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Cross Talk of Nitric Oxide and Reactive Oxygen Species in Various Processes of Plant Development: Past and Present

  • Lekshmy SatheeEmail author
  • Hari Singh Meena
  • Sandeep B. Adavi
  • Shailendra K. Jha
Chapter

Abstract

As a reactive and diffusible gaseous signal, nitric oxide (NO) regulates many physiological processes including, cell wall biosynthesis, reactive oxygen species (ROS) metabolism, stress-induced or constitutive gene expression, programmed cell death, ripening, and senescence. It also regulates plant responses to different biotic and abiotic stimuli. It also acts as a stress protectant, for example, exogenous application of NO protects rice leaves from paraquat toxicity, oxidative stress, and osmotic stress by up-regulating antioxidant defense. Similarly, NO application alleviates aluminum, lead, and cadmium toxicity by suppressing oxidative out-burst. NO production in higher plants classically involves a reductive pathway involving both nitrate reductase or non-enzymatic reduction and an oxidative pathway involving putative nitric oxide synthase (NOS)-like enzyme. The cellular NO homeostasis is maintained by reversible reaction with glutathione (GSH) producing S-nitrosoglutathione (GSNO). GSNO is metabolized by GSNO reductase (GSNOR) which controls NO and nitrosothiol levels in response to biotic and abiotic stimuli. It has recently been suggested that apart from stress responses GSNO regulates nitrate uptake and assimilation in plants.

Keywords

ROS signaling Nitric oxide Oxidative stress Stress tolerance 

References

  1. Ahlfors R, Brosche M, Kollist H, Kangasjarvi J (2009) Nitric oxide modulates ozone induced cell death hormone biosynthesis and gene expression in Arabidopsis thaliana. Plant J 58:1–12PubMedCrossRefGoogle Scholar
  2. Allan AC, Fluhr R (1997) Two distinct sources of elicited reactive oxygen species in tobacco epidermal cells. Plant Cell 9:1559–1572PubMedPubMedCentralCrossRefGoogle Scholar
  3. Allen DJ, Mckee IF, Farage PK, Baker NR (1997) Analysis of limitations to CO2 assimilation on exposure of leaves of two Brassica napus cultivars to UV-B. Plant Cell Environ 20:633–640CrossRefGoogle Scholar
  4. Asada K (1999) The water cycle in chloroplasts scavenging of active oxygens and dissipation of excess photons. Annu Rev Plant Biol 50:601–639CrossRefGoogle Scholar
  5. Astier J, Kulik A, Koen E, Besson Bard A, Bourque S, Jeandroz S, Lamotte O, Wendehenne D (2012) Protein S-nitrosylation what’s going on in plants. Free Radic Biol Med 53:1101–1110PubMedCrossRefGoogle Scholar
  6. Balazadeh S, Siddiqui H, Allu AD, Matallana Ramirez LP, Caldana C, Mehrnia M (2010) A gene regulatory network controlled by the NAC transcription factor ANA C0 92/At NAC 2/ ORE1during salt promoted senescence. Plant J 62:250–264PubMedCrossRefGoogle Scholar
  7. Banfi B, Molnar G, Maturana A, Steger K, Hegedus B, Demaurex N, Krause KH (2001) A Ca2+ activated NADPH oxidase in testis, spleen, and lymph nodes. J Biol Chem 276:37594–37601PubMedCrossRefGoogle Scholar
  8. Barroso JB, Corpas FJ, Carreras A, Sandalio LM, Valderrama R, Palma JM, Lupianez JA, del Río LA (1999) Localizationof nitric oxide in plant peroxisomes. J Biol Chem 274:36729–36733PubMedCrossRefGoogle Scholar
  9. Baudouin E (2011) The language of nitric oxide signalling. Plant Biol (Stuttg) 13:233–242CrossRefGoogle Scholar
  10. Becker JD, Boavida LC, Carneiro J, Haury M, Feijo JA (2003) Transcriptional profiling of Arabidopsis tissues reveals the unique characteristics of the pollen transcriptome. Plant Physiol 133:713–725PubMedPubMedCentralCrossRefGoogle Scholar
  11. Besson Bard A, Pugin A, Wendehenne D (2008) New insights into nitric oxide signaling in plants. Annu Rev Plant Biol 59:21–39PubMedCrossRefGoogle Scholar
  12. Bethke PC, Gubler F, Jacobsen JV, Jones RL (2004) Dormancy of Arabidopsis seeds and barley grains can be broken by nitric oxide. Planta 219:847–855PubMedCrossRefGoogle Scholar
  13. Biehler K, Fock H (1996) Evidence for the contribution of the Mehler POD reaction in dissipating excess electrons in drought stressed wheat. Plant Physiol 112:265–272PubMedPubMedCentralCrossRefGoogle Scholar
  14. Blume YB, Krasylenko YA, Demchuk OM, Yemets AI (2013) Tubulin tyrosine nitration regulates microtubule organization in plant cells. Front Plant Sci 4:530–544Google Scholar
  15. Blumthaler M, Ambach W (1990) Indication of increasing solar ultraviolet-B radiation flux in alpine regions. Science 248:206–208PubMedCrossRefGoogle Scholar
  16. Boo YC, Jung J (1999) Water deficit induced oxidative stress and antioxidative defenses in rice plants. J Plant Physiol 155:255–261CrossRefGoogle Scholar
  17. Bogdan C (2001) Nitric oxide and the regulation of gene expression. Trends Cell Biol 11:66–75Google Scholar
  18. Bozorov TA, Baldwin IT, Kim SG (2012) Identification and profiling of miRNAs during herbivory reveals jasmonate dependent and independent patterns of accumulation in Nicotiana attenuata. BMC Plant Biol 12:209PubMedPubMedCentralCrossRefGoogle Scholar
  19. Bricchi I, Leitner M, Foti M, Mithofer A, Boland W, Maffei ME (2010) Robotic mechanical wounding (MecWorm) versus herbivore induced responses early signaling and volatile emission in Lima bean (Phaseolus lunatus L.). Planta 232:719–729Google Scholar
  20. Butt Y, Lum J, Lo S (2003) Proteomic identification of plant proteins probed by mammalian nitric oxide synthase antibodies. Planta 216(5):762–771PubMedGoogle Scholar
  21. Cakmak I, Horst WJ (1991) Effect of aluminium on lipid peroxidation, superoxide dismuatse, catalase, and peroxidase activities in root tips of soybean (Glycine max). Physiol Plant 83:463–468CrossRefGoogle Scholar
  22. Cardenas L, McKenna ST, Kunkel JG, Hepler PK (2006) NAD(P)H oscillates in pollen tubes and is correlated with tip growth. Plant Physiol 142:1460–1468PubMedPubMedCentralCrossRefGoogle Scholar
  23. Chaki M, Valderrama R, Fernandez Ocana AM, Carreras A, Gomez Rodriguez MV, Pedrajas JR, Begara Morales JC, Sanchez Calvo B, Luque F, Leterrier M et al (2011) Mechanical wounding induces a nitrosative stress by down-regulation of GSNO reductase and an increase in S-nitrosothiols in sunflower (Helianthus annuus) seedlings. J Exp Bot 62:1803–1813PubMedCrossRefGoogle Scholar
  24. Chandok MR, Ytterberg AJ, van Wijk KJ, Klessig D (2003) The pathogen inducible nitric oxide synthase (iNOS) in plants is a variant of the p protein of the glycine decarboxylase complex. Cell 113:469–482PubMedCrossRefGoogle Scholar
  25. Corpas FJ, Alché JDD, Barroso JB (2013) Current overview of S-nitrosoglutathione (GSNO) in higher plants. Front Plant Sci 4:126PubMedPubMedCentralGoogle Scholar
  26. Corpas FJ, Barroso JB, Carreras A, Valderrama R, Palma JM, Leon AM et al (2006) Constitutive argininedependent nitric oxide synthase activity in different organs of pea seedlings during plant development. Planta 54:224–246Google Scholar
  27. Corpas FJ, Chaki M, Leterrier M, Barroso JB (2009) Protein tyrosine nitration: a new challenge in plants. Plant Sign Behav 4:920–923Google Scholar
  28. Correa-Aragunde N, Lombardo C, Lamattina L (2008) Nitric oxide: an active nitrogen molecule that modulates cellulose synthesis in tomato roots. New Phytol 179:386–396PubMedCrossRefGoogle Scholar
  29. Cui MH, Ok SH, Yoo KS, Jung KW, Yoo SD, Shin JS (2013) An Arabidopsis cell growth defect factor related protein CRS promotes plants enescence by increasing the production of hydrogen peroxide. Plant Cell Physiol 54:155–167PubMedCrossRefGoogle Scholar
  30. Dafni A, Motte Maues M (1998) A rapid and simple procedure to determine stigma receptivity. Sexual Plant Rep 11:177–180CrossRefGoogle Scholar
  31. Dat J, Vandenabeele S, Vranova E, Van Montagu M, Inze D, Van Breusegem F (2000) Dual action of the active oxygen species during plant stress responses. Cell Mol Life Sci 57:779–795PubMedCrossRefGoogle Scholar
  32. Del Rio LA, Corpas FJ, Sandalio LM, Palma JM, Gomez M, Barroso JB (2002) Reactive oxygen species antioxidant systems and nitric oxide in peroxisomes. J Exp Bot 53:1255–1272PubMedCrossRefGoogle Scholar
  33. Delledonne M, Xia Y, Dixon RA, Lamb C (1998) Nitric oxide functions as a signaling plant disease resistance. Nature 394:585–588PubMedCrossRefGoogle Scholar
  34. 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 98:13454–13459PubMedCrossRefGoogle Scholar
  35. Di Stasi AM, Mallozzi C, Macchia G, Maura G, Petrucci TC, Minetti M (2002) Peroxy nitrite affects exocytosis and SNARE complex formation and induces tyrosine nitration of synaptic proteins. J Neuro Chem 82:420–429Google Scholar
  36. Dresselhaus T (2006) Cell-cell communication during double fertilization. Curr Opin Plant Biol 9:41–47PubMedCrossRefGoogle Scholar
  37. Du S, Zhang Y, Lin X, Wang Y, Tang C (2008) Regulation of nitrate reductase by nitric oxide in Chinese cabbage pakchoi (Brassica chinensis L.). Plant Cell Environ 31(2):195–204PubMedGoogle Scholar
  38. Du S, Zhang R, Zhang P, Liu H, Yan M, Chen N, Ke S (2015) Elevated CO2-induced production of nitric oxide (NO) by NO synthase differentially affects nitrate reductase activity in Arabidopsis plants under different nitrate supplies. J Exp Bot 67(3):893–904PubMedCrossRefGoogle Scholar
  39. Dupuis I, Dumas C (1990) Biochemical markers of female receptivity in maize (Zea mays L.) assessed using in vitro fertilization. Plant Sci 70:11–20CrossRefGoogle Scholar
  40. Duan YH, Zhang YL, Ye LT, Fan XR, Xu GH, Shen QR (2007) Responses of rice cultivars with different nitrogen use efficiency to partial nitrate nutrition. Ann Bot 99:1153–1160PubMedPubMedCentralCrossRefGoogle Scholar
  41. Durner J, Wendehenne D, Klessig F (1998) Defense gene induction in tobacco by nitric oxide cyclic GMP and cyclic ADP ribose. Proc Natl Acad Sci U S A 95:10328–10333PubMedPubMedCentralCrossRefGoogle Scholar
  42. Elias M, Cvckova F, Obermeyer G, Zarsky V (2001) Microinjection of guanine nucleotide analogue into lily pollen tubes results in isodiametric tip expansion. Plant Biol 3:489–493CrossRefGoogle Scholar
  43. Espunya MC, De Michele R, Gomez Cadenas A, Martinez MC (2012) S-Nitrosoglutathione is a component of wound and salicylic acid induced systemic responses in Arabidopsis thaliana. J Exp Bot 63:3219–3227PubMedPubMedCentralCrossRefGoogle Scholar
  44. Feijo JA, Sainhas J, Holdaway Clarke T, Cordeiro S, Kunkel JG, Hepler PK (2001) Cellular oscillations and the regulation of growth the pollen tube paradigm. Bioessays 23:86–94PubMedCrossRefGoogle Scholar
  45. Feijó JA, Sainhas J, Holdaway-Clarke T, Cordeiro MS, Kunkel JG, Hepler PK (2001) Cellular oscillations and the regulation of growth: the pollen tube paradigm. Bioessays 23:86–94PubMedCrossRefGoogle Scholar
  46. Feijo JA, Costa SS, Prado AM, Becker JD, Certal AC (2004) Signalling by tips. Curr Opin Plant Biol 7:589–598PubMedCrossRefGoogle Scholar
  47. Feio JA, Sainhas J, Hackett GR, Kunkel JG, Hepler PK (1999) Growing pollen tubes possess a constitutive alkaline band in theclear zone and a growth dependent acidic tip. J Cell Biol 144:483–496CrossRefGoogle Scholar
  48. Foreman J, Demidchik V, Bothwell JHF, Mylona P, Miedema H, Torres MA, Linstead P, Costa S, Brownlee C, Jones JDG, Davies JM, Dolan L (2003) Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422:442–446PubMedCrossRefGoogle Scholar
  49. Foyer CH, Harbinson J (1994) Oxygen metabolism and the regulation of photosynthetic electron transport. In: Foyer CH, Mullineaux PM (eds) Causes of photo oxidative stresses and amelioration of defense system in plants. CRC, Boca Raton, FL, pp 1–42Google Scholar
  50. Foyer CH, Noctor G (2000) Oxygen processing in photosynthesis regulation and signaling. New Phytol 146:359–388CrossRefGoogle Scholar
  51. Franklin-Tong VE (2002) The difficult question of sex: plants play the mating game. Curr Opin Plant Biol 5:14–18PubMedCrossRefGoogle Scholar
  52. Frungillo L, Skelly MJ, Loake GJ, Spoel SH, Salgado I (2014) S-nitrosothiols regulate nitric oxide production and storage in plants through the nitrogen assimilation pathway. Nat Commun 5:5401PubMedPubMedCentralCrossRefGoogle Scholar
  53. Fryer MJ, Andrews JR, Oxborough K, Blowers DA, Baker NR (1998) Relationship between CO2 assimilation, photosynthetic electron transport, and active O2 metabolism in leaves of maize in the field during periods of low temperature. Plant Physiol 116:571–580Google Scholar
  54. 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 66:26–33PubMedCrossRefGoogle Scholar
  55. Gallego SM, Benavides MP, Tomaro ML (1996) Effect of heavy metal ion excess on sunflower leaves evidence for involvement of oxidative stress. Plant Sci 121:151–159CrossRefGoogle Scholar
  56. Gallego S, Benavides M, Tomaro M (2002) Involvement of an antioxidant defence system in the adaptive response to heavy metal ions in Helianthus annuus L. cells. Plant Growth Regul 36:267–273CrossRefGoogle Scholar
  57. Gao Q, Zhang L (2008) Ultraviolet-B-induced oxidative stress and antioxidant defense system responses in ascorbatedeficientvtc1 mutants of Arabidopsis thaliana. J Plant Physiol 165:138–148PubMedCrossRefGoogle Scholar
  58. Gaupels F, Kuruthukulangarakoola GT, Durner J (2011) Upstream and downstream signals of nitric oxide in pathogen defence. Curr Opin Plant Biol 14:707–714PubMedCrossRefGoogle Scholar
  59. Gechev TS, Van Breusegem F, Stone JM, Denev I, Laloi C (2006) Reactive oxygen species as signals that modulate plant stress responses and programmed cell death. Bioessays 28:1091–1101PubMedCrossRefGoogle Scholar
  60. Giannakoula A, Moustakas M, Syros T, Yupsanis T (2010) Aluminum stress induces up regulation of an efficient antioxidant system in the Al tolerant maize line but not in the Al sensitive line. Environ Exp Bot 67:487–494CrossRefGoogle Scholar
  61. Gibbs SM, Truman JM (1998) Nitric oxide and cyclic GMP regulate retinal patterning in the optic lobe of Drosophila. Neuron 20:83–93PubMedCrossRefGoogle Scholar
  62. Grob F, Durner J, Gaupels F (2013) Nitric oxide, antioxidants and prooxidants in plant defence responses. Front Plant Sci 4:419Google Scholar
  63. Grun S, Lindermayr C, Sell S, Durner J (2006) Nitric oxide and gene regulation in plants. J Exp Bot 57:507–516PubMedCrossRefGoogle Scholar
  64. Guo FQ, Okamoto M, Crawford NM (2003) Identification of a plant nitric oxide synthase gene involved in hormonal signalling. Science 302:100–103PubMedCrossRefGoogle Scholar
  65. Gupta KJ, Fernie AR, Kaiser WM, van Dongen JT (2011) On the origins of nitric oxide. Trends Plant Sci 16:160–168PubMedCrossRefGoogle Scholar
  66. Halliwell B, Gutteridge JMC (1989) Free radicals in biology and medicine, 2nd edn. Oxford University Press, OxfordGoogle Scholar
  67. Halliwell B, Gutteridge JMC (1999) Free radicals in biology and medicine. Oxford University Press, OxfordGoogle Scholar
  68. Han C, Liu Q, Yang Y (2009) Short-term effects of experimental warming and enhanced ultraviolet-B radiation on photosynthesis and antioxidant defense of Piceaa sperata seedlings. Plant Growth Regul 58:153–162CrossRefGoogle Scholar
  69. Hancock JT, Smirnoff N, Foyer CH (2006) Oxygen metabolism coming up ROSes: a holistic view of the redox metabolism of plant cells. J Exp Bot 57:ivCrossRefGoogle Scholar
  70. He J, Huang LK, Chow WS, White cross ML, Anderson JM (1993) Effects of supplementary ultraviolet-B radiation on rice and pea plants. Aust J Plant Physiol 20:129–142Google Scholar
  71. He Y, Tang RH, Hao Y, Stevens RD, Cook CW, Ahn SM et al (2004) Nitric oxide represses the Arabidopsis floral transition. Science 305:1968–1971PubMedCrossRefGoogle Scholar
  72. HediyeSekmen A, Turkan I, Takio S (2007) Differential responses of anti oxidative enzymes and lipid peroxidation to salt stress in salt-tolerant Plantagomaritima and salt sensitive Plantago media. Physiol Plant 131:399–411CrossRefGoogle Scholar
  73. Henzler T, Steudle E (2000) Transport and metabolic degradation of hydrogen peroxide in Chara corallina: model calculations and measurements with the pressure probe suggest transport of H2O2 across water channels. J Exp Bot 51:2053–2066PubMedCrossRefGoogle Scholar
  74. Hepler PK, Vidali L, Cheung AY (2001) Polarized cell growth in higher plants. Annu Rev Cell Dev Biol 17:159–187PubMedCrossRefGoogle Scholar
  75. Hern andez JA, Jim enez A, Mullineaux P, Sevilla F (2000) Tolerance of pea (Pisum sativum L.) to long-term salt stress is associated with induction of antioxidant defences. Plant Cell Environ 23:853–862CrossRefGoogle Scholar
  76. Herrero M (2003) Male and female synchrony and the regulation of mating in flowering plants. Philos Trans R Soc Lond Ser B 358:1019–1024CrossRefGoogle Scholar
  77. Heslop-Harrison J (1978) Recognition and response in the pollen–stigma interaction. In: Curtis A (ed) Cell-cell recognition, Society for Experimental Biology Symposium Series, vol 32. Society for Experimental Biology, Cambridge, pp 121–138Google Scholar
  78. Hideg E, Kalai T, Kos PB, Asada K, Hideg K (2006) Singlet oxygen in plants its significance and possible detection with double (fluorescent and spin) indicator reagents. Photo Chem Photo Biol 82:1211–1218CrossRefGoogle Scholar
  79. Hiscock SJ (2000) Genetic control of self-incompatibility in Senecio squalidus L. (Asteraceae): a successful colonizing species. Heredity 85:10–19PubMedCrossRefGoogle Scholar
  80. Hiscock SJ, McInnis SM (2003) The diversity of self-incompatibility systems in flowering plants. Plant Biol 5:23–32CrossRefGoogle Scholar
  81. Hong JK, Yun BW, Kang JG, Raja MU, Kwon E, Sorhagen K et al (2008) Nitric oxide function and signaling in plant disease resistance. J Exp Bot 59:147–154PubMedCrossRefGoogle Scholar
  82. Hu J, Aguirre M, Peto C, Alonso J, Ecker J, Chory J (2002) A role for peroxisomes in photo morphogenesis and development of Arabidopsis. Science 297:405–410PubMedCrossRefGoogle Scholar
  83. Hu WH, Song XS, Shi K, Xia XJ, Zhou YH, Yu JQ (2008) Changes in electron transport, superoxide dismutase and ascorbate peroxidase isoenzymes in chloroplasts and mitochondria of cucumber leaves as influenced by chilling. Photosynthetica 46:581–588CrossRefGoogle Scholar
  84. Hung KT, Chang CJ, Kao CH (2002) Paraquat toxicity is reduced by nitric oxide in rice leaves. J Plant Physiol 159:159–166CrossRefGoogle Scholar
  85. Huang M, Guo Z (2006) Responses of antioxidative system to chilling stress in two rice cultivars differing in sensitivity. Plant Physiol Biochem 44:828–836CrossRefGoogle Scholar
  86. Hulskamp M, Schneitz K, Pruitt RE (1995) Genetic evidence for a long range activity that directs pollen tube guidance in Arabidopsis. Plant Cell 7:57–64PubMedPubMedCentralCrossRefGoogle Scholar
  87. Ignarro J (2000) In: Ignarro JL (ed) Nitric Oxide Biology and Patho biology. Academic Press, San Diego, CA, pp 3–380CrossRefGoogle Scholar
  88. Jahnke LS, Hull MR, Long SP (1991) Chilling stress and oxygen metabolizing enzymes in Zea mays and Zeadiplo perennis. Plant Cell Environ 14:97–104CrossRefGoogle Scholar
  89. Jeandroz S, Wipf D, Stuehr DJ, Lamattina L, Melkonian M, Tian Z, Zhu Y, Carpenter EJ, Wong GKS, Wendehenne D (2016) Occurrence, structure, and evolution of nitric oxide synthase–like proteins in the plant kingdom. Sci Signal 9(417):re2–re2PubMedCrossRefGoogle Scholar
  90. Jiang H, Chen Y, Li M, Xu X, Wu G (2011) Overex pression of SGR results in oxidative stress and lesion-mimic cell death in rice seedlings. J Integr Plant Biol 53:375–387PubMedCrossRefGoogle Scholar
  91. Jing HC, Hebeler R, Oeljeklaus S, Sitek B, Stuhler K, Meyer HE et al (2008) Early leaf senescence is associated with an altered cellular redox balance in Arabidopsis cpr5/old1 mutants. Plant Biol (Stuttg) 10(Suppl 1):85–98CrossRefGoogle Scholar
  92. Johnson MA, Preuss D (2002a) Plotting a course multiple signals guide pollen tubes to their targets. Dev Cell 2:273–281PubMedCrossRefGoogle Scholar
  93. Johnson MA, Preuss D (2002b) Plotting a course: multiple signals guide pollen tubes to their targets. Dev Cell 2:273–281PubMedCrossRefGoogle Scholar
  94. KarrayBouraoui N, Harbaoui F, Rabhi M et al (2011) Different antioxidant responses to salt stress in two different provenances of Carthamus tinctorius L. Acta Physiol Plant 33:1435–1444CrossRefGoogle Scholar
  95. Keller T, Damude HG, Werner D, Doerner P, Dixon RA, Lamb C (1998) A plant homolog of the neutrophil NADPH oxidase gp91phox subunit gene encodes a plasma membrane protein with Ca2+ binding motifs. Plant Cell 10:255–266PubMedPubMedCentralGoogle Scholar
  96. Kerr EM, Fry SC (2004) Extracellular cross-linking of xylan and xyloglucan in maize cell-suspension cultures: the role of oxidative phenolic coupling. Planta 219:73–83PubMedCrossRefGoogle Scholar
  97. Khraiwesh B, Zhu JK, Zhu J (2012) Role of miRNAs and siRNAs in biotic and abiotic stress responses of plants. Biochim Biophys Acta 1819:137–148PubMedCrossRefGoogle Scholar
  98. Kjellbom P, Snogerup L, Stohr C, Reuzeau C, Mccabe PF, Pennell RI (1997) Oxidative cross-linking of plasma membrane arabinogalactan proteins. Plant J 12:1189–1196PubMedCrossRefGoogle Scholar
  99. Kong X, Zhang D, Pan J, Zhou Y, Li D (2013) Hydrogen peroxide is involved in nitric oxide induced cell death in maize leaves. Plant Biol (Stuttg) 15:53–59CrossRefGoogle Scholar
  100. Kovtun Y, Chiu WL, Tena G, Sheen J (2000) Functional analysis of oxidative stress-activated mitogen-activated protein kinase cascade in plants. Proc Natl Acad Sci U S A 97:2940–2945PubMedPubMedCentralCrossRefGoogle Scholar
  101. Kwak JM, Mori IC, Pei ZM, Leonhardt N, Torres MA, Dangl JL, Bloom RE, Bodde S, Jones JDG, Schroeder JI (2003) NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis. EMBO J 22:2623–2633PubMedPubMedCentralCrossRefGoogle Scholar
  102. Lamattina L, Garcia Mata C, Graziano M, Pagnussat G (2003) Nitric oxide: the versatility of an extensive signal molecule. Annu Rev Plant Biol 54:109–136PubMedCrossRefGoogle Scholar
  103. Leitner M, Vandelle E, Gaupels F, Bellin D, Delledonne M (2009) NO signal sinthehaze: nitric oxide signaling in plant defence. Curr Opin Plant Biol 12:451–458PubMedCrossRefGoogle Scholar
  104. Lim PO, Kim HJ, Nam HG (2007) Leaf senescence. Annu Rev Plant Biol 58:115–136PubMedCrossRefGoogle Scholar
  105. Lin CC, Jih PJ, Lin HH, Lin JS, Chang LL, Shen YH, Jeng ST (2011) Nitric oxide activates superoxide dismutase and ascorbate peroxidase to repress the cell death induced by wounding. Plant Mol Biol 77:235–249PubMedCrossRefGoogle Scholar
  106. Lin JS, Lin CC, Lin HH, Chen YC, Jeng ST (2012a) MicroR828 regulates lignin and H2O2 accumulation in sweet potato on wounding. New Phytol 196:427–440PubMedCrossRefGoogle Scholar
  107. Lin A, Wang Y, Tang J, Xue P, Li C, Liu L et al (2012b) Nitric oxide and protein S-nitrosylation are integral to hydrogen peroxide induced leaf cell death in rice. Plant Physiol 158:451–464PubMedCrossRefGoogle Scholar
  108. Liu WZ, Kong DD, Gu XX, Gao HB, Wang JZ, Xia M et al (2013) Cytokinin scan act as suppressors of nitricoxide in Arabidopsis. Proc Natl Acad Sci U S A 110:1548–1553PubMedPubMedCentralCrossRefGoogle Scholar
  109. Logan BA, Kornyeyev D, Hardison J, Holaday AS (2006) The role of antioxidant enzymes in photo protection. Photosynth Res 88:119–132PubMedCrossRefGoogle Scholar
  110. Ludidi N, Gehring C (2003) Identification of a novel protein with guanylyl cyclase activity in Arabidopsis thaliana. J Biol Chem 278:6490–6494Google Scholar
  111. Lush WM, Grieser F, Wolters Arts M (1998) Directional guidance of Nicotiana alatapollen tubes in vitro and on the stigma. Plant Physiol 118:733–741PubMedPubMedCentralCrossRefGoogle Scholar
  112. Maheshwari R, Dubey RS (2009) Nickel-induced oxidative stress and the role of antioxidant defence in rice seedlings. Plant Growth Regul 59:37–49CrossRefGoogle Scholar
  113. María JJQ, Rosario C, Elena LC, Jose AT, Antonio JC, Gonzalo MC, Juan DDA (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 68:23–37CrossRefGoogle Scholar
  114. Masclaux Daubresse C, Purdy S, Lemaitre T, Pourtau N, Taconnat L, Renou JP et al (2007) Genetic variation suggests interaction between cold acclimation and metabolic regulation of leaf senescence. Plant Physiol 143:434–446PubMedPubMedCentralCrossRefGoogle Scholar
  115. McInnis SM, Costa LM, Gutiérrez-Marcos JF, Henderson CA, Hiscock SJ (2005) Isolation and characterization of a polymorphic stigma-specific class III peroxidase gene from Senecio squalidus L. (Asteraceae). Plant Mol Biol 57:659–677PubMedCrossRefGoogle Scholar
  116. McInnis SM, Emery DC, Porter R, Desikan R, Hancock JT, Hiscock SJ (2006) The role of stigma peroxidases in flowering plants: insights from further characterization of a stigma-specific peroxidase (SSP) from Senecio squalidus (Asteraceae). J Exp Bot 57:1835–1846PubMedCrossRefGoogle Scholar
  117. Messerli MA, Creton R, Jaffe LF, Robinson KR (2000) Periodic increases in elongation rate precede increases in cytosolic Ca2+ during pollen tube growth. Dev Biol 222:84–98PubMedCrossRefGoogle Scholar
  118. Miller JD, Arteca RN, Pell EJ (1999) Senescence associated gene expression during ozone induced leaf senescence in Arabidopsis. Plant Physiol 120:1015–1024PubMedPubMedCentralCrossRefGoogle Scholar
  119. Mishina TE, Lamb C, Zeier J (2007) Expression of a nitric oxide degrading enzyme induces a senescence programme in Arabidopsis. Plant Cell Environ 30:39–52PubMedCrossRefGoogle Scholar
  120. Mishra S, Dubey RS (2005) Heavy metal toxicity induced alterations in photosynthetic metabolism in plants. In: Pessarakli MED (ed) Handbook of photosynthesis, pp 845–863Google Scholar
  121. Mishra P, Kumari B, Dubey RS (2013) Differential responses of antioxidative defense system to prolonged salinity stress in salt tolerant and salt sensitive Indica rice (Oryza sativa L.) seedlings. Protoplasma 250(1):3–19PubMedCrossRefGoogle Scholar
  122. Mittal R, Dubey RS (1991) Behaviour of peroxidases in rice: changes in enzymatic activity and isoforms in relation to salt tolerance. Plant Physiol Biochem 29:31–40Google Scholar
  123. Monshausen GB, Bibikova TN, Messerli MA, Shi C, Gilroy S (2007) Oscillations in extracellular pH and reactive oxygen species modulate tip growth of Arabidopsis root hairs. Proc Natl Acad Sci USA 104:20996–21001Google Scholar
  124. Moreau M, Lindermayr C, Durner J, Klessig DF (2010) NO synthesis and signaling in plants where do we stand. Physiol Plant 138:372–383PubMedCrossRefPubMedCentralGoogle Scholar
  125. Moussa R, Abdel Aziz SM (2008) Comparative response of drought tolerant and drought sensitive maize genotypes to water stress. Aust J Crop Sci 1:31–36Google Scholar
  126. Moustakas M, Lanaras T, Symeonidis L, Karataglis S (1994) Growth and some photosynthetic characteristics of field grown Avena sativa under copper and lead stress. Photosynthetica 30:389–396Google Scholar
  127. Moutinho A, Hussey PJ, Trewavas AT, Malho R (2001) cAMP acts as a second messenger in pollen tube growth and reorientation. Proc Natl Acad Sci U S A 98:10481–10486PubMedPubMedCentralCrossRefGoogle Scholar
  128. Munns R (2005) Genes and salt tolerance: bringing them together. New Phytol 167:645–663PubMedCrossRefGoogle Scholar
  129. Murgia I, Vazzola V, Tarantino D, Cellier F, Ravet K, Briat JF et al (2007) Knock out off erritin At Fer1 causes earlier onset of age dependent leaf senescence in Arabidopsis. Plant Physiol Biochem 45:898–907PubMedCrossRefGoogle Scholar
  130. Navabpour S, Morris K, Allen R, Harrison EAH, Mackerness S, Buchanan Wollaston V (2003) Expression of senescence enhanced genes in response to oxidative stress. J Exp Bot 54:2285–2292PubMedCrossRefGoogle Scholar
  131. Neill S, Desikan R, Han- cock J (2002) Hydrogen peroxide signalling. Curr Opin Plant Biol 5:388–395PubMedCrossRefPubMedCentralGoogle Scholar
  132. Nishiyama M, Hoshino A, Tsai L, Henley JR, Goshima Y, Tessier Lavigne M, Poo MM, Hong K (2003) Cyclic AMP/GMP dependent modulation of Ca2+ channels sets the polarity of nerve growth cone inducing turning. Nature 423:990–995PubMedCrossRefGoogle Scholar
  133. Niu YH, Guo FQ (2012) Nitric oxide regulates dark induced leaf senescence through EIN2 in Arabidopsis. J Integr Plant Biol 54:516–525PubMedCrossRefGoogle Scholar
  134. Noctor G, Veljovic-Jovanovic S, Foyer CH (2000) Peroxide process in gin photosynthesis: antioxidant coupling and redox signalling. Philos Trans R Soc Lond B Biol Sci 355:1465–1475PubMedPubMedCentralCrossRefGoogle Scholar
  135. Noctor G, Veljovic Jovanovic S, Driscoll S, Novitskaya L, Foyer CH (2002) Drought and oxidative load in the leaves of C3 plants a predominant role for photorespiration. Ann Bot 89:841–850PubMedPubMedCentralCrossRefGoogle Scholar
  136. Noritake T, Kawakita K, Doke N (1996) Nitric oxide induces phytoalexin accumulation in potato tuber tissues. Plant Cell Physiol 37:113–116CrossRefGoogle Scholar
  137. Oger E, Marino D, Guigonis JM, Pauly N, Puppo A (2012) Sulfenylated proteins in the Medicago truncatula Sinorhizobium meliloti symbiosis. J Proteomics 75:4102–4113PubMedCrossRefGoogle Scholar
  138. Orozco Cardenas ML, Ryan CA (2002) Nitric oxide negatively modulates wound signaling in tomato plants. Plant Physiol 130:487–493PubMedPubMedCentralCrossRefGoogle Scholar
  139. Orozco-Cardenas ML, Narvaez Vasquez J, Ryan CA (2001) Hydrogen peroxide acts as a second messenger for the induction of defense genes in tomato plants in response to wounding, system in, and methyl jasmonate. Plant Cell 13:179–191PubMedPubMedCentralCrossRefGoogle Scholar
  140. Palanivelu R, Preuss D (2000) Pollen tube targeting and axon guidance parallels in tip growth mechanisms. Trends Cell Biol 10:517–524PubMedCrossRefGoogle Scholar
  141. Palanivelu R, Brass L, Edlund AF, Preuss D (2003) Pollen tube growth and guidance is regulated by POP2, an Arabidopsis gene that controls GABA levels. Cell 114:47–59PubMedCrossRefGoogle Scholar
  142. Penson SP, Schuurink RC, Fath A, Gubler F, Jacobsen JV, Jones RL (1996) cGMP is required for gibberellic acid-induced gene expression in barley aleurone. Plant Cell 8:2325–2333PubMedPubMedCentralCrossRefGoogle Scholar
  143. Perez Lopez U, Robredo A, Lacuesta M et al (2009) The oxidative stress caused by salinity in two barley cultivars is mitigated by elevated CO2. Physiol Plant 135:29–42PubMedCrossRefGoogle Scholar
  144. Pourtau N, Mares M, Purdy S, Quentin N, Ruel A, Wingler A (2004) Interactions of abscisic acid and sugar signaling in the regulation of leaf senescence. Planta 219:765–772PubMedCrossRefGoogle Scholar
  145. Prado AM, Porterfield DM, Feijo JA (2004) Nitric oxide is involved in growth regulation and reorientation of pollen tubes. Development 131:2707–2714PubMedCrossRefGoogle Scholar
  146. Prasad TK (1997) Role of catalase in inducing chilling tolerance in pre-emergent maize seedlings. Plant Physiol 114:1369–1376PubMedPubMedCentralCrossRefGoogle Scholar
  147. Radyuk MS, Domanskaya IN, Shcherbakov RA, Shalygo NV (2009) Effect of low above zero temperature on the content of low molecular antioxidants and activities of antioxidant enzymes in green barley leaves. Russ J Plant Physiol 56:175–180CrossRefGoogle Scholar
  148. Rao MV, Davis KR (2001) The physiology of ozone induced cell death. Planta 213:682–690PubMedCrossRefGoogle Scholar
  149. Rao MV, Paliyath G, Ormrod DP (1996) Ultraviolet-B and ozone induced biochemical changes in antioxidant enzymes of Arabidopsis thaliana. Plant Physiol 110:125–136PubMedPubMedCentralCrossRefGoogle Scholar
  150. Rasul S, DubreuilMaurizi C, Lamotte O, Koen E, Poinssot B, Alcaraz G, Wendehenne D, Jeandroz S (2012) Nitric oxide production mediates oligogalacturonide triggered immunity and resistance to Botrytis cinerea in sexta and is important for jasmonate-elicited responses in Nicotiana attenuata. J Exp Bot 62:4605–4616Google Scholar
  151. Reeves EP, Lu H, Jacobs HL, Messina CGM, Bolsover S, Gabella G, Potma EO, Warley A, Roes J, Segal AW (2002) Killing activity of neutrophils is mediated through activation of proteases by K+ flux. Nature 416:291–297PubMedCrossRefGoogle Scholar
  152. Robek Sokolnik AZ, Asard H, Gorska Koplinska K, Gorecki RJ (2009) Cadmium and zinc-mediated oxidative burst in tobacco BY-2 cell suspension cultures. Acta Physiol Plant 31:43–49CrossRefGoogle Scholar
  153. 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 53:103–110PubMedCrossRefGoogle Scholar
  154. Romero Puertas MC, Laxa M, Matte A, Zaninotto F, Finkemeier I, Jones AM, Perazzolli M, Vandelle E, Dietz KJ, Delledonne M (2007) S-nitrosylation of peroxiredoxin II E promotes peroxynitrite mediated tyrosine nitration. Plant Cell 19:4120–4130PubMedPubMedCentralCrossRefGoogle Scholar
  155. Sagi M, Fluhr R (2001) Superoxide production by plant homologues of the gp91phox NADPH oxidase. Modulation of activity by calcium and by tobacco mosaic virus infection. Plant Physiol 126:1281–1290PubMedPubMedCentralCrossRefGoogle Scholar
  156. Sagi M, Davydov O, Orazova S, Yesbergenova Z, Ophir R, Stratmann JW, Fluhr R (2004) Plant respiratory burst oxidase homologs impinge on wound responsiveness and development in Lycopersicon esculentum. Plant Cell 16:616–628PubMedPubMedCentralCrossRefGoogle Scholar
  157. Sairam RK, Deshmukh PS, Saxena DC (1998) Role of antioxidant systems in wheat genotypes tolerance to water stress. Biol Plant 41:387–394CrossRefGoogle Scholar
  158. Sakamoto A, Ueda M, Morikawa H (2002) Arabidopsis glutathione- dependent formaldehyde dehydrogenase is an S-nitrosoglutathione reductase. FEBS Lett 515:20–24PubMedCrossRefGoogle Scholar
  159. Salt DE, Blaylock M, Kumar NPBA et al (1995) Phytoremediation: a novel strategy for the removal of toxic metals from the environment using plants. Biotechnology 13:468–474PubMedGoogle Scholar
  160. Salmi ML, Clark G, Roux SJ Jr (2013) Current status and proposed roles for nitric oxide as a key mediator of the effects of extracellular nucleotides on plant growth. Front Plant Sci 4:427PubMedPubMedCentralCrossRefGoogle Scholar
  161. Sandalio LM, Rodrıguez Serrano MLA, Rlo d, Romero Puertas MC (2009) Reactive oxygen species and signaling in cadmium toxicity. In: Rio LA, Puppo A (eds) Reactive oxygen species in plant signaling. Springer, Berlin, pp 175–189CrossRefGoogle Scholar
  162. Santolini J, André F, Jeandroz S, Wendehenne D (2017) Nitric oxide synthase in plants: where do we stand? Nitric Oxide 63:30–38PubMedCrossRefGoogle Scholar
  163. Sayfzadeh S, Rashidi M (2011) Response of antioxidant enzymes activities of sugar beet to drought stress. ARPN J Agri Biol Sci 6:27–33Google Scholar
  164. Schlicht M, Kombrink E (2013) The role of nitric oxide in the interaction of Arabidopsis thaliana with the biotrophic fungi, Golovinomyces orontii and Erysiphe pisi. Front Plant Sci 4:351PubMedPubMedCentralCrossRefGoogle Scholar
  165. Sgherri C, Stevanovic B, Navari Izzo F (2011) Role of phenolic acids during dehydration and rehydration of Ramondaserbica. Physiol Plant 122:478–485CrossRefGoogle Scholar
  166. Shah K, Kumar RG, Verma S, Dubey RS (2001) Effect of cadmium on lipid peroxidation, superoxide anion generation and activities of antioxidant enzymes in growing rice seedlings. Plant Sci 161:1135–1144CrossRefGoogle Scholar
  167. Shalata A, Mittova V, Volokita M, Guy M, Tal M (2001) Response of the cultivated tomato and its wild salt tolerant relative Lycopersiconpennelliito salt dependent oxidative stress: the root antioxidative system. Physiol Plant 112:487–494PubMedCrossRefGoogle Scholar
  168. Sharma SS, Dietz KJ (2009) The relationship between metal toxicity and cellular redox imbalance. Trends Plant Sci 14:43–50PubMedCrossRefGoogle Scholar
  169. Sharma P, Dubey RS (2005) Drought induces oxidative stress and enhances the activities of antioxidant enzymes in growing rice seedlings. Plant Growth Regul 46:209–221CrossRefGoogle Scholar
  170. Sharma P, Dubey RS (2007) Involvement of oxidative stress and role of antioxidative defense system in growing rice seedlings exposed to toxic concentrations of aluminum. Plant Cell Rep 26:2027–2038PubMedCrossRefGoogle Scholar
  171. Shimizu KK, Okada K (2000) Attractive and repulsive interactions between female and male gametophyte in Arabidopsis pollen tube guidance. Development 127:4511–4518PubMedGoogle Scholar
  172. Singh HP, Bati DR, Kaur G, Arora K, Kohli RK (2008) Nitric oxide (as sodium nitroprusside) supplementation ameliorates cd toxicity in hydroponically grown wheat roots. Environ Exp Bot 63:158–167CrossRefGoogle Scholar
  173. Srivastava S, Dubey RS (2011) Manganese-excess induces oxidative stress, lowers the pool of antioxidants and elevates activities of key antioxidative enzymes in rice seedlings. Plant Growth Regul 64:1–16CrossRefGoogle Scholar
  174. Srivastava S, Srivastava AK, Suprasanna P, Dsouza SF (2010) Comparative antioxidant profiling of tolerant and sensitive varieties of Brassica juncea L. to arsenate and arsenite exposure. Bull Environ Contam Toxicol 84:342–346PubMedCrossRefGoogle Scholar
  175. Staiger D, Korneli C, Lummer M, Navarro L (2013) Emerging role for RNA based regulation in plant immunity. New Phytol 197:394–404PubMedCrossRefGoogle Scholar
  176. Stone LM, Seaton KA, Kuo J, Mccomb JA (2004) Fast pollen tube growth in Conospermum species. Ann Bot 93:369–378PubMedPubMedCentralCrossRefGoogle Scholar
  177. Strid A, Chow WS, Anderson JM (1994) UV-B damage and protection at the molecular level in plants. Photosynth Res 39:475–489PubMedCrossRefGoogle Scholar
  178. Suzuki N, Miller G, Morales J, Shulaev V, Torres MA, Mittler R (2011) Respiratory burst oxidases the engines of ROS signaling. Curr Opin Plant Biol 14:691–699PubMedCrossRefGoogle Scholar
  179. Tadege M, Kuhlemeier C (1997) Aerobic fermentation during tobacco pollen development. Plant Mol Biol 35:343–354PubMedCrossRefGoogle Scholar
  180. Tanou G, Molassiotis A, Diamantidis G (2009) Induction of reactive oxygen species and necrotic death-like destruction in strawberry leaves by salinity. Environ Exp Bot 65:270–281CrossRefGoogle Scholar
  181. Tessier Lavigne M, Goodman CS (1996) The molecular biology of axon guidance. Science 274:1123–1160PubMedCrossRefGoogle Scholar
  182. Thomas DD, Liu X, Kantrow SP, Lancaster JR (2001) The biological life time of nitric oxide: implications for the perivascular dynamics of NO and O2. Proc Natl Acad Sci U S A 98:355–360PubMedCrossRefGoogle Scholar
  183. Tischner R, Galli M, Heimer YM, Bielefeld S, Okamoto M, Mack A, Crawford NM (2007) Interference with the citrulline-based nitric oxide synthase assay by argininosuccinate lyase activity in Arabidopsis extracts. FEBS J 274(16):4238–4245PubMedCrossRefGoogle Scholar
  184. Torres MA, Onouchi H, Hamada S, Machida C, Hammond-Kosack KE, Jones JDG (1998) Six Arabidopsis thaliana homologues of the human respiratory burst oxidase (gp91phox). Plant J 14:365–370PubMedCrossRefGoogle Scholar
  185. Torres MA, Dangl JL, Jones JDG (2002) Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. Proc Natl Acad Sci USA 99:517–522PubMedCrossRefGoogle Scholar
  186. Vaidyanathan H, Sivakumar P, Chakrabarty R, Thomas G (2003) Scavenging of reactive oxygen species in NaCl stressed rice (Oryza sativa L.) differential response in salt tolerant and sensitive varieties. Plant Sci 165:1411–1418CrossRefGoogle Scholar
  187. Valderrama R, Corpas FJ, Carreras A et al (2006) The dehydrogenase mediated recycling of NADPH is a key antioxidant system against salt induced oxidative stress in olive plants. Plant Cell Environ 29:1449–1459PubMedCrossRefGoogle Scholar
  188. Vandelle E, Delledonne M (2011) Peroxynitrite formation and function in plants. Plant Sci 181:534–539PubMedCrossRefGoogle Scholar
  189. Vanlerberghe GC (2013) Alternative oxidase: a mitochondrial respiratory pathway to maintain metabolicand signaling homeostasis during abiotic and biotic stress in plants. Int J Mol Sci 14:6805–6847PubMedPubMedCentralCrossRefGoogle Scholar
  190. Verma S, Dubey RS (2003) Lead toxicity induces lipid peroxidation and alters the activities of antioxidant enzymes in growing rice plants. Plant Sci 164:645–655CrossRefGoogle Scholar
  191. Vinit DF, Epron D, Alaoui SB, Badot PM (2002) Effects of copper on growth and on photosynthesis of mature and expanding leaves in cucumber plants. Plant Sci 163:53–58CrossRefGoogle Scholar
  192. Wang X, Yang P, Gao Q et al (2008) Proteomic analysis of the response to high-salinity stress in Physcomitrella patens. Planta 228:167–177PubMedCrossRefGoogle Scholar
  193. Wang S, Liang D, Li C, Hao Y, Ma F, Shu H (2012) Influence of drought stress on the cellular ultra structure and antioxidant system in leaves of drought-tolerant and drought-sensitive apple rootstocks. Plant Physiol Biochem 51:81–89PubMedCrossRefGoogle Scholar
  194. Weckx JEJ, Clijsters HMM (1996) Oxidative damage and defense mechanisms in primary leaves of Phaseolus vulgaris as a result of root assimilation of toxic amounts of copper. Physiol Plant 96:506–512CrossRefGoogle Scholar
  195. Wildt J, Kley D, Rockel A, Rockel P, Segschneider HJ (1997) Emission of NO from several higher plant species. J Geophys Res Atmos 102(D5):5919–5927CrossRefGoogle Scholar
  196. Wilkins KA, Bancroft J, Bosch M, Ings J, Smirnoff N, Franklin-Tong VE (2011) ROS and NO mediate actinre organization and programmed cell death in the self-incompatibility response of Papaver. Plant Physiol 156:404–416PubMedPubMedCentralCrossRefGoogle Scholar
  197. Wu XY, Kuai BK, Jia JZ, Jing HC (2012) Regulation of leaf senescence and crop genetic improvement. J Integr Plant Biol 54:936–952PubMedCrossRefGoogle Scholar
  198. Wunsche H, Baldwin IT, Wu J (2011) S-Nitrosoglutathione reductase (GSNOR) mediates the biosynthesis of jasmonic acid and ethylene induced by feeding of the insect herbivore Manduca sexta and is important for jasmonate-elicited responses in Nicotiana attenuata. J Exp Bot 62(13):4605–4616PubMedPubMedCentralCrossRefGoogle Scholar
  199. Xiong J, Lu H, Lu K, Duan Y, An L, Zhu C (2009) Cadmium decreases crown root number by decreasing endogenous nitric oxide, which is indispensable for crown root primordia initiation in rice seedlings. Planta 230:599–610PubMedCrossRefGoogle Scholar
  200. Yaacov YL, Wills RB, 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
  201. Yadav S, David A, Baluska F, Bhatla SC (2013) Rapid auxin- induced nitric oxide accumulation and subsequent tyrosine nitration of proteins during adventitious root formation in sunflower hypocotyls. Plant Signal Behav 8(3):e23196PubMedPubMedCentralCrossRefGoogle Scholar
  202. Yamamoto Y, Hachiya A, Matsumoto H (1997) Oxidative damage to membranes by a combination of aluminum and iron in suspension-cultured tobacco cells. Plant Cell Physiol 38:1333–1339CrossRefGoogle Scholar
  203. Yu M, Yun BW, Spoel SH, Loake GJ (2012) A sleigh ride through the SNO: regulation of plant immune function by protein Snitrosylation. Curr Opin Plant Biol 15:424–430PubMedCrossRefGoogle Scholar
  204. Yun BW, Feechan A, Yin M, Saidi NB, Le Bihan T, Yu M, Moore JW, Kang JG, Kwon E, Spoel SH et al (2011) S-nitrosylation of NADPH oxidase regulates cell death in plant immunity. Nature 478:264–268PubMedCrossRefGoogle Scholar
  205. Zhang H, Shen WB, Xu LL (2003) Effects of nitric oxide on the germination of wheat seeds and its reactive oxygen species metabolisms under osmotic stress. Acta Bot Sin 45:901–905Google Scholar
  206. Zhang Y, Luo Y, Hou YX, Jiang H, Chen Q, Tang RH (2008a) Chilling acclimation induced changes in the distribution of H2O2 and antioxidant system of strawberry leaves. Agric J 3:286–291Google Scholar
  207. Zhang Y, Tang HR, Luo Y (2008b) Variation in antioxidant enzyme activities of two strawberry cultivars with shortterm low temperature stress. World J Agric Sci 4:458–462Google Scholar
  208. Zhou YH, Yu JQ, Mao WH, Huang LF, Song XS, Nogues S (2006) Genotypic variation of Rubisco expression, photosynthetic electron flow and antioxidant metabolism in the chloroplasts of chill-exposed cucumber plants. Plant Cell Physiol 47:192–199PubMedCrossRefGoogle Scholar
  209. Zonia L, Cordeiro S, Tupy J, Feijo JA (2002) Oscillatory chloride efflux at the pollen tube apical tip has a role in growth and osmoregulation and is linked to inositol polyphosphate signaling pathways. Plant Cell 14:2233–2249PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Lekshmy Sathee
    • 1
    Email author
  • Hari Singh Meena
    • 1
  • Sandeep B. Adavi
    • 1
  • Shailendra K. Jha
    • 2
  1. 1.Division of Plant PhysiologyICAR-Indian Agricultural Research InstituteNew DelhiIndia
  2. 2.Division of GeneticsICAR-Indian Agricultural Research InstituteNew DelhiIndia

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