Plant Biotechnology Reports

, Volume 12, Issue 2, pp 77–92 | Cite as

Nitric oxide-induced salt stress tolerance in plants: ROS metabolism, signaling, and molecular interactions

  • Mirza Hasanuzzaman
  • Hirosuke Oku
  • Kamrun Nahar
  • M. H. M. Borhannuddin Bhuyan
  • Jubayer Al Mahmud
  • Frantisek Baluska
  • Masayuki Fujita


Nitric oxide (NO), a non-charged, small, gaseous free-radical, is a signaling molecule in all plant cells. Several studies have proposed multifarious physiological roles for NO, from seed germination to plant maturation and senescence. Nitric oxide is thought to act as an antioxidant, quenching ROS during oxidative stress and reducing lipid peroxidation. NO also mediates photosynthesis and stomatal conductance and regulates programmed cell death, thus providing tolerance to abiotic stress. In mitochondria, NO participates in the electron transport pathway. Nitric oxide synthase and nitrate reductase are the key enzymes involved in NO-biosynthesis in aerobic plants, but non-enzymatic pathways have been reported as well. Nitric oxide can interact with a broad range of molecules, leading to the modification of protein activity, GSH biosynthesis, S-nitrosylation, peroxynitrite formation, proline accumulation, etc., to sustain stress tolerance. In addition to these interactions, NO interacts with fatty acids to form nitro-fatty acids as signals for antioxidant defense. Polyamines and NO interact positively to increase polyamine content and activity. A large number of genes are reprogrammed by NO; among these genes, proline metabolism genes are upregulated. Exogenous NO application is also shown to be involved in salinity tolerance and/or resistance via growth promotion, reversing oxidative damage and maintaining ion homeostasis. This review highlights NO-mediated salinity-stress tolerance in plants, including NO biosynthesis, regulation, and signaling. Nitric oxide-mediated ROS metabolism, antioxidant defense, and gene expression and the interactions of NO with other bioactive molecules are also discussed. We conclude the review with a discussion of unsolved issues and suggestions for future research.


Abiotic stress Antioxidant defense Glutathione Hydrogen sulfide Polyamines Stress tolerance 



Abscisic acid


Ascorbate peroxidase




Adenosine triphosphate






Dehydroascorbate reductase




Glutathione peroxidase




Glutathione reductase




GSNO reductase


Glutathione S-transferase


Hydrogen sulfide


Mitogen-activated protein kinase




Monodehydroascorbate reductase




Nitro-fatty acids


Nitric oxide


NO synthase


Nitrate reductase




Programmed cell death


Plasma membrane


Guiacol peroxidase


Post-translational modification


Reactive oxygen species


Reactive nitrogen species


Ribulose-1,5-bisphosphate carboxylase/oxygenase




Sodium nitroprusside


Superoxide dismutase


Xanthine oxidoreductase



We thank Ms. Khursheda Parvin and Abdul Awal Chowdhury Masud for their critical reading of the manuscript. The first author acknowledges Japan Society for the Promotion of Sciences (JSPS) for providing research grants.


  1. Ahmad P, Latef AAA, Hashem A, Abd_Allah EF, Gucel S, Tran L-SP (2016) Nitric oxide mitigates salt stress by regulating levels of osmolytes and antioxidant enzymes in chickpea. Front Plant Sci. Google Scholar
  2. Akter S, Huang J, Waszczak C, Jacques S, Gevaert K, Van Breusegem F, Messens J (2015) Cysteines under ROS attack in plants: a proteomics view. J Exp Bot 66:2935–2944PubMedGoogle Scholar
  3. Ali Q, Daud MK, Haider MZ, Ali S, Aslam N, Noman A, Iqbal N, Shahzad F, Rizwan M, Deeba F, Ali I, Jin ZS (2017) Seed priming by sodium nitroprusside improves salt tolerance in wheat (Triticum aestivum L.) by enhancing physiological and biochemical parameters. Plant Physiol Biochem 119:50–58PubMedGoogle Scholar
  4. Arasimowicz M, Floryszak-Wieczorek J (2007) Nitric oxide as a bioactive signalling molecule in plant stress responses. Plant Sci 172:876–887Google Scholar
  5. Arora D, Jain P, Singh N, Kaur H, Bhatla SC (2016) Mechanisms of nitric oxide crosstalk with reactive oxygen species scavenging enzymes during abiotic stress tolerance in plants. Free Radic Res 50:291–303PubMedGoogle Scholar
  6. Baudouin E (2011) The language of nitric oxide signalling. Plant Biol 13:233–242PubMedGoogle Scholar
  7. Begara-Morales JC, Sánchez-Calvo B, Luque F, Leyva-Pérez MO, Leterrier M, Corpas FJ, Barroso JB (2014) Differential transcriptomic analysis by RNA-Seq of GSNO-responsive genes between Arabidopsis roots and leaves. Plant Cell Physiol 55:1080–1095PubMedGoogle Scholar
  8. Bellin D, Asai S, Delledonne M, Yoshioka H (2013) Nitric oxide as a mediator for defense responses. Mol Plant Microbe Interact 26:271–277PubMedGoogle Scholar
  9. 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 177:302–309Google Scholar
  10. Bethke PC, Badger MR, Jones RL (2004) Apoplastic synthesis of nitric oxide by plant tissues. Plant Cell 16:332–341PubMedPubMedCentralGoogle Scholar
  11. Bose J, Munns R, Shabala S, Gilliham M, Pogson B, Tyerman SD (2017) Chloroplast function and ion regulation in plants growing on saline soils: lessons from halophytes. J Exp Bot 68:3129–3143PubMedGoogle Scholar
  12. Camejo D, Romero-Puertas MC, Rodríguez-Serrano M, Sandalio LM, Lázaro JJ, Jiménez A, Sevilla F (2013) Salinity-induced changes in S-nitrosylation of pea mitochondrial proteins. J Proteom 79:87–99Google Scholar
  13. Chen WW, Yang JL, Qin C, Jin CW, Mo JH, Ye T, Zheng SJ (2010) Nitric oxide acts downstream of auxin to trigger root ferric-chelate reductase activity in response to iron deficiency in Arabidopsis. Plant Physiol 154:810–819PubMedPubMedCentralGoogle Scholar
  14. Chen J, Xiao Q, Wang C, Wang WH, Wu FH, Chen J, He BY, Zhu Z, Ru QM, Zhang LL, Zheng HL (2014) Nitric oxide alleviates oxidative stress caused by salt in leaves of a mangrove species, Aegiceras corniculatum. Aquat Bot 117:41–47Google Scholar
  15. 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 5:12516PubMedPubMedCentralGoogle Scholar
  16. Cheng T, Shi J, Dong Y, Ma Y, Peng Y, Hu X, Chen J (2017) Hydrogen sulfide enhances poplar tolerance to high-temperature stress by increasing S-nitrosoglutathione reductase (GSNOR) activity and reducing reactive oxygen/nitrogen damage. Plant Growth Regul. Google Scholar
  17. Chokshi K, Pancha I, Ghosh A, Mishra S (2017) Salinity induced oxidative stress alters the physiological responses and improves the biofuel potential of green microalgae Acutodesmus dimorphus. Bioresour Technol 244:1376–1383PubMedGoogle Scholar
  18. Christou A, Manganaris GA, Fotopoulos V (2014) Systemic mitigation of salt stress by hydrogen peroxide and sodium nitroprusside in strawberry plants via transcriptional regulation of enzymatic and non-enzymatic antioxidants. Environ Exper Bot 107:46–54Google Scholar
  19. Corpas FJ, Barroso JB (2014) Peroxynitrite (ONOO–) is endogenously produced in arabidopsis peroxisomes and is overproduced under cadmium stress. Ann Bot 113:87–96PubMedGoogle Scholar
  20. Corpas FJ, Alché JD, Barroso JB (2013) Current overview of S-nitrosoglutathione (GSNO) in higher plants. Front Plant Sci 4:126. PubMedPubMedCentralGoogle Scholar
  21. Crawford NM (2006) Mechanisms for nitric oxide synthesis in plants. J Exp Bot 57:471–478PubMedGoogle Scholar
  22. 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 256:148–159PubMedGoogle Scholar
  23. 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 98:13454–13459PubMedPubMedCentralGoogle Scholar
  24. 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 35:910–920PubMedGoogle Scholar
  25. Egbichi I, Keyster M, Ludidi N (2014) Effect of exogenous application of nitric oxide on salt stress responses of soybean. South Afr J Bot 90:131–136Google Scholar
  26. Fan H, Guo S, Jiao Y, Zhang R, Li J (2007) Effects of exogenous nitric oxide on growth, active oxygen species metabolism, and photosynthetic characteristics in cucumber seedlings under NaCl stress. Front Agric China 1:308–314Google Scholar
  27. Fancy NN, Bahlmann A-K, Loake GJ (2017) Nitric oxide function in plant abiotic stress. Plant Cell Environ 40:462–472PubMedGoogle Scholar
  28. Fares A, Rossignol M, Peltier JB (2011) Proteomics investigation of endogenous S-nitrosylation in Arabidopsis. Biochem Biophys Res Commun 416:331–336PubMedGoogle Scholar
  29. Fatma M, Khan NA (2014) Nitric oxide protects photosynthetic capacity inhibition by salinity in Indian mustard. J Funct Environ Bot 4:106–116Google Scholar
  30. Fatma M, Masood A, Per TS, Rasheed F, Khan NA (2016a) Interplay between nitric oxide and sulfur assimilation in salt tolerance in plants. Crop J 4:153–161Google Scholar
  31. Fatma M, Masood A, Per TS, Khan NA (2016b) Nitric oxide alleviates salt stress inhibited photosynthetic performance by interacting with sulfur assimilation in mustard. Front Plant Sci. Google Scholar
  32. Feng J, Wang C, Chen Q, Chen H, Ren B, Li X, Zuo J (2013) S-Nitrosylation of phosphotransfer proteins represses cytokinin signaling. Nat Commun 4:1529. PubMedGoogle Scholar
  33. 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 22:3816–3830PubMedPubMedCentralGoogle Scholar
  34. Gadelha CG, Miranda RS, Alencar NLM, Costa JH, Prisco JT, Gomes-Filhoa 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 212:69–79PubMedGoogle Scholar
  35. Galatro A, Puntarulo S, Guiamet JJ, Simontacchi M (2013) Chloroplast functionality has a positive effect on nitric oxide level in soybean cotyledons. Plant Physiol Biochem 66:26–33PubMedGoogle Scholar
  36. 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 signaling pathways. Proc Natl Acad Sci USA 100:11116–11121PubMedPubMedCentralGoogle Scholar
  37. Gaupels F, Kuruthukulangarakoola GT, Durner J (2011) Upstream and down stream signals of nitric oxide in pathogen defence. Curr Opin Plant Biol 14:707–714PubMedGoogle Scholar
  38. 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 Cont 3:136Google Scholar
  39. Gill SS, Tuteja N (2010) Polyamines and abiotic stress tolerance in plants. Plant Signal Behav 5:26–33PubMedPubMedCentralGoogle Scholar
  40. 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 63:254–261PubMedGoogle Scholar
  41. Gill SS, Anjum NA, Gill R, Tuteja N (2016) Abiotic stress signaling in plants—an overview. In: Gill SS, Anjum NA, Gill R, Tuteja N (eds) Abiotic Stress Response in Plants Vol. 1. Wiley, Weinheim. pp 3–12Google Scholar
  42. Gong B, Wen D, Wang X, Wei M, Yang F, Li Y, Shi Q (2014) S-nitrosoglutathione reductase-modulated redox signaling controls sodic alkaline stress responses in Solanum lycopersicum L. Plant Cell Physiol 56:790–802Google Scholar
  43. Guo Y, Tian Z, Yan D, Zhang J, Qin P (2009) Effects of nitric oxide on salt stress tolerance in Kosteletzkya virginica. Life Sci J 6:67–75Google Scholar
  44. Gupta KJ, Fernie AR, KaiserWM, van Dongen JT (2011) On the origins of nitric oxide. Trends Plant Sci 16:160–168PubMedGoogle Scholar
  45. 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 411:483–498Google Scholar
  46. Hancock JT, Neill SJ, Wilson ID (2011) Nitric oxide and ABA in the control of plant function. Plant Sci 181:555–559PubMedGoogle Scholar
  47. Hao GP, Zhang JH (2010) The role of nitric oxide as a bioactive signaling molecule in plants under abiotic stress. In: Hayat S, Mori M, Pichtel J, Ahmad A (eds) Nitric oxide in plant physiology. Wiley, Weinheim, pp 115–138Google Scholar
  48. Harrison R (2002) Structure and function of xanthine oxidoreductase: where are we now? Free Radic Biol Med 33:774–797PubMedGoogle Scholar
  49. Hasanuzzaman M, Hossain MA, Fujita M (2011) Nitric oxide modulates antioxidant defense and methylglyoxal detoxification system and reduces salinity induced damage in wheat seedling. Plant Biotechnol Rep 5:353–365Google Scholar
  50. Hasanuzzaman M, Nahar K, Alam MM, Fujita M (2012) Exogenous nitric oxide alleviates high temperature induced oxidative stress in wheat (Triticum aestivum) seedlings by modulating the antioxidant defense and glyoxalase system. Aust J Crop Sci 6:1314–1323Google Scholar
  51. Hasanuzzaman M, Nahar K, Fujita M (2013a) Plant response to salt stress and role of exogenous protectants to mitigate salt-induced damages. In: Ahmed P, Azooz MM, Prasad MNV (eds) Ecophysiology and responses of plants under salt stress. Springer, New York, pp 25–87Google Scholar
  52. Hasanuzzaman M, Nahar K, Fujita M, Ahmad P, Chandna R, Prasad MNV, Ozturk M (2013b) Enhancing plant productivity under salt stress: relevance of poly-omics. In: Ahmad P, Azooz MM, Prasad MNV (eds) Salt stress in plants: signaling, omics and adaptations. Springer, New York, pp 113–156Google Scholar
  53. Hasanuzzaman M, Gill SS, Fujita M (2013c) Physiological role of nitric oxide in plants grown under adverse environmental conditions. In: Tuteja N, Singh Gill S (eds) Plant acclimation to environmental stress. Springer, New York, pp 269–322Google Scholar
  54. Hasanuzzaman M, Nahar K, Hossain MS, Mahmud JA, Rahman A, Inafuku M, Oku H. Fujita M (2017a) Coordinated actions of glyoxalase and antioxidant defense systems in conferring abiotic stress tolerance in plants. Int J Mol Sci 18:200PubMedCentralGoogle Scholar
  55. Hasanuzzaman M, Nahar K, Hossain MS, Anee TI, Parvin K, Fujita M (2017b) Nitric oxide pretreatment enhances antioxidant defense and glyoxalase systems to confer PEG-induced oxidative stress in rapeseed. J Plant Interact 12:323–331Google Scholar
  56. Hayat S, Yadav S, Wani AS, Irfan M, Alyemini MN, Ahmad A (2012) Impact of sodium nitroprusside on nitrate reductase, proline content, and antioxidant system in tomato under salinity stress. Hortic Environ Biotechnol 53:362–367Google Scholar
  57. Hill BG, Dranka BP, Bailey SM, Lancaster JRJ, Darley-Usmar VM (2010) What part of NO don’t you understand. Some answers to the cardinal questions in nitric oxide biology. J Biol Chem 285:19699–19704PubMedPubMedCentralGoogle Scholar
  58. Huang X, Chen MH, Yang LT, Li YR, Wu JM (2015) Effects of exogenous abscisic acid on cell membrane and endogenous hormone contents in leaves of sugarcane seedlings under cold stress. Sugar Technol 17:59–64Google Scholar
  59. Iakimova ET, Woltering EJ (2015) Nitric oxide prevents wound-induced browning and delays senescence through inhibition of hydrogen peroxide accumulation in fresh-cut lettuce. Innovative Food Sci Emerg Technol 30:157–169Google Scholar
  60. Ibrahim EA (2016) Seed priming to alleviate salinity stress in germinating seeds. J Plant Physiol 192:38–46PubMedGoogle Scholar
  61. Kausar F, Shahbaz M, Ashraf M (2013) Protective role of foliar-applied nitric oxide in Triticum aestivum under saline stress. Turkish J Bot 37:1155–1165Google Scholar
  62. Khokon MD, Okuma EIJI., Hossain MA, Munemasa S, Uraji M, Nakamura Y, Mori IC, Murata Y (2011) Involvement of extracellular oxidative burst in salicylic acid-induced stomatal closure in Arabidopsis. Plant Cell Environ 34:434–443PubMedGoogle Scholar
  63. Kibria MG, Hossain M, Murata Y, Hoque MA (2017) Antioxidant defense mechanisms of salinity tolerance in rice genotypes. Rice Sci 24:155–162Google Scholar
  64. 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 55:9. PubMedPubMedCentralGoogle Scholar
  65. 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 38:61Google Scholar
  66. Kumar D, Klessig DF (2000) Differential induction of tobacco MAP kinases by the defense signals nitric oxide, salicylic acid, ethylene, and jasmonic acid. Mol Plant Microb Interact 13:347–351Google Scholar
  67. Lamotte O, Bertoldo JB, Besson-Bard A, Rosnoblet C, Aimé S, Hichami S, Wendehenne D (2015) Protein S-nitrosylation: specificity and identification strategies in plants. Front Chem 2:114. PubMedPubMedCentralGoogle Scholar
  68. Lang T, Sun H, Li N, Lu Y, Shen Z, Jing X, Xiang M, Shen X, Chen S (2014) Multiple signaling networks of extracellular ATP, hydrogen peroxide, calcium, and nitric oxide in the mediation of root ion fluxes in secretor and non-secretor mangroves under salt stress. Aquat Bot 119:33–43Google Scholar
  69. Leitner M, Vandelle E, Gaupels F, Bellin D, Delledonne M (2009) NO signals in the haze: nitric oxide signalling in plant defence. Curr Opin Plant Biol 12:451–458PubMedGoogle Scholar
  70. Leterrier M, Airaki M, Palma JM, Chaki M, Barroso JB, Corpas FJ (2012) Arsenic triggers the nitric oxide (NO) and S-nitrosoglutathione (GSNO) metabolism in Arabidopsis. Environ Pollut 166:136–143PubMedGoogle Scholar
  71. Liao W, Huang G, Yu J, Zhang M, Shi X (2011) Nitric oxide and hydrogen peroxide are involved in indole-3-butyric acid-induced adventitious root development in marigold. J Hortic Sci Biotechnol 86:159–165Google Scholar
  72. Lin A, Wang Y, Tang J, Xue P, Li C, Liu L, Hu B, Yang F, Loake GJ, Chu C (2012) Nitric oxide and protein S-nitrosylation are integral to hydrogen peroxide-induced leaf cell death in rice. Plant Physiol 158:451–464PubMedGoogle Scholar
  73. Liu Y, He C (2017) A review of redox signaling and the control of MAP kinase pathway in plants. Redox Biol 11:192–204PubMedGoogle Scholar
  74. 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 168:343–356PubMedPubMedCentralGoogle Scholar
  75. Liu A, Fan J, Gitau MM, Chen L, Fu J (2016) Nitric oxide involvement in bermuda grass response to salt stress. J Am Soc Hortic Sci 141:425–433Google Scholar
  76. Lu S, Su W, Li H, Guo Z (2009) Abscisic acid improves drought tolerance of triploid bermudagrass and involves H2O2 and NO-induced antioxidant enzyme activities. Plant Physiol Biochem 47:132–138PubMedGoogle Scholar
  77. Machado RMA, Serralheiro RP (2017) Soil salinity: effect on vegetable crop growth. Management practices to prevent and mitigate soil salinization. Horticulture 3:30. Google Scholar
  78. Marvasi M (2017) Potential use and perspectives of nitric oxide donors in agriculture. J Sci Food Agric 97:1065–1072PubMedGoogle Scholar
  79. Mata-Pérez C, Sánchez-Calvo B, Padilla MN, Begara-Morales JC, Valderrama R, Corpas FJ, Barroso JB (2017) Nitro-fatty acids in plant signaling: new key mediators of nitric oxide metabolism. Redox Biol 11:554–561PubMedPubMedCentralGoogle Scholar
  80. Memon AR, Durakovic C (2014) Signal perception and transduction in plants. Period Eng Nat Sci 2:15–29Google Scholar
  81. Molassiotis A, Tanou G, Diamantidis G (2010) NO says more than ‘YES’ to salt tolerance: salt priming and systemic nitric oxide signaling in plants. Plant Signal Behav 5:209–212PubMedPubMedCentralGoogle Scholar
  82. Munns R, Tester M (2008) Mechanisms of salinity tolerance. Ann Rev Plant Biol 59:651–681Google Scholar
  83. Munns R, James RA, Läuchli (2006) Approaches to increasing the salt tolerance of wheat and other cereals. J Exp Bot 57:1025–1043PubMedGoogle Scholar
  84. Mur LA, Mandon J, Persijn S, Cristescu SM, Moshkov IE, Novikova GV, Hall MA, Harren FJ, Hebelstrup KH, Gupta KJ (2013) Nitric oxide in plants: an assessment of the current state of knowledge. AoB Plants 5:pls052. PubMedGoogle Scholar
  85. 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 126:245–255PubMedGoogle Scholar
  86. 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: El-Esawi M (ed) Phytohormones-signaling mechanisms and crosstalk in plant development and stress responses. InTech, Rijeka, pp 117–141Google Scholar
  87. Niu L, Liao W (2016) Hydrogen peroxide signaling in plant development and abiotic responses: crosstalk with nitric oxide and calcium. Front Plant Sci 7:230. PubMedPubMedCentralGoogle Scholar
  88. Palavan-Unsal N, Arisan D (2009) Nitric oxide signaling in plants. Bot Rev 75:203–229Google Scholar
  89. Pagnussat GC, Lanteri ML, Lombardo MC, Lamattina L (2004) Nitric oxide Mediates the indole acetic acid induction activation of a mitogen-activated protein kinase cascade involved in adventitious root development. Plant Physiol 135:279–286PubMedPubMedCentralGoogle Scholar
  90. Rahman A, Nahar K, Hasanuzzaman M, Fujita M (2016) Calcium supplementation improves Na+/K+ ratio, antioxidant defense and glyoxalase systems in salt-stressed rice seedlings. Front Plant Sci 7:609PubMedPubMedCentralGoogle Scholar
  91. Rahman A, Nahar K, Mahmud JA, Hasanuzzaman M, Hossain MS, Fujita M (2017) Salt stress tolerance in rice: emerging role of exogenous phytoprotectants. In: Li J (ed) Advances in international rice research. InTech, Rijeka, pp 139–174Google Scholar
  92. Rajput VD, Yaning C, Ayup M, Minkina T, Sushkova S, Mandzhieva S (2017) Physiological and hydrological changes in Populus euphratica seedlings under salinity stress. Acta Ecol Sin 37:229–235Google Scholar
  93. Reddy INBL., Kim B-K, Yoon I-N, Kim KH, Kwon TR (2017) Salt tolerance in rice: focus on mechanisms and approaches. Rice Sci 24:123–144Google Scholar
  94. Romero-Puertas MC, Rodríguez-Serrano M, Sandalio LM (2013) Protein S-nitrosylation in plants under abiotic stress: an overview. Front Plant Sci 4:373. PubMedPubMedCentralGoogle Scholar
  95. Roychoudhury A, Paul S, Basu S (2013) Cross-talk between abscisic acid dependent and abscisic acid-independent pathways during abiotic stress. Plant Cell Rep 32:985–1006PubMedGoogle Scholar
  96. Rümer S, Gupta KJ, Kaiser WM (2009) Plant cells oxidize hydroxylamines to NO. J Exp Bot 60:2065–2072PubMedPubMedCentralGoogle Scholar
  97. Sang J, Zhang A, Lin F, Tan M, Jiang M (2008) Cross-talk between calcium-calmodulin and nitric oxide in abscisic acid signaling in leaves of maize plants. Cell Res 18:577–588PubMedGoogle Scholar
  98. Schreiber F, Wunderlin P, Udert KM, Wells GF (2012) Nitric oxide and nitrous oxide turnover in natural and engineered microbial communities: biological pathways, chemical reactions, and novel technologies. Front Microbiol 3:372. PubMedPubMedCentralGoogle Scholar
  99. Serrano I, Romero-Puertas MC, Rodríguez Serrano M, Sandalio LM, Olmedilla A (2012) Role of peroxynitrite in programmed cell death induced in self-incompatible pollen. Plant Signal Behav 7:779–781PubMedPubMedCentralGoogle Scholar
  100. Setia R, Gottschalk P, Smith P, Marschner P, Baldock J, Setia D, Smith J (2013) Soil salinity decreases global soil organic carbon stocks. Sci Total Environ 465:267–272PubMedGoogle Scholar
  101. Sevilla F, Camejo D, Ortiz-Espín A, Calderón A, Lázaro JJ, Jiménez A (2015) The thioredoxin/peroxiredoxin/sulfiredoxin system: current overview on its redox function in plants and regulation by reactive oxygen and nitrogen species. J Exp Bot 66:2945–2955PubMedGoogle Scholar
  102. Shabala S, Cuin TA (2007) Potassium transport and plant salt tolerance. Physiol Plant 133:651–669Google Scholar
  103. 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 14:355–362PubMedGoogle Scholar
  104. Sheokand S, Bhankar V, Sawhney V (2010) Ameliorative effect of exogenous nitric oxide on oxidative metabolism in NaCl treated chickpea plants. Braz J Plant Physiol 22:81–90Google Scholar
  105. Shi H, Ye T, Zhu JK, Chan Z (2014) Constitutive production of nitric oxide leads to enhanced drought stress resistance and extensive transcriptional reprogramming in Arabidopsis. J Exp Bot 65(15):4119–4131PubMedPubMedCentralGoogle Scholar
  106. Shi K, Li X, Zhang H, Zhang G, Liu Y, Zhou Y et al (2015) Guard cell hydrogen peroxide and nitric oxide mediate elevated CO2-induced stomatal movement in tomato. New Phytol 208:342–353PubMedGoogle Scholar
  107. 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 22:123–131PubMedGoogle Scholar
  108. Siddiqui MH, Al-Whaibi MH, Basalah MO (2011) Role of nitric oxide in tolerance of plants to abiotic stress. Protoplasma 248:447–455PubMedGoogle Scholar
  109. Stavridou E, Hastings A, Webster RJ, Robson PRH (2017) The impact of soil salinity on the yield, composition and physiology of the bioenergy grass Miscanthus × giganteus. Gcb Bioenergy 9:92–104Google Scholar
  110. Tanou G, Job C, Rajjou L, Arc E, Belghazi M, Diamantidis G et al (2009) Proteomics reveals the overlapping roles of hydrogen peroxide and nitric oxide in the acclimation of citrus plants to salinity. Plant J 60(5):795–804PubMedGoogle Scholar
  111. Tavakkoli E, Rengasamy P, McDonald GK (2010) High concentrations of Na+ and Cl ions in soil solution have simultaneous detrimental effects on growth of faba bean under salinity stress. J Exp Bot 61:4449–4459PubMedPubMedCentralGoogle Scholar
  112. Tichá T, Lochman J, Činčalová L, Luhová L, Petřivalský M (2017) Redox regulation of plant S-nitrosoglutathione reductase activity through post-translational modifications of cysteine residues. Biochem Biophys Res Commun 494:27–33PubMedGoogle Scholar
  113. 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 47:346–354PubMedGoogle Scholar
  114. Wang P, Du Y, Li Y, Ren D, Song CP (2010) Hydrogen peroxide–mediated activation of MAP kinase 6 modulates nitric oxide biosynthesis and signal transduction in Arabidopsis. Plant Cell 22:2981–2998PubMedPubMedCentralGoogle Scholar
  115. 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 35:891–900Google Scholar
  116. Wang C, El-Shetehy M, Shine MB, Yu K, Navarre D, Wendehenne D, Kachroo P (2014) Free radicals mediate systemic acquired resistance. Cell Rep 7:348–355PubMedGoogle Scholar
  117. Wodala B, Deák Z, Vass I, Erdei L, Altorjay I, Horváth F (2008) In vivo target sites of nitric oxide in photosynthetic electron transport as studied by chlorophyll fluorescence in pea leaves. Plant Physiol 146:1920–1927PubMedPubMedCentralGoogle Scholar
  118. Wrzaczek M, Brosché M, Salojärvi J, Kangasjärvi S, Idänheimo N, Mersmann S, Robatzek S, Karpiński S, Karpińska B, Kangasjärvi J (2010) Transcriptional regulation of the CRK/DUF26 group of receptor-like protein kinases by ozone and plant hormones in Arabidopsis. BMC Plant Biol 10:95. PubMedPubMedCentralGoogle Scholar
  119. Wu XX, Ding HD, Chen JL, Zhang HJ, Zhu WM (2010) Attenuation of salt-induced changes in photosynthesis by exogenous nitric oxide in tomato (Lycopersicon esculentum Mill. L.) seedlings. Afr J Biotechnol 9:7837–7846Google Scholar
  120. 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 33:1199–1209Google Scholar
  121. Wu P, Shou H, Xu G, Lian X (2013) Improvement of phosphorus efficiency in rice on the basis of understanding phosphate signaling and homeostasis. Curr Opin Plant Biol 16:205–212PubMedGoogle Scholar
  122. 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 21:132–139PubMedGoogle Scholar
  123. Xu LL, Fan ZY, Dong YJ, Kong J, Bai XY (2015) Effects of exogenous salicylic acid and nitric oxide on physiological characteristics of two peanut cultivars under cadmium stress. Biol Plant 59:171–182Google Scholar
  124. 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 23:43–58PubMedGoogle Scholar
  125. 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 4:128–129PubMedGoogle Scholar
  126. Yang H, Mu J, Chen L, Feng J, Hu J, Li L, Zhou JM, Zuo J (2015) S-Nitrosylation positively regulates ascorbate peroxidase activity during plant stress responses. Plant Physiol 167:1604–1615PubMedPubMedCentralGoogle Scholar
  127. Yu M, Lamattina L, Spoel SH, Loake GJ (2014) Nitric oxide function in plant biology: a redox cue in deconvolution. New Phytol 202:1142–1156PubMedGoogle Scholar
  128. 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 224:545–555PubMedGoogle Scholar
  129. Zhang A, Jiang M, Zhang J, Ding H, Xu S, Hu X, Tan M (2007) Nitric oxide induced by hydrogen peroxide mediates abscisic acid-induced activation of the mitogen-activated protein kinase cascade involved in antioxidant defense in maize leaves. New Phytol 175:36–50PubMedGoogle Scholar
  130. 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 134:849–857PubMedPubMedCentralGoogle Scholar
  131. 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 67:222–227Google Scholar
  132. Ziogas V, Tanou G, Filippou P, Diamantidis G, Vasilakakis M, Fotopoulos V, Molassiotis A (2013) Nitrosative responses in citrus plants exposed to six abiotic stress conditions. Plant Physiol Biochem 68:118–126PubMedGoogle Scholar
  133. Zuccarelli R, Coelho AC, Peres LE, Freschi L (2017) Shedding light on NO homeostasis: light as a key regulator of glutathione and nitric oxide metabolisms during seedling deetiolation. Nitric Oxide 68:77–90PubMedGoogle Scholar

Copyright information

© Korean Society for Plant Biotechnology and Springer Japan KK, part of Springer Nature 2018

Authors and Affiliations

  • Mirza Hasanuzzaman
    • 1
    • 2
  • Hirosuke Oku
    • 1
  • Kamrun Nahar
    • 3
  • M. H. M. Borhannuddin Bhuyan
    • 4
  • Jubayer Al Mahmud
    • 5
  • Frantisek Baluska
    • 6
  • Masayuki Fujita
    • 4
  1. 1.Molecular Biotechnology Group, Center of Molecular BiosciencesUniversity of the RyukyusNishiharaJapan
  2. 2.Department of Agronomy, Faculty of AgricultureSher-e-Bangla Agricultural UniversityDhakaBangladesh
  3. 3.Department of Agricultural Botany, Faculty of AgricultureSher-e-Bangla Agricultural UniversityDhakaBangladesh
  4. 4.Laboratory of Plant Stress Responses, Faculty of AgricultureKagawa UniversityTakamatsuJapan
  5. 5.Department of Agroforestry and Environment, Faculty of AgricultureSher-e-Bangla Agricultural UniversityDhakaBangladesh
  6. 6.Department of Plant Cell Biology, Institute of Cellular and Molecular Botany (IZMB)University of BonnBonnGermany

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