Hydrogen Peroxide and Nitric Oxide Signaling Network

  • Lijuan Niu
  • Jihua Yu
  • Weibiao LiaoEmail author
  • Jian Yu


Nitric oxide (NO), as a diatomic free radical gas, appears to be involved in development, growth, and biotic/abiotic responses in plants. Also, hydrogen peroxide (H2O2), a reactive oxygen species, has been considered as an important signaling molecule that regulates various physiological and biochemical processes in plants. A large of evidences implied that NO and H2O2 signaling could affect each other at different levels of regulation under common conditions. Meanwhile, NO might have similar kinetics with H2O2. The interaction between NO and H2O2 is complex which has essential role in mediating signaling transduction pathway in plants. This chapter aims to introduce these evidences in our understanding of the roles of NO and H2O2 signaling network in plants and their interaction.


Nitric oxide Hydrogen peroxide Signaling molecules Interaction 



This research was supported by the National Natural Science Foundation of China (Grant Nos. 31860568, 31560563, and 31160398), the Research Fund of Higher Education of Gansu, China (Grant No. 2018C-14), the Post-Doctoral Foundation of China (Grant Nos. 20100470887 and 2012T50828), the Natural Science Foundation of Gansu Province, China (Grant Nos. 1606RJZA073, 1606RJZA077, and 1606RJYA252), Scientific Research Foundation for the Yong Graduate Supervisor of Gansu Agricultural University in Lanzhou, China (GAU-QNDS-201709), and Feitian and Fuxi Excellent Talents in Gansu Agricultural University.


  1. Agurla S, Gayatri G, Raghavendra AS (2014) Nitric oxide as a secondary messenger during stomatal closure as a part of plant immunity response against pathogens. Nitric Oxide 43:89–96PubMedCrossRefPubMedCentralGoogle Scholar
  2. 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 7:347PubMedPubMedCentralGoogle Scholar
  3. Airaki M, Leterrier M, Valderrama R, Chaki M, Begara-Morales JC, Barroso JB, del Río LA, Palma JM, Corpas FJ (2015) Spatial and temporal regulation of the metabolism of reactive oxygen and nitrogen species during the early development of pepper (Capsicum annuum) seedlings. Ann Bot 116:679–693PubMedPubMedCentralCrossRefGoogle Scholar
  4. Akram NA, Iqbal M, Muhammad A, Ashraf M, Al-Qurainy F, Shafiq S (2018) Aminolevulinic acid and nitric oxide regulate oxidative defense and secondary metabolisms in canola (Brassica napus L.) under drought stress. Protoplasma 255:163–174PubMedCrossRefGoogle Scholar
  5. Alamri SA, Siddiqui MH, Al-Khaishany MY, Khan MN, Ali HM, Alakeel KA (2018) Nitric oxide-mediated cross-talk of proline and heat shock proteins induce thermotolerance in Vicia faba L. Environ Exp Bot.
  6. Amooaghaie R, Tabatabaie F (2017) Osmopriming-induced salt tolerance during seed germination of alfalfa most likely mediates through H2O2 signaling and upregulation of heme oxygenase. Protoplasma 254:1791–1803PubMedCrossRefPubMedCentralGoogle Scholar
  7. Arora D, Bhatla SC (2017) Melatonin and nitric oxide regulate sunflower seedling growth under salt stress accompanying differential expression of Cu/Zn SOD and Mn SOD. Free Radic Biol Med 106:315–328PubMedCrossRefPubMedCentralGoogle Scholar
  8. Asgher M, Per TS, Masood A, Fatma M, Freschi L, Corpas FJ, Khan NA (2017) Nitric oxide signaling and its crosstalk with other plant growth regulators in plant responses to abiotic stress. Environ Sci Pollut Res Int 24:2273–2285PubMedCrossRefPubMedCentralGoogle Scholar
  9. Astier J, Gross I, Durner J (2018) Nitric oxide production in plants: an update. J Exp Bot 69:3401–3411PubMedCrossRefGoogle Scholar
  10. Bassiri Rad H, Gutschick VP, Lussenhop J (2001) Root system adjustments: regulation of plant nutrient uptake and growth responses to elevated CO2. Oecologia 126:305–320CrossRefGoogle Scholar
  11. Brewer TF, Garcia FJ, Onak CS, Carroll KS, Chang CJ (2015) Chemical approaches to discovery and study of sources and targets of hydrogen peroxide redox signaling through NADPH oxidase proteins. Annl Rev Biochem 84:765–790CrossRefGoogle Scholar
  12. Brychkova G, Yarmolinsky D, Fluhr R, Sagi M (2012) The determination of sulfite level sand its oxidation in plant leaves. Plant Sci 190:123–130PubMedCrossRefPubMedCentralGoogle Scholar
  13. Cao Z, Duan X, Yao P, Cui W, Cheng D, Zhang J, Jin Q, Chen J, Dai T, Shen W (2017) Hydrogen gas is involved in auxin-induced lateral root formation by modulating nitric oxide synthesis. Int J Mol Sci 18:2084PubMedCentralCrossRefGoogle Scholar
  14. Chang Q, Tang H (2014) Optical determination of glucose and hydrogen peroxide using an anocomposite prepared from glucose oxidase and magnetite nanoparticles immobilized on graphene oxide. Microchim Acta 181:527–534CrossRefGoogle Scholar
  15. Chen Z, Gu Q, Yu X, Huang L, Xu S, Wang R, Shen W, Shen W (2018) Hydrogen peroxide acts downstream of melatonin to induce lateral root formation. Ann Bot 121:1127–1136PubMedCrossRefGoogle Scholar
  16. Chinnusamy V, Zhu JH, Zhu JK (2007) Cold stress regulation of gene expression in plants. Trend Plant Sci 12:444–451CrossRefGoogle Scholar
  17. Cona A, Rea G, Botta M, Corelli F, Federico R, Angelini R (2006) Flavin-containing polyamine oxidase is a hydrogen peroxide source in the oxidative response to the protein phosphatase inhibitor cantharidin in Zea mays L. J Exp Bot 57:2277–2289PubMedCrossRefGoogle Scholar
  18. Corpas FJ, Barroso JB, del Río LA (2004) Enzymatic sources of nitric oxide in plant cells-beyond one protein–one function. New Phytol 162:246–248CrossRefGoogle Scholar
  19. Corpas FJ, Barroso JB, Carreras A, Valderrama R, Palma JM, León AM, Sandalio LM, del Río LA (2006) Constitutive arginine-dependent nitric oxide synthase activity in different organs of pea seedlings during plant development. Planta 224:246–254PubMedCrossRefPubMedCentralGoogle Scholar
  20. Corpas FJ, Barroso JB, Palma JM, Rodriguez-Ruiz M (2017) Plant peroxisomes: a nitro-oxidative cocktail. Redox Biol 11:535–542PubMedPubMedCentralCrossRefGoogle Scholar
  21. Corpas FJ, Freschi L, Rodríguez-Ruiz M, Mioto PT, González-Gordo S, Palma JM (2018) Nitro-oxidative metabolism during fruit ripening. J Exp Bot 69:3449–3463PubMedCrossRefPubMedCentralGoogle Scholar
  22. del Río LA (2015) ROS and RNS in plant physiology: an overview. J Exp Bot 66:2827–2837PubMedCrossRefGoogle Scholar
  23. Deng XG, Zhu T, Zou LJ, Han XY, Zhou X, Xi DH, Zhang DW, Lin HH (2016) Orchestration of hydrogen peroxide and nitric oxide in brassinosteroid-mediated systemic virus resistance in Nicotiana benthamiana. Plant J 85:478–493PubMedCrossRefPubMedCentralGoogle Scholar
  24. Diao QN, Song YJ, Shi DM, Qi HY (2017) Interaction of polyamines, abscisic acid, nitric oxide, and hydrogen peroxide under chilling stress in tomato (Lycopersicon esculentum Mill.) seedlings. Front Plant Sci 8:203PubMedPubMedCentralCrossRefGoogle Scholar
  25. Dickinson BC, Chang CJ (2011) Chemistry and biology of reactive oxygen species in signaling or stress responses. Nat Chem Biol 7:504–511PubMedPubMedCentralCrossRefGoogle Scholar
  26. Ding ZJ, Yan JY, Xu XY, Yu DQ, Li GX, Zhang SQ, Zheng SJ (2014) Transcription factor WRKY 46 regulates osmotic stress responses and stomatal movement independently in Arabidopsis. Plant J 79:13–27PubMedCrossRefPubMedCentralGoogle Scholar
  27. Dong N, Li Y, Qi J, Chen Y, Hao Y (2018) Nitric oxide synthase-dependent nitric oxide production enhances chilling tolerance of walnut shoots in vitro via involvement chlorophyll fluorescence and other physiological parameter levels. Scient Horti 230:68–77CrossRefGoogle Scholar
  28. Duan X, Li X, Ding F, Zhao J, Guo A, Zhang L, Yao J, Yang YL (2015) Interaction of nitric oxide and reactive oxygen species and associated regulation of root growth in wheat seedlings under zinc stress. Ecotox Environ Safe 113:95–102CrossRefGoogle Scholar
  29. Esringu A, Aksakal O, Tabay D, Kara AA (2016) Effects of sodium nitroprusside (SNP) pretreatment on UV-B stress tolerance in lettuce (Lactuca sativa L.) seedlings. Environ Sci Pollut Res 23:589–597CrossRefGoogle Scholar
  30. Eum HL, Kim HB, Choi SB, Lee SK (2009) Regulation of ethylene biosynthesis by nitric oxide in tomato (Solanum lycopersicum L.) fruit harvested at different ripening stages. Eur Food Res Technol 228:331CrossRefGoogle Scholar
  31. Fahey JM, Girotti AW (2017) Nitric oxide-mediated resistance to photodynamic therapy in a human breast tumor xenograft model: improved outcome with NOS2 inhibitors. Nitric Oxide 62:52–61PubMedCrossRefPubMedCentralGoogle Scholar
  32. Fedurayev PV, Mironov KS, Gabrielyan DA, Bedbenov VS, Zorina AA, Shumskaya M, Los DA (2018) Hydrogen peroxide participates in perception and transduction of cold stress signal in Synechocystis. Plant Cell Physiol 59:1255–1264PubMedCrossRefPubMedCentralGoogle Scholar
  33. Floryszak-Wieczorek J, Arasimowicz-Jelonek M (2016) Contrasting regulation of NO and ROS in potato defense-associated metabolism in response to pathogens of different lifestyles. PLoS One 11:e0163546PubMedPubMedCentralCrossRefGoogle Scholar
  34. Förstermann U, Closs EI, Pollock JS, Nakane M, Schwarz P, Gath I, Kleinert H (1994) Nitric oxide synthase isozymes. Characterization, purification, molecular cloning, and functions. Hypertension 23:1121–1131PubMedCrossRefGoogle Scholar
  35. Francoz E, Ranocha P, Nguyen-Kim H, Jamet E, Burlat V, Dunand C (2015) Roles of cell wall peroxidases in plant development. Phytochemistry 112:15–21PubMedCrossRefGoogle Scholar
  36. Freitas VS, de Souza Miranda R, Costa JH, de Oliveira DF, de Oliveira Paula S, de Castro Miguel E, Souza Freire R, Tarquinio Prisco J, Gomes Filho E (2018) Ethylene triggers salt tolerance in maize genotypes by modulating polyamine catabolism enzymes associated with H2O2 production. Environ Exp Bot 145:75–86CrossRefGoogle Scholar
  37. Freschi L (2013) Nitric oxide and phytohormone interactions: current status and perspectives. Front Plant Sci 4:398PubMedPubMedCentralCrossRefGoogle Scholar
  38. González A, delos Ángeles Cabrera M, Henríquez MJ, Contreras RA, Morales B, Moenne A (2012) Crosstalk among calcium, hydrogen peroxide, and nitric oxide and activation of gene expression involving calmodulins and calcium-dependent protein kinases in Ulva compressa exposed to copper excess. Plant Physiol 158:1451–1462PubMedPubMedCentralCrossRefGoogle Scholar
  39. Gow AJ, Ischiropoulos H (2001) Nitric oxide chemistry and cellular signaling. J Cell Physiol 187:277–282PubMedCrossRefPubMedCentralGoogle Scholar
  40. Guo F, Okamoto M, Crawford NM (2003) Identification of a plant nitric oxide synthase gene involved in hormonal signaling. Science 302:100–103PubMedCrossRefPubMedCentralGoogle Scholar
  41. Gusarov I, Shatalin K, Starodubtseva M, Nudler E (2009) Endogenous nitric oxide protects bacteria against a wide spectrum of antibiotics. Science 325:1380–1384PubMedPubMedCentralCrossRefGoogle Scholar
  42. Hasanuzzaman M, Nahar K, Gill SS, Alharby HF, Razafindrabe BH, Fujita M (2017) Hydrogen peroxide pretreatment mitigates cadmium-induced oxidative stress in Brassica napus L.: An intrinsic study on antioxidant defense and glyoxalase systems. Front Plant Sci 8:115PubMedPubMedCentralGoogle Scholar
  43. Hasanuzzaman M, Nahar K, Rahman A, Inafuku M, Oku H, Fujita M (2018) Exogenous nitric oxide donor and arginine provide protection against short-term drought stress in wheat seedlings. Physiol Mol Biol Plants 24:1–12CrossRefGoogle Scholar
  44. He J, Ren Y, Chen X, Chen H (2014) Protective roles of nitric oxide on seed germination and seedling growth of rice (Oryza sativa L.) under cadmium stress. Ecotoxicol Environ Saf 108:114–119PubMedCrossRefPubMedCentralGoogle Scholar
  45. He JM, Ma XG, Zhang Y, Sun TF, Xu FF, Chen YP, Liu X, Yue M (2013) Role and interrelationship of Ga protein, hydrogen peroxide, and nitric oxide in ultra violet B-induced stomatal closure in Arabidopsis leaves. Plant Physiol 161:1570–1583PubMedPubMedCentralCrossRefGoogle Scholar
  46. He H, Huang W, Oo TL, Gu M, He LF (2017) Nitric oxide inhibits aluminum-induced programmed cell death in peanut (Arachis hypogaea L.) root tips. J Hazard Mater 333:285–292PubMedCrossRefGoogle Scholar
  47. Houmani H, Rodríguez-Ruiz M, Palma JM, Corpas FJ (2018) Mechanical wounding promotes local and long distance response in the halophyte Cakile maritima through the involvement of the ROS and RNS metabolism. Nitric Oxide 74:93–101PubMedCrossRefGoogle Scholar
  48. Hu X, Bidney DL, Yalpani N, Duvick JP, Crasta O, Folkerts O, Lu G (2003) Overexpression of a gene encoding hydrogen peroxide-generating oxalate oxidase evokes defense responses in sunflower. Plant Physiol 133:170–181PubMedPubMedCentralCrossRefGoogle Scholar
  49. Hu J, Yang H, Mu J, Lu T, Peng J, Deng X, Kong Z, Bao S, Cao X, Zuo J (2017) Nitric oxide regulates protein methylation during stress responses in plants. Mol Cell 67:702–710PubMedCrossRefGoogle Scholar
  50. Iakimova ET, Woltering EJ (2015) Nitric oxide prevents wound-induced browning and delays senescence through inhibition of hydrogen peroxide accumulation in fresh-cut lettuce. Innov Food Sci Emerg 30:157–169CrossRefGoogle Scholar
  51. Jansen MAK, Bornman JF (2012) UV-B radiation: from generic stressor to specific regulator. Physiol Plant 145:501–504PubMedCrossRefGoogle Scholar
  52. Jiménez-Quesada MJ, Carmona R, Lima-Cabello E, Traverso JÁ, Castro AJ, Claros MG, Alché JD (2017) Generation of nitric oxide by olive (Olea europaea L.) pollen during in vitro germination and assessment of the S-nitroso- and nitro-proteomes by computational predictive methods. Nitric Oxide 68:23–37PubMedCrossRefGoogle Scholar
  53. Jin X, Liao WB, Yu JH, Ren PJ, Dawuda MM, Wang M, Niu LJ, Li XP, Xu XT (2017) Nitric oxide is involved in ethylene-induced adventitious rooting in marigold (Tagetes erecta L.). Can J Plant Sci 97:620–631Google Scholar
  54. Karpets YV, Kolupaev YE, Vayner AA (2015) Functional interaction between nitric oxide and hydrogen peroxide during formation of wheat seedling induced heat resistance. Russ J Plant Physl 62:65–70CrossRefGoogle Scholar
  55. Keshavarz-Tohid V, Taheri P, Taghavi SM, Tarighi S (2016) The role of nitric oxide in basal and induced resistance in relation with hydrogen peroxide and antioxidant enzymes. J Plant Physiol 199:29–38PubMedCrossRefGoogle Scholar
  56. Khan A, Anwar Y, Hasan MM, Iqbal A, Ali M, Alharby HF, Hakeem KR, Hasanuzzaman M (2017) Attenuation of drought stress in Brassica seedlings with exogenous application of Ca2+ and H2O2. Plants 6:20PubMedCentralCrossRefPubMedGoogle Scholar
  57. Lanteri ML, Pagnussat GC, Lamattina L (2006) Calcium and calcium-dependent protein kinases are involved in nitric oxide-and auxin-induced adventitious root formation in cucumber. J Exp Bot 57:1341–1351PubMedCrossRefGoogle Scholar
  58. Li XP, Xu QQ, Liao WB, Ma ZJ, Xu XT, Wang M, Ren PJ, Niu LJ, Jin X, Zhu YC (2016) Hydrogen peroxide is involved in abscisic acid-induced adventitious rooting in cucumber (Cucumis sativus L.) under drought stress. J Plant Biol 59:536–548CrossRefGoogle Scholar
  59. Li G, Zhu S, Wu W, Zhang C, Peng Y, Wang Q, Shi J (2017a) Exogenous nitric oxide induces disease resistance against Monilinia fructicola through activating the phenylpropanoid pathway in peach fruit. J Sci Food Agric 97:3030–3038PubMedCrossRefGoogle Scholar
  60. Li Q, Wang YJ, Liu CK, Pei ZM, Shi WL (2017b) The crosstalk between ABA, nitric oxide, hydrogen peroxide, and calcium in stomatal closing of Arabidopsis thaliana. Biologia 72:1140–1146Google Scholar
  61. Li Z, Xu J, Gao Y, Wang C, Guo G, Luo Y, Huang Y, Hu W, Sheteiwy MS, Guan Y, Hu J (2017c) The synergistic priming effect of exogenous salicylic acid and H2O2 on chilling tolerance enhancement during maize (Zea mays L.) seed germination. Front Plant Sci 8:1153PubMedPubMedCentralCrossRefGoogle Scholar
  62. Li R, Jia Y, Yu L, Yang W, Chen Z, Chen H, Hu X (2018) Nitric oxide promotes light-initiated seed germination by repressing PIF1 expression and stabilizing HFR1. Plant Physiol Biochem 123:204–212PubMedCrossRefGoogle Scholar
  63. Li ZG, Luo LJ, Sun YF (2015) Signal crosstalk between nitric oxide and hydrogen sulfide may be involved in hydrogen peroxide-induced thermotolerance in maize seedlings. Russ J Plant Physiol 62:507–514CrossRefGoogle Scholar
  64. Liao WB, Huang GB, Yu JH, Zhang ML (2012) Nitric oxide and hydrogen peroxide alleviate drought stress in marigold explants and promote its adventitious root development. Plant Physiol Biochem 58:6–15PubMedCrossRefGoogle Scholar
  65. Liao WB, Zhang ML, Yu JH (2013) Role of nitric oxide in delaying senescence of cut rose flowers and its interaction with ethylene. Sci Hortic 155:30–38CrossRefGoogle Scholar
  66. Lin AH, Wang YQ, Tang JY, Xue P, Li CL, Liu LC, Hu B, Yang FQ, Loake GJ, Chu CC (2012) Nitric oxide and protein S-nitrosylation are integral to hydrogen peroxide-induced leaf cell death in rice. Plant Physiol 158:451–464PubMedCrossRefPubMedCentralGoogle Scholar
  67. Lindermayr C (2018) Crosstalk between reactive oxygen species and nitric oxide in plants: key role of S-nitrosoglutathione reductase. Free Radic Biol Med 122:110–115PubMedCrossRefGoogle Scholar
  68. Liu J, Zhang C, Wei C, Wang M, Liu X, Yu F, Xie Q, Tu J (2015) The RING finger ubiquitin E3 ligase OsHTAS enhances heat tolerance by promoting H2O2-induced stomatal closure in rice. Plant Physiol 170:429–443PubMedPubMedCentralCrossRefGoogle Scholar
  69. Lu SY, Su W, Li HH, Guo ZF (2009) Abscisic acid improves drought tolerance of triploid bermudagrass and involves H2O2-and NO- induced antioxidant enzyme activities. Plant Physiol Biochem 47:132–138PubMedCrossRefGoogle Scholar
  70. Liu XY, Deng ZJ, Cheng HY, He XH, Song SQ (2011) Nitrite, sodium nitroprusside, potassium ferricyanide and hydrogen peroxide release dormancy of Amaranthus retroflexus seeds in a nitric oxide-dependent manner. Plant Growth Regul 64:155–161CrossRefGoogle Scholar
  71. Lv X, Ge S, Jalal Ahammed G, 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 58:1963–1975PubMedCrossRefGoogle Scholar
  72. Lv X, Li H, Chen X, Xiang X, Guo Z, Yu J, Zhou Y (2018) The role of calcium-dependent protein kinase in hydrogen peroxide, nitric oxide and ABA-dependent cold acclimation. J Exp Bot 69:4127–4139PubMedPubMedCentralCrossRefGoogle Scholar
  73. Ma Z, Marsolais F, Bykova NV, Igamberdiev AU (2016) Nitric oxide and reactive oxygen species mediate metabolic changes in barley seed embryo during germination. Front Plant Sci 7:138PubMedPubMedCentralGoogle Scholar
  74. Maksimov N, Evmenyeva A, Breygina M, Yermakov I (2018) The role of reactive oxygen species in pollen germination in Picea pungens (blue spruce). Plant Reprod 31:357–365PubMedCrossRefGoogle Scholar
  75. Mehler AH (1951) Studies on reactions of illuminated chloroplasts II. Stimulation and inhibition of their action with molecular oxygen. Arch Biochem Biophys 33:339–351CrossRefGoogle Scholar
  76. Mei Y, Chen H, Shen W, Shen W, Huang L (2017) Hydrogen peroxide is involved in hydrogen sulfide-induced lateral root formation in tomato seedlings. BMC Plant Biol 17:162PubMedPubMedCentralCrossRefGoogle Scholar
  77. Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trend Plant Sci 7:405–410CrossRefGoogle Scholar
  78. Mishra BB, Lovewell RR, Olive AJ, Zhang G, Wang W, Eugenin E, Smith CM, Phuah JY, Long JE, Dubuke ML, Palace SG, Goguen JD, Baker RE, Nambi S, Mishra R, Booty MG, Baer CE, Shaffer SA, Dartois V, McCormick BA, Chen X, Sassetti CM (2017) Nitric oxide prevents a pathogen-permissive granulocytic inflammation during tuberculosis. Nat Microbiol 2:17072PubMedPubMedCentralCrossRefGoogle Scholar
  79. Mostofa MG, Fujita M, Tran LSP (2015) Nitric oxide mediates hydrogen peroxide-and salicylic acid-induced salt tolerance in rice (Oryza sativa L.) seedlings. Plant Growth Regul 77:265–277CrossRefGoogle Scholar
  80. Nathan CF, Hibbs JB (1991) Role of nitric oxide synthesis in macrophage antimicrobial activity. Curr Opin Immunol 3:65–70PubMedCrossRefGoogle Scholar
  81. 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 8:1684PubMedPubMedCentralCrossRefGoogle Scholar
  82. Noctor G, Foyer CH (2016) Intracellular redox compartmentation and ROS-related communication in regulation and signaling. Plant Physiol 171:1581–1592PubMedPubMedCentralCrossRefGoogle Scholar
  83. Oksanen E, Häikiö E, Sober J, Karnosky DF (2004) Ozone-induced H2O2 accumulation in field-grown aspen and birch is linked to foliar ultrastructure and peroxisomal activity. New Phytol 161:791–799CrossRefGoogle Scholar
  84. 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 135:279–286PubMedPubMedCentralCrossRefGoogle Scholar
  85. Pasqualini S, Cresti M, Del Casino C, Faleri C, Frenguelli G, Tedeschini E, Ederli L (2015) Roles for NO and ROS signalling in pollen germination and pollen-tube elongation in Cupressus arizonica. Biol Plant 59:735–744CrossRefGoogle Scholar
  86. Prado AM, Porterfield DM, Feijó JA (2004) Nitric oxide is involved in growth regulation and re-orientation of pollen tubes. Development 131:2707–2714PubMedCrossRefGoogle Scholar
  87. Recalde L, Vázquez A, Groppa MD, Benavides MP (2018) Reactive oxygen species and nitric oxide are involved in polyamine-induced growth inhibition in wheat plants. Protoplasma 255:1295–1307PubMedCrossRefPubMedCentralGoogle Scholar
  88. Qi F, Xiang Z, Kou N, Cui W, Xu D, Wang R, Zhu D, Shen W (2017) Nitric oxide is involved in methane-induced adventitious root formation in cucumber. Physiol Plant 159:366–377PubMedCrossRefGoogle Scholar
  89. Qu Y, Wang Q, Guo J, Wang P, Song P, Jia Q, Zhang X, Kudla J, Zhang W, Zhang Q (2017) Peroxisomal CuAOζ and its product H2O2 regulate the distribution of auxin and IBA-dependent lateral root development in Arabidopsis. J Exp Bot 68:4851–4867PubMedCrossRefPubMedCentralGoogle Scholar
  90. Rockel P, Strube F, Rockel A, Wildt J, Kaiser WM (2002) Regulation of nitric oxide (NO) production by plant nitrate reductase in vivo and in vitro. J Exp Bot 53:103–110PubMedCrossRefPubMedCentralGoogle Scholar
  91. Sanz L, Albertos P, Mateos I, Sánchez-Vicente I, Lechón T, Fernández-Marcos M, Lorenzo O (2015) Nitric oxide (NO) and phytohormones crosstalk during early plant development. J Exp Bot 66:2857–2868PubMedCrossRefPubMedCentralGoogle Scholar
  92. Scuffi D, Núñez Á, Laspina N, Gotor C, Lamattina L, García-Mata C (2014) Hydrogen sulfide generated by L-cysteine desulfhydrase acts upstream of nitric oxide to modulate ABA-dependent stomatal closure. Plant Physiol 166:2065–2076PubMedPubMedCentralCrossRefGoogle Scholar
  93. Shan C, Zhang S, Ou X (2018) The roles of H2S and H2O2 in regulating AsA-GSH cycle in the leaves of wheat seedlings under drought stress. Protoplasma 255:1257–1262PubMedCrossRefGoogle Scholar
  94. Shi H, Ye T, Chan Z (2014) Nitric oxide-activated hydrogen sulfide is essential for cadmium stress response in bermuda grass (Cynodon dactylon L. Pers.). Plant Physiol Biochem 74:99–107PubMedCrossRefGoogle Scholar
  95. Shi C, Qi C, Ren H, Huang A, Hei S, She X (2015) Ethylene mediates brassinosteroid-induced stomatal closure via Gα protein-activated hydrogen peroxide and nitric oxide production in Arabidopsis. Plant J 82:280–301PubMedCrossRefGoogle Scholar
  96. Singh SP, Singh Z, Swinny EE (2009) Postharvest nitric oxide fumigation delays fruit ripening and alleviates chilling injury during cold storage of Japanese plums (Prunus salicina Lindell). Postharvest Biol Technol 53:101–108CrossRefGoogle Scholar
  97. Sivakumaran A, Akinyemi A, Mandon J, Cristescu SM, Hall MA, Harren FJ, Mur LA (2016) ABA suppresses Botrytis cinerea elicited NO production in tomato to influence H2O2 generation and increase host susceptibility. Front Plant Sci 7:709PubMedPubMedCentralCrossRefGoogle Scholar
  98. Skiba U, Smith KA, Fowler D (1993) Nitrification and denitrification as sources of nitric oxide and nitrous oxide in a sandy loam soil. Soil Biol Biochem 25:1527–1536CrossRefGoogle Scholar
  99. Stöhr C, Strube F, Marx G, Ullrich WR, Rockel P (2001) A plasma membrane-bound enzyme of tobacco roots catalyses the formation of nitric oxide from nitrite. Planta 212:835–841PubMedCrossRefPubMedCentralGoogle Scholar
  100. Sun C, Liu L, Lu L, Jin C, Lin X (2018) Nitric oxide acts downstream of hydrogen peroxide in regulating aluminum-induced antioxidant defense that enhances aluminum resistance in wheat seedlings. Environ Exp Bot 145:95–103CrossRefGoogle Scholar
  101. Tan JL, Wang CY, Xiang B, Han RH, Guo ZF (2013) Hydrogen peroxide and nitric oxide mediated cold-and dehydration-induced myo-inositol phosphate synthase that confers multiple resistances to abiotic stresses. Plant Cell Environ 36:288–299PubMedCrossRefGoogle Scholar
  102. Tian S, Wang X, Li P, Wang H, Ji H, Xie J, Qui Q, Shen D, Dong H (2016) Plant aquaporin AtPIP1; 4 links apoplastic H2O2 induction to disease immunity pathways. Plant Physiol 171:1635–1650PubMedPubMedCentralCrossRefGoogle Scholar
  103. Tossi V, Lamattina L, Jenkins GI, Cassia RO (2014) Ultraviolet-B-induced stomatal closure in Arabidopsis is regulated by the UV RESISTANCE LOCUS8 photoreceptor in a nitric oxide-dependent mechanism. Plant Physiol 164:2220–2230PubMedPubMedCentralCrossRefGoogle Scholar
  104. Tripathi DK, Singh S, Singh S, Srivastava PK, Singh VP, Singh S, Prasad SM, Singh PK, Dubey NK, Pandey AC, Chauhan DK (2017) Nitric oxide alleviates silver nanoparticles (AgNps)-induced phytotoxicity in Pisum sativum seedlings. Plant Physiol Biochem 110:167–177PubMedCrossRefPubMedCentralGoogle Scholar
  105. Wang Y, Chen T, Zhang C, Hao H, Liu P, Zheng M, Baluska F, Samai J, Lin J (2009) Nitric oxide modulates the influx of extracellular Ca2+ and actin filament organization during cell wall construction in Pinus bungeana pollen tubes. New Phytol 182:851–862PubMedCrossRefPubMedCentralGoogle Scholar
  106. Wang L, Guo Y, Jia L, Chu H, Zhou S, Chen K, Zhao L (2014) Hydrogen peroxide acts upstream of nitric oxide in the heat shock pathway in Arabidopsis seedlings. Plant Physiol 164:2184–2196PubMedPubMedCentralCrossRefGoogle Scholar
  107. Wang J, Wang Y, Lv Q, Wang L, Du J, Bao F, He YK (2017) Nitric oxide modifies root growth by S-nitrosylation of plastidial glyceraldehyde-3-phosphate dehydrogenase. Biochem Biophys Res Commun 488:88–94PubMedCrossRefPubMedCentralGoogle Scholar
  108. Wang M, Liao WB (2016) Carbon monoxide as a signaling molecule in plants. Front Plant Sci 7:572PubMedPubMedCentralGoogle Scholar
  109. Wang X, Dong X, Feng Y, Liu X, Wang J, Zhang Z, Li J, Shi S, Tu P (2018) H2O2 and NADPH oxidases involve in regulation of 2-(2-phenylethyl) chromones accumulation during salt stress in Aquilaria sinensis calli. Plant Sci 269:1–11PubMedCrossRefPubMedCentralGoogle Scholar
  110. Wojtyla Ł, Lechowska K, Kubala S, Garnczarska M (2016) Different modes of hydrogen peroxide action during seed germination. Front Plant Sci 7:66PubMedPubMedCentralCrossRefGoogle Scholar
  111. Wu Q, Su NN, Zhang XY, Liu YY, Cui J, Liang YC (2016) Hydrogen peroxide, nitric oxide and UV RESISTANCE LOCUS8 interact to mediate UV-B-induced anthocyanin biosynthesis in radish sprouts. Sci Rep 6:29164PubMedPubMedCentralCrossRefGoogle Scholar
  112. Xia XJ, Gao CJ, Song LX, Zhou YH, Shi K, Yu JQ (2014) Role of H2O2 dynamics in brassinosteroid-induced stomatal closure and opening in Solanum lycopersicum. Plant Cell Environ 37:2036–2050PubMedCrossRefPubMedCentralGoogle Scholar
  113. Xu L, Yue Q, Xiang G, Bian FE, Yao Y (2018) Melatonin promotes ripening of grape berry via increasing the levels of ABA, H2O2, and particularly ethylene. Horticult Res 5:41CrossRefGoogle Scholar
  114. Yu QX, Ahammed GJ, Zhou YH, Shi K, Zhou J, Yu YL, Yu JQ, Xia XJ (2017) Nitric oxide is involved in the oxytetracycline-induced suppression of root growth through inhibiting hydrogen peroxide accumulation in the root meristem. Sci Rep 7:43096PubMedPubMedCentralCrossRefGoogle Scholar
  115. Zhang F, Wang YP, Yang YL, Wu H, Wang D, Liu JQ (2007) Involvement of hydrogen peroxide and nitric oxide in salt resistance in the calluses from Populus euphratica. Plant Cell Environ 30:775–785PubMedCrossRefPubMedCentralGoogle Scholar
  116. Zhang TY, Li FC, Fan CM, Li X, Zhang FF, He JM (2017) Role and interrelationship of MEK1-MPK6 cascade, hydrogen peroxide and nitric oxide in darkness-induced stomatal closure. Plant Sci 262:190–199PubMedCrossRefPubMedCentralGoogle Scholar
  117. Zhou J, Wang J, Li X, Xia XJ, Zhou YH, Shi K, Chen ZX, Yu JQ (2014) H2O2 mediates the crosstalk of brassinosteroid and abscisic acid main tomato responses to heat and oxidative stresses. J Exp Bot 65:4371–4383PubMedPubMedCentralCrossRefGoogle Scholar
  118. Zhu Y, Liao W, Niu L, Wang M, Ma Z (2016) Nitric oxide is involved in hydrogen gas-induced cell cycle activation during adventitious root formation in cucumber. BMC Plant Biol 16:146PubMedPubMedCentralCrossRefGoogle Scholar
  119. Zhu XF, Zhu CQ, Wang C, Dong XY, Shen RF (2017) Nitric oxide acts upstream of ethylene in cell wall phosphorus reutilization in phosphorus-deficient rice. J Exp Bot 68:753–760PubMedPubMedCentralGoogle Scholar
  120. Zou LJ, Deng XG, Zhang LE, Zhu T, Tan WR, Muhammad A, Zhu LJ, Zhang C, Zhang DW, Lin HH (2018) Nitric oxide as a signaling molecule in brassinosteroid-mediated virus resistance to Cucumber mosaic virus in Arabidopsis thaliana. Physiol Plant 163:196–210PubMedCrossRefPubMedCentralGoogle Scholar

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© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.College of HorticultureGansu Agricultural UniversityLanzhouChina

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