo C, Ramirez L, Lamattina L (2019) The era of nitric oxide in plant biology: Twenty years tying up loose ends. Nitric Oxide 85:17–27
Cheng G, Yang E, Lu W, Jia Y, Jiang Y, Duan X (2009) Effect of nitric oxide on ethylene synthesis and softening of banana fruit slice during ripening. J Agric Food Chem 57:5799–5804
Chen K, Song L, Rao B, Zhu T, Zhang YT (2010) Nitric oxide plays a role as the second messenger in the ultraviolet-B irradiated green alga Chlorella pyrenoidosa. Folia Microbiol (Praha) 55:53–60
Chen J, Wang WH, Wu FH (2015) Hydrogen sulfide enhances salt tolerance through nitric oxide-mediated maintenance of ion homeostasis in barley seedling roots. Sci Rep 5:1–19
Clarke A, Desikan R, Hurst RD, Hancock JT, Neil SJ (2000) NO way back nitric oxide and programmed cell death in Arabidopsis thaliana suspension cultures. Plant J 24:667–677
Corpas FJ (2016) Reactive nitrogen species (RNS) in plants under physiological and adverse environmental conditions: current view. Prog Botany 78:97–119
Corpas FJ, Barroso JB (2015) Nitric oxide from a “green” perspective. Nitric Oxide 45:15–1926
Corpas FJ, Barroso JB (2017) Lead-induced stress, which triggers the production of nitric oxide (NO) and superoxide anion (O2.−) in Arabidopsis peroxisomes, affects catalase activity. Nitric Oxide 68:103–110
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 184:9–14
Corpas FJ, Barroso JB, Palma JM, Rodriguez-Ruiz M (2017) Plant peroxisomes: a nitro-oxidative cocktail. Redox Biol 11:535–542
Corpas FJ, del Rio LA, Palma JM (2019) Plant peroxisomes at the crossroad of NO and H2O2 metabolism. J Integr Plant Biol. https://doi.org/10.1111/jipb.12772
Crawford NM, Guo FQ (2005) New insights into nitric oxide metabolism and regulatory functions. Trends Plant Sci 10:195–200
da Silva CJ, Modolo LV (2018) Hydrogen sulfide: A new endogenous player in an old mechanism of plant tolerance to high salinity. Acta Bot Bras 32(1):150–216
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 140:342–354
Davière J, Achard P (2015) A pivotal role of dellas in regulating multiple hormone signals: review article. Mol Plant. https://doi.org/10.1016/j.molp.2015.09.011
de Lucas M, Davie`re JM, Rodrı´guez-Falco´ M, Pontin M, Iglesias-Pedraz JM, Lorrain S, Fankhauser C, Bla´ zquez MA, Titarenko E, Prat S (2008) A molecular framework for light and gibberellin control of cell elongation. Nature 451:480–484
Delledonne M (2005) NO news is good news for plants. Curr Opin Plant Biol 8:390–396
Delledonne M, Xia Y, Dixon RA, Lamb C (1998) Nitric oxide functions as a signal in plant disease resistance. Nature 394:585–588
Delledonne M, Zeier J, Marocco A, Lamb C (2001) Signal interactions between nitric oxide and reactive oxygen intermediates in the plant hypersensitive disease resistance response. Proc Natl Acad Sci USA 98:13454–13459
Dong YJ, Wang ZL, Zhang JW, Liu S, He HL, He MR (2015) Interaction effects of nitric oxide and salicylic acid in alleviating salt stress of Gossypium hirsutumL. J Soil Sci Plant Nutr 5(3):561–573
Duan Q, Kita D, Johnson EA, Aggarwal M, Gates L, Wu HM, Cheung AY (2014) Reactive oxygen species mediate pollen tube rupture to release sperm for fertilization in Arabidopsis. Nat Commun. https://doi.org/10.1038/ncomms4129
Durner J, Wendehenne D, Klessig DF (1998) Defence gene induction in tobacco by nitric oxide, cyclic GMP, and cyclic ADP-ribose. Proc Natl Acad Sci USA 95:10328–10333
Fan HF, Du CX, Guo SR (2013) Nitric oxide enhances salt tolerance in cucumber seedlings by regulating free polyamine content. Environ Exp Bot 86:52–59
Farhangi-Abriz S, Ghassemi-Golezani K (2019) Jasmonates: Mechanisms and functions in abiotic stress tolerance of plants. Biocatal Agric Biotechnol. https://doi.org/10.1016/j.bcab.2019.101210
Farooq M, Hussain M, Wakeel A, Siddique HM (2015) Salt stress in maize: effects, resistance mechanisms, and management. A review. Agron Sustain Dev 35(2):461–481
Fernández-Marcos M, Sanz L, Lewis DR, Muday GK, Lorenzo O (2011) Nitric oxide causes root apical mersitem defects and growth inhibition while reducing PIN-FORMED 1 (PIN1)- dependent acropetal auxin transport. Proc Natl Acad Sci USA 108:18506–18511
Foissner I, Wendehenne D, Langebartels C, Durner J (2000) In vivo imaging of an elicitor-induced nitric oxide burst in tobacco. Plant J 23:817–824
Food and agriculture organization of united nations (2015) Status of the World’s Soil Resources | Main Report
Foresi N, Correa- Aragunde N, Parisi G, Calo 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 22:3816–3830
Freschi L (2013) Nitric oxide and phytohormone interactions: current status and perspectives. Front Plant Sci 4:398
Garcı́á-Mata C, Lamattina L (2001) Nitricoxide induces stomatal closure and enhances the adaptive plant responses against drought stress. Plant Physiol 26(3):1196–1204
Garcia-Mata C, Gay R, Sokolovski S, Hills A, Lamattina L, Blatt MR (2003) Nitric oxide regulates K+ and Cl– channels in guard cells through a subset of abscisic acid-evoked signalling pathways. Proc Natl Acad Sci USA 100:11116–11121
Gomes MAC, Pestana IA, Santa-Catarina C, Hauser-Davis RA, Suzuki MS (2017) Salinity effects on photosynthetic pigments, proline, biomass and nitric oxide in Salvinia auriculata Aubl. Acta Limnol Bras 29:9
Goretski JT, Hollocher TC (1988) Trapping of nitric-oxide produced during denitrification by extracellular hemoglobin. J Biol Chem 263:2316–2323
Guo FQ, Okamoto NI, Crawford NM (2003) Identification of a plant nitric oxide synthase gene involved in hormonal signaling. Science 302:100–103
Gupta KJ, Stoimenova M, Kaiser WM (2005) In higher plants, only root mitochondria, but not leaf mitochondria reduce nitrite to NO, in vitro and in situ. J Exp Bot 56:2601–2609
Gupta KJ, Fernie AR, Kaiser WM, van Dongen JT (2011) On the origins of nitric oxide. Trends Plant Sci 16:160–168
Hasanuzzaman M, Oku H, Nahar K, Borhannuddin Bhuyan MHM, 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 12:77–92. https://doi.org/10.1007/s11816-018-0480-0
Horchani F, Prevot M, Boscari A, Evangelisti E, Meilhoc E, Bruand C, Raymond P, Boncompagni E, Aschi-Smiti S, Puppo A, Brouquisse R (2011) Both plant and bacterial nitrate reductases contribute to nitric oxide production in Medicago truncatula nitrogen-fixing nodules. Plant Physiol 155:1023–1036
Hossain MA, Bhattacharjee S, Armin S, Qian P, Xin W, Li H, Burritt DJ, Tran FM (2015) Hydrogen peroxide priming modulates abiotic oxidative stress tolerance: insights from ROS detoxification and scavenging. Front Plant Sci. https://doi.org/10.3389/fpls.2015.00420
Hossain MS, Dietz KJ (2016) Tuning of redox regulatory mechanisms, reactive oxygen species and redox homeostasis under salinity stress. Front Plant Sci. https://doi.org/10.3389/fpls.2016.00548
Husain T, FatimaA SM, Singh S, Sharma A, Prasad SM, Singh VP (2020) Abrief appraisal of ethylene signaling under abioticstress in plants. Plant Signal Behav. https://doi.org/10.1080/15592324.2020.1782051
Hung KT, Kao CH (2005) Nitric oxide counteracts the senescence of rice leaves induced by hydrogen peroxide. Bot Bull Acad Sin 146:21–28
Jagodzik P, Tajdel-Zielinska M, Ciesla A, Marczak M, Ludwikow A (2018) Mitogen activated protein kinase cascades in plant hormone signaling. Front Plant Physiol. https://doi.org/10.3389/fpls.2018.01387
Jamil A, Riaz S, Ashraf M, Foolad MR (2011) Gene expression profiling of plants under salt stress. Crit Rev Plant Sci 30(5):435–458
Jeandroz S, Lamotte O, Astier J, Rasul S, Trapet P, Besson-Bard A, Bourque S, Nicolas-Frances V, Ma W, Berkowitz GA, Wendehenne D (2013) There’s more to the picture than meets the eye: nitric oxide cross talk with Ca2+ signaling. Plant Physiol 163:459–470
Jeandroz S, Wipf D, Stuehr DJ, Lamattina L, Melkonian M, Tian Z, Zhu Y, Carpenter EJ, Wong GK, Wendehenne D (2016) Occurrence, structure, and evolution of nitric oxide synthase-like proteins in the plant kingdom. Signal Sci. https://doi.org/10.1126/scisignal.aad4403
Kaya C, Ashraf M, Sonmez O (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 39:909–919
Klepper L (1979) Nitric-oxide (NO) and nitrogen-dioxide (NO2) emissions from herbicide-treated soybean plants. Atmos Envirn 13:537–542
Kolbert Z, Barroso JB, Brouquisse R, Corpas FJ, Gupta KJ, Lindermayr C, Loake GJ, Palma JM, Petřivalský M, Wendehenne D, Hancock JT (2019) A forty year journey: The generation and roles of NO in plants. Nitric Oxide 93:53–70
Kopyra M, Gwozdz EA (2003) Nitric oxide stimulates seed germination and counteracts the inhibitory effect of heavy metal and salinity on root growth of Lupinus luteus. Plant Physiol Biochem 41:1011–1017. https://doi.org/10.1016/j.plaphy.2003.09.003
Kovacs I, Durner J, Lindermayr C (2015) Crosstalk between nitric oxide and glutathione is required for non expressor of pathogenesis related genes 1 (NPR1) dependent defense signaling in Arabidopsis thaliana. New Phytol 208:860–872
Kumar D, Kalita P (2017) Reducing postharvest losses during storage of grain crops to strengthen food security in developing countries. Foods. https://doi.org/10.3390/foods6010008
Lamattina L, Garcia-Mata C, Graziano M, Pagnussat G (2003) Nitric oxide: the versatility of an extensive signal molecule. Annu Rev Plant Biol 54:109–136
Lamotte O, Gould K, Lecourieux D, Sequeira-Legrand A, Lebrun-Garcia A, Durner J, Pugin A, Wendehenne D (2004) Analysis of nitric oxide signalling functions in tobacco cells challenged by the elicitor cryptogein. Plant Physio1 35:516–529
Le TN, McQueen-Mason SJ (2006) Desiccation-tolerant plants in dry environments. Rev Environ Sci Bio 5:269–279
Leshem YY, Haramaty E (1996) The characterization and contrasting effects of the nitric oxide free radical in vegetative stress and senescence of Pisum sativum Linn. foliage. J Plant Physiol 148:258–263
Li Y, Gao L, Han R (2016) Endogenous nitric oxide mediates He-Ne laser-induced adaptive responses in salt stressed-tall fescue leaves. Biosci Biotechnol Biochem 80(10):1887–1897
Li K, Zhang L, Ahammed GI, Li Y, Wei J, Han ML (2019) Salicylic acid acts upstream of nitric oxide in elevated carbon dioxide-induced flavonoid biosynthesis in tea plant (Camellia sinensis L.). Environ Exp Bot 161:367–374
Li X, Zhang L, Ahammed GJ, Li Z, Wei J, Shen C, Yan P, Zhang L, Han W (2017) Nitric oxide mediates brassinosteroid-induced flavanoid biosynthesis in Camelia sinensis L. J Plant Physiol 214:145–151
Lin YC, Chang-Chien GP, Chiang PC, Chen WH, Lin YC (2013) Multivariate analysis of heavy metal contaminations in seawater and sediments from a heavily industrialized harbor in Southern Taiwan. Mar Pollut Bull 76:266–275
Liu ZJ, Guo YK, Bai JO (2010a) Exogenous hydrogen peroxide changes antioxidant enzyme activity and protects ultrastructure in leaves of two cucumber ecotypes under osmotic stress. J Plant Growth Regul 29:171–183
Liu XM, Kim CE, Kim KC, Nguyen XC, Han RI, Jung MS (2010b) Cadmium activates Arabidopsis MPK3 and MPK6 via accumulation of reactive oxygen species. Phytochemistry 71:614–618
Liu WZ, Kong DD, Gu XX, Gao HB, Wang JZ, Xia M, He YK (2013) Cytokinins can act as suppressors of nitric oxide in Arabidopsis. Proc Natl Acad Sci USA 110:1548–1553
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 168:343–356
Liu R, Shi L, Zhu T, Yang T, Ren A, Zhu J, Zhao MW (2018) Cross-talk between nitric oxide and calcium-calmodulin regulate ganoderic acid biosynthesis in Ganoderma lucidum under heat stress. Appl Environ Microbiol. https://doi.org/10.1128/AEM.00043-18
Lv X, Ge S, Ahammed GJ, Xiang X, Guo Z, Yu J, Zhou Y (2017) Crosstalk between nitric oxide and MPK1/2 mediates cold acclimation-induced chilling tolerance in tomato. Plant Cell Physiol 58(11):1963–1975
Mallick N, Rai LC, Mohn FH, Soeder CJ (1999) Studies on nitric oxide (NO) formation by the greet alga Scenedesmus obliquus and the diazotrophic cyanobacterium Anabaena Doliolum. Chemosphere 39:1601–1610
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 14:433–446
Metternicht GI, Zinck JA (2003) Remote sensing of soil salinity: potentials and constraints. Remote Sens Environ 85:1–20
Molassiotis A, Job D, Ziogas V et al (2016) Citrus plants: a model system for unlocking the secrets of NO and ROS-inspired priming against salinity and drought. Front Plant Sci. https://doi.org/10.3389/fpls.2016.00229
Moreau M, Lee GI, Wang Y, Crane BR, Klessig DF (2008) AtNOS/AtNOA1 is a functional Arabidopsis thalianc cGTPase and not a nitric-oxide synthase. J Biol Chem 283(47):32957–32967
Mostofa MG, Saegusa D, Fujita M, Tran LSP (2015) Hydrogen sulfide regulates salt tolerance in rice by maintaining Na+/K+ balance, mineral homeostasis and oxidative metabolism under excessive salt stress. Front Plant Sci. https://doi.org/10.3389/fpls.2015.01055
Mukherjee S (2019) Recent advancements in the mechanism of nitric oxide signaling associated with hydrogen sulfide and melatonin crosstalk during ethylene-induced fruit ripening in plants. Nitric Oxide 82:25–34
Munns R (2002) Comparative physiology of salt and water stress. Plant Cell Environ 25:239–250
Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–801
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. https://doi.org/10.3389/fpls.2013.00215
Nabi RBS, Tayade R, Hussain A, Kulkarni KP, Imran QM, Mun B, Yun B (2019) Nitric oxide regulates plant responses to drought, salinity, and heavy metal stress. Environ Exp Bot 161:120–133
Navarre DA, Wendehenne D, Durner J, Noad R, Klessig DF (2000) Plant Physiol 122:573–582
Nawaz F, Shabbir RN, Shahbaz M, Majeed S, Raheel M, Hassan W, Sohail MA (2017) Cross talk between nitric oxide and phytohormones regulate plant development during abiotic stresses, in Phytohormones-Signaling Mechanisms and Crosstalk in Plant Development and Stress Responses. InTech. https://doi.org/10.5772/intechopen.69812
Ninnemann H, Maier J (1996) Indications for the occurrence of nitric oxide synthases in fungi and plants and the involvement in photoconidiation of Neurospora crassa. Photochem Photobiol 64:393–398
Niu L, Yu J, Liao W, Yu J, Zhang M, Dawuda MM (2017) Calcium and calmodulin are involved in nitric oxide-induced adventitious rooting of cucumber under simulated osmotic stress. Front Plant Sci. https://doi.org/10.3389/fpls.2017.01684
Palmer RMJ, Ferrige AG, Moncada S (1987) Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor. Nature 327:524–526
Parihar P, Singh S, Singh R, Singh VP, Prasad SM (2015) Effect of salinity stress on plants and its tolerance strategies: a review. Environ Sci Pollut Res 22:4056–4075
Patel BB, Dave RS (2011) Studies on infiltration of saline–alkali soils of several parts of Mehsana and Patan districts of north Gujarat. J Appl Technol Environ Sanitat. 1(1):87–92
Prakash V, Singh VP, Tripathi DK, Sharma S, Corpas FC (2019) Crosstalk between nitric oxide (NO) and abscisic acid (ABA) signalling molecules in higher plants. Environ Exp Bot 161:41–49
Prochazkova D, Haisel D, Pavlikova D (2014) Nitric oxide biosynthesis in plants-the short overview. Plant Soil Environ 60:129–134
Qiao WH, Xiao SH, Yu L, Fan LM (2009) Expression of a rice gene OsNOA1 re-establishes nitric oxide synthesis and stress-related gene expression for salt tolerance in Arabidopsis nitric oxide-associated 1 mutant Atnoa1. Environ Exp Bot 65:90–98
Rai KK, Rai N, Rai SP (2018) Salicylic acid and nitric oxide alleviate high temperature induced oxidative damage in Lablab purpureus L plants by regulating bio-physical processes and DNA methylation. Plant Physiol Biochem 128:72–88
Rengasamy P (2006) World salinization with emphasis on Australia. J Exp Bot 57:1017–1023
Rockel P, Strube F, Rockel A, Wlldt J, Kaiser WM (2002) Regulation of nitric oxide (NO) production by plane nitrate reductase in vivo and in vitro. J Exp Hot 53(366):103–110
Ross C, Kupper FC, Jacobs RS (2006) Involvement of reactive oxygen species and reactive nitrogen species in the wound response of Dasycladus vermicularis. Chem Biol 13:353–364
Rubio F, Alemán F, Nieves-Cordones M, Martínez V (2010) Studies on Arabidopsis double mutants disclose the range of concentrations at which AtHAK5, AtAKT1 and unknown systems mediate K+ uptake. Physiol Plant 139:220–228
Saddhe AA, Malvankar MR, Karle SB, Kumar K (2018) Reactive Nitrogen Species: Paradigms of Cellular Signaling and Regulation of Salt Stress in Plants. Environ Exp Bot https://doi.org/10.1016/j.envexpbot.2018.11.010
Sakihama Y, Nakamura S, Yamasaki H (2002) Nitric oxide production mediated by nitrate reductase in the green alga Chlamydomonas reinhardtii: an alternative NO production pathway in photosynthetic organisms. Plan Cell Physiol 43(3):7290–7297
Sami F, Faizan F, Faraz A, Siddiqui H, Yusuf M, Hayat S (2018) Nitric oxide-mediated integrative alterations in plant metabolism to confer abiotic stress tolerance, NO crosstalk with phytohormones and NO-mediated post translational modifications in modulating diverse plant stress. Nitric Oxide 73:22–38
Santner A, Calderon- Villalobos LI, Estelle M (2009) Plant hormones are versatile chemical regulators of plant growth. Nat Chem Biol 5:301–307
Santolini J, André F, Jeandroz S, Wendehenne D (2017) Nitric oxide synthase in plants: where do we stand? Nitric Oxide 63:30–38
Sanz L, FernándezMarcos M, Modrego A, Lewis DR, Muday GK, Pollmann S, Dueñas M, SantosBuelga C (2014) Nitric oxide plays a role in stem cell niche homeostasis through its interaction with auxin. Plant Physiol 166:1972–1984
Shahbaz M, Ashraf M (2013) Improving salinity tolerance in cereals. Crit Rev Plant Sci 32:237–249
Sharma DK, Singh A (2015) Salinity research in India-achievements, challenges and future prospects. In: Conference Paper in Water and Energy International 58(6):35–45
Shi H, Zhu JK (2002) Regulation of expression of the vacuolar Na+/H+ antiporter gene AtNHX1 by salt stress and abscisic acid. Plant Mol Biol 50(3):543–550
Shi Q, Ding F, Wang X, Wei M (2007) Exogenous nitric oxide protect cucumber roots against oxidative stress induced by salt stress. Plant Physiol Biochem 45:542–550
Shrivastava P, Kumar R (2015) Soil salinity: a serious environmental issue and plant growth promoting bacteria as one of the tools for its alleviation. Saudi J Biol Sci 22(2):123–131
Siddiqui MH, Alamri SA, Al-Khaishany MY, Al-Qutami MA, Ali 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
Simontacchi M, Galatro A, Ramos-Artuso F, Santa-María GE (2015) Plant Survival in a changing environment: the role of nitric oxide in plant responses to abiotic stress. Front Plant Sci. https://doi.org/10.3389/fpls.2015.009776
Singh G (2009) Salinity-related desertification and management strategies: Indian experience. Land Degrad Dev 20:367–385
Singh S, Prasad SM (2019) Management of chromium (VI) toxicity by calcium and sulfur in tomato and brinjal: implication of nitric oxide. J Hazard Matr 373:212–223
Singh M, Kumar J, Singh S, Singh VP, Prasad SM (2015) Roles of osmoprotectants in improving salinity and drought tolerance in plants: a review. Rev Environ Sci Biotechnol 14:407–426
Singh S, Kumar V, Kapoor D, Kumar SS, Dhanjal DS, Datta S, Samuel J, Dey P, Wang S, Prasad R, Singh J (2019) Revealing on hydrogen sulfide and nitric oxide signals coordination for plant growth under stress conditions. Physiol Planta. https://doi.org/10.1111/ppl.13002
Singh R, Parihar P, Prasad SM (2020) Interplay of calcium and nitric oxide in improvement of growth and Arsenic induced toxicity in mustard seedlings. Sci Rep. https://doi.org/10.1038/s41598-020-62831-0
Singh S, Husain T, Kushwaha BK, Suhel M, Fatima A, Mishra V, Singh SK, Tripathi DK, Rai M, Prasad SM, Dubey NK, Chauhan DK, Bhatt JA, Fotopoulos V, Singh VP (2020) Regulation of ascorbate-glutathione cycle by exogenous nitric oxide and hydrogen peroxide in soybean roots under arsenate stress. J Hazard Mater. https://doi.org/10.1016/j.jhazmat.2020.123686
Sun YF, Liu SB, Meng FL, Liu JY, Jin Z, Kong LT, Liu JH (2012) Metal oxide nanostructures and their gas sensing properties: a review. Sensors 12:2610–2631
Szabolcs I (1974) Salt affected soils in Europe. Martinus Nijhoff. The Hague, p 63
Tan DX, Hardeland R, Manchester LC, Korkmaz A, Ma S, Rosales-Corral S, Reiter RJ (2012) Functional roles of melatonin in plants, and perspectives in nutritional and agricultural science. J Exp Bot 63:577–597
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
Uchida A, Jagendorf AT, Hibino T, Takabe T, Takabe T (2002) Effects of hydrogen peroxide and nitric oxide on both salt and heat stress tolerance in rice. Plant Sci 163:515–523
Valderrama R, Corpas FJ, Carrera A, Gomez-Rodriguez MV, Chaki M, Pedrajas JR, Fernandez-Ocana A, Del Rio LA, Barroso JB (2006) The dehydrogenase-mediated recycling of NADPH is a key antioxidant system against salt-induced oxidative stress in olive plants. Plant Cell Environ 29:1449–1459
Vandelle E, Poinssot B, Wendehenne D (2006) Integrated signaling network involving calcium, nitric oxide, and active oxygen species but not mitogen activated protein kinases in BcPG1-elicited grapevine defenses. Mol Plant-Microbe Interact 19:429–440
Wang H, Liang X, Wan Q, Wang X, Bi Y (2009) Ethylene and nitric oxide are involved in maintaining ion homeostasis in Arabidopsis callus under salt stress. Planta 230:293–307
Wang YQ, Li L, Cui WT, Xu S, Shen WB, Wang R (2012) Hydrogen sulfide enhances alfalfa (Medicago sativa) tolerance against salinity during seed germination by nitric oxide pathway. Plant Soil 351:107–119
Weisslocker-Schaetzel M, Andre F, Touazi N, Foresi N, Lembrouk M, Dorlet P, Frelet-Barrand A, Lamattina L, Santolini J (2017) The NOS-like protein from the microalgae Ostreococcus tauri is a genuine and ultrafast NO-producing enzyme. Plant Sci 265:100–111
Wendehenne D, Durner J, Klessig DF (2004) Nitric oxide: A new player in plant signalling and defence responses. Curr Opin Plant Biol 7:449–455
Wicke B (2011) The global technical and economic potential of bioenergy from salt -affected soils. Energy Environ Sci 4:2669–2681
Xiao J, Jin R, Wagner D (2017) Developmental transitions: integrating environmental cues with hormonal signaling in the chromatin landscape in plants. Genome Biol. https://doi.org/10.1186/s13059-017-1228-9
Yadu S, Devangan TL, Chandrakar VKS (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
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 468:89–92
Yensen NP (2008) Halophyte uses for the twenty-first century. In: Khan MA, Weber DJ (eds) Ecophysiology of high salinity tolerant plants. Springer, Berlin, pp 367–396
Yi Z, Li S, Liana Y et al (2018) Effects of exogenous spermidine and elevated CO2 on physiological and biochemical changes in tomato plants under iso-osmotic salt stress. J Plant Growth Regul 37:1222–1234
Zeng H, Xu L, Singh A, Wang H, Du L, Poovaiah BW (2015) Involvement of calmodulin and calmodulin-like proteins in plant responses to abiotic stresses. Front Plant Sci. https://doi.org/10.3389/fpls.2015.00600
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 224:545–555
Zhang Z, Wu P, Zhang W, Yang Z, Liu H, Ahammed GJ, Cui G (2020) Calcium is involved in exogenous NO-induced enhancement of photosynthesis in cucumber (Cuclonis sativas L.) seedlings under low temperature. Sci Hortic 261:108953
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 134:849–857
Zhao MG, Tian QY, Zhang WH (2007) Nitric oxide synthase-dependent nitric oxide production is associated with salt tolerance in Arabidopsis. Plant Physiol 144:206–217
Zhao G, Zhao Y, Yu X, Kiprotich F, Han H, Guan R, Wang R, Shen W (2018) Nitric Oxide is required for melatonin-enhanced tolerance against salinity stress in rapeseed (Brassica napus L) seedlings. Int J Mol Sci. https://doi.org/10.3390/ijms19071912
Zhou S, Jia L, Chu H, Wu D, Peng X, Liu X, Zhang J, Zhao J, Chen K, Zhao L (2016) Arabidopsis CaM1 and CaM4 promote nitric oxide production and salt resistance by inhibiting S-Nitrosoglutathione Reductase via direct binding. PLoS Genet. https://doi.org/10.1371/journal.pgen.1006255
Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273
Acknowledgements
A.F., T.H., and M.S are thankful to the University Grants Commission, New Delhi, for providing D.Phil. Scholarship. Professor Sheo Mohan Prasad is thankful to the SERB-DST, New Delhi (EMR/2016/004745), for providing financial assistance. Dr. Vijay Pratap Singh is grateful to the SERB, New Delhi (EMR/2017/000518), for providing financial assistance.
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SMP and VPS conceived idea. AF, TH, and MS wrote the manuscript. SMP and VPS corrected the manuscript.
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Fatima, A., Husain, T., Suhel, M. et al. Implication of Nitric Oxide Under Salinity Stress: The Possible Interaction with Other Signaling Molecules. J Plant Growth Regul 41, 163–177 (2022). https://doi.org/10.1007/s00344-020-10255-5
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DOI: https://doi.org/10.1007/s00344-020-10255-5