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Nitric oxide in plants: an ancient molecule with new tasks

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Abstract

Multitasking capability of nitric oxide (NO) makes it a highly investigating signaling molecule in plant biology. In plants including inflection of hormonal levels, fruit ripening, wound suppression and defensive responses, and regulation of programmed cell death, much progress in NO signaling cascades has been achieved. Additionally, growing evidences suggest the interactive behavior of NO with auxin, salicylic acid, abscisic acid, jasmonic acid and thus regulates their signaling pathways. Parallel to this, reactive oxygen species (ROS) along with NO are supposed to accomplish various developmental and stress responses. Under biotic stress, signaling initiated by NO was found to be mediated by two specific protein i.e. pathogenesis-related 1 (PR-1) and phenylalanine ammonia lyase. The above mentioned genes were also promoted by second messengers like cyclic GMP (cGMP) and cyclic ADP-ribose (cADPR), which further initiate and regulate NO signaling. In plants, important mechanism is programmed cell death regulating various growth and developmental aspects by acting as a damage control. Under stress condition the infected cells are removed by involving signaling agents i.e. NO and ROS which is a matter of crosstalk in recent years. Keeping above facts into consideration, present work mainly deals with NO signaling under adverse conditions as well as its interaction with different phytohormones and ROS.

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References

  • Alavi SM, Arvin MJ, Manoochehri KK (2014) Salicylic acid and nitric oxide alleviate osmotic stress in wheat (Triticum aestivum L.) seedlings. J Plant Interact 9:683–688

    Article  CAS  Google Scholar 

  • Ali R, Ma W, Lemtiri-Chlieh F, Tsaltas D, Leng Q, von Bodman S, Berkowitz GA (2007) Death don’t have no mercy and neither does calcium: Arabidopsis CYCLIC NUCLEOTIDE GATED CHANNEL2 and innate immunity. Plant Cell 19:1081–1095

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arasimowicz M, Floryszak-Wieczorek J, Milczarek G, Jelonek T (2009) Nitric oxide, induced by wounding, mediates redox regulation in pelargonium leaves. Plant Biol 11:650–663

    Article  CAS  PubMed  Google Scholar 

  • Arc E, Sechet J, Corbineau F, Rajjou L, Marion-Poll A (2013) ABA crosstalk with ethylene and nitric oxide in seed dormancy and germination. Front Plant Sci 4:63

    PubMed  PubMed Central  Google Scholar 

  • 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 24:2273–2285

    Article  CAS  Google Scholar 

  • Astier J, Lindermayr C (2012) Nitric oxide-dependent posttranslational modification in plants: an update. Int J Mol Sci 13:15193–15208

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baudouin E (2011) The language of nitric oxide signalling. Plant Biol 13:233–242

    Article  CAS  PubMed  Google Scholar 

  • Begara-Morales JC, Chaki M, Valderrama R, Sánchez-Calvo B, Mata-Pérez C, Padilla MN, Corpas FJ, Barroso JB (2018) Nitric oxide buffering and conditional nitric oxide release in stress response. J Exp Bot 69:3425–3438

    Article  CAS  PubMed  Google Scholar 

  • Beligni MV, Lamattina L (1999) Nitric oxide counteracts cytotoxic processes mediated by reactive oxygen species in plant tissues. Planta 208:337–344

    Article  CAS  Google Scholar 

  • Beligni MV, Lamattina L (2000) Nitric oxide stimulates seed germination and de-etiolation, and inhibits hypocotyl elongation, three light-inducible responses in plants. Planta 210:215–221

    Article  CAS  PubMed  Google Scholar 

  • Beligni MV, Lamattina L (2001) Nitric oxide: a non-traditional regulator of plant growth. Trends Plant Sci 6:508–509

    Article  CAS  PubMed  Google Scholar 

  • Besson-Barda A, Courtoisa C, Gauthiera A, Dahana J, Dobrowolskab G, Jeandrozc S, Pugina A, Wendehenne D (2008) Nitric oxide in plants: production and cross-talk with Ca2 + signaling. Mol Plant 1:218–228

    Article  CAS  Google Scholar 

  • Bethke PC, Gubler F, Jacobsen JV, Jones RL (2004) Dormancy of Arabidopsis seeds and barley grains can be broken by nitric oxide. Planta 219:847–855

    Article  CAS  PubMed  Google Scholar 

  • Bethke PC, Libourel IGL, Jones RL (2006a) Nitric oxide reduces seed dormancy in Arabidopsis. J Exp Bot 57:517–526

    Article  CAS  PubMed  Google Scholar 

  • Bethke PC, Libourel IGL, Reinöhl V, Jones RL (2006b) Sodium nitroprusside, cyanide, nitrite, and nitrate break Arabidopsis seed dormancy in a nitric oxide-dependent manner. Planta 223:805–812

    Article  CAS  PubMed  Google Scholar 

  • Bozhkov PV, Lam E (2011) Green death: revealing programmed cell death in plants. Cell Death Differ 18:1239–1240

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bright J, Desikan R, Hancock JT, Weir IS, Neill SJ (2006) ABA-induced NO generation and stomatal closure in Arabidopsis are dependent on H2O2 synthesis. Plant J 45:113–122

    Article  CAS  PubMed  Google Scholar 

  • Broniowska KA, Hogg N (2012) The chemical biology of S-nitrosothiols. Antioxid Redox Signal 17:669–680

    Article  CAS  Google Scholar 

  • Chakraborty N, Acharya K (2017) “NO way”! Says the plant to abiotic stress. Plant Gene 11:99–105

    Article  CAS  Google Scholar 

  • Chaudhuri A, Singh KL, Kar RK (2013) Interaction of hormones with reactive oxygen species in regulating seed germination of Vigna radiata (L.) Wilczek. J Plant Biochem Physiol 1:103

    Google Scholar 

  • Chen J, Xiao Q, Wu F, Dong X, He J, Pei Z, Zheng H, Näsholm T (2010) Nitric oxide enhances salt secretion and Na+ sequestration in a mangrove plant, Avicennia marina, through increasing the expression of H(+)-ATPase and Na(+)/H(+) antiporter under high salinity. Tree Physiol 30:1570–1585

    Article  CAS  PubMed  Google Scholar 

  • Corpas FJ, Palma JM (2018) Nitric oxide on/off in fruit ripening. Plant Biol 20:805–807

    Article  CAS  PubMed  Google Scholar 

  • Corpas FJ, Chaki M, Leterrier M, Barroso JB (2009) Protein tyrosine nitration: a new challenge in plants. Plant Signal Behav 4:920–923

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Correa-Aragunde N, Graziano M, Lamattina L (2004) Nitric oxide plays a central role in determining lateral root development in tomato. Planta 218:900–905

    Article  CAS  PubMed  Google Scholar 

  • Courtois C, Besson A, Dahan J, Bourque S, Dobrowolska G, Pugin A, Wendehenne D (2008) Nitric oxide signalling in plants: interplays with Ca2+ and protein kinases. J Exp Bot 59:155–163

    Article  CAS  PubMed  Google Scholar 

  • Crawford NM, Galli M, Tischner R, Heimer YM, Okamoto M, Mack A (2006) Response to Zemojtel et al.: plant nitric oxide synthase: back to square one. Trends Plant Sci 11:526–527

    Article  CAS  Google Scholar 

  • Cui MH, Ok SH, Yoo KS, Jung KW, Yoo SD, Shin JS (2013) An Arabidopsis cell growth defect factor-related protein, CRS, promotes plant senescence by increasing the production of hydrogen peroxide. Plant Cell Physiol 54:155–167

    Article  CAS  PubMed  Google Scholar 

  • de Pinto MC, Locato V, De Gara L (2012) Redox regulation in plant programmed cell death. Plant, Cell Environ 35:234–244

    Article  CAS  Google Scholar 

  • de Pinto MC, Locato V, Sgobba A, Romero-Puertas MC, Gadaleta C, Delledonne M, De Gara L (2013) S-nitrosylation of ascorbate peroxidase is part of programmed cell death signaling in tobacco Bright Yellow-2 cells. Plant Physiol 163:1766–1775

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • del Rio LA, Corpas FJ, Sandalio LM, Palma JM, Barroso JB (2003) Plant peroxisomes, reactive oxygen metabolism and nitric oxide. IUBMB Life 55:71–81

    Article  PubMed  Google Scholar 

  • Delledonne M (2005) NO news is good news for plants. Curr Opin Plant Biol 8:390–396

    Article  CAS  PubMed  Google Scholar 

  • Delledonne M, Xia Y, Dixon RA, Lamb C (1998) Nitric oxide functions as a signal in plant disease resistance. Nature 394:585–588

    Article  CAS  PubMed  Google Scholar 

  • 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 98:13454–13459

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Desikan R, Griffiths R, Hancock J, Neill S (2002) A new role for an old enzyme: nitrate reductase-mediated nitric oxide generation is required for abscisic acid-induced stomatal closure in Arabidopsis thaliana. Proc Natl Acad Sci USA 99:16314–16318

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Desikan R, Cheung MK, Bright J, Henson D, Hancock JT, Neill SJ (2004) ABA, hydrogen peroxide and nitric oxide signaling in stomatal guard cells. J Exp Bot 55:205–212

    Article  CAS  PubMed  Google Scholar 

  • Domingos P, Prado AM, Wong A, Gehring C, Feijo JA (2015) Nitric oxide: a multitasked signaling gas in plants. Mol Plant 8:506–520

    Article  CAS  PubMed  Google Scholar 

  • Dordas C, Hasinoff BB, Rivoal J, Hill RD (2004) Class-1 hemoglobins, nitrate and NO levels in anoxic maize cell suspension cultures. Planta 219:66–72

    Article  CAS  PubMed  Google Scholar 

  • Du ST, Zhang YS, Lin XY, Wang Y, Tang CX (2008) Regulation of nitrate reductase by nitric oxide in Chinese cabbage pakchoi (Brassica chinensis L.). Plant, Cell Environ 31:195–204

    CAS  Google Scholar 

  • Durner J, Wendehenne D, Klessig DF (1998) Defense gene induction in tobacco by nitric oxide, cyclic GMP and cyclic ADP-ribose. Proc Natl Acad Sci USA 95:10328–10333

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fares A, Rossignol M, Peltier JB (2011) Proteomics investigation of endogenous S-nitrosylation in Arabidopsis. Biochem Biophys Res Commun 416:331–336

    Article  CAS  PubMed  Google Scholar 

  • Fernández M, Sanz L, Lewis DR, Muday GK, Lorenzo O (2011) Nitric oxide causes root apical meristem defects and growth inhibition while reducing PIN-FORMED 1 (PIN1)- dependent acropetal auxin transport. Proc Natl Acad Sci USA 108:18506–18511

    Article  Google Scholar 

  • Fernández-Marcos M, Sanz L, Lorenzo O (2012) Nitric oxide: an emerging regulator of cell elongation during primary root growth. Plant Signal Behav 7:196–200

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Flores-Pérez Ú, Sauret-Güeto S, Gas E, Jarvis P, Rodríguez-Concepción M (2008) A mutant impaired in the production of plastome-encoded proteins uncovers a mechanism for the homeostasis of isoprenoid biosynthetic enzymes in Arabidopsis plastids. Plant Cell 20:1303–1315

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Freschi L (2013) Nitric oxide and phytohormones interactions: current status and perspectives. Front Plant Sci 4:198. https://doi.org/10.3389/fpls.2013.00398

    Article  Google Scholar 

  • Freschi L, Rodrigues MA, Domingues DS, Purgatto E, Van Sluys MA, Magalhaes JR, Kaiser WM, Mercier H (2010) Nitric oxide mediates the hormonal control of Crassulacean acid metabolism expression in young pineapple plants. Plant Physiol 152:1971–1985

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fröhlich A, Durner J (2011) The hunt for plant nitric oxide synthase (NOS): is one really needed? Plant Sci 181:401–404

    Article  PubMed  CAS  Google Scholar 

  • Furihata T, Maruyama K, Fujita Y, Umezawa T, Yoshida R, Shinozaki K, Yamaguchi-Shinozak K (2008) Abscisic acid-dependent multisite phosphorylation regulates the activity of a transcription activator AREB1. Proc Natl Acad Sci USA 103:1988–1993

    Article  CAS  Google Scholar 

  • Galatro A, Puntarulo S (2014) An update to the understanding of nitric oxide metabolism in plants. In: Khan MN, Mohammad MMF, Corpas FJ (eds) Nitric oxide in plants: metabolism and role in stress physiology. Springer, Switzerland, pp 3–16

    Chapter  Google Scholar 

  • Garcês H, Durzan D, Pedroso MC (2001) Mechanical stress elicits nitric oxide formation and DNA fragmentation in Arabidopsis thaliana. Ann Bot 87:553–707

    Article  CAS  Google Scholar 

  • Garcia-Mata C, Lamattina L (2001) Nitric oxide induces stomatal closure and enhances the adaptive plant responses against drought stress. Plant Physiol 126:1196–1204

    Article  CAS  PubMed  Google Scholar 

  • García-Mata C, Lamattina L (2002) Nitric oxide and abscisic acid cross talk in guard cells. Plant Physiol 128:790–792

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • García-Mata C, Lamattina L (2007) Abscisic acid (ABA) inhibits light induced stomatal opening through calcium- and nitric oxide-mediated signaling pathways. Nitric Oxide 17:143–151

    Article  PubMed  CAS  Google Scholar 

  • Garcia-Mata C, Gay R, Sokolovski S, Hills A, Lamattina L, Blatt MR (2003) Nitric oxide regulates K+ and Cl− channels in guard cells through a subset of abscisic acid-evoked signaling pathways. Proc Natl Acad Sci USA 100:11116–11121

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 28:1091–1101

    Article  CAS  PubMed  Google Scholar 

  • Grant JJ, Loake GJ (2000) Role of reactive oxygen intermediates and cognate redox signaling in disease resistance. Plant Physiol 124:21–29

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Groß F, Durner J, Gaupels F (2013) Nitric oxide, antioxidants and prooxidants in plant defense responses. Front Plant Sci 7:419. https://doi.org/10.3389/fpls.2013.00419

    Article  Google Scholar 

  • Guo FQ, Okamoto M, Crawford NM (2003) Identification of a plant nitric oxide synthase gene involved in hormonal signaling. Science 302:100–103

    Article  CAS  PubMed  Google Scholar 

  • Halliwell B, Gutteridge J (2007) What is an antioxidant? Freeradic Biol Med 4:79–186

    Google Scholar 

  • Hao GP, Zhang JH (2010) The role of nitric oxide as a bioactive signaling molecule in plants under abiotic stress. In: Hayat S, Mori M, Pichtel J, Ahmad A (eds) Nitric oxide in plant physiology. Wiley-VCH Verlag, Weinheim, pp 115–138

    Google Scholar 

  • Hossain MA, Ye W, Munemasa S, Nakamura Y, Mori IC, Murata Y (2014) Cyclic adenosine 5′-diphosphoribose (cADPR) cyclic guanosine 3′,5′-monophosphate positively function in Ca2 + elevation in methyl jasmonate-induced stomatal closure, cADPR is required for methyl jasmonate-induced ROS accumulation NO production in guard cells. Plant Biol 16:1140–1144

    CAS  PubMed  Google Scholar 

  • Hu X, Neill SJ, Tang Z, Cai W (2005) Nitric oxide mediates gravitropic bending in soybean roots. Plant Physiol 137:663–670

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang X, von Rad U, Durner J (2002) Nitric oxide induces transcriptional activation of the nitric oxide-tolerant alternative oxidase in Arabidopsis suspension cells. Planta 215:914–923

    Article  CAS  PubMed  Google Scholar 

  • Huang X, Stettmaier K, Michel C, Hutzler P, Mueller MJ, Durner J (2004) Nitric oxide is induced by wounding and influences jasmonic acid signaling in Arabidopsis thaliana. Planta 218:938–946

    Article  CAS  PubMed  Google Scholar 

  • Jeandroz S, Wipf D, Stuehr DJ, Lamattina L, Melkonian M, Tian Z, Zhu Y, Carpenter EJ, Wong GK, Wendehenne D (2016) Occurrence, structure, and evolution of nitric oxide synthase-like proteins in the plant kingdom. Plant Biol 9:417

    Google Scholar 

  • Ji Y, Liu J, Xing D (2016) Low concentrations of salicylic acid delay methyl jasmonate-induced leaf senescence by up-regulating nitric oxide synthase activity. J Exp Bot 67:280

    Article  CAS  Google Scholar 

  • Jing HC, Schippers JH, Hille J, Dijkwel PP (2005) Ethylene-induced leaf senescence depends on age-related changes and OLD genes in Arabidopsis. J Exp Bot 56:2915–2923. https://doi.org/10.1093/jxb/eri287

    Article  CAS  PubMed  Google Scholar 

  • Klepper L (1979) Nitric oxide (NO) and nitrogen dioxide (NO2) emissions from herbicide-treated soybean plants. Atmos Environ 13:537–542

    Article  CAS  Google Scholar 

  • Klessig D, Durner J, Noad R, Navarre DA, Wendehenne D, Kumar D, Zhou JM, Shah J, Zhang S, Kachroo P, Trifa Y, Pontier D, Lam E, Silva H (2000) Nitric oxide and salicylic acid signaling in plant defense. Proc Natl Acad Sci USA 97:8849–8855

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kobayashi Y, Murata M, Minami H, Yamamoto S, KagayaY Hobo T, Yamamoto A, Hattori T (2005) Abscisic acid-activated SNRK2 protein kinases function in the generegulation pathway of ABA signal transduction by phosphorylating ABA response element-binding factors. Plant J44:939–949

    Google Scholar 

  • Kolbert Z, Feigl G, Bordé Á, Molnár Á, Erdei L (2017) Protein tyrosine nitration in plants: present knowledge, computational prediction and future perspectives. Plant Physiol Biochem 113:56–63

    Article  CAS  PubMed  Google Scholar 

  • 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 15:53–59

    Article  CAS  PubMed  Google Scholar 

  • Kovacs I, Holzmeister C, Wirtz M, Geerlof A, Fröhlich T, Römling G, Kuruthukulangarakoola GT, Linster E, Hell R, Arnold GJ, Durner J, Lindermayr C (2016) ROS-mediated inhibition of s-nitrosoglutathione reductase contributes to the activation of anti-oxidative mechanisms. Front Plant Sci 7:1669

    Article  PubMed  PubMed Central  Google Scholar 

  • Lamotte O, Gould K, Lecourieux D, Sequeira-Legrand A, Lebun-Garcia A, Durner J, Pugin A, Wendehenne D (2004) Analysis of nitric oxide signaling functions in tobacco cells challenged by the elicitor cryptogein. Plant Physiol 135:516–529

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lanteri ML, Pagnussat GC, Lamattina L (2006) Calciumand calcium-dependent protein kinases are involved in nitric oxide and auxin-induced adventitious root formation in cucumber. J Exp Bot 57:1341–1351

    Article  CAS  PubMed  Google Scholar 

  • Lee U, Wie C, Fernandez BO, Feelisch M, Vierling E (2008) Modulation of nitrosative stress by S-nitroso glutathione reductase is critical for thermo tolerance and plant growth in Arabidopsis. Plant Cell 20:786–802

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leshem Y, Pinchasov Y (2000) Non-invasive photoacoustic spectroscopic determination of relative endogenous nitric oxide and ethylene content stoichiometry during the ripening of strawberries Fragaria anannasa (Duch.) and avocados Persea americana (Mill.). J Exp Bot 51:1471–1473

    CAS  PubMed  Google Scholar 

  • Li H, Poulos TL (2005) Structure–function studies on nitric oxide synthases. JInorg Biochem 99:293–305

    CAS  Google Scholar 

  • Libourel IGL, Bethke PC, De Michele R, Jones RL (2006) Nitric oxide gas stimulates germination of dormant Arabidopsis seeds: use of a flow through apparatus for delivery of nitric oxide. Planta 223:813–820

    Article  CAS  PubMed  Google Scholar 

  • Liu F, Guo F (2013) Nitric oxide deficiency accelerates chlorophyll breakdown and stability loss of thylakoid membranes during dark-induced leaf senescence in Arabidopsis. PLoS ONE 8(2):e56345. https://doi.org/10.1371/journal.pone.0056345

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu YG, Shi L, Ye NH, Liu R, Jia WS, Zhang JH (2009) Nitric oxide induced rapid decrease of abscisic acid concentration is required in breaking seed dormancy in Arabidopsis. New Phytol 183:1030–1042

    Article  CAS  PubMed  Google Scholar 

  • Liu WZ, Kong DD, Gu XX, Gao HB, Wang JZ, Xia M (2013) Cytokinins can act as suppressors of nitric oxide in Arabidopsis. Proc Natl Acad Sci USA 110:1548–1553. https://doi.org/10.1073/pnas.1213235110

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu Y, Yang X, Zhu S, Wang Y (2016) Postharvest application of MeJA and NO reduced chilling injury in cucumber (Cucumis sativus) through inhibition of H2O2 accumulation. Postharvest Biol Technol 119:77–83

    Article  CAS  Google Scholar 

  • Lombardo MC, Graziano M, Polacco JC, Lamattina L (2006) Nitric oxide functions as a positive regulator of root hair development. Plant Signal Behav 1:28–33

    Article  PubMed  PubMed Central  Google Scholar 

  • Lozano-Juste J, León J (2011) Nitric oxide regulates DELLA content and PIF expression to promote photo-morphogenesis in Arabidopsis. Plant Physiol 156:1410–1423

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Méndez-Bravo A, Raya-González J, Herrera-Estrella L, López-Bucio J (2010) Nitric oxide is involved in alkamide-induced lateral root development in Arabidopsis. Plant Cell Physiol 51:1612–1626

    Article  PubMed  CAS  Google Scholar 

  • Meyer C, Lea US, Provan F, Kaiser WM, Lillo C (2005) Is nitrate reductase a major player in the plant NO (nitric oxide) game? Photosynth Res 83:181–189

    Article  CAS  PubMed  Google Scholar 

  • Mioto PT, Mercier H (2013) Abscisic acid and nitric oxide signaling in two different portions of detached leaves of Guzmania monostachia with CAM up-regulated by drought. J Plant Physiol 170:996–1002

    Article  CAS  PubMed  Google Scholar 

  • Mishina TE, Lamb C, Zeier J (2007) Expression of a nitric oxide degrading enzyme induces a senescence programme in Arabidopsis. Plant, Cell Environ 30:39–52

    Article  CAS  Google Scholar 

  • Mittler R, Vanderauwera S, Suzuki N, Miller G, Tognetti VB, Vandepoele K, Gollery M, Shulaev V, Van Breusegem F (2011) ROS signaling: the new wave? Trends Plant Sci 16:300–309

    Article  CAS  PubMed  Google Scholar 

  • Mohn MA, Thaqi B, Fischer-Schrader K (2019) Isoform-specific NO synthesis by Arabidopsis thaliana nitrate reductase. Plants 8:67

    Article  CAS  PubMed Central  Google Scholar 

  • Mor A, Koh E, Weiner L, Rosenwasser S, Sibony-Benyamini H, Fluhr R (2014) Singlet oxygen signatures are detected independent of light or chloroplasts in response to multiple stresses. Plant Physiol 165:249–261

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moreau M, Lee GI, Wang Y, Crane BR, Klessig DF (2008) AtNOS/AtNOA1 is a functional Arabidopsis thaliana cGTPase and not a nitric-oxide synthase. J Biol Chem 283:32957–32967

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mur LAJ, Kenton P, Atzorn R, Miersch O, Wasternack C (2006) The outcomes of concentration-specific interactions between salicylate and jasmonate signaling include synergy, antagonism, and oxidative stress leading to cell death. Plant Physiol 140:249–262

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Navabpour S, Morris K, Allen R, Harrison E, Mackerness SAH, Buchanan-Wollaston V (2003) Expression of senescence-enhanced genes in response to oxidative stress. J Exp Bot 54:2285–2292

    Article  CAS  PubMed  Google Scholar 

  • Neill SJ, Desikan R, Clarke A, Hurst RD, Hancock JT (2002) Hydrogen peroxide and nitric oxide as signalling molecules in plants. J Exp Bot 53:1237–1247

    Article  CAS  PubMed  Google Scholar 

  • Niu YH, Guo FQ (2012) Nitric oxide regulates dark-induced leaf senescence through EIN2 in Arabidopsis. J Integr Plant Biol 54:516–525

    Article  CAS  PubMed  Google Scholar 

  • Ötvös K, Pasternak TP, Miskolczi P, Domoki M, Dorjgotov D, Szucs A, Bottka, Dudits D, Fehér A (2005) Nitric oxide is required for and promotes auxin-mediated activation of cell division and embryogenic cell formation but does not influence cell cycle progression in alfalfa cell cultures. Plant J 43:849–860

    Article  PubMed  CAS  Google Scholar 

  • Overmyer K, Brosché M, Kangasjärvi J (2003) Reactive oxygen species and hormonal control of cell death. Trends Plant Sci 8:335–342

    Article  CAS  PubMed  Google Scholar 

  • 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 132:1241–1248

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 135:279–286

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pedroso MC, Magalhaes JR, Durzan D (2000) A nitric oxide burst precedes apoptosis in angiosperm and gymnosperm callus cells and foliar tissues. J Exp Bot 51:1027–1036

    Article  CAS  PubMed  Google Scholar 

  • Pii Y, Crimi M, Cremonese G, Spena A, Pandolfini T (2007) Auxin and nitric oxide control indeterminate nodule formation. BMC Plant Biol 7:21

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Qi Z, Verma R, Gehring C, Yamaguchi Y, Zhao Y, Ryan CA, Berkowitz GA (2010) Ca2+ signaling by plant Arabidopsis thaliana Pep peptides depends on AtPepR1, a receptor with guanylyl cyclase activity, and cGMP-activated Ca2+ channels. PNAS 107:21193–21198

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qian H, Chen W, Li J, Wang J, Zhou Z, Liu W, Fu Z (2009) The effect of exogenous nitric oxide on alleviating herbicide damage in Chlorella vulgaris. Aquat Toxicol 92:250–257

    Article  CAS  PubMed  Google Scholar 

  • Qiao W, Li C, Fan L (2014) Cross-talk between nitric oxide and hydrogen peroxide in plant responses to abiotic stresses. Environ Exp Bot 100:84–93

    Article  CAS  Google Scholar 

  • Rasul S, Wendehenne D, Jeandroz S (2012) Study of oligogalacturonides-triggered nitric oxide (NO) production provokes new questioning about the origin of NO biosynthesis in plants. Plant Signal Behav 7:1031–1033

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 53:103–110

    Article  CAS  PubMed  Google Scholar 

  • Rodríguez-Serrano M, Romero-Puertas MC, Sparkes I, Hawes C, del Río LA, Sandalio LM (2009) Peroxisome dynamics in Arabidopsis plants under oxidative stress induced by cadmium. Free Radic Biol Med 47:1632–1639

    Article  PubMed  CAS  Google Scholar 

  • Romanov GA, Lomin SN, Rakova NY, Heyl A, Schmülling T (2008) Does NO play a role in cytokinin signal transduction?. FEBS Lett 582:874–880

    Article  CAS  PubMed  Google Scholar 

  • Romero-Puertas MC, Rodríguez-Serrano M, Sandalio LM (2013) Protein S-nitrosylation in plants under abiotic stress: an overview. Front Plant Sci 4:373

    Article  PubMed  PubMed Central  Google Scholar 

  • Sandalio LM, Rodríguez-Serrano M, Romero-Puertas MC, del Río LA (2013) Role of peroxisomes as a source of reactive oxygen species (ROS) signaling molecules. Subcell Biochem 69:231–255

    Article  CAS  PubMed  Google Scholar 

  • Santolini J, Andre F, Jeandroz S, Wendehenne D (2017) Nitric oxide synthase in plants: where do we stand? Nitric Oxide 63:30–38

    Article  CAS  PubMed  Google Scholar 

  • Serrano I, Romero-Puertas MC, Sandalio LM, Olmedilla A (2015) The role of reactive oxygen species and nitric oxide in programmed cell death associated with self in-compatibility. J Exp Bot 66:2869–2876

    Article  CAS  PubMed  Google Scholar 

  • Shabbir RN, Waraich EA, Ali H, Nawaz F, Ashraf MY, Ahmad R, Awan MI, Ahmad S, Irfan M, Hussain S, Ahmad Z (2016) Supplemental exogenous NPK application alters biochemical processes to improve yield and drought tolerance in wheat (Triticum aestivum L.). Environ Sci Pollut Res 23:2651–2662

    Article  CAS  Google Scholar 

  • Sharma P, Jha AB, Dubey RS, Pessarakli M (2012) Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. J Bot. https://doi.org/10.1155/2012/217037

    Article  Google Scholar 

  • Singh R, Singh S, Parihar P, Mishra RK, Tripathi DK, Singh VP, Chauhan DK, Prasad SM (2016) Reactive oxygen species (ROS): beneficial companions of plants’ developmental processes. Front Plant Sci 7:1299. https://doi.org/10.3389/fpls.2016.01299

    Article  PubMed  PubMed Central  Google Scholar 

  • Singh R, Parihar P, Singh S, Singh MPVVB, Singh VP, Prasad SM (2017) MicroRNAs and nitric oxide cross talk in stress tolerance in plants. Plant Growth Regul 83:199–205

    Article  CAS  Google Scholar 

  • Tan J, Zhuo C, Guo Z (2013) Nitric oxide mediates cold and dehydration-induced expression of an ovel MfHyPRP that confers tolerance to abiotic stress. Physiol Planta. https://doi.org/10.1111/ppl.12032

    Article  Google Scholar 

  • Tiwari S, Verma N, Singh VP, Prasad SM (2019) Nitric oxide ameliorates aluminium toxicity in Anabaena PCC7120: regulation of aluminium accumulation, exopolysaccharides secretion, photosynthesis and oxidative stress markers. Environ Exp Bot 161:218–227

    Article  CAS  Google Scholar 

  • Tonón C, Terrile CM, Iglesias MJ, Lamattina L, Casalongué C (2010) Extracellular ATP, nitric oxide and superoxide act coordinately to regulate hypocotyls growth in etiolated Arabidopsis seedlings. J Plant Physiol 167:540–546

    Article  PubMed  CAS  Google Scholar 

  • 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 164:2220–2230

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tun NN, Santa-Catarina C, Begum T, Silveira V, Handro W, Floh EI, Scherer GF (2006) Polyamines induce rapid biosynthesis of nitric oxide (NO) in Arabidopsis thaliana seedlings. Plant Cell Physiol 47:346–354

    Article  CAS  PubMed  Google Scholar 

  • Tun NN, Livaja M, Kieber JJ, Scherer GF (2008) Zeatin-induced nitric oxide (NO) biosynthesis in Arabidopsis thaliana mutants of NO biosynthesis and of two-component signaling genes. New Phytol 178:515–531

    Article  CAS  PubMed  Google Scholar 

  • Umezawa T, Yoshida R, Maruyama K, Yamaguchi-Shinozaki K, Shinozaki K (2004) SRK2C, a SNF1-related protein kinase 2, improves drought tolerance by controlling stress-responsive gene expression in Arabidopsis thaliana. Proc Natl Acad Sci USA 101:17306–17311

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Van Doorn WG (2005) Plant programmed cell death and the point of no return. Trends Plant Sci 10:478–483

    Article  PubMed  CAS  Google Scholar 

  • Wang Y, Loake G, Chu C (2013) Cross-talk of nitric oxide and reactive oxygen species in plant programmed cell death. Front Plant Sci 4:314

    PubMed  PubMed Central  Google Scholar 

  • Wendehenne D, Pugin A, Klessig D, Durner J (2001) Nitric oxide: comparative synthesis and signaling in animal and plant cells. Trends Plant Sci 6:177–183

    Article  CAS  PubMed  Google Scholar 

  • Wendehenne D, Durner J, Klessig DF (2004) Nitric oxide: a new player in plant signaling and defence responses. Curr Opin Plant Biol 7:449–455

    Article  CAS  PubMed  Google Scholar 

  • Wrzaczek M, Brosché M, Kangasjärvi J (2013) ROS signaling loops: production, perception, regulation. Curr Opin Plant Biol 16:575–582

    Article  CAS  PubMed  Google Scholar 

  • Xiao-Ping S, Xi-Gui S (2006) Cytokinin and auxin induced stomatal opening is related to the change of nitric oxide levels in guard cells in broad bean. Physiol Plant 128:569–579. https://doi.org/10.1111/j.1399-3054.2006.00782

    Article  Google Scholar 

  • Xu W, Huang W (2017) Calcium-dependent protein kinases in phytohormone signaling pathways. Int J Mol Sci. https://doi.org/10.3390/ijms18112436

    Article  PubMed  PubMed Central  Google Scholar 

  • Xu S, Guerra D, Lee U, Vierling E (2013) S-nitroso glutathione reductases are low-copy number, cysteine-rich proteins in plants that control multiple developmental and defense responses in Arabidopsis. Front Plant Sci 4:430

    Article  PubMed  PubMed Central  Google Scholar 

  • Yamasaki H, Sakihama Y (2000) Simultaneous production of nitric oxide and peroxynitrite by plant nitrate reductase: in vitro evidence for the NR-dependent formation of active nitrogen species. FEBS Lett 468:89–92

    Article  CAS  PubMed  Google Scholar 

  • Yun BW, Skelly MJ, Yin M, Yu M, Mun BG, Lee SU, Hussain A, Spoel SH, Loake G (2016) Nitric oxide and S-nitrosoglutathione function additively during plant immunity. New Phytol 21:516–526

    Article  CAS  Google Scholar 

  • Zemojtel T, Fröhlich A, Palmieri MC, Kolanczyk M, Mikula I, Wyrwicz LS, Wanker EE, Mundlos S, Vingron M, Martasek P, Durner J (2006) Plant nitric oxide synthase: a never-ending story? Trends Plant Sci 11:524–525

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

Nidhi Verma and Santwana Tiwari are grateful to the University Grants Commission, New Delhi for granting D.Phil. Scholarship. Dr. Vijay Pratap Singh is obliged to the Department of Biotechnology, New Delhi (BT/PR12980/BPA/118/80/2015) for providing financial assistance. Professor Sheo Mohan Prasad is pleased to the SERB-DST, New Delhi (EMR/2016/004745) for providing financial assistance.

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  1. Ranjan Plant Physiology and Biochemistry Laboratory, Department of Botany, University of Allahabad, Prayagraj, 211002, India

    Nidhi Verma, Santwana Tiwari & Sheo Mohan Prasad

  2. Department of Botany, C.M.P. Degree College, A Constituent Post Graduate College of University of Allahabad, Prayagraj, 211002, India

    Vijay Pratap Singh

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  1. Nidhi Verma
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Verma, N., Tiwari, S., Singh, V.P. et al. Nitric oxide in plants: an ancient molecule with new tasks. Plant Growth Regul 90, 1–13 (2020). https://doi.org/10.1007/s10725-019-00543-w

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