Nitric oxide imbalance provokes a nitrosative response in plants under abiotic stress

Plant Science

Volumn 181, Issue 5, 2011, Pages 604-611

  Corpas, Francisco J ^a   Leterrier, Marina ^a   Valderrama, Raquel ^b   Airaki, Morad ^a   Chaki, Mounira ^a   Palma, José M ^a   Barroso, Juan B ^b  

^a CSIC   (Spain)

^b UNIVERSITY OF JAÉN   (Spain)

Author keywords

Abiotic stress; Nitric oxide; Nitrosative stress; Nitrotyrosine; Reactive nitrogen species; Salinity

Indexed keywords

NITRIC OXIDE; OZONE; REACTIVE NITROGEN SPECIES;

CHEMISTRY; DRUG EFFECT; ENVIRONMENT; METABOLISM; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PLANT; REVIEW; SIGNAL TRANSDUCTION;

ENVIRONMENT; NITRIC OXIDE; OZONE; PLANTS; REACTIVE NITROGEN SPECIES; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL;

EID: 80052421534     PISSN: 01689452     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.plantsci.2011.04.005     Document Type: Review

References (108)

1. Palmer R.M.J., Ferrige A.G., Moncada S. Nitric-oxide release accounts for the biological-activity of endothelium-derived relaxing factor. Nature 1987, 327:524-526.
2. Ignarro L.J., Buga G.M., Wood K.S., Byrns R.E., Chaudhuri G.G. Endothelium-derived relaxing factor produced and released from artery and vein is nitric oxide. Proceedings of the National Academy of Sciences United States of America 1987, 84:9265-9269.
3. Alderton W.K., Cooper C.E., Knowles R.G. Nitric oxide synthases: structure, function and inhibition. Biochemical Journal 2001, 357:593-615.
4. Moncada S Nitric oxide: discovery and impact on clinical medicine. Journal of the Royal Society of Medicine 1999, 92:164-169.
5. Lamattina L., Garcia-Mata C., Graziano M., Pagnussat G. Nitric oxide: the versatility of an extensive signal molecule. Annual Review of Plant Biology 2003, 54:109-136.
6. Shapiro A.D. Nitric oxide signaling in plants. Plant Hormones 2005, 72:339-398.
7. Corpas F.J., Carreras A., Valderrama R., Chaki M., Palma J.M., del Río L.A., Barroso J.B. Reactive nitrogen species and nitrosative stress in plants. Plant Stress 2007, 1:37-41.
8. 2+ signaling. Molecular Plant 2008, 1:218-228.
9. Neill S., Barros R., Bright J., Desikan R., Hancock J., Harrison J., Morris P., Ribeiro D., Wilson I. Nitric oxide, stomatal closure, and abiotic stress. Journal of Experimental Botany 2008, 59:165-176.
10. Zafra A, Rodríguez-García M.I., Alché J.D. Cellular localization of ROS and NO in olive reproductive tissues during flower development. BMC Plant Biology 2010, 10.
11. Neill S.J., Desikan R., Hancock J.T. Nitric oxide signalling in plants. New Phytologist 2003, 159:11-35.
12. Corpas F.J., Palma J.M., del Rio L.A., Barroso J.B. Evidence supporting the existence of l-arginine-dependent nitric oxide synthase activity in plants. New Phytologist 2009, 184:9-14.
13. Corpas F.J., Barroso J.B., del Rio L.A. Enzymatic sources of nitric oxide in plant cells - beyond one protein-one function. New Phytologist 2004, 162:246-248.
14. Wilson I.D., Neill S.J., Hancock J.T. Nitric oxide synthesis and signalling in plants. Plant Cell and Environment 2008, 31:622-631.
15. Chaki M., Valderrama R., Fernández-Ocaña A., Carreras A., Gómez-Rodríguez M.V., Pedrajas J.R., Begara-Morales J.C., Sánchez-Calvo B., Luque F., Leterrier M., Corpas F.J., Barroso J.B. Mechanical wounding induces a nitrosative stress by down-regulation of GSNO reductase and an increase in S-nitrosothiols in sunflower (Helianthus annuus) seedlings. Journal of Experimental Botany 2011, 62:1803-1813.
16. Gas E., Flores-Pérez U., Sauret-Güeto S., Rodríguez-Concepción M. Hunting for plant nitric oxide synthase provides new evidence of a central role for plastids in nitric oxide metabolism. Plant Cell 2009, 21:18-23.
17. K.J. Gupta, A.R. Fernie, W.M. Kaiser, J.T. van Dongen, On the origins of nitric oxide, Trends in Plant Science, doi:10.1016/j.tplants.2010.11.007.
18. Foresi N., Correa-Aragunde N., Parisi G., Caló G., Salerno G., Lamattina L. 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 2010, 22:3816-3830.
19. Yamasaki H., Sakihama Y., Takahashi S. An alternative pathway for nitric oxide production in plants: new features of an old enzyme. Trends in Plant Science 1999, 4:128-129.
20. Modolo L.V., Augusto O., Almeida I.M.G., Magalhaes J.R., Salgado I. Nitrite as the major source of nitric oxide production by Arabidopsis thaliana in response to Pseudomonas syringae. FEBS Letters 2005, 579:3814-3820.
21. Wojtaszek P. Nitric oxide in plants - To NO or not to NO. Phytochemistry 2000, 54:1-4.
22. del Río L.A., Corpas F.J., Barroso J.B. Nitric oxide and nitric oxide synthase activity in plants. Phytochemistry 2004, 65:783-792.
23. Tun N.N., Santa-Catarina C., Begum T., Silveira V., Handro W., Floh E.I.S., Scherer G.F.E. Polyamines induce rapid biosynthesis of nitric oxide (NO) in Arabidopsis thaliana seedlings. Plant and Cell Physiology 2006, 47:346-354.
24. Groppa M.D., Benavides M.P. Polyamines and abiotic stress: recent advances. Amino Acids 2008, 34:35-45.
25. Durzan D.J., Pedroso M.C. Nitric oxide and reactive nitrogen oxide species in plants. Biotechnology and Genetic Engineering Reviews 2002, 19:293-337.
26. Halliwell B., Gutteridge Free Radicals in Biology and Medecine 2007, Oxford University Press, Oxford. 4th ed.
27. Singh R.J., Hogg N., Joseph J., Kalyanaraman B. Mechanism of nitric oxide release from S-nitrosothiols. Journal of Biological Chemistry 1996, 271:18596-18603.
28. Liu Z.G., Rudd M.A., Freedman J.E., Loscalzo J. S-transnitrosation reactions are involved in the metabolic fate and biological actions of nitric oxide. Journal of Pharmacology and Experimental Therapeutics 1998, 284:526-534.
29. Corpas F.J., del Río L.A., Barroso J.B. Need of biomarkers of nitrosative stress in plants. Trends in Plant Science 2007, 12:436-438.
30. Corpas F.J., del Río L.A., Barroso J.B. Post-translational modifications mediated by reactive nitrogen species: Nitrosative stress responses or components of signal transduction pathways?. Plant Signaling and Behavior 2008, 3:301-303.
31. Valderrama R., Corpas F.J., Carreras A., Fernández-Ocaña A., Chaki M., Luque F., Gómez-Rodríguez M.V., Colmenero-Varea P., del Río L.A., Barroso J.B. Nitrosative stress in plants. FEBS Letters 2007, 581:453-461.
32. Ng E.S.M., Kubes P. The physiology of S-nitrosothiols: carrier molecules for nitric oxide. Canadian Journal of Physiology and Pharmacology 2003, 81:759-764.
33. Durner J., Klessig D.F. Nitric oxide as a signal in plants. Current Opinion in Plant Biology 1999, 2:369-374.
34. Diaz M., Achkor H., Titarenko E., Martinez M.C. The gene encoding glutathione-dependent formaldehyde dehydrogenase/GSNO reductase is responsive to wounding, jasmonic acid and salicylic acid. FEBS Letters 2003, 543:136-139.
35. Wang J, Fillebeen C., Chen G.H., Andriopoulos B., Pantopoulos K. Sodium nitroprusside promotes IRP2 degradation via an increase in intracellular iron and in the absence of S-nitrosylation at C178. Molecular and Cellular Biology 2006, 26:1948-1954.
36. Liu L.M., Hausladen A., Zeng M., Que L., Heitman J., Stamler J.S. A metabolic enzyme for S-nitrosothiol conserved from bacteria to humans. Nature 2001, 410:490-494.
37. Leterrier M., Chaki M., Airaki M., Valderrama R., Palma J.M., Barroso J.B., Corpas F.J. Function of S-nitrosoglutathione reductase (GSNOR) in plant development and under biotic/abiotic stress. Plant Signaling and Behavior 2011, 6. 10.4161/psb.6.6.15161.
38. Sakamoto A., Ueda M., Morikawa H. Arabidopsis glutathione-dependent formaldehyde dehydrogenase is an S-nitrosoglutathione reductase. FEBS Letters 2002, 515:20-24.
39. Achkor H., Diaz M., Fernández M.R., Biosca J.A., Pares X., Martinez M.C. Enhanced formaldehyde detoxification by overexpression of glutathione-dependent formaldehyde dehydrogenase from Arabidopsis. Plant Physiology 2003, 132:2248-2255.
40. Barroso J.B., Corpas F.J., Carreras A., Rodríguez-Serrano M., Esteban F.J., Fernández-Ocaña A., Chaki M., Romero-Puertas M.C., Valderrama R., Sandalio L.M., del Río L.A. Localization of S-nitrosoglutathione and expression of S-nitrosoglutathione reductase in pea plants under cadmium stress. Journal of Experimental Botany 2006, 57:1785-1793.
41. Corpas F.J., Chaki M., Fernández-Ocaña A., Valderrama R., Palma J.M., Carreras A., Begara-Morales J.C., Airaki M., del Río L.A., Barroso J.B. Metabolism of reactive nitrogen species in pea plants under abiotic stress conditions. Plant and Cell Physiology 2008, 49:1711-1722.
42. Chaki M., Valderrama R., Fernández-Ocaña A.M., Carreras A., López-Jaramillo J., Luque F., Palma J.M., Pedrajas J.R., Begara-Morales J.C., Sánchez-Calvo B., Gómez-Rodríguez M.V., Corpas F.J., Barroso J.B. Protein targets of tyrosine nitration in sunflower (Helianthus annuus L.) hypocotyls. Journal of Experimental Botany 2009, 60:4221-4234.
43. Gorren A.C.F., Schrammel A., Schmidt K., Mayer B. Decomposition of S-nitrosoglutathione in the presence of copper ions and glutathione. Archives of Biochemistry and Biophysics 1996, 330:219-228.
44. Smith J.N., Dasgupta T.P. Kinetics and mechanism of the decomposition of S-nitrosoglutathione by L-ascorbic acid and copper ions in aqueous solution to produce nitric oxide. Nitric Oxide-Biology and Chemistry 2000, 4:57-66.
45. KashibaIwatsuki M., Yamaguchi M., Inoue M. Role of ascorbic acid in the metabolism of S-nitroso-glutathione. FEBS Letters 1996, 389:149-152.
46. Martínez-Ruíz A., Lamas S. Two decades of new concepts in nitric oxide signaling: from the discovery of a gas messenger to the mediation of nonenzymatic posttranslational modifications. IUBMB Life 2009, 61:91-98.
47. Foster M.W., McMahon T.J., Stamler J.S. S-nitrosylation in health and disease. Trends in Molecular Medicine 2003, 9:160-168.
48. Wang Y., Yun B.W., Kwon E., Hong J.K., Yoon J., Loake G.J. S-nitrosylation: an emerging redox-based post-translational modification in plants. Journal Experimental Botany 2006, 57:1777-1784.
49. Radi R. Nitric oxide, oxidants, and protein tyrosine nitration. Proceedings of the National Academy of Sciences of the United States of America 2004, 101:4003-4008.
50. Boyer J.S Plant productivity and environment. Science 1982, 218:443-448.
51. Hernández J.A., Corpas F.J., Gómez M., del Río L.A., Sevilla F. Salt-induced oxidative stress mediated by activated oxygen species in pea leaf mitochondria. Physiologia Plantarum 1993, 89:103-110.
52. Hernández J.A., Olmos E., Corpas F.J., Sevilla F., del Ríio L.A. Salt-induced oxidative stress in chloroplasts of pea-plants. Plant Science 1995, 105:151-167.
53. Valderrama R., Corpas F.J., Carreras A., Gómez-Rodríguez M.V., Chaki M., Pedrajas J.R., Fernández-Ocaña A., del Río L.A., Barroso J.B. The dehydrogenase-mediated recycling of NADPH is a key antioxidant system against salt-induced oxidative stress in olive plants. Plant Cell and Environment 2006, 29:1449-1459.
54. Munns R., Tester M. Mechanisms of salinity tolerance. Annual Review of Plant Biology 2008, 59:651-681.
55. Zhao L.Q., Zhang F., Guo J.K., Yang Y.L., Li B.B., Zhang L.X. Nitric oxide functions as a signal in salt resistance in the calluses from two ecotypes of reed. Plant Physiology 2004, 134:849-857.
56. + antiport in the tonoplast. Planta 2006, 224:545-555.
57. David A., Yadav S., Bhatla S.C. Sodium chloride stress induces nitric oxide accumulation in root tips and oil body surface accompanying slower oleosin degradation in sunflower seedlings. Physiologia Plantarum 2010, 140:342-354.
58. Kopyra M., Gwozdz E.A. Nitric oxide stimulates seed germination and counteracts the inhibitory effect of heavy metals and salinity on root growth of Lupinus luteus. Plant Physiology and Biochemistry 2003, 41:1011-1017.
59. Li W.Q., Liu X.J., Khan M.A., Yamaguchi S. The effect of plant growth regulators, nitric oxide, nitrate, nitrite and light on the germination of dimorphic seeds of Suaeda salsa under saline conditions. Journal of Plant Research 2005, 118:207-214.
60. Xie Y.J., Ling T.F., Han Y., Liu K.L., Zheng Q.S., Huang L.Q., Yuan X.X., He Z.Y., Hu B., Fang L., Shen Z., Yang Q., Shen W.B. Carbon monoxide enhances salt tolerance by nitric oxide-mediated maintenance of ion homeostasis and up-regulation of antioxidant defence in wheat seedling roots. Plant Cell and Environment 2008, 31:1864-1881.
61. Uchida A., Jagendorf A.T., Hibino T., Takabe T. Effects of hydrogen peroxide and nitric oxide on both salt and heat stress tolerance in rice. Plant Science 2002, 163:515-523.
62. Tanou G., Molassiotis A., Diamantidis G. Hydrogen peroxide- and nitric oxide-induced systemic antioxidant prime-like activity under NaCl-stress and stress-free conditions in citrus plants. Journal of Plant Physiology 2009, 166:1904-1913.
63. Tanou G., Job C., Rajjou L., Arc E., Belghazi M., Diamantidis G., Molassiotis A., Job D. Proteomics reveals the overlapping roles of hydrogen peroxide and nitric oxide in the acclimation of citrus plants to salinity. Plant Journal 2009, 60:795-804.
64. Wawer I., Bucholc M., Astier J., Anielska-Mazur A., Dahan J., Kulik A., Wyslouch-Cieszynska A., Zareba-Koziol M., Krzywinska E., Dadlez M., Dobrowolska G., Wendehenne D. Regulation of Nicotiana tabacum osmotic stress-activated protein kinase and its cellular partner GAPDH by nitric oxide in response to salinity. Biochemical Journal 2010, 429:73-83.
65. Corpas F.J., Hayashi M., Mano S., Nishimura M., Barroso J.B. Peroxisomes are required for in vivo nitric oxide accumulation in the cytosol following salinity stress of Arabidopsis plants. Plant Physiology 2009, 151:2083-2094.
66. García-Mata C., Lamattina L. Nitric oxide induces stomatal closure and enhances the adaptive plant responses against drought stress. Plant Physiology 2001, 126:1196-1204.
67. Sang J.R., Jiang M.Y., Lin F., Xu S.C., Zhang A., Tan M.P. Nitric oxide reduces hydrogen peroxide accumulation involved in water stress-induced subcellular anti-oxidant defense in maize plants. Journal of Integrative Plant Biology 2008, 50:231-243.
68. Hao G.P., Xing Y., Zhang J.H. Role of nitric oxide dependence on nitric oxide synthase-like activity in the water stress signaling of maize seedling. Journal of Integrative Plant Biology 2008, 50:435-442.
69. Arasimowicz-Jelonek M., Floryszak-Wieczorek J., Kubis J. Involvement of nitric oxide in water stress-induced responses of cucumber roots. Plant Science 2009, 177:682-690.
70. Larkindale J., Vierling E. Core genome responses involved in acclimation to high temperature. Plant Physiology 2008, 146:748-761.
71. Kotak S., Larkindale J., Lee U., von Koskull-Doring P., Vierling E., Scharf K.D. Complexity of the heat stress response in plants. Current Opinion in Plant Biology 2007, 10:310-316.
72. Locato V., Gadaleta C., De Gara L., De Pinto M.C. Production of reactive species and modulation of antioxidant network in response to heat shock: a critical balance for cell fate. Plant Cell and Environment 2008, 31:1606-1619.
73. Suzuki N., Mittler R. Reactive oxygen species and temperature stresses: a delicate balance between signaling and destruction. Physiologia Plantarum 2006, 126:45-51.
74. 2 is required for effective expression of heat shock genes in Arabidopsis. Plant Molecular Biology 2006, 61:733-746.
75. Leshem Y.Y., Wills R.B.H., Ku V.V.V. Evidence for the function of the free radical gas - nitric oxide (NO center dot) - as an endogenous maturation and senescence regulating factor in higher plants. Plant Physiology and Biochemistry 1998, 36:825-833.
76. Gould K.S., Lamotte O., Klinguer A., Pugin A., Wendehenne D. Nitric oxide production in tobacco leaf cells: a generalized stress response?. Plant Cell and Environment 2003, 26:1851-1862.
77. Lee U., Wie C., Fernández B.O., Feelisch M., Vierling E. Modulation of nitrosative stress by S-nitrosoglutathione reductase is critical for thermotolerance and plant growth in Arabidopsis. Plant Cell 2008, 20:786-802.
78. Song L.L., Ding W., Shen J., Zhang Z.G., Bi Y.R., Zhang L.X. Nitric oxide mediates abscisic acid induced thermotolerance in the calluses from two ecotypes of reed under heat stress. Plant Science 2008, 175:826-832.
79. Sharma P., Sharma N., Deswal R. The molecular biology of the low-temperature response in plants. Bioessays 2005, 27:1048-1059.
80. M. Airaki, M. Leterrier, R.M. Mateos, R. Valderrama, M. Chaki, J.B. Barroso, L.A. del Río, J.M. Palma, F.J. Corpas, Metabolism of reactive oxygen species and reactive nitrogen species in pepper (Capsisum annuum L.) plants under low temperature stress, Plant Cell and Environment, 34 (2011) doi:10.1111/j.1365-3040.2011.02310.x.
81. Cantrel C., Vazquez T., Puyaubert J., Rezé N., Lesch M., Kaiser W.M., Dutilleul C., Guillas I., Zachowski A., Baudouin E. Nitric oxide participates in cold-responsive phosphosphingolipid formation and gene expression in Arabidopsis thaliana. New Phytologist 2011, 189:415-427.
82. Zhao M.G., Chen L., Zhang L.L., Zhang W.H. Nitric reductase-dependent nitric oxide production is involved in cold acclimation and freezing tolerance in Arabidopsis. Plant Physiology 2009, 151:755-767.
83. Abat J.K., Deswal R. 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 2009, 9:4368-4380.
84. Reymond P., Weber H., Damond M., Farmer E.E. Differential gene expression in response to mechanical wounding and insect feeding in Arabidopsis. Plant Cell 2000, 12:707-719.
85. Schilmiller A.L., Howe G.A. Systemic signaling in the wound response. Current Opinion in Plant Biology 2005, 8:369-377.
86. Orozco-Cardenas M.L., Ryan C.A. Nitric oxide negatively modulates wound signaling in tomato plants. Plant Physiology 2002, 130:487-493.
87. Huang X., Stettmaier K., Michel C., Hutzler P., Mueller M.J., Durner J. Nitric oxide is induced by wounding and influences jasmonic acid signaling in Arabidopsis thaliana. Planta 2004, 218:938-946.
88. Mackerness S.A.H., John C.F., Jordan B., Thomas B. Early signaling components in ultraviolet-B responses: distinct roles for different reactive oxygen species and nitric oxide. FEBS Letters 2001, 489:237-242.
89. An L.Z., Liu Y.H., Zhang M.X., Chen T., Wang X.L. Effects of nitric oxide on growth of maize seedling leaves in the presence or absence of ultraviolet-B radiation. Journal of Plant Physiology 2005, 162:317-326.
90. Tossi V., Cassia R., Lamattina L. Apocynin-induced nitric oxide production confers antioxidant protection in maize leaves. Journal of Plant Physiology 2009, 166:1336-1341.
91. Tossi V., Lamattina L., Cassia R. An increase in the concentration of abscisic acid is critical for nitric oxide-mediated plant adaptive responses to UV-B irradiation. New Phytologist 2009, 181:871-879.
92. Shi S.Y., Wang G., Wang Y.D., Zhang L.G., Zhang L.X. Protective effect of nitric oxide against oxidative stress under ultraviolet-B radiation. Nitric Oxide-Biology and Chemistry 2005, 13:1-9.
93. He J.M., Xu H., She X.P., Song X.G., Zhao W.M. The role and the interrelationship of hydrogen peroxide and nitric oxide in the UV-B-induced stomatal closure in broad bean. Functional Plant Biology 2005, 32:237-247.
94. 2 synthesis. Plant Journal 2006, 45:113-122.
95. Zhang L., Zhao L. Production of nitric oxide under ultraviolet-b irradiation is mediated by hydrogen peroxide through activation of nitric oxide synthase. Journal of Plant Biology 2008, 51:395-400.
96. Santa-Cruz D.M., Pacienza N.A., Polizio A.H., Balestrasse K.B., Tomaro M.L., Yannarelli G.G. Nitric oxide synthase-like dependent NO production enhances heme oxygenase up-regulation in ultraviolet-B-irradiated soybean plants. Phytochemistry 2010, 71:1700-1707.
97. Qu Y., Feng H.Y., Wang Y.B., Zhang M.X., Cheng J.Q., Wang X.L., An L.Z. Nitric oxide functions as a signal in ultraviolet-B induced inhibition of pea stems elongation. Plant Science 2006, 170:994-1000.
98. He J.M., Bai X.L., Wang R.B., Cao B., She X.P. The involvement of nitric oxide in ultraviolet-B-inhibited pollen germination and tube growth of Paulownia tomentosa in vitro. Physiologia Plantarum 2007, 131:273-282.
99. Prado A.M., Colaco R., Moreno N., Silva A.C., Feijo J.A. Targeting of pollen tubes to ovules is dependent on nitric oxide (NO) signaling. Molecular Plant 2008, 1:703-714.
100. Prado A.M., Porterfield D.M., Feijo J.A. Nitric oxide is involved in growth regulation and re-orientation of pollen tubes. Development 2004, 131:2707-2714.
101. Barroso J.B., Corpas F.J., Carreras A., Sandalio L.M., Valderrama R., Palma J.M., Lupiáñez J.A., del Río L.A. Localization of nitric-oxide synthase in plant peroxisomes. Journal of Biological Chemistry 1999, 274:36729-36733.
102. Corpas F.J., Barroso J.B., Carreras A., Quiros M., León A.M., Romero-Puertas M.C., Esteban F.J., Valderrama R., Palma J.M., Sandalio L.M., Gómez M., del Río L.A. Cellular and subcellular localization of endogenous nitric oxide in young and senescent pea plants. Plant Physiology 2004, 136:2722-2733.
103. Rao M.V., Davis K.R. The physiology of ozone induced cell death. Planta 2001, 213:682-690.
104. Ahlfors R., Brosche M., Kollist H., Kangasjarvi J. Nitric oxide modulates ozone-induced cell death, hormone biosynthesis and gene expression in Arabidopsis thaliana. Plant Journal 2009, 58:1-12.
105. Mahalingam R, Jambunathan N., Gunjan S.K., Faustin E., Weng H., Ayoubi P. Analysis of oxidative signalling induced by ozone in Arabidopsis thaliana. Plant Cell and Environment 2006, 29:1357-1371.
106. Ederli L., Morettini R., Borgogni A., Wasternack C., Miersch O., Reale L., Ferranti F., Tosti N., Pasqualini S. Interaction between nitric oxide and ethylene in the induction of alternative oxidase in ozone-treated tobacco plants. Plant Physiology 2006, 142:595-608.
107. Velikova V., Pinelli P., Pasqualini S., Reale L., Ferranti F., Loreto F. Isoprene decreases the concentration of nitric oxide in leaves exposed to elevated ozone. New Phytologist 2005, 166:419-426.
108. Velikova V., Fares S., Loreto F. Isoprene and nitric oxide reduce damages in leaves exposed to oxidative stress. Plant Cell and Environment 2008, 31:1882-1894.