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Nitric oxide as a key component in hormone-regulated processes

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Abstract

Nitric oxide (NO) is a small gaseous molecule, with a free radical nature that allows it to participate in a wide spectrum of biologically important reactions. NO is an endogenous product in plants, where different biosynthetic pathways have been proposed. First known in animals as a signaling molecule in cardiovascular and nervous systems, it has turned up to be an essential component for a wide variety of hormone-regulated processes in plants. Adaptation of plants to a changing environment involves a panoply of processes, which include the control of CO2 fixation and water loss through stomatal closure, rearrangements of root architecture as well as growth restriction. The regulation of these processes requires the concerted action of several phytohormones, as well as the participation of the ubiquitous molecule NO. This review analyzes the role of NO in relation to the signaling pathways involved in stomatal movement, plant growth and senescence, in the frame of its interaction with abscisic acid, auxins, gibberellins, and ethylene.

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References

  • 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: 4368–4380

  • 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: 2862–2872

    Google Scholar 

  • Abu-Abied M, Szwerdszarf D, Mordehaev I et al (2012) Microarray analysis revealed upregulation of nitrate reductase in juvenile cuttings of Eucalyptus grandis, which correlated with increased nitric oxide production and adventitious root formation. Plant J 71:787–799

    Article  PubMed  CAS  Google Scholar 

  • Achard P, Cheng H, De Grauwe L, Decat J, Schoutteten H, Moritz T, van der Straeten D, Peng J, Harberd NP (2006) Integration of plants responses to environmentally activated phytohormonal signals. Science 331:91–94

    Article  CAS  Google Scholar 

  • Achard P, Renou JP, Berthomé R, Harberd NP, Genschik P (2008) Plant DELLAs restrain growth and promote survival of adversity by reducing the levels of reactive oxygen species. Current Biol 18:656–660

    Article  CAS  Google Scholar 

  • Arita NO, Cohen MF, Tokuda G, Yamasaki H (2006) Fluorometric detection of nitric oxide with diaminofluoresceins (DAFs): applications and limitations for plant NO research. In: Lamattina L, Polacco JC, Eds. Nitric oxide in plant growth. Plant Cell Monographs 6:269–280

    Google Scholar 

  • Asai S, Ohta K, Yoshioka H (2008) MAPK signaling regulates nitric oxide and NADPH oxidase-dependent oxidative bursts in Nicotiana benthamiana. Plant Cell 20:1390–1406

    Article  PubMed  CAS  Google Scholar 

  • Assmann SM (1993) Signal transduction in guard cells. Annu Rev Cell Biol 9:345–375

    Article  PubMed  CAS  Google Scholar 

  • Astier J, Rasul S, Koen E, Manzoor H, Besson-Bard A, Lamotte O, Jeandroz S, Durner J, Lindermayr C, Wendehenne D (2011) S-nitrosylation: an emerging post-translational protein modification in plants. Plant Sci 181:527–533

    Article  PubMed  CAS  Google Scholar 

  • 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 53:1101–1110

    Article  PubMed  CAS  Google Scholar 

  • Bai X, Yang L, Yang Y, Ahmad P, Yang Y, Hu X (2011) Deciphering the protective role of nitric oxide against salt stress at the physiological and proteomic levels in maize. J Proteome Res 10:4349–4364

    Article  PubMed  CAS  Google Scholar 

  • Bai X, Todd CD, Desikan R, Yang Y, Hu X (2012) N-3-oxo-decanoyl-l-homoserine-lactone activates auxin-induced adventitious root formation via hydrogen peroxide- and nitric oxide-dependent cyclic GMP signaling in mung bean. Plant Physiol 158:725–736

    Article  PubMed  CAS  Google Scholar 

  • Barroso JB, Corpas FJ, Carreras A, Rodríguez-Serrano M, Esteban FJ, Fernández-Ocaña A, Chaki M, Romero-Puertas MC, Valderrama R, Sandalio LM, del Río L (2006) Localization of S-nitrosoglutathione and expression of S-nitrosoglutathione reductase in pea plants under cadmium stress. J Exp Bot 57:1785–1793

    Article  PubMed  CAS  Google Scholar 

  • Bartoli CG, Yu J, Gómez F, Fernández L, McIntosh L, Foyer CH (2006) Inter-relationships between light and respiration in the control of ascorbic acid synthesis and accumulation in Arabidopsis thaliana leaves. J Exp Bot 57:1621–1631

    Article  PubMed  CAS  Google Scholar 

  • Bartoli CG, Casalongué CA, Simontacchi M, Marquez-García B, Foyer C (2012) Interactions between hormone and redox signalling pathways in the control of growth and cross tolerance to stress. Environ Exp Bot http://dx.doi.org/10.1016/j.envexpbot.2012.05.003

  • Bauer P, Ling H-Q, Guerinot ML (2007) FIT, the FER-LIKE IRON DEFICIENCY INDUCED TRANSCRIPTION FACTOR in Arabidopsis. Plant Physiol Biochem 45:260–261

    Article  PubMed  CAS  Google Scholar 

  • Bechtold U, Rabbani N, Mullineaux PM, Thornalley PJ (2009) Quantitative measurement of specific biomarkers for protein oxidation, nitration and glycation in Arabidopsis leaves. Plant J 59:661–671

    Article  PubMed  CAS  Google Scholar 

  • Begara-Morales JC, Chaki M, Sánchez-Calvo B, Mata-Pérez C, Leterrier M, Palma JM, Barroso JB, Corpas FJ (2013) Protein tyrosine nitration in pea roots during development and senescence. J Exp Bot 64: 1121–1134

    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  PubMed  CAS  Google Scholar 

  • 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 129:1642–1650

    Article  PubMed  CAS  Google Scholar 

  • Benková E, Bielach A (2010) Lateral root organogenesis––from cell to organ. Curr Op Plant Biol 13:677–683

    Article  Google Scholar 

  • Besson-Bard A, Griveau S, Bedioui F, Wendehenne D (2008) Real-time electrochemical detection of extracellular nitric oxide in tobacco cells exposed to cryptogein, an elicitor of defence responses. J Exp Bot 59:3407–3414

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Blatt MR (2000) Cellular signalling and volume control in stomatal movements in plants. Annu Rev Cell Dev Biol 16:221

    Article  PubMed  CAS  Google Scholar 

  • Bowyer MC, Wills RBH, Badiyan D, Ku VVV (2003) Extending the postharvest life of carnations with nitric oxide-comparison of fumigation and in vivo delivery. Postharvest Biol Tech 30:281–286

    Article  CAS  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  PubMed  CAS  Google Scholar 

  • Cecconi D, Orzetti S, Vandelle E, Rinalducci S, Zolla L, Delledonne M (2009) Protein nitration during defense response in Arabidopsis thaliana. Electrophoresis 30:2460–2468

    Article  PubMed  CAS  Google Scholar 

  • Chaki M, Valderrama R, Fernández-Ocaña AM et al (2009) Protein targets of tyrosine nitration in sunflower (Helianthus annuus L.) hypocotyls. J Exp Bot 60:4221–4234

    Article  PubMed  CAS  Google Scholar 

  • Chaki M et al (2011) High temperature triggers the metabolism of S-nitrosothiols in sunflower mediating a process of nitrosative stress which provokes the inhibition of ferredoxin-NADP reductase by tyrosine nitration. Plant Cell Environ 34:1803–1818

    Article  PubMed  CAS  Google Scholar 

  • Chen WW, Yang JL, Qin C, Jin CW, Mo JH, Ye T, Zheng SJ (2010) Nitric oxide acts downstream of auxin to trigger root ferric-chelate reductase activity in response to iron deficiency in arabidopsis. Plant Physiol 154:810–819

    Article  PubMed  CAS  Google Scholar 

  • Chen YH, Chao YY, Hsu YY, Hong CY, Kao CH (2012) Heme oxygenase is involved in nitric oxide- and auxin-induced lateral root formation in rice. Plant Cell Rep 31:1085–1091

    Article  PubMed  CAS  Google Scholar 

  • Cheng G, Yang E, Lu W, Jia Y, Jiang Y, Duan X (2009) Effect of nitric oxide on ethylene synthesis and softening of banana fruit slice during ripening. J Agric Food Chem 57:5799–5804

    Article  PubMed  CAS  Google Scholar 

  • Clyde Hill A, Bennett JH (1970) Inhibition of apparent photosynthesis by nitrogen oxides. Atmos Environ 4:341–348

    Article  Google Scholar 

  • Corpas FJ, Palma JM, Leterrier M, del Río LA, Barroso JA (2010) Nitric oxide and abiotic stress in plants. In: Hayat S, Mori M, Pichtel J, Ahmad A (eds) Nitric oxide in plant physiology. Wiley-Blackwell, Germany, pp 51–63

    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  PubMed  CAS  Google Scholar 

  • Correa-Aragunde N, Lanteri ML, García-Mata C, Ten Have A, Laxalt AM, Graziano M, Lamattina L (2007) Nitric oxide functions as intermediate in auxin, abscisic acid, and lipid signaling pathways. In: Lamattina L, Polacco JC (eds) Plant Cell Monographs. Nitric oxide in plant growth. Heidelberg, Springer-Verlag, Berlin, pp 113–130

    Chapter  Google Scholar 

  • Crawford NM (2006) Mechanisms for nitric oxide synthesis in plants. J Exp Bot 57:471–478

    Article  PubMed  CAS  Google Scholar 

  • Culotta E, Koshland DE (1992) NO news is good news. Science 258:1862–1865

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Depuydt S, Hardtke CS (2011) Hormone signalling crosstalk in plant growth regulation. Current Biol 21:R365–R373

    Article  CAS  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 99:16314–16318

    Article  PubMed  CAS  Google Scholar 

  • Dharmasiri N, Dharmasiri S, Estelle M (2005) The F-box protein TIR1 is an auxin receptor. Nature 435:441–445

    Article  PubMed  CAS  Google Scholar 

  • Distéfano AM, García-Mata C, Lamattina L, Laxalt AM (2008) Nitric oxide-induced phosphatidic acid accumulation: a role for phospholipases C and D in stomatal closure. Plant Cell Environ 31:187–194

    Article  PubMed  CAS  Google Scholar 

  • Distéfano AM, Scuffi D, García-Mata C, Lamattina L, Laxalt AM (2012) Phospholipase D is involved in nitric oxide-induced stomatal closure. Planta. doi:10.1007/s00425-012-1745-4

    PubMed  Google Scholar 

  • Dreyer I, Uozumi N (2011) Potassium channels in plant cells. FEBS J 278:4293–4303

    Article  PubMed  CAS  Google Scholar 

  • Dubovskaya LV, Bakakina YS, Kolesneva EV, Sodel DL, McAinsh MR, Hetherington AM, Volotovski ID (2011) cGMP-dependent ABA-induced stomatal closure in the ABA-insensitive Arabidopsis mutant abi1-1. New Phytol 191:57–69

    Article  PubMed  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 95:10328–10333

    Article  PubMed  CAS  Google Scholar 

  • Feechan A, Kwon E, Yun BW, Wang Y, Pallas JA, Loake GJ (2005) A central role for S-nitrosothiols in plant disease resistance. Proc Natl Acad Sci 102:8054–8059

    Article  PubMed  CAS  Google Scholar 

  • Fernández-Marcos M, Sanz L, Lewis DR, 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 108:18506–18511

    Article  PubMed  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  CAS  Google Scholar 

  • Floryszak-Wieczorek J, Milczarek G, Arasimowicz M, Ciszewski A (2006) Do nitric oxide donors mimic endogenous NO-related response in plants? Planta 224:1363–1372

    Article  PubMed  CAS  Google Scholar 

  • Foresi N, Correa-Aragunde N, Parisi G, Caló G, Salerno G, Lamattina L (2010) Characterization of a nitric oxide synthase from the plant kingdom: NO generation from the gree alga Ostreococcus tauri is light irradiance and growth phase dependent. Plant Cell 22:3816–3830

    Article  PubMed  CAS  Google Scholar 

  • Foyer CH, Noctor G (2009) Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications. Antioxid Redox Signal 11:861–905

    Article  PubMed  CAS  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 

  • Fu X, Harberd NP (2003) Auxin promotes Arabidopsis root growth by modulating gibberellin response. Nature 421:740–743

    Article  PubMed  CAS  Google Scholar 

  • Fu X, Richards DE, Ait-alia T, Hynesa LW, Oughamb H, Peng J, Harberd NP (2002) Gibberellin-mediated proteasome-dependent degradation of the barley DELLA protein SLN1 repressor. Plant Cell 14:3191–3200

    Article  PubMed  CAS  Google Scholar 

  • Fu X, Richards DE, Fleck B, Xie D, Burton N, Harberd NP (2004) The Arabidopsis mutant sleepy1gar2–1 protein promotes plant growth byincreasing the affinity of the SCFSLY1 E3 ubiquitin ligase for DELLA protein substrates. Plant Cell 16:1406–1418

    Article  PubMed  CAS  Google Scholar 

  • Fujii H, Chinnusamy V, Rodrigues A, Rubio S, Antoni R, Park S-Y, Cutler SR, Sheen J, Rodriguez PL, Zhu J-K (2009) In vitro reconstitution of an abscisic acid signalling pathway. Nature 462:660–664

    Article  PubMed  CAS  Google Scholar 

  • Galetski D, Lohscheider JN, Kononikhin AS, Popov IA, Nikolaev EN, Adamska I (2011) Phosphorylation and nitration levels of photosynthetic proteins are conversely regulated by light stress, Plant Mol Biol, 77: 461–473

    Google Scholar 

  • Galetskiy D, Lohscheider JN, Kononikhin AS, Popov IA, Nikolaev EN, Adamska I (2011) Phosphorylation and nitration levels of photosynthetic proteins are conversely regulated by light stress. Plant Mol Biol 77:461–473

    Article  PubMed  CAS  Google Scholar 

  • García-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  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  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 Biol Chem 17:143–151

    Article  CAS  Google Scholar 

  • García-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 100:11116–11121

    Article  PubMed  CAS  Google Scholar 

  • Gergoff-Grozeff GE, Chaves AR, Bartoli CG (2013) Low irradiance pulses improve postharvest quality of spinach leaves (Spinacia oleraceae L. cv Bison). Postharvest Biol Technol 77:35–42

    Article  CAS  Google Scholar 

  • Gould KS, Lamotte O, Klinger A, Pugin A, Wendehenne D (2003) Nitric oxide production in tobacco leaf cells: a generalized stress response? Plant Cell Environ 26:1851–1862

    Article  CAS  Google Scholar 

  • Gouvêa CMCP, Souza JF, Magalhães ACN, Martins IS (1997) NO––releasing substances that induce growth elongation in maize root segments. Plant Growth Reg 21:183–187

    Article  Google Scholar 

  • Graziano M, Lamattina L (2007a) Nitric oxide accumulation is required for molecular and physiological responses to iron deficiency in tomato roots. Plant J 52:949–960

    Article  PubMed  CAS  Google Scholar 

  • Graziano M, Lamattina L (2007b) Nitric oxide and dinitrosyl iron complexes: roles in plant iron sensing and metabolism. In: Van Faassen E, Vanin A (eds) Radicals for life: the various forms of nitric oxide. Elsevier, Amsterdam

    Google Scholar 

  • Graziano M, Beligni MV, Lamattina L (2002) Nitric oxide improves internal iron availability in plants. Plant Physiol 130:1852–1859

    Article  PubMed  CAS  Google Scholar 

  • Grün S, Lindermayr C, Sell S, Durner J (2006) Nitric oxide and gene regulation in plants. J Exp Bot 57:507–516

    Article  PubMed  CAS  Google Scholar 

  • Gubler F, Chandler PM, White RG, Llewellyn DJ, Jacobsen JV (2002) Gibberellin signaling in barley aleurone cells. control of SLN1 and GAMYB expression. Plant Physiol 129:191–200

    Article  PubMed  CAS  Google Scholar 

  • Guo FQ, Crawford NM (2005) Arabidopsis nitric oxide synthase1 is targeted to mitochondria and protects against oxidative damage and dark-induced senescence. Plant Cell 17:3436–3450

    Article  PubMed  CAS  Google Scholar 

  • Gupta KJ, Fernie AR, Kaiser WM, van Dongen JT (2011) On the origins of nitric oxide. Trends Plant Sci 16:160–168

    Article  PubMed  CAS  Google Scholar 

  • Hao F, Zhao S, Dong H, Zhang H, Sun L, Miao C (2010) Nia1 and Nia2 are involved in exogenous salicylic acid-induced nitric oxide generation and stomatal closure in Arabidopsis. J Integr Plant Biol 52:298–307

    Article  PubMed  CAS  Google Scholar 

  • Harberd NP, Belfield E, Yasumura Y (2009) The angiosperm gibberellin-GID1-DELLA growth regulatory mechanism: how an “inhibitor of an inhibitor” enables flexible response to fluctuating environments. Plant Cell 21:1328–1339

    Article  PubMed  CAS  Google Scholar 

  • Hayat S, Yadav S, Ali B, Ahmad A (2010) Interactive effect of nitric oxide and brassinosteroids on photosynthesis and the antioxidant system of lycopersicon esculentum. Russ J Plant Physiol 57:212–221

    Article  CAS  Google Scholar 

  • He H-Y, He L-F, Gu M-H, Li X-F (2012) Nitric oxide improves aluminum tolerance by regulating hormonal equilibrium in the root apices of rye and wheat. Plant Sci 183:123–130

    Article  PubMed  CAS  Google Scholar 

  • Hedden P (2003) The genes of the green revolution. Trends Genetic 19:5–9

    Article  CAS  Google Scholar 

  • Hetherington AM, Woodward FI (2003) The role of stomata in sensing and driving environmental change. Nature 424:901–908

    Article  PubMed  CAS  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  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Hughes MN (1999) Relationships between nitric oxide, nitroxyl ion, nitrosonium cation and peroxynitrite. Biochim Biophys Acta––Bioenergetics 1411:263–272

    Article  CAS  Google Scholar 

  • Huie RE, Padmaja S (1993) The reaction of NO with superoxide. Free Radic Res Commun 18:195–199

    Article  PubMed  CAS  Google Scholar 

  • Ignarro LJ, Wood KS, Ballot B, Wolin MS (1984) Guanylate cyclase from bovine lung. Evidence that enzyme activation by phenylhydrazine is mediated by iron-phenyl hemoprotein complexes. J Biol Chem 259:5923–5931

    PubMed  CAS  Google Scholar 

  • Innocenti G, Pucciariello C, Le Gleuher M, Hopkins J, Stefano M, Delledonne M, Puppo A, Baudouin E, Frendo P (2007) Glutathione synthesis is regulated by nitric oxide in Medicago truncatula roots. Planta 225:1597–1602

    Article  PubMed  CAS  Google Scholar 

  • Ischiropoulos H, Zhu L, Beckman JS (1992) Peroxynitrite formation from macrophage-derived nitric oxide. Arch Biochem Biophys 298:446–451

    Article  PubMed  CAS  Google Scholar 

  • Jacob T, Ritchie S, Assmann SM, Gilroy S (1999) Abscisic acid signal transduction in guard cells is mediated by phospholipase D activity. Proc Natl Acad Sci 96:12192–12197

    Article  PubMed  CAS  Google Scholar 

  • Jasid S, Galatro A, Villordo JJ, Puntarulo S, Simontacchi M (2009) Role of nitric oxide in soybean cotyledon senescence. Plant Sci 176:662–668

    Article  CAS  Google Scholar 

  • Jensen DE, Belka GK, Du Bois GC (1998) S-nitrosoglutathione is a substrate for rat alcohol dehydrogenase class III isoenzyme. Biochem J 331:659–668

    PubMed  CAS  Google Scholar 

  • Jin CW, Du ST, Zhang YS, Tang C, Lin XY (2009) Atmospheric nitric oxide stimulates plant growth and improves the quality of spinach (Spinacia oleracea). Ann Appl Biol 155:113–120

    Article  CAS  Google Scholar 

  • Jin CW, Du ST, Shamsi IH, Luo BF, Lin XY (2011) NO synthase-generated NO acts downstream of auxin in regulating Fe-deficiency-induced root branching that enhances Fe-deficiency tolerance in tomato plants. J Exp Bot 62:3875–3884

    Article  PubMed  CAS  Google Scholar 

  • Jourd′heuil D (2002) Increased nitric oxide-dependent nitrosylation of 4,5-diaminofluorescein by oxidants: implications for the measurement of intracellular nitric oxide. Free Radic Biol Med 33:676–684

    Article  PubMed  Google Scholar 

  • Kader AA (2002) Postharvest biology and technology: an overview. In: Kader AA (ed) Postharvest technology of horticultural crops, Publication 3311. University of California Agriculture and Natural Resources, pp 39–47

  • Kang J, Hwang J-U, Lee M, Kim Y–Y, Assmann SM, Martinoia E, Lee Y (2010) PDR-type ABC transporter mediates cellular uptake of the phytohormone abscisic acid. Proc Natl Acad Sci 107:2355–2360

    Article  PubMed  CAS  Google Scholar 

  • Kato H, Takemoto D, Kawakita K (2012) Proteomic analysis of S-nitrosylated proteins in potato plant. Physiol Plant. doi:10.1111/j.1399-3054.2012.01684.x

  • Kaur J, Deswal R (2010) Posttranslational modifications of proteins by nitric oxide: a new tool of metabolome regulation. In: Haya S, Mori M, Pichtel J, Ahmad A (eds) Nitric oxide in plant physiology. Wiley-VCH, Weinheim, pp 189–201

  • Kepinski S, Leyser O (2005) The Arabidopsis F-box protein TIR1 is an auxin receptor. Nature 435:446–451

    Article  PubMed  CAS  Google Scholar 

  • Kim T-H, Bihmer M, Hu H, Nishimura N, Schroeder JI (2010) Guard cell signal transduction network: advances in understanding abscisic acid, CO2, and Ca2+ signaling. Annu Rev Plant Biol 61:561–591

    Article  PubMed  CAS  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 

  • Klerk G-J, Krieken W, Jong JC (1999) Review the formation of adventitious roots: new concepts, new possibilities. In Vitro Cell Develop Biol––Plant 35:189–199

    Article  Google Scholar 

  • Kolbert Z, Bartha B, Erdei L (2008) Exogenous auxin-induced NO synthesis is nitrate reductase-associated in Arabidopsis thaliana root primordia. J Plant Physiol 165:967–975

    Article  PubMed  CAS  Google Scholar 

  • Lamattina L, García-Mata C, Graziano M, Pagnussat G (2003) Nitric oxide: the versatility of an extensive signal molecule. Annu Rev Plant Biol 54:109–136

    Article  PubMed  CAS  Google Scholar 

  • Lamotte O, Gould K, Lecourieux D, Sequeira-Legrand A, Lebrun-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  PubMed  CAS  Google Scholar 

  • Lamotte O, Courtois C, Dobrowolska G, Besson A, Pugin A, Wendehenne D (2006) Mechanisms of nitric-oxide-induced increase of free cytosolic Ca2+ concentration in Nicotiana plumbaginifolia cells. Free Radic Biol Med 40:1369–1376

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Lanteri ML, Laxalt AM, Lamattina L (2008) Nitric oxide triggers phosphatidic acid accumulation via phospholipase D during auxin-induced adventitious root formation in cucumber. Plant Physiol 147:188–198

    Article  PubMed  CAS  Google Scholar 

  • Lecourieux D, Mazars C, Pauly N, Ranjeva R, Pugin A (2002) Analysis and effects of cytosolic free calcium increases in response to elicitors in Nicotiana Plumbaginifolia cells. Plant Cell 14:2627–2641

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Leshem YY, Wills RBH, Veng-Va KuV (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 36:825–833

    Article  CAS  Google Scholar 

  • Li X, Li C (2004) Is ethylene involved in regulation of root ferric reductase activity of dicotyledonous species under iron deficiency? Plant Soil 261:147–153

    Article  CAS  Google Scholar 

  • Lingam S, Mohrbacher J, Brumbarova T, Potuschak T, Fink-Straube C, Blondet E, Genschik P, Bauer P (2011) Interaction between the bHLH Transcription factor FIT and ETHYLENE INSENSITIVE3/ETHYLENE INSENSITIVE3-LIKE1 reveals molecular linkage between the regulation of iron acquisition and ethylene signaling in Arabidopsis. Plant Cell 23:1815–1829

    Article  PubMed  CAS  Google Scholar 

  • Liu J, Liu G, Hou L, Liu X (2010) Ethylene-induced nitric oxide production and stomatal closure in Arabidopsis thaliana depending on changes in cytosolic pH. Chin Sci Bull 55:2403–2409

    Article  CAS  Google Scholar 

  • Liu W-Z, Kong D–D, Gu X–X, Gao H-B, Wang J-Z, Xia M, Gao Q, Tian L–L, Xu Z-H, Bao F, Hu Y, Ye N-S, Pei Z-M, He Y-K (2013) Cytokinins can act as suppressors of nitric oxide in Arabidopsis. Proc Natl Acad Sci 110:1548–1553

    Article  PubMed  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  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Lozano-Juste J, Colom-Moreno R, León J (2011) In vivo protein tyrosine nitration in Arabidopsis thaliana. J Exp Bot 62:3501–3517

    Article  PubMed  CAS  Google Scholar 

  • Lyndermayr C, Durner J (2009) S-nitrosylation in plants: pattern and function. J Prot 73:1–9

    Article  CAS  Google Scholar 

  • Lyndermayr C, Saalbach G, Durner J (2005) Proteomic identification of S-nitrosylated proteins in Arabidopsis, Plant Physiol, 137: 921–930

    Google Scholar 

  • Lyndermayr C, Saalbach G, Bahnweg G, Durner J (2006) Differential inhibition of Arabidopsis methionine adenosyl transferases by protein S-nitrosylation. JBC 281:4285–4291

    Google Scholar 

  • Ma Y, Szostkiewicz I, Korte A, Moes D, Yang Y, Christmann A, Grill E (2009) Regulators of PP2C phosphatase activity function as abscisic acid sensors. Science 324:1064–1068

    PubMed  CAS  Google Scholar 

  • Malik SI, Hussain A, Yun B-W, Spoel SH, Loake GJ (2011) GSNOR-mediated de-nitrosylation in the plant defence response. Plant Sci 181:540–544

    Article  PubMed  CAS  Google Scholar 

  • Manjunatha G, Gupta KJ, Lokesh V, Mur LAJ, Neelwarne B (2012) Nitric oxide counters ethylene effects on ripening fruits. Plant Signal Behav 7:476–483

    Article  PubMed  CAS  Google Scholar 

  • Meiser J, Lingam S, Bauer P (2011) Posttranslational regulation of the iron deficiency basic helix-loop-helix transcription factor FIT is affected by iron and nitric oxide. Plant Physiol 157:2154–2166

    Article  PubMed  CAS  Google Scholar 

  • Meng ZB, Chen LQ, Suo D, Li GX, Tang CX, Zheng SJ (2012) Nitric oxide is the shared signalling molecule in phosphorus––and iron-deficiency-induced formation of cluster roots in white lupin (Lupinus albus). Ann Bot 109:1055–1064

    Article  PubMed  CAS  Google Scholar 

  • Millar AH, Day DA (1996) Nitric oxide inhibits the cytochrome oxidase but not the alternative oxidase of plant mitochondria. FEBS Lett 398:155–158

    Article  PubMed  CAS  Google Scholar 

  • Moriconi JI, Buet A, Simontacchi M, Santa-María GE (2012) Near-isogenic wheat lines carrying altered function alleles of the Rht-1 genes exhibit differential responses to potassium deprivation. Plant Sci 185(186):199–207

    Article  PubMed  CAS  Google Scholar 

  • Morot-Gaudry-Talarmain Y, Rockel P, Moureaux T, Quillere I, Leydecker MT, Kaiser WM, Morot-Gaudry JF (2002) Nitrite accumulation and nitric oxide emission in relation to cellular signaling in nitrite reductase antisense tobacco. Planta 215:708–715

    Article  PubMed  CAS  Google Scholar 

  • Muday GK, Haworth P (1994) Tomato root growth, gravitropism, and lateral development: correlation with auxin transport. Plant Physiol Biochem 32:193–203

    PubMed  CAS  Google Scholar 

  • Murgia I, Delledonne M, Soave C (2002) Nitric oxide mediates iron-induced ferritin accumulation in Arabidopsis. Plant J 30:521–528

    Article  PubMed  CAS  Google Scholar 

  • Murgia I, Concetta de Pinto M, Delledonne M, Soave C, De Gara L (2004) Comparative effects of various nitric oxide donors on ferritin regulation, programmed cell death, and cell redox state in plant cells. J Plant Physiol 161:777–783

    Article  PubMed  CAS  Google Scholar 

  • Nacry P, Canivenc G, Muller B, Azmi A, Van Onckelen H, Rossignaol M, Doumas P (2005) A role for auxin redistribution in the responses of the root system architecture to phosphate starvation in arabidopsis. Plant Physiol 138:2061–2074

    Article  PubMed  CAS  Google Scholar 

  • Negi S, Santisree P, Kharshiing EV, Sharma R (2010) Inhibition of the ubiquitin-proteasome pathway alters cellular levels of nitric oxide in tomato seedlings. Mol Plant 3:854–869

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Neill SJ, Desikan R, Hancock JT (2003) Nitric oxide signalling in plants. New Phytol 159:11–35

    Article  CAS  Google Scholar 

  • Nooden LD, Guiamet JJ, John I (1997) Senescence mechanisms. Physiol Plant 101:746–753

    Article  CAS  Google Scholar 

  • O’Donnell VB, Freeman BA (2001) Interactions between nitric oxide and lipid oxidation pathways: implications for vascular disease. Circulation Res 88:12–21

    Article  PubMed  Google Scholar 

  • Ortega-Galisteo Ap, Rodríguez-Serrano M, Pazmiño DM, Gupta DK, Sandalio LM, Romero-Puertas MC (2012) S-nitrosylated proteins in pea (Pisum sativum L.) leaf peroxisomes: changes under abiotic stress. J Exp Bot 63:2089–2103

  • Pagnussat GC, Simontacchi M, Puntarulo S, Lamattina L (2002) Nitric oxide is required for root organogenesis. Plant Physiol 129:954–956

    Article  PubMed  CAS  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  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Parani M, Rudrabhatla S, Myers R, Weirich H, Smith B, Leaman DW, Goldman SL (2004) Microarray analysis of nitric oxide responsive transcripts in Arabidopsis. Plant Biotechnol J 2:359–366

    Article  PubMed  CAS  Google Scholar 

  • Park S-Y, Fung P, Nishimura N et al (2009) Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science 324:1068–1071

    PubMed  CAS  Google Scholar 

  • Peng J, Richards DE, Hartley NM et al (1999) “Green revolution” genes encode mutant gibberellin response modulators. Nature 400:256–261

    Article  PubMed  CAS  Google Scholar 

  • Polverari A, Molesini B, Pezzotti M, Buonaurio R, Marte M, Delledonne M (2003) Nitric oxide-mediated transcriptional changes in Arabidopsis thaliana. Mol Plant-Microbe Int 16(12):1094–1105

    Article  CAS  Google Scholar 

  • Puntarulo S, Jasid S, Boveris A, Simontacchi M (2010) Electron paramagnetic resonance as a tool to study nitric oxide generation in plants. In: Hayat S, Mori M, Pitchel J, Ahmad A (eds) Nitric Oxide in Plant Physiology. Wiley-Blackwell, New york, pp 17–29

    Google Scholar 

  • Radi R (2004) Nitric oxide, oxidants, and protein tyrosine nitration. Proc Natl Acad Sci 101:4003–4008

    Article  PubMed  CAS  Google Scholar 

  • Ramirez L, Simontacchi M, Murgia I, Zabaleta E, Lamattina L (2011) Nitric oxide, nitrosyl iron complexes, ferritin and frataxin: a well equipped team to preserve plant iron homeostasis. Plant Sci 181:582–592

    Article  PubMed  CAS  Google Scholar 

  • Robinson NJ, Procter CM, Connolly EL, Guerinot ML (1999) A ferric-chelate reductase for iron uptake from soils. Nature 397:694–697

    Article  PubMed  CAS  Google Scholar 

  • Romero-Puertas MC, Laxa M, Mattè A, Zaninotto F, Finkemeier I, Jones AME, Perazzolli M, Vandelle E, Dietz K-J, Delledonne M (2007) S-nitrosylation of peroxiredoxin II E promotes peroxynitrite-mediated tyrosine nitration. Plant Cell 19:4120–4130

    Article  PubMed  CAS  Google Scholar 

  • Rubbo H, Radi R (2008) Protein and lipid nitration: role in redox signaling and injury. Biochim Biophys Acta––Gen Sub 1780:1318–1324

    Article  CAS  Google Scholar 

  • Rubbo H, Radi R, Anselmi D, Kirk M, Barnes S, Butler J, Eiserich JP, Freeman BA (2000) Nitric oxide reaction with lipid peroxyl radicals spares alpha-tocopherol during lipid peroxidation. Greater oxidant protection from the pair nitric oxide/alpha-tocopherol than alpha-tocopherol/ascorbate. J Biol Chem 275:10812–10818

    Article  PubMed  CAS  Google Scholar 

  • Saito S, Yamamoto-Katou A, Yoshioka H, Doke N, Kawakita K (2006) Peroxynitrite generation and tyrosine nitration in defense responses in tobacco BY-2 cells. Plant Cell Physiol 47:689–697

    Article  PubMed  CAS  Google Scholar 

  • Saito N, Nakamura Y, Mori IC, Murata Y (2009) Nitric oxide functions in both methyl jasmonate signaling and abscisic acid signaling in Arabidopsis guard cells. Plant Signal Behav 4:119–120

    Article  PubMed  CAS  Google Scholar 

  • Santiago J, Rodrigues A, Saez A, Rubio S, Antoni R, Dupeux F, Park S-Y, Marquez JA, Cutler SR, Rodriguez PL (2009) Modulation of drought resistance by the abscisic acid receptor PYL5 through inhibition of clade A PP2Cs. Plant J 60:575–588

    Article  PubMed  CAS  Google Scholar 

  • Schmidt W, Bartels M (1996) Formation of root epidermal transfer cells in plantago. Plant Physiol 110:217–225

    PubMed  CAS  Google Scholar 

  • Schroeder JI, Allen GJ, Hugouvieux V, Kwak JM, Waner D (2001) Guard cell signal transduction. Ann Rev Plant Physiol Plant Mol Biol 52:627–658

    Article  CAS  Google Scholar 

  • Serpa V, Vernal J, Lamattina L, Grotewold E, Cassia R, Terenzi H (2007) Inhibition of AtMYB2 DNA-binding by nitric oxide involves cysteine S-nitrosylation. Biochem Biophys Res Comm 361:1048–1053

    Article  PubMed  CAS  Google Scholar 

  • Sokolovski S, Blatt MR (2004) Nitric oxide block of outward-rectifying K+ channels indicates direct control by protein nitrosylation in guard cells. Plant Physiol 136:4275–4284

    Article  PubMed  CAS  Google Scholar 

  • Stamler JS, Singel DJ, Loscalzo J (1992) Biochemistry of nitric oxide and its redox-activated forms. Science 258:1898–1902

    Google Scholar 

  • Stamler JS, Lamas S, Fang FC (2001) Nitrosylation: the prototypic redox-based signaling mechanism. Cell 106:675–683

    Article  PubMed  CAS  Google Scholar 

  • Staxen I, Pical C, Montgomery LT, Gray JE, Hetherington AM, McAinsh MR (1999) Abscisic acid induces oscillations in guard-cell cytosolic free calcium that involve phosphoinositide-specific phospholipase C. Proc Natl Acad Sci 96:1779–1784

    Article  PubMed  CAS  Google Scholar 

  • Sun T-P (2011) The molecular mechanism and evolution of the GA-GID1-DELLA signaling module in plants. Current Biol 21:338–345

    Article  CAS  Google Scholar 

  • Tan X, Calderon-Villalobos LIA, Sharon M, Zheng C, Robinson CV, Estelle M, Zheng N (2007) Mechanism of auxin perception by the TIR1 ubiquitin ligase. Nature 446:640–645

    Article  PubMed  CAS  Google Scholar 

  • Tanou G, Job C, Rajjou L, Arc E, Belghazi M, Diamantidis G, Molassiotis A (2009) Job D (2009) Proteomics reveals the overlapping roles of hydrogen peroxide and nitric oxide in the acclimation of citrus plants to salinity. Plant J 60:795–804

    Article  PubMed  CAS  Google Scholar 

  • Terrile MC, París R, Calderón-Villalobos LIA, Iglesias MJ, Lamattina L, Estelle M, Caslongué CA (2012) Nitric oxide influences auxin signaling through S-nitrosylation of the Arabidopsis TRANSPORT INHIBITOR RESPONSE 1 auxin receptor. Plant J 70:492–500

    Article  PubMed  CAS  Google Scholar 

  • Ueguchi-Tanaka M, Ashikari M, Itoh H, Katoh E, Kobayashi M, Chow T-Y, Hsing Y-iC, Kitano H, Yamaguchi I, Matsuoka M (2005) Gibberellin insensitive dwarf1 encodes a soluble receptor for gibberellin. Nature 437:693–698

    Article  PubMed  CAS  Google Scholar 

  • Wang YQ, Feechan A, Yun BW, Shafiei R, Hofmann A, Taylor P, Xue P, Yang FQ, Xie ZS, Pallas JA et al (2009) S-nitrosylation of AtSABP3 antagonizes the expression of plant immunity. J Biol Chem 284:2131–2137

    Google Scholar 

  • Wang BL, Tang XY, Cheng LY, Zhang AZ, Zhang WH, Zhang FS, Liu JQ, Cao Y, Allan DL, Vance CP, Shen JB (2010) Nitric oxide is involved in phosphorus deficiency-induced cluster-root development and citrate exudation in white lupin. New Phytol 187:1112–1123

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Wills RBH, Ku VVV, Leshem YY (2000) Fumigation with nitric oxide to extend the postharvest life of strawberries. Postharvest Biol Technol 18:75–79

    Article  CAS  Google Scholar 

  • Wink DA, Mitchell JB (1998) Chemical biology of nitric oxide: insights into regulatory, cytotoxic, and cytoprotective mechanisms of nitric oxide. Free Radic Biol Med 25:434–456

    Article  PubMed  CAS  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

    Article  CAS  Google Scholar 

  • Xiong J, Tao L, Zhu C (2009) Does nitric oxide play a pivotal role downstream of auxin in promoting crown root primordia initiation in monocots? Plant Signal Behav 4:999–1001

    Article  PubMed  CAS  Google Scholar 

  • Xiong J, Fu G, Yang Y, Zhu C, Tao L (2012) Tungstate: is it really a specific nitrate reductase inhibitor in plant nitric oxide research? J Exp Bot 63:33–41

    Article  PubMed  CAS  Google Scholar 

  • Xu J, Wang W, Yin H, Liu X, Sun H, Mi Q (2010) Exogenous nitric oxide improves antioxidative capacity and reduces auxin degradation in roots of Medicago truncatula seedlings under cadmium stress. Plant Soil 326:321–330

    Article  CAS  Google Scholar 

  • Yadav S, David A, Bhatla SC (2011) Nitric oxide accumulation and actin distribution during auxin-induced adventitious root development in sunflower. Sci Hortic 129:159–166

    Article  CAS  Google Scholar 

  • Zaharah SS, Singh Z (2011) Mode of action of nitric oxide in inhibiting ethylene biosynthesis and fruit softening during ripening and cool storage of ‘Kensington Pride’ mango. Postharvest Biol Technol 62:258–266

    Article  CAS  Google Scholar 

  • Zeng C-L, Liu L, Xu G-Q (2011) The physiological responses of carnation cut flowers to exogenous nitric oxide. Sci Hortic 127:424–430

    Article  CAS  Google Scholar 

  • Zhang X, Takemiya A, Kinoshita T, Shimazaki K (2007) Nitric oxide inhibits blue light-specific stomatal opening via abscisic acid signaling pathways in vicia guard cells. Plant Cell Physiol 48:715–723

    Article  PubMed  CAS  Google Scholar 

  • Zhu S, Zhou J (2007) Effect of nitric oxide on ethylene production in strawberry fruit during storage. Food Chem 100:1517–1522

    Article  CAS  Google Scholar 

  • Zhu S, Liu M, Zhou J (2006) Inhibition by nitric oxide of ethylene biosynthesis and lipoxygenase activity in peach fruit during storage. Postharvest Biol Technol 42:41–48

    Article  CAS  Google Scholar 

  • Zottini M, Costa A, de Michele R, Ruzzene M, Carimi F, Lo Schiavo F (2007) Salicylic acid activates nitric oxide synthesis in Arabidopsis. J Exp Bot 58:1397–1405

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We are grateful to Agencia Nacional de Promoción Científica y Tecnológica (ANPCyT) and Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET) for financial support. MS, CG-M, CGB, GS-M, and LL are career investigators from CONICET.

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Authors and Affiliations

  1. Instituto de Fisiología Vegetal (INFIVE) CC327, Universidad Nacional de La Plata-CONICET, Diagonal 113 y calle 61 N°495, CP 1900, La Plata, Buenos Aires, Argentina

    Marcela Simontacchi & Carlos G. Bartoli

  2. Instituto de Investigaciones Biológicas, Universidad Nacional de Mar del Plata-CONICET, 7600, Mar del Plata, Buenos Aires, Argentina

    Carlos García-Mata & Lorenzo Lamattina

  3. Instituto Tecnológico Chascomús (IIB-INTECH), CONICET, Camino Circunvalación Laguna Km 8.5, 7130, Chascomús, Buenos Aires, Argentina

    Guillermo E. Santa-María

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  1. Marcela Simontacchi
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  2. Carlos García-Mata
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  3. Carlos G. Bartoli
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  4. Guillermo E. Santa-María
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  5. Lorenzo Lamattina
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Correspondence to Marcela Simontacchi.

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Communicated by P. Kumar.

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Simontacchi, M., García-Mata, C., Bartoli, C.G. et al. Nitric oxide as a key component in hormone-regulated processes. Plant Cell Rep 32, 853–866 (2013). https://doi.org/10.1007/s00299-013-1434-1

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