Abstract
Nitric oxide (·NO) and derived molecules, referred to as reactive nitrogen species (RNS), have become a new area of plant research. These molecules are involved in almost all physiological plant processes, ranging from seed germination, development, senescence, stomatal movement, fruit ripening, and reproduction to mechanisms of response to adverse environmental conditions possibly associated with nitro-oxidative stress. ·NO can perform a dual function depending on its rate of production; at low concentrations, it acts as a signal molecule and, at high concentrations, like a stress molecule. Although in some cases the simultaneous high ·NO production with other reactive oxygen species (ROS) can be useful to the cells as mechanism of defense, for example, against pathogens. All these processes are usually mediated by the chemical interactions of ·NO whose functions are affected by other molecules. It is worth pointing out that the post-translational modifications of target proteins caused by nitration and S-nitrosylation have been best described in plants. However, ·NO can also regulate gene expression through direct interaction with DNA or through interaction with transcription factors. This review provides a comprehensive overview of the role played by RNS in the physiology of plants and their involvement in the mechanism of response to a diverse range of adverse environmental conditions.
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References
Airaki M, Leterrier M, Mateos RM, Valderrama R, Chaki M, Barroso JB, del Río LA, Palma JM, Corpas FJ (2012) Metabolism of reactive oxygen species and reactive nitrogen species in pepper (Capsicum annuum L.) plants under low temperature stress. Plant Cell Environ 35:281–295
Airaki M, Leterrier M, Valderrama R, Chaki M, Begara-Morales JC, Barroso JB, del Río LA, Palma JM, Corpas FJ (2015) Spatial and temporal regulation of the metabolism of reactive oxygen and nitrogen species during the early development of pepper (Capsicum annuum) seedlings. Ann Bot 116:679–693
Arasimowicz-Jelonek M, Floryszak-Wieczorek J (2011) Understanding the fate of peroxynitrite in plant cells--from physiology to pathophysiology. Phytochemistry 72:681–688
Arasimowicz-Jelonek M, Floryszak-Wieczorek J, Gwóźdź EA (2011) The message of nitric oxide in cadmium challenged plants. Plant Sci 181:612–620
Askew SC, Barnett DJ, McAninly J, Williams DLH (1995) Catalysis by Cu2+ of nitric oxide release from S-nitrosothiols (RSNO). J Chem Soc Perkin Trans 2:741–745
Astier J, Besson-Bard A, Lamotte O, Bertoldo J, Bourque S, Terenzi H, Wendehenne D (2012) Nitric oxide inhibits the ATPase activity of the chaperone-like AAA+ ATPase CDC48, a target for S-nitrosylation in cryptogein signalling in tobacco cells. Biochem J 447:249–260
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 LA (2006) Localization of S-nitrosoglutathione and expression of S-nitrosoglutathione reductase in pea plants under cadmium stress. J Exp Bot 57:1785–1793
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
Begara-Morales JC, Sánchez-Calvo B, Luque F, Leyva-Pérez MO, Leterrier M, Corpas FJ, Barroso JB (2014a) Differential transcriptomic analysis by RNA-Seq of GSNO-responsive genes between Arabidopsis roots and leaves. Plant Cell Physiol 55:1080–1095
Begara-Morales JC, Sánchez-Calvo B, Chaki M, Valderrama R, Mata-Pérez C, López-Jaramillo J, Padilla MN, Carreras A, Corpas FJ, Barroso JB (2014b) Dual regulation of cytosolic ascorbate peroxidase (APX) by tyrosine nitration and S-nitrosylation. J Exp Bot 65:527–538
Begara-Morales JC, Sánchez-Calvo B, Chaki M, Mata-Pérez C, Valderrama R, Padilla MN, López-Jaramillo J, Luque F, Corpas FJ, Barroso JB (2015) Differential molecular response of monodehydroascorbate reductase and glutathione reductase by nitration and S-nitrosylation. J Exp Bot 66:5983–5996
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
Berton P, Domínguez-Romero JC, Wuilloud RG, Sánchez-Calvo B, Chaki M, Carreras A, Valderrama R, Begara-Morales JC, Corpas FJ, Barroso JB, Gilbert-López B, García-Reyes JF, Molina-Díaz A (2012) Determination of nitrotyrosine in Arabidopsis thaliana cell cultures with a mixed-mode solid-phase extraction cleanup followed by liquid chromatography time-of-flight mass spectrometry. Anal Bioanal Chem 404:1495–1503
Besson-Bard A, Pugin A, Wendehenne D (2008) New insights into nitric oxide signaling in plants. Annu Rev Plant Biol 59:21–39
Besson-Bard A, Gravot A, Richaud P, Auroy P, Duc C, Gaymard F, Taconnat L, Renou JP, Pugin A, Wendehenne D (2009) Nitric oxide contributes to cadmium toxicity in Arabidopsis by promoting cadmium accumulation in roots and by up-regulating genes related to iron uptake. Plant Physiol 149:1302–1315
Blokhina O, Fagerstedt KV (2010) Reactive oxygen species and nitric oxide in plant mitochondria: origin and redundant regulatory systems. Physiol Plant 138:447–462
Cabrera JJ, Sánchez C, Gates AJ, Bedmar EJ, Mesa S, Richardson DJ, Delgado MJ (2011) The nitric oxide response in plant-associated endosymbiotic bacteria. Biochem Soc Trans 39:1880–1885
Cai W, Liu W, Wang WS, Fu ZW, Han TT, Lu YT (2015) Overexpression of rat neurons nitric oxide synthase in rice enhances drought and salt tolerance. PLoS One 10(6), e0131599
Calcagno C, Novero M, Genre A, Bonfante P, Lanfranco L (2012) The exudate from an arbuscular mycorrhizal fungus induces nitric oxide accumulation in Medicago truncatula roots. Mycorrhiza 22:259–269
Calcerrada P, Peluffo G, Radi R (2011) Nitric oxide-derived oxidants with a focus on peroxynitrite: molecular targets, cellular responses and therapeutic implications. Curr Pharm Des 17:3905–3932
Camejo D, Jiménez A, Palma JM, Sevilla F (2015) Proteomic identification of mitochondrial carbonylated proteins in two maturation stages of pepper fruits. Proteomics 15:2634–2642
Castillo MC, Lozano-Juste J, González-Guzmán M, Rodriguez L, Rodriguez PL, León J (2015) Inactivation of PYR/PYL/RCAR ABA receptors by tyrosine nitration may enable rapid inhibition of ABA signaling by nitric oxide in plants. Sci Signal 8(392):ra89.
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
Chaki M, Fernández-Ocaña AM, Valderrama R, Carreras A, Esteban FJ, Luque F, Gómez-Rodríguez MV, Begara-Morales JC, Corpas FJ, Barroso JB (2009) Involvement of reactive nitrogen and oxygen species (RNS and ROS) in sunflower-mildew interaction. Plant Cell Physiol 50:265–279
Chaki M, Valderrama R, Fernández-Ocaña AM, Carreras A, Gómez-Rodríguez MV, López-Jaramillo J, Begara-Morales JC, Sánchez-Calvo B, Luque F, Leterrier M, Corpas FJ, Barroso JB (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
Chaki M, Álvarez de Morales P, Ruiz C, Begara-Morales JC, Barroso JB, Corpas FJ, Palma JM (2015a) Ripening of pepper (Capsicum annuum) fruit is characterized by an enhancement of protein tyrosine nitration. Ann Bot 116:637–647
Chaki M, Shekariesfahlan A, Ageeva A, Mengel A, von Toerne C, Durner J, Lindermayr C (2015b) Identification of nuclear target proteins for S-nitrosylation in pathogen-treated Arabidopsis thaliana cell cultures. Plant Sci 238:115–126
Chen R, Sun S, Wang C, Li Y, Liang Y, An F, Li C, Dong H, Yang X, Zhang J, Zuo J (2009) The Arabidopsis PARAQUAT RESISTANT2 gene encodes an S-nitrosoglutathione reductase that is a key regulator of cell death. Cell Res 19:1377–1387
Chen J, Xiong DY, Wang WH, Hu WJ, Simon M, Xiao Q, Chen J, Liu TW, Liu X, Zheng HL (2013) Nitric oxide mediates root K+/Na + balance in a mangrove plant, Kandelia obovata, by enhancing the expression of AKT1-type K+ channel and Na+/H+ antiporter under high salinity. PLoS One 8(8), e71543
Chen J, Vandelle E, Bellin D, Delledonne M (2014) Detection and function of nitric oxide during the hypersensitive response in Arabidopsis thaliana: where there’s a will there’s a way. Nitric Oxide 43:81–88
Cheng T, Chen J, Allah EFA, Wang P, Wang G, Hu X, Shi J (2015) Quantitative proteomics analysis reveals that S-nitrosoglutathione reductase (GSNOR) and nitric oxide signaling enhance poplar defense against chilling stress. Planta 242:1361–1390
Chmielowska-Bąk J, Gzyl J, Rucińska-Sobkowiak R, Arasimowicz-Jelonek M, Deckert J (2014) The new insights into cadmium sensing. Front Plant Sci 5:245
Clark D, Durner J, Navarre DA, Klessig DF (2000) Nitric oxide inhibition of tobacco catalase and ascorbate peroxidase. Mol Plant Microbe Interact 13:1380–1384
Corpas FJ, Barroso JB (2013) Nitro-oxidative stress vs oxidative or nitrosative stress in higher plants. New Phytol 199:633–635
Corpas FJ, Barroso JB (2014) Peroxynitrite (ONOO-) is endogenously produced in Arabidopsis peroxisomes and is overproduced under cadmium stress. Ann Bot 113:87–96
Corpas FJ, Barroso JB (2015a) Nitric oxide from a green perspective. Nitric Oxide 45:15–19
Corpas FJ, Barroso JB (2015b) Functions of nitric oxide (NO) in roots during development and under adverse stress conditions. Plants 4:240–252
Corpas FJ, Barroso JB, Carreras A, Quirós M, León AM, Romero-Puertas MC, Esteban FJ, Valderrama R, Palma JM, Sandalio LM, Gómez M, del Río LA (2004) Cellular and subcellular localization of endogenous nitric oxide in young and senescent pea plants. Plant Physiol 136:2722–2733
Corpas FJ, Barroso JB, Carreras A, Valderrama R, Palma JM, León AM, Sandalio LM, del Río LA (2006) Constitutive arginine-dependent nitric oxide synthase activity in different organs of pea seedlings during plant development. Planta 224:246–254
Corpas FJ, del Río LA, Barroso JB (2007) Need of biomarkers of nitrosative stress in plants. Trends Plant Sci 12:436–438
Corpas FJ, Chaki M, Fernández-Ocaña A, Valderrama R, Palma JM, Carreras A, Begara-Morales JC, Airaki M, del Río LA, Barroso JB (2008) Metabolism of reactive nitrogen species in pea plants under abiotic stress conditions. Plant Cell Physiol 49:1711–1722
Corpas FJ, Hayashi M, Mano S, Nishimura M, Barroso JB (2009a) Peroxisomes are required for in vivo nitric oxide accumulation in the cytosol following salinity stress of Arabidopsis plants. Plant Physiol 151:2083–2894
Corpas FJ, Palma JM, del Río LA, Barroso JB (2009b) Evidence supporting the existence of l-arginine-dependent nitric oxide synthase activity in plants. New Phytol 184:9–14
Corpas FJ, Leterrier M, Valderrama R, Airaki M, Chaki M, Palma JM, Barroso JB (2011) Nitric oxide imbalance provokes a nitrosative response in plants under abiotic stress. Plant Sci 181:604–611
Corpas FJ, Palma JM, del Río LA, Barroso JB (2013) Protein tyrosine nitration in higher plants grown under natural and stress conditions. Front Plant Sci 4:29
Corpas FJ, Begara-Morales JC, Sánchez-Calvo B, Chaki C, Barroso JB (2015) Nitration and S-nitrosylation: two post-translational modifications (PTMs) mediated by reactive nitrogen species (RNS) and their role in signalling processes of plant cells. In: KJ Gupta, AU Igamberdiev (eds) Reactive oxygen and nitrogen species signaling and communication in plants, signaling and communication in plants, vol 23. Springer International Publishing, Switzerland, pp 267–281. ISBN: 978-3-319-10078-4
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
Creus CM, Graziano M, Casanovas EM, Pereyra MA, Simontacchi M, Puntarulo S, Barassi CA, Lamattina L (2005) Nitric oxide is involved in the Azospirillum brasilense-induced lateral root formation in tomato. Planta 221:297–303
del Giudice J, Cam Y, Damiani I, Fung-Chat F, Meilhoc E, Bruand C, Brouquisse R, Puppo A, Boscari A (2011) Nitric oxide is required for an optimal establishment of the Medicago truncatula-Sinorhizobium meliloti symbiosis. New Phytol 191:405–417
Dixit V, Pandey V, Shyam R (2001) Differential antioxidative responses to cadmium in roots and leaves of pea (Pisum sativum L. cv. Azad). J Exp Bot 52:1101–1109
Domingos P, Prado AM, Wong A, Gehring C, Feijo JA (2015) Nitric oxide: a multitasked signaling gas in plants. Mol Plant 8:506–520
Duan X, Li X, Ding F, Zhao J, Guo A, Zhang L, Yao J, Yang Y (2014) Interaction of nitric oxide and reactive oxygen species and associated regulation of root growth in wheat seedlings under zinc stress. Ecotoxicol Environ Saf 113C:95–102
Espunya MC, Diaz M, Moreno-Romero J, Martinez MC (2006) Modification of intracellular levels of glutathione-dependent formaldehyde dehydrogenase alters glutathione homeostasis and root development. Plant Cell Environ 29:1002–1011
Estévez AG, Jordán J (2002) Nitric oxide and superoxide, a deadly cocktail. Ann N Y Acad Sci 962:207–211
Fares A, Nespoulous C, Rossignol M, Peltier JB (2014) Simultaneous identification and quantification of nitrosylation sites by combination of biotin switch and ICAT labeling. Methods Mol Biol 1072:609–620
Fazzari M, Trostchansky A, Schopfer FJ, Salvatore SR, Sánchez-Calvo B, Vitturi D, Valderrama R, Barroso JB, Radi R, Freeman BA, Rubbo H (2014) Olives and olive oil are sources of electrophilic fatty acid nitroalkenes. PLoS One 9(1), e84884
Fernández-Marcos M, Sanz L, Lewis DR, Muday GK, Lorenzo O (2011) Nitric oxide causes root apical meristem defects and growth inhibition while reducing PINFORMED 1 (PIN1)-dependent acropetal auxin transport. Proc Natl Acad Sci U S A 108:18506–18511
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 green alga Ostreococcus tauri is light irradiance and growth phase dependent. Plant Cell 22:3816–3830
Foster MW, Forrester MT, Stamler JS (2009) A protein microarray-based analysis of S-nitrosylation. Proc Natl Acad Sci U S A 106:18948–18953
Freschi L (2013) Nitric oxide and phytohormone interactions: current status and perspectives. Front Plant Sci 4:398
Gayatri G, Agurla S, Raghavendra AS (2013) Nitric oxide in guard cells as an important secondary messenger during stomatal closure. Front Plant Sci 4:425
Gill SS, Hasanuzzaman M, Nahar K, Macovei A, Tuteja N (2013) Importance of nitric oxide in cadmium stress tolerance in crop plants. Plant Physiol Biochem 63:254–261
Gniazdowska A, Krasuska U, Debska K, Andryka P, Bogatek R (2010) The beneficial effect of small toxic molecules on dormancy alleviation and germination of apple embryos is due to NO formation. Planta 232:999–1005
Gray B, Carmichael AJ (1992) Kinetics of superoxide scavenging by dismutase enzymes and manganese mimics determined by electron spin resonance. Biochem J 281:795–802
Guo K, Xia K, Yang Z-M (2008) Regulation of tomato lateral root development by carbon monoxide and involvement in auxin and nitric oxide. J Exp Bot 59:3443–3452
Guo Z, Tan J, Zhuo C, Wang C, Xiang B, Wang Z (2014) Abscisic acid, H2O2 and nitric oxide interactions mediated cold-induced S-adenosylmethionine synthetase in Medicago sativa subsp. falcata that confers cold tolerance through up-regulating polyamine oxidation. Plant Biotechnol J 12:601–612
Han P, Zhou X, Huang B, Zhang X, Chen C (2008) On-gel fluorescent visualization and the site identification of S-nitrosylated proteins. Anal Biochem 377:150–155
Han B, Yang Z, Xie Y, Nie L, Cui J, Shen W (2014) Arabidopsis HY1 confers cadmium tolerance by decreasing nitric oxide production and improving iron homeostasis. Mol Plant 7:388–403
Hasanuzzaman M, Fujita M (2013) Exogenous sodium nitroprusside alleviates arsenic-induced oxidative stress in wheat (Triticum aestivum L.) seedlings by enhancing antioxidant defense and glyoxalase system. Ecotoxicology 22:584–596
Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annu Rev Plant Physiol Plant Mol Biol 51:463–499
He Y, Tang RH, Hao Y, Stevens RD, Cook CW, Ahn SM, Jing L, Yang Z, Chen L, Guo F, Fiorani F, Jackson RB, Crawford NM, Pei ZM (2004) Nitric oxide represses the Arabidopsis floral transition. Science 305:1968–1971
Hernández LE, Sobrino-Plata J, Montero-Palmero MB, Carrasco-Gil S, Flores-Cáceres ML, Ortega-Villasante C, Escobar C (2015) Contribution of glutathione to the control of cellular redox homeostasis under toxic metal and metalloid stress. J Exp Bot 66:2901–2911
Hichri I, Boscari A, Castella C, Rovere M, Puppo A, Brouquisse R (2015) Nitric oxide: a multifaceted regulator of the nitrogen-fixing symbiosis. J Exp Bot 66:2877–2887
Holzmeister C, Gaupels F, Geerlof A, Sarioglu H, Sattler M, Durner J, Lindermayr C (2015) Differential inhibition of Arabidopsis superoxide dismutases by peroxynitrite-mediated tyrosine nitration. J Exp Bot 66:989–999
Jaffrey SR (2005) Detection and characterization of protein nitrosothiols. Methods Enzymol 396:105–118
Kashyap P, Sehrawat A, Deswal R (2015) Nitric oxide modulates Lycopersicon esculentum C-repeat binding factor 1 (LeCBF1) transcriptionally as well as post-translationally by nitrosylation. Plant Physiol Biochem 96:115–123
Kato H, Takemoto D, Kawakita K (2013) Proteomic analysis of S-nitrosylated proteins in potato plant. Physiol Plantarum 148:371–386
Kopyra M, Gwózdz EA (2003) Nitric oxide stimulates seed germination and counteracts the inhibitory effect of heavy metals and salinity on root growth of Lupinus luteus. Plant Physiol Biochem 41:1011–1017
Kovacs I, Durner J, Lindermayr C (2015) Crosstalk between nitric oxide and glutathione is required for NONEXPRESSOR OF PATHOGENESIS-RELATED GENES 1 (NPR1)-dependent defense signaling in Arabidopsis thaliana. New Phytol. 208:860–872
Kubienová L, Kopečný D, Tylichová M, Briozzo P, Skopalová J, Šebela M, Navrátil M, Tâche R, Luhová L, Barroso JB, Petřivalský M (2013) Structural and functional characterization of a plant S-nitrosoglutathione reductase from Solanum lycopersicum. Biochimie 95:889–902
Kulik A, Noirot E, Grandperret V, Bourque S, Fromentin J, Salloignon P, Truntzer C, Dobrowolska G, Simon-Plas F, Wendehenne D (2015) Interplays between nitric oxide and reactive oxygen species in cryptogein signalling. Plant Cell Environ 38:331–348
Kwon E, Feechan A, Yun BW, Hwang BH, Pallas JA, Kang JG, Loake GJ (2012) AtGSNOR1 function is required for multiple developmental programs in Arabidopsis. Planta 236:887–900
Lamotte O, Courtois C, Barnavon L, Pugin A, Wendehenne D (2005) Nitric oxide in plants: the biosynthesis and cell signalling properties of a fascinating molecule. Planta 221:1–4
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
Leshem YY, Pinchasov Y (2000) Non-invasive photoacoustic spectroscopic determination of relative endogenous nitric oxide and ethylene content stoichiometry during the ripening of strawberries Fragaria ananassa (Dutch.) and avocados Persea americana (Mill.). J Exp Bot 51:1471–1473
Leterrier M, Chaki M, Airaki M, Valderrama R, Palma JM, Barroso JB, Corpas FJ (2011) Function of S-nitrosoglutathione reductase (GSNOR) in plant development and under biotic/abiotic stress. Plant Signal Behav 6:789–793
Leterrier M, Airaki M, Palma JM, Chaki M, Barroso JB, Corpas FJ (2012) Arsenic triggers the nitric oxide (NO) and S-nitrosoglutathione (GSNO) metabolism in Arabidopsis. Environ Pollut 166:136–143
Leterrier M, Barroso JB, Valderrama R, Begara-Morales JC, Sánchez-Calvo B, Chaki M, Luque F, Viñegla B, Palma JM, Corpas FJ (2016) Peroxisomal NADP-isocitrate dehydrogenase is required for Arabidopsis stomatal movement. Protoplasma. 253:403–415
Lindermayr C, Saalbac G, Durner J (2005) Proteomic identification of S-nitrosylated proteins in Arabidopsis. Plant Physiol 137:921–930
Liu S, Yang R, Pan Y, Ma M, Pan J, Zhao Y, Cheng Q, Wu M, Wang M, Zhang L (2015) Nitric oxide contributes to minerals absorption, proton pumps and hormone equilibrium under cadmium excess in Trifolium repens L. plants. Ecotoxicol Environ Saf 119:35–46
Lozano-Juste J, Leon J (2010) Enhanced abscisic acid-mediated responses in nia1nia2noa1-2 triple mutant impaired in NIA/NR- and AtNOA1-dependent nitric oxide biosynthesis in Arabidopsis. Plant Physiol 152:891–903
Lu Y, Li N, Sun J, Hou P, Jing X, Zhu H, Deng S, Han Y, Huang X, Ma X, Zhao N, Zhang Y, Shen X, Chen S (2013) Exogenous hydrogen peroxide, nitric oxide and calcium mediate root ion fluxes in two non-secretor mangrove species subjected to NaCl stress. Tree Physiol 33:81–95
Manai J, Gouia H, Corpas FJ (2014a) Redox and nitric oxide homeostasis are affected in tomato (Solanum lycopersicum) roots under salinity-induced oxidative stress. J Plant Physiol 171:1028–1035
Manai J, Kalai T, Gouia H, Corpas FJ (2014b) Exogenous nitric oxide (NO) ameliorates salinity-induced oxidative stress in tomato (Solanum lycopersicum) plants. J Soil Sci Plant Nutr 14:433–446
Manjunatha G, Lokesh V, Neelwarne B (2010) Nitric oxide in fruit ripening: trends and opportunities. Biotechnol Adv 28:489–499
McInnis SM, Desikan R, Hancock JT, Hiscock SJ (2006) Production of reactive oxygen species and reactive nitrogen species by angiosperm stigmas and pollen: potential signalling crosstalk? New Phytol 172:221–228
Meilhoc E, Boscari A, Bruand C, Puppo A, Brouquisse R (2011) Nitric oxide in Legume-Rhizobium symbiosis. Plant Sci 181:573–581
Molassiotis A, Tanou G, Diamantidis G (2010) NO says more than ‘YES’ to salt tolerance: salt priming and systemic nitric oxide signaling in plants. Plant Signal Behav 5:209–212
Molina-Favero C, Creus CM, Simontacchi M, Puntarulo S, Lamattina L (2008) Aerobic nitric oxide production by Azospirillum brasilense Sp245 and its influence on root architecture in tomato. Mol Plant Microbe Interact 21:1001–1009
Neill SJ, Desikan R, Hancock JT (2003) Nitric oxide signaling in plants. New Phytol 159:11–35
Neill S, Barros R, Bright J, Desikan R, Hancock J, Harrison J, Morris P, Ribeiro D, Wilson I (2008) Nitric oxide, stomatal closure, and abiotic stress. J Exp Bot 59:165–176
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
Peng D, Wang X, Li Z, Zhang Y, Peng Y, Li Y, He X, Zhang X, Ma X, Huang L, Yan Y (2015) NO is involved in spermidine-induced drought tolerance in white clover via activation of antioxidant enzymes and genes. Protoplasma. doi:10.1007/s00709-015-0880-8
Pfeiffer S, Mayer B, Hemmens B (1999) Nitric oxide: chemical puzzles posed by a biological messenger. Angew Chem Int Ed 38:1714–1731
Piterková J, Luhová L, Mieslerová B, Lebeda A, Petřivalský M (2013) Nitric oxide and reactive oxygen species regulate the accumulation of heat shock proteins in tomato leaves in response to heat shock and pathogen infection. Plant Sci 207:57–65
Prado AM, Porterfield DM, Feijó JA (2004) Nitric oxide is involved in growth regulation and re-orientation of pollen tubes. Development 131:2707–2714
Prado AM, Colaço R, Moreno N, Silva AC, Feijó JA (2008) Targeting of pollen tubes to ovules is dependent on nitric oxide (NO) signaling. Mol Plant 1:703–714
Prats E, Mur LA, Sanderson R, Carver TL (2005) Nitric oxide contributes both to papilla-based resistance and the hypersensitive response in barley attacked by Blumeria graminis f. sp. hordei. Mol Plant Pathol 6:65–78
Puyaubert J, Baudouin E (2014) New clues for a cold case: nitric oxide response to low temperature. Plant Cell Environ 37:2623–2630
Rockel P, Strube F, Rockel AJ, Wildt JWM, Kaiser WM (2002) Regulation of nitric oxide (NO) production by plant nitrate reductase in vivo and in vitro. J Exp Bot 53:103–110
Rodríguez-Serrano M, Romero-Puertas MC, Zabalza A, Corpas FJ, Gómez M, del Río LA, Sandalio LM (2006) Cadmium effect on oxidative metabolism of pea (Pisum sativum L.) roots. Imaging of reactive oxygen species and nitric oxide accumulation in vivo. Plant Cell Environ 29:1532–1544
Romero-Puertas MC, Laxa M, Mattè 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 19:4120–4130
Romero-Puertas MC, Campostrini N, Mattè A, Righetti PG, Perazzolli M, Zolla L, Roepstorff P, Delledonne M (2008) Proteomic analysis of S-nitrosylated proteins in Arabidopsis thaliana undergoing hypersensitive response. Proteomics 8:1459–1469
Rubbo H, Radi R (2008) Protein and lipid nitration: role in redox signaling and injury. Biochim Biophys Acta 1780:1318–1324
Sainz M, Pérez-Rontomé C, Ramos J, Mulet JM, James EK, Bhattacharjee U, Petrich JW, Becana M (2013) Plant hemoglobins may be maintained in functional form by reduced flavins in the nuclei, and confer differential tolerance to nitro-oxidative stress. Plant J 76:875–887
Sainz M, Calvo-Begueria L, Pérez-Rontomé C, Wienkoop S, Abián J, Staudinger C, Bartesaghi S, Radi R, Becana M (2015) Leghemoglobin is nitrated in functional legume nodules in a tyrosine residue within the heme cavity by a nitrite/peroxide-dependent mechanism. Plant J 81:723–735
Sakamoto A, Ueda M, Morikawa H (2002) Arabidopsis glutathione-dependent formaldehyde dehydrogenase is an S-nitrosoglutathione reductase. FEBS Lett 515:20–24
Sánchez-Calvo B, Barroso JB, Corpas FJ (2013) Hypothesis: nitro-fatty acids play a role in plant metabolism. Plant Sci 199–200:1–6
Santisree P, Bhatnagar-Mathur P, Sharma KK (2015) NO to drought-multifunctional role of nitric oxide in plant drought: do we have all the answers? Plant Sci 239:44–55
Sanz L, Albertos P, Mateos I, Sánchez-Vicente I, Lechón T, Fernández-Marcos M, Lorenzo O (2015) Nitric oxide (NO) and phytohormones crosstalk during early plant development. J Exp Bot 66:2857–2868
Scheler C, Durner J, Astier J (2013) Nitric oxide and reactive oxygen species in plant biotic interactions. Curr Opin Plant Biol 16:534–539
Sehrawat A, Deswal R (2014) S-nitrosylation analysis in Brassica juncea apoplast highlights the importance of nitric oxide in cold-stress signalling. J Proteome Res 13:2599–25619
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 Commun 361:1048–1053
Shi YF, Wang DL, Wang C, Culler AH, Kreiser MA, Suresh J, Cohen JD, Pan J, Baker B, Liu JZ (2015) Loss of GSNOR1 function leads to compromised auxin signaling and polar auxin transport. Mol Plant 8:1350–1365
Signorelli S, Möller MN, Coitiño EL, Denicola A (2011) Nitrogen dioxide solubility and permeation in lipid membranes. Arch Biochem Biophys 512:190–196
Signorelli S, Corpas FJ, Borsani O, Barroso JB, Monza J (2013) Water stress induces a differential and spatially distributed nitro-oxidative stress response in roots and leaves of Lotus japonicus. Plant Sci 201–202:137–146
Simontacchi M, Jasid S, Puntarulo S (2004) Nitric oxide generation during early germination of Sorghum seeds. Plant Sci 167:839–847
Singh HP, Kaur S, Batish DR, Sharma VP, Sharma N, Kohli RK (2009) Nitric oxide alleviates arsenic toxicity by reducing oxidative damage in the roots of Oryza sativa (rice). Nitric Oxide 20:289–297
Singh VP, Srivastava PK, Prasad SM (2013) Nitric oxide alleviates arsenic-induced toxic effects in ridged Luffa seedlings. Plant Physiol Biochem 71:155–163
Szabó C, Ischiropoulos H, Radi R (2007) Peroxynitrite: biochemistry, pathophysiology and development of therapeutics. Nat Rev Drug Discov 6:662–680
Szuba A, Kasprowicz-Maluśki A, Wojtaszek P (2015) Nitration of plant apoplastic proteins from cell suspension cultures. J Proteomics 120:158–168
Tanou G, Job C, Rajjou L, Arc E, Belghazi M, Diamantidis G, Molassiotis A, Job D (2009a) Proteomics reveals the overlapping roles of hydrogen peroxide and nitric oxide in the acclimation of citrus plants to salinity. Plant J 60:795–804
Tanou G, Molassiotis A, Diamantidis G (2009b) Hydrogen peroxide- and nitric oxide-induced systemic antioxidant prime-like activity under NaCl-stress and stress-free conditions in citrus plants. J Plant Physiol 166:1904–1913
Tanou G, Filippou P, Belghazi M, Job D, Diamantidis G, Fotopoulos V, Molassiotis A (2012) Oxidative and nitrosative-based signaling and associated post-translational modifications orchestrate the acclimation of citrus plants to salinity stress. Plant J 72:585–599
Tavares CP, Vernal J, Delena RA, Lamattina L, Cassia R, Terenzi H (2014) S-nitrosylation influences the structure and DNA binding activity of AtMYB30 transcription factor from Arabidopsis thaliana. Biochim Biophys Acta 1844:810–817
Terrile MC, París R, Calderón-Villalobos LI, Iglesias MJ, Lamattina L, Estelle M, Casalongué CA (2012) Nitric oxide influences auxin signaling through S-nitrosylation of the Arabidopsis TRANSPORT INHIBITOR RESPONSE 1 auxin receptor. Plant J 70:492–500
Trostchansky A, Bonilla L, González-Perilli L, Rubbo H (2013) Nitro-fatty acids: formation, redox signaling, and therapeutic potential. Antioxid Redox Signal 19:1257–1265
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
Valderrama R, Corpas FJ, Carreras A, Fernández-Ocaña A, Chaki M, Luque F, Gómez-Rodríguez MV, Colmenero-Varea P, Del Río LA, Barroso JB (2007) Nitrosative stress in plants. FEBS Lett 581:453–461
Vanin AF, Malenkova IV, Serezhenkov VA (1997) Iron catalyzes both decomposition and synthesis of S-nitrosothiols: optical and electron paramagnetic resonance studies. Nitric Oxide 1:191–203
Vanzo E, Ghirardo A, Merl-Pham J, Lindermayr C, Heller W, Hauck SM, Durner J, Schnitzler JP (2014) S-nitroso-proteome in poplar leaves in response to acute ozone stress. PLoS One 9(9), e106886
Wang H, Xian M (2011) Chemical methods to detect S-nitrosation. Curr Opin Chem Biol 15:32–37
Wang P, Du Y, Hou YJ, Zhao Y, Hsu CC, Yuan F, Zhu X, Tao WA, Song CP, Zhu JK (2015) Nitric oxide negatively regulates abscisic acid signaling in guard cells by S-nitrosylation of OST1. Proc Natl Acad Sci U S A 112:613–618
Wendehenne D, Gao QM, Kachroo A, Kachroo P (2014) Free radical-mediated systemic immunity in plants. Curr Opin Plant Biol 20:127–134
Wimalasekera R, Tebartz F, Scherer GFE (2011a) Polyamines, polyamine oxidases and nitric oxide in development, abiotic and biotic stresses. Plant Sci 181:593–603
Wimalasekera R, Villar C, Begum T, Scherer GF (2011b) COPPER AMINE OXIDASE1 (CuAO1) of Arabidopsis thaliana contributes to abscisic acid- and polyamine-induced nitric oxide biosynthesis and abscisic acid signal transduction. Mol Plant 4:663–678
Wojtaszek P (2000) Nitric oxide in plants. To NO or not to NO. Phytochemistry 54:1–4
World Health Organization (2007) Health risks of heavy metals from long-range transboundary air pollution, p 130. Germany, ISBN: 978 92 890 7179 6
Wünsche 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 62:4605–4616
Xu S, Guerra D, Lee U, Vierling E (2013) S-nitrosoglutathione reductases are low-copy number, cysteine-rich proteins in plants that control multiple developmental and defense responses in Arabidopsis. Front Plant Sci 4:430
Yamasaki H, Sakihama Y, Takahashi S (1999) An alternative pathway for nitric oxide production in plants: new features of an old enzyme. Trends Plant Sci 4:128–129
Yang H, Mu J, Chen L, Feng J, Hu J, Li L, Zhou JM, Zuo J (2015) S-nitrosylation positively regulates ascorbate peroxidase activity during plant stress responses. Plant Physiol 167:1604–1615
Yu M, Yun BW, Spoel SH, Loake GJ (2012) A sleigh ride through the SNO: regulation of plant immune function by protein S-nitrosylation. Curr Opin Plant Biol 15:424–430
Yun BW, Feechan A, Yin M, Saidi NB, Le Bihan T, Yu M, Moore JW, Kang JG, Kwon E, Spoel SH, Pallas JA, Loake GJ (2011) S-nitrosylation of NADPH oxidase regulates cell death in plant immunity. Nature 478:264–268
Zafra A, Rodríguez-García MI, Alché JD (2010) Cellular localization of ROS and NO in olive reproductive tissues during flower development. BMC Plant Biol 10:36
Zhang YY, Wang LL, Liu YL, Zhang Q, Wei QP, Zhang WH (2006) Nitric oxide enhances salt tolerance in maize seedlings through increasing activities of proton-pump and Na+/H+ antiport in the tonoplast. Planta 224:545–555
Zhao J (2007) Interplay among nitric oxide and reactive oxygen species: a complex network determining cell survival or death. Plant Signal Behav 2:544–547
Zhao FJ, McGrath SP, Meharg AA (2010) Arsenic as a food chain contaminant: mechanisms of plant uptake and metabolism and mitigation strategies. Annu Rev Plant Biol 61:535–559
Zhou J, Jia F, Shao S, Zhang H, Li G, Xia X, Zhou Y, Yu J, Shi K (2015) Involvement of nitric oxide in the jasmonate-dependent basal defense against root-knot nematode in tomato plants. Front Plant Sci 6:193
Acknowledgements
Work in my laboratory is supported by ERDF co-financed grants from the Ministry of Science and Innovation (Recupera 2020-20134R056) and the Junta de Andalucía (group BIO192) in Spain.
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Corpas, F.J. (2016). Reactive Nitrogen Species (RNS) in Plants Under Physiological and Adverse Environmental Conditions: Current View. In: Cánovas, F., Lüttge, U., Matyssek, R. (eds) Progress in Botany Vol. 78. Progress in Botany, vol 78. Springer, Cham. https://doi.org/10.1007/124_2016_3
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