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Nitric Oxide and Reactive Oxygen Species Interactions in Plant Tolerance and Adaptation to Stress Factors

Chapter

Abstract

The research on the regulatory role of reactive oxygen species (ROS) and reactive nitrogen species (RNS) in plants’ life indisputably proved the involvement of these compounds in numerous life processes, including developmental and stress ones. Generation of both ROS and RNS occurs concomitantly, leading to some specific plant responses, and each group of compound interacts with the other one, which involves complexity and is sometimes difficult to understand and study. For this reason, the chapter will integrate the papers on biotic and abiotic stress response and provides an overview of the molecular mechanism of:
  • ROS/RNS signalling

  • The phenotypic response

  • The perspective of use ROS and RNS in biotechnology and food production

Keywords

Hydrogen peroxide ROS RNS Phytohormones Plans stress response ROS and RNS signalling Shelf life of fruits 

References

  1. Abat JK, Deswal R (2009) Differential modulation of S-nitrosoproteome of Brassica juncea by low temperature: change in S-nitrosylation of Rubisco is responsible for the inactivation of its carboxylase activity. Proteomics 9:4368–4380PubMedCrossRefGoogle Scholar
  2. Abat JK, Mattoo AK, Deswal R (2008) S-nitrosylated proteins of a medicinal CAM plant Kalanchoe pinnata–ribulose-1, 5-bisphosphate carboxylase/oxygenase activity targeted for inhibition. FEBS J 275:2862–2872PubMedCrossRefGoogle Scholar
  3. Albertos P, Romero-Puertas MC, Tatematsu K et al (2015) S-nitrosylation triggers ABI5 degradation to promote seed germination and seedling growth. Nat Commun 6:8669.  https://doi.org/10.1038/ncomms9669CrossRefPubMedPubMedCentralGoogle Scholar
  4. Alderton WK, Cooper CE, Knowles RG (2001) Nitric oxide synthases: structure, function and inhibition. Biochem J 357:593–615PubMedPubMedCentralCrossRefGoogle Scholar
  5. Ambrozova G, Martiskova H, Koudelka A et al (2016) Nitro-oleic acid modulates classical and regulatory activation of macrophages and their involvement in pro-fibrotic responses. Free Radic Biol Med 90:252–260PubMedCrossRefGoogle Scholar
  6. Arasimowicz-Jelonek M, Floryszak-Wieczorek J, Gwóźdź E (2011) The messenger of nitric oxide in cadmium-challenged plants. Plant Sci 181:612–620PubMedCrossRefGoogle Scholar
  7. Asada K (1994a) Mechanisms for scavenging reactive molecules generated in chloroplasts under light stress. In: Baker NR, Bowyer JR (eds) Photoinhibition of photosynthesis: from molecular mechanisms to the field. Bios Scientific Publishers, Oxford, pp 129–142Google Scholar
  8. Asada K (1994b) Production and action of active oxygen species in photosynthetic tissues. In: Foyer CH, Mullineaux PM (eds) Causes of photooxidative stress and amelioration of defense system in plants. CRC Press, Boca Raton, pp 77–104Google Scholar
  9. Bączek-Kwinta R, Miszalski Z, Niewiadomska E (2005) Physiological role of reactive oxygen species in chill-sensitive plants. Phyton – Annales Rei Botanicae 45:25–37Google Scholar
  10. Badiyan D, Wills RBH, Bowyer MC (2004) Use of a nitric oxide donor compound to extend the vase life of cut flowers. Hortscience 39:1371–1372Google Scholar
  11. Bai X, Yang L, Tian M et al (2011) Nitric oxide enhances desiccation tolerance of recalcitrant Antiaris toxicaria seeds via protein S-nitrosylation and carbonylation. PLoS One 6(6):e20714.  https://doi.org/10.1371/journal.pone.0020714CrossRefPubMedPubMedCentralGoogle Scholar
  12. Bailly C (2004) Active oxygen species and antioxidants in seed biology. Seed Sci Res 14:93–107CrossRefGoogle Scholar
  13. Barna B, Fodor J, Harrach BD et al (2012) The Janus face of reactive oxygen species in resistance and susceptibility of plants to necrotrophic and biotrophic pathogens. Plant Physiol Biochem 59:37–43PubMedCrossRefGoogle Scholar
  14. Bartoli CG, Simontacchi M, Montaldi ER et al (1997) Oxidants and antioxidants during aging of chrysanthemum petals. Plant Sci 129:157–165CrossRefGoogle Scholar
  15. Bartoli CC, Casalongué C, Simintacchi M et al (2013) Interactions between hormone and redox signaling pathways in the control of growth and cross tolerance to stress. Environ Exp Bot 94:73–88CrossRefGoogle Scholar
  16. Belenhgi B, Romero-Puertas M-C, Vercammen D et al (2007) Metacaspase activity of Arabidopsis thaliana is regulated by nitrosylation of a critical cysteine residue. J Biol Chem 282:1352–1358CrossRefGoogle Scholar
  17. Beligni MV, Lamattina L (2000) Nitric oxide stimulates seed germination and de-etiolation, and inhibits hypocotyl elongation, three light-inducible responses in plants. Planta 210:215–221PubMedCrossRefGoogle Scholar
  18. Beligni MV, Fath A, Bethke PC, Lamattina L, Jones RL (2002) Nitric oxide acts as an antioxidant and delays programmed cell death in barley aleurone layers. Plant Physiol 129(4):1642–1650PubMedPubMedCentralCrossRefGoogle Scholar
  19. Bellin D, Asai S, Delledonne M et al (2013) Nitric oxide as a mediator for defense responses. MPMI 26:271–277PubMedCrossRefGoogle Scholar
  20. Besson-Bard A, Pugin A, Wendehenne D (2008) New insights into nitric oxide signalling in plants. Annu Rev Plant Biol 59:21–39PubMedCrossRefGoogle Scholar
  21. Boscari A, Del Giudice J, Ferrarini A et al (2013) Expression dynamics of the Medicago truncatula transcriptome during the symbiotic interaction with Sinorhizobium meliloti: which role for nitric oxide? Plant Physiol 161:425–439PubMedCrossRefGoogle Scholar
  22. Bowyer MC, Wills RBH, Badiyan D et al (2003) Extending the postharvest life of carnations with nitric oxide comparison of fumigation and in vivo delivery. Postharvest Biol Technol 30:281–286CrossRefGoogle Scholar
  23. Bright J, Desikan R, Hancock JT et al (2006) ABA-induced NO generation and stomatal closure in Arabidopsis are dependent on H2O2 synthesis. Plant J 45:113–122PubMedCrossRefGoogle Scholar
  24. Brody AL, Strupinsky EL, Kline LR (eds) (2001) Active packaging for food applications. CRC Press, Boca Raton, pp 112–120Google Scholar
  25. Cai MZ, Zhang SN, Wang FM et al (2011) Protective effect of exogenously applied nitric oxide on aluminum-induced oxidative stress in soybean plants. Russ J Plant Physiol 58:791–779CrossRefGoogle Scholar
  26. Camejo D, Romero-Puertas MC, Rodríguez-Serrano M et al (2013) Salinity-induced changes in S-nitrosylation of pea mitochondrial proteins. J Proteome 79:87–99CrossRefGoogle Scholar
  27. Chaki M, Carreras A, Lopez-Jaramillo J et al (2013) Tyrosine nitration provokes inhibition of sunflower carbonic anhydrase (beta-CA) activity under high temperature stress. Nitric Oxide 29:30–33PubMedCrossRefGoogle Scholar
  28. Chen Z, Gallie DR (2004) The ascorbic acid redox state controls guard cell signalling and stomatal movement. Plant Cell 16:1143–1162PubMedPubMedCentralCrossRefGoogle Scholar
  29. Chen R, Sun S, Wang C et al (2009) The Arabidopsis PARAQUATRESISTANT2 gene encodes an S-nitrosoglutathione reductase that is a key regulator of cell death. Cell Res 19:1377–1387PubMedCrossRefGoogle Scholar
  30. Chen Z, Zhang L, Zhu C (2015) Exogenous nitric oxide mediates alleviation of mercury toxicity by promoting auxin transport in roots or preventing oxidative stress in leaves of rice seedlings. Acta Physiol Plant 37:197.  https://doi.org/10.1007/s11738-015-1931-7CrossRefGoogle Scholar
  31. Cheng G, Yang E, Lu W et al (2009) Effect of nitric oxide on ethylene synthesis and softening of banana fruit slice during ripening. J Agric Food Chem 57:5799–5804PubMedCrossRefGoogle Scholar
  32. Corpas FJ (2015) What is the role of hydrogen peroxide in plant peroxisomes? Plant Biol J 17:1099–1103CrossRefGoogle Scholar
  33. Corpas FJ, Leterrier M, Valderrama R et al (2011) Nitric oxide imbalance provokes a nitrosative response in plants under abiotic stress. Plant Sci 181:604–611PubMedCrossRefGoogle Scholar
  34. Corpas FJ, Alché JD, Barroso JB (2013) Current overview of S-nitrosoglutathione (GSNO) in higher plants. Front Plant Sci 4:126.  https://doi.org/10.3389/fpls.2013.00126CrossRefPubMedPubMedCentralGoogle Scholar
  35. Daszkowska-Golec A, Szarejko I (2013) Open or close the gate – stomata action under the control of phytohormones in drought stress conditions. Front Plant Sci 4:138.  https://doi.org/10.3389/fpls.2013.00138CrossRefPubMedPubMedCentralGoogle Scholar
  36. Delledonne M, Xia Y, Dixon RA et al (1998) Nitric oxide functions as a signal in plant disease resistance. Nature 394:585–588PubMedCrossRefGoogle Scholar
  37. Delledonne M, Zeier J, Marocco A et al (2001) Signal interactions between nitric oxide and reactive oxygen intermediates in the plant hypersensitive disease response. Proc Natl Acad Sci U S A 98:13454–13459PubMedPubMedCentralCrossRefGoogle Scholar
  38. Desikan R, Hancock JT, Bright J et al (2005) A role for ETR1 in hydrogen peroxide signaling in stomatal guard cells. Plant Physiol 137:831–834PubMedPubMedCentralCrossRefGoogle Scholar
  39. Desikan R, Last K, Harrett-Williams R et al (2006) Ethylene-induced stomatal closure in Arabidopsis occurs via AtrbohF-mediated hydrogen peroxide synthesis. Plant J 47:907–916PubMedCrossRefGoogle Scholar
  40. Driscoll JA (1997) Acid rain demonstration: the formation of nitrogen oxides as a by-product of high-temperature flames in connection with internal combustion engines. J Chem Educ 74:1424.  https://doi.org/10.1021/ed074p1424CrossRefGoogle Scholar
  41. Durner J, Wendehenne D, Klessig DF (1998) Defense gene induction in tobacco by nitric oxide, cyclic GMP, and cyclic ADPribose. Proc Natl Acad Sci U S A 95:10328–11033PubMedPubMedCentralCrossRefGoogle Scholar
  42. Farnese FS, Oliveira JA, Paiva EAS et al (2017) The involvement of nitric oxide in integration of plant physiological and ultrastructural adjustments in response to arsenic. Front Plant Sci 8:516.  https://doi.org/10.3389/fpls.2017.00516CrossRefPubMedPubMedCentralGoogle Scholar
  43. Farneti B, Khomenko J, Cappellin L et al (2015) Dynamic volatile organic compound fingerprinting of apple fruit during processing. LWT Food Sci Technol 63:21–28CrossRefGoogle Scholar
  44. Fath A, Bethke PC, Jones RL (2001) Enzymes that scavenge reactive oxygen species are down-regulated prior to gibberellic acid-induced programmed cell death in barley aleurone. Plant Physiol 126:156–166PubMedPubMedCentralCrossRefGoogle Scholar
  45. Feechan A, Kwon E, Yun B-W et al (2005) A central role for S-nitrosothiols in plant disease resistance. Proc Natl Acad Sci 102:8054–8059PubMedPubMedCentralCrossRefGoogle Scholar
  46. Floryszak-Wieczorek J, Arasimowicz M, Milczarek G et al (2007) Only an early nitric oxide burst and the following wave of secondary nitric oxide generation enhanced effective defence responses of pelargonium to a necrotrophic pathogen. New Phytol 175:718–730PubMedCrossRefGoogle Scholar
  47. Foyer CH, Noctor G (2005) Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. Plant Cell 17:1866–1875PubMedPubMedCentralCrossRefGoogle Scholar
  48. Foyer CH, Shigeoka S (2011) Understanding oxidative stress and antioxidant functions to enhance photosynthesis. Plant Physiol 155:93–100PubMedCrossRefGoogle Scholar
  49. Foyer CH, Lopez-Delgado H, Dat JF et al (1997) Hydrogen peroxide- and glutathione-associated mechanism of acclimatory stress tolerance and signalling. Physiol Plant 100:241–254CrossRefGoogle Scholar
  50. Galatro A, Puntarulo S, Guiamet JJ et al (2013) Chloroplast functionality has a positive effect on nitric oxide level in soybean cotyledons. Plant Physiol Biochem 66:26–33PubMedCrossRefGoogle Scholar
  51. García-Mata C, Lamattina L (2003) Abscisic acid, nitric oxide and stomatal closure – is nitrate reductase one of the missing links? Trends Plant Sci 1:20–26CrossRefGoogle Scholar
  52. Grefen C, Städele K, Ruzicka K et al (2008) Subcellular localization and in vivo interactions of the Arabidopsis thaliana ethylene receptor family members. Mol Plant 1:308–320PubMedCrossRefGoogle Scholar
  53. Gupta KJ, Fernie AR, Kaiser WM et al (2011) On the origins of nitric oxide. Trends Plant Sci 16:160–168PubMedCrossRefGoogle Scholar
  54. Hasanuzzaman M, Fujita M (2013) Exogenous sodium nitroprusside alleviates arsenic-induced oxidative stress in wheat (Triticum aestivum L.) seedlings by enhancing antioxidant defense and glyoxalase system. Ecotoxicology 22:584–596PubMedCrossRefGoogle Scholar
  55. He YK, Tang RH, Yi H et al (2004) Nitric oxide represses the Arabidopsis floral transition. Science 305:1968–1971PubMedCrossRefGoogle Scholar
  56. Herrera-Vásquez A, Salinas P, Holuigue L (2015) Salicylic acid and reactive oxygen species interplay in the transcriptional control of defense genes expression. Front Plant Sci 5:171.  https://doi.org/10.3389/fpls.2015.00171CrossRefGoogle Scholar
  57. Hess DT, Matsumoto A, Kim S et al (2005) Protein S-nitrosylation: purview and parameters. Nat Rev Mol Cell Biol 6:150–166PubMedCrossRefGoogle Scholar
  58. Hu X, Neill SJ, Tang Z et al (2005) Nitric oxide mediates gravitropic bending in soybean roots. Plant Physiol 137:663–670PubMedPubMedCentralCrossRefGoogle Scholar
  59. Huque R, Wills RBH, Pristijono P et al (2013) Effect of nitric oxide (NO) and associated control treatments on the metabolism of fresh-cut apple slices in relation to development of surface browning. Postharvest Biol Technol 78:16–23CrossRefGoogle Scholar
  60. Hura K, Hura T, Bączek-Kwinta R et al (2014) Induction of defense mechanisms in seedlings of oilseed winter rape inoculated with Phoma lingam (Leptosphaeria maculans). Phytoparasitica 42:145–154CrossRefGoogle Scholar
  61. Ignarro IJ, Buga GM, Wood KS et al (1987) Endothelium-derived relaxing factor produced and released from artery and vein is nitric oxide. Proc Natl Acad Sci U S A 84:9265–9269PubMedPubMedCentralCrossRefGoogle Scholar
  62. Jeandroz S, Wipf D, Stuehr DJ et al (2016) Occurrence, structure, and evolution of nitric oxide synthaselike proteins in the plant kingdom. Sci Signal 9(417):re 2.  https://doi.org/10.1126/scisignal.aad4403CrossRefGoogle Scholar
  63. Karpinski S, Szechynska-Hebda M (2010) Secret life of plants. From memory to intelligence. Plant Signal Behav 5:1391–1394PubMedPubMedCentralCrossRefGoogle Scholar
  64. Kato H, Takemoto D, Kawakita K (2013) Proteomic analysis of S-nitrosylated proteins in potato plant. Physiol Plant 148:371–386PubMedCrossRefGoogle Scholar
  65. Kazemi N, Khavari-Nejad RA, Fahimi H et al (2010) Effects of exogenous salicylic acid and nitric oxide on lipid peroxidation and antioxidant enzyme activities in leaves of Brassica napus L. under nickel stress. Sci Hortic 126:402–407CrossRefGoogle Scholar
  66. Khan MI, Fatma M, Per TS et al (2015) Salicylic acid-induced abiotic stress tolerance and underlying mechanisms in plants. Front Plant Sci 6:462.  https://doi.org/10.3389/fpls.2015.00462CrossRefPubMedPubMedCentralGoogle Scholar
  67. Kopczewski T, Kuzniak E (2013) Redox signals as a language of interorganellar communication in plant cells. Centr Eur J Biol 8:1153–1183Google Scholar
  68. Kopyra M, Gwóźdź E (2003) Nitric oxide stimulates seeds germination and counteracts the inhibitory effect of heavy metal and salinity on root growth of Lupinus luteus. Plant Physiol Biochem 441:1011–1017CrossRefGoogle Scholar
  69. Kreslavski VD, Los DA, Allakhverdiev SI et al (2012) Signaling role of reactive oxygen species in plants under stress. Russ J Plant Physiol 59:141–154CrossRefGoogle Scholar
  70. Kusznierewicz B, Bączek-Kwinta R, Bartoszek A et al (2012) The dose-dependent influence of zinc and cadmium contamination of soil on their uptake and glucosinolate content in white cabbage (Brassica oleracea var. capitata f. alba). Environ Toxicol Chem 31:2482–2489PubMedCrossRefGoogle Scholar
  71. Lamotte O, Bertoldo JB, Besson-Bard A et al (2015) Protein S-nitrosylation: specificity and identification strategies in plants. Front Chem 2:114.  https://doi.org/10.3389/fchem.2014.00114CrossRefPubMedPubMedCentralGoogle Scholar
  72. Lee U, Wie C, Fernandez BO et al (2008) Modulation of nitrosative stress by S-nitrosoglutathione reductase is critical for themotolerance and plant growth in Arabidopsis. Plant Cell 20:786–802.  https://doi.org/10.1105/tpc.107.052647CrossRefPubMedPubMedCentralGoogle Scholar
  73. Leshem YY (1988) Plant senescence processes and free radicals. Free Rad Biol Med 5:39–49PubMedCrossRefGoogle Scholar
  74. Leshem YY, Wills RBH, Ku VVV (1998) Evidence for the function of the free radical gas nitric oxide (NO) as an endogenous maturation and senescence regulating factor in higher plants. Plant Physiol Biochem 36:825–833CrossRefGoogle Scholar
  75. Leterrier M, Airaki M, Palma JM et al (2012) Arsenic triggers the nitric oxide (NO) and S-nitrosoglutathione (GSNO) metabolism in Arabidopsis. Environ Pollut 166:136–143PubMedCrossRefGoogle Scholar
  76. Lin A, Wang Y, Tang J et al (2012) Nitric oxide and protein S-nitrosylation are integral to hydrogen peroxide-induced leaf cell death in rice. Plant Physiol 158:451–464PubMedCrossRefGoogle Scholar
  77. Lindermayr C, Saalbach G, Durner J (2005) Proteomic identification of S-nitrosylated proteins in Arabidopsis. Plant Physiol 137:921–930PubMedPubMedCentralCrossRefGoogle Scholar
  78. Lozano-Juste J, Leon J (2011) Nitric oxide regulates DELLA content and PIF expression to promote photomorphogenesis in Arabidopsis. Plant Physiol 156:1410–1423PubMedPubMedCentralCrossRefGoogle Scholar
  79. Malik SI, Hussain A, Yun BW et al (2011) GSNOR-mediated de-nitrosylation in the plant defence response. Plant Sci 181:540–544PubMedCrossRefGoogle Scholar
  80. Manjunatha G, Lokesh V, Neelwarne B (2010) Nitric oxide in fruit ripening: trends and opportunities. Biotechnol Adv 28:489–499PubMedCrossRefGoogle Scholar
  81. Mata-Pérez C, Sánchez-Calvo B, Padilla-Serrano MN et al (2016) Nitro-fatty acids in plant signaling: nitro-linolenic acid induces the molecular chaperone network in Arabidopsis. Plant Physiol 170:686–670PubMedCrossRefGoogle Scholar
  82. Mata-Pérez C, Sánchez-Calvo B, Padilla MN et al (2017) Nitro-fatty acids in plant signaling: new key mediators of nitric oxide metabolism. Redox Biol 11:554–561.  https://doi.org/10.1016/j.redox.2017.01.002CrossRefPubMedPubMedCentralGoogle Scholar
  83. Mor A, Koh E, Weiner L et al (2014) Singlet oxygen signatures are detected independent of light in chloroplast in response to multiple stresses. Plant Physiol 165:249–261PubMedPubMedCentralCrossRefGoogle Scholar
  84. Moreau M, Lindermayr C, Durner J et al (2010) NO synthesis and signalling in plants – where do we stand? Physiol Plant 138:372–383PubMedCrossRefGoogle Scholar
  85. Noritake T, Kawakita K, Doke N (1996) Nitric oxide induces phytoalexin accumulation in potato tuber tissues. Plant Cell Physiol 37:113–116CrossRefGoogle Scholar
  86. Pagnussat GC, Lanteri ML, Lamattina L (2003) Nitric oxide and cyclic GMP are messengers in the indole acetic acid-induced adventitious rooting process. Plant Physiol 132:1241–1248PubMedPubMedCentralCrossRefGoogle Scholar
  87. Palmer RMJ, Ferrige AG, Moncada S (1987) Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor. Nature 327:524–526PubMedCrossRefGoogle Scholar
  88. Pei Z-M, Murata Y, Benning G et al (2000) Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells. Nature 406:731–734PubMedCrossRefGoogle Scholar
  89. Politycka B (1996) Peroxidase activity and lipid peroxidation in roots of cucumber seedlings influenced by derivatives of cinnamic and benzoic acids. Acta Physiol Plant 18:365–370Google Scholar
  90. Portmann RW, Daniel JS, Ravishankara AS (2012) Stratospheric ozone depletion due to nitrous oxide: influences of other gases. Philos Trans R Soc Lond B Biol Sci 367:1256–1264PubMedPubMedCentralCrossRefGoogle Scholar
  91. Pristijono P, Wills RBH, Golding JB (2008) Use of the nitric oxide-donor compound, diethylenetriamine-nitric oxide (DETANO), as an inhibitor of browning in apple slices. J Hortic Sci Biotechnol 83:555–558CrossRefGoogle Scholar
  92. Romero-Puertas MC, Campostrini N, Mattè A et al (2008) Proteomic analysis of S-nitrosylated proteins in Arabidopsis thaliana undergoing hypersensitive response. Proteomics 8:1459–1469PubMedCrossRefGoogle Scholar
  93. Rümer S, Kapuganti JG, Kaiser W (2009) Oxidation of hydroxylamines to NO by plant cells. Plant Signal Behav 4:853–855PubMedPubMedCentralCrossRefGoogle Scholar
  94. Sahay S, Gupta M (2017) An update on nitric oxide and its benign role in plant responses under metal stress. Nitric Oxide 67:39–52.  https://doi.org/10.1016/j.niox.2017.04.011CrossRefPubMedGoogle Scholar
  95. Saito S, Yamamoto-Katou A, Yoshioka H et al (2006) Peroxynitrite generation and tyrosine nitration in defense responses in tobacco BY-2 cells. Plant Cell Physiol 47:689–697PubMedCrossRefGoogle Scholar
  96. Schopfer P, Liszkay A, Bechtold M et al (2002) Evidence that hydroxyl radicals mediate auxin-induced extension growth. Planta 214:821–828PubMedCrossRefGoogle Scholar
  97. Shah FR, Ahmad N, Masood KR et al (eds) (2010) Plant adaptation and phytoremediation. Springer, New York, pp 71–97CrossRefGoogle Scholar
  98. Shi S, Wang G, Wang Y et al (2005) Protective effect of nitric oxide against oxidative stress under ultraviolet-Β radiation. Nitric Oxide 13:1–9PubMedCrossRefGoogle Scholar
  99. Silva L, Carvalho H (2013) Possible role of glutamine synthetase in the NO signaling response in root nodules by contributing to the antioxidant defenses. Front Plant Sci 4:372.  https://doi.org/10.3389/fpls.2013.00372CrossRefPubMedPubMedCentralGoogle Scholar
  100. Soegiarto L, Wills RBH (2004) Short term fumigation with nitric oxide gas in air to extend the postharvest life of broccoli, green bean, and bok choy. HortTechnology 14:538–540Google Scholar
  101. Solanki R, Dhankhar R (2011) Biochemical changes and adaptive strategies of plants under heavy metal stress. Biologia 66:195–204CrossRefGoogle Scholar
  102. Sun B, Jing Y, Chen K et al (2007) Protective effect of nitric oxide on iron deficiency-induced oxidative stress in maize (Zea mays). J Plant Physiol 164:536–543PubMedCrossRefGoogle Scholar
  103. Terrile MC, París R, Calderón-Villalobos LI et al (2012) Nitric oxide influences auxin signaling through S-nitrosylation of the Arabidopsis TRANSPORT INHIBITOR RESPONSE 1 auxin receptor. Plant J 70:492–500PubMedPubMedCentralCrossRefGoogle Scholar
  104. Tuteja N, Chandra M, Tuteja R et al (2004) Nitric oxide as a unique bioactive signaling messenger in physiology and pathophysiology. J Biomed Biotechnol 4:227–237CrossRefGoogle Scholar
  105. Valderrama R, Corpas FJ, Carreras A et al (2007) Nitrosative stress in plants. FEBS Lett 581:453–461PubMedCrossRefGoogle Scholar
  106. Van Doorn VG (2011) Classes of programmed cell death in plants, compared to those in animals. J Exp Bot 62:4749–4761PubMedCrossRefGoogle Scholar
  107. Vanlerberghe GC (2013) Alternative oxidase: amitochondrial respiratory pathway to maintain metabolic and signaling homeostasis during abiotic and biotic stress in plants. Int J Mol Sci 14:6805–6847PubMedPubMedCentralCrossRefGoogle Scholar
  108. Vellosillo T, Vicente J, Kulasekaran S et al (2010) Emerging complexity in reactive oxygen species production and signaling during the response of plants to pathogens. Plant Physiol 154:444–448PubMedPubMedCentralCrossRefGoogle Scholar
  109. Villacorta L, Gao Z, Schopfer FJ et al (2015) Nitro-fatty acids in cardiovascular regulation and diseases: characteristics and molecular mechanisms. Front Biosci (Landmark Ed) 21:873–889CrossRefGoogle Scholar
  110. Vreeburg AM, Fry SC (2005) Reactive oxygen species in cell walls. In: Smirnoff N (ed) Antioxidants and reactive oxygen species in plants. Blackwell Publishing, Oxford, pp 197–214Google Scholar
  111. Wang BL, Tang XY, Cheng LY et al (2010) Nitric oxide is involved in phosphorus deficiency-induced cluster-root development and citrate exudation in white lupin. New Phytol 187:1112–1123PubMedCrossRefGoogle Scholar
  112. Wang Y, Loake GJ, Chu C (2013) Cross-talk of nitric oxide and reactive oxygen species in plant programmed cell death. Front Plant Sci 4:314.  https://doi.org/10.3389/fpls.2013.00314CrossRefPubMedPubMedCentralGoogle Scholar
  113. Wendehenne D, Pugin A, Klessig DF et al (2001) Nitric oxide: comparative synthesis and signaling in animal and plant cells. Trends Plant Sci 6:177–183PubMedCrossRefGoogle Scholar
  114. Xiong J, An L, Lu H et al (2009) Exogenous nitric oxide enhances cadmium tolerance of rice by increasing pectin and hemicelluloses content in root cell wall. Planta 230:755–765PubMedCrossRefGoogle Scholar
  115. Xu J, Wang W, Yin H et al (2010) Exogenous nitric oxide improves antioxidative capacity and induces auxin degradation in roots of Medicago truncatula seedlings under cadmium stress. Plant Soil 326:321–330CrossRefGoogle Scholar
  116. Xu S, Guerra D, Lee U et al (2013) S-nitrosoglutathione reductases are low-copy number, cysteine-rich proteins in plants that control multiple developmental and defense responses in Arabidopsis. Front Plant Sci 4:430.  https://doi.org/10.3389/fpls.2013.00430CrossRefPubMedPubMedCentralGoogle Scholar
  117. Yang Z, Zhong X, Fan Y et al (2015) Burst of reactive oxygen species in pedicel-mediated fruit abscission after carbohydrate supply was cut off in longan (Dimocarpus longan). Front Plant Sci 6:360.  https://doi.org/10.3389/fpls.2015.00360CrossRefPubMedPubMedCentralGoogle Scholar
  118. Zaharah SS, Singh Z (2011) Postharvest nitric oxide fumigation alleviates chilling injury, delays fruit ripening and maintains quality in cold-stored ‘Kensington Pride’ mango. Postharvest Biol Technol 60:202–210CrossRefGoogle Scholar
  119. Zhang X, Zhang L, Dong F et al (2001) Hydrogen peroxide is involved in abscisic acid-induced stomatal closure in Vicia faba. Plant Physiol 126:1438–1448PubMedPubMedCentralCrossRefGoogle Scholar
  120. Zhang DD, Cheng GP, Li J et al (2007) Effect of nitric oxide on disorder development and quality maintenance of plum stored at low temperature. ISHS Acta Hortic 804:549–554Google Scholar
  121. Zhang XW, Dong YJ, Qiu XK et al (2012) Exogenous nitric oxide alleviates iron-deficiency chlorosis in peanut growing on calcareous soil. Plant Soil Environ 58:111–120CrossRefGoogle Scholar
  122. Zhou J, Wang J, Li X et al (2014) H2O2 mediates the crosstalk of brassinosteroid and abscisic acid in tomato responses to heat and oxidative stress. J Exp Bot 65:4371–4383PubMedPubMedCentralCrossRefGoogle Scholar
  123. Zhu S, Zhou E (2007) Effect of nitric oxide on ethylene production in strawberry fruit during storage. Food Chem 100:1517–1522CrossRefGoogle Scholar
  124. Zhu S, Lina S, Mengchen L et al (2008) Effect of nitric oxide on reactive oxygen species and antioxidant enzymes in kiwi fruit during storage. J Sci Food Agric 88:2324–2331CrossRefGoogle Scholar
  125. Żur I, Dubas E, Krzewska M et al (2014) Antioxidant activity and ROS tolerance in triticale (x Triticosecale Wittm.) anthers affect the efficiency of microspore embryogenesis. Plant Cell Tissue Organ Cult 119:79–97CrossRefGoogle Scholar

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© Springer Nature Singapore Pte Ltd. 2018

Authors and Affiliations

  1. 1.Faculty of Agriculture and Economics, Department of Plant PhysiologyUniversity of Agriculture in CracowCracowPoland

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