Chapter 22
The Role of Nitric Oxide in the Antioxidant Defense of Plants Exposed to UV-B Radiation
Raúl Cassia,
Melina Amenta,
María Belén Fernández,
Macarena Nocioni,
Valeria Dávila,
Raúl Cassia
Instituto de Investigaciones Biológicas, Facultad de Ciencias Exactas y Naturales, Universidad Nacional de Mar del Plata-Consejo Nacional de Investigaciones Científicas y Técnicas, Mar del Plata, Argentina
Search for more papers by this authorMelina Amenta
Laboratorio de Bioquímica Vegetal y Microbiana, Facultad de Cs. Agrarias, Universidad Nacional de Mar del Plata, Balcarce, Argentina
Search for more papers by this authorMaría Belén Fernández
Instituto de Investigaciones Biológicas, Facultad de Ciencias Exactas y Naturales, Universidad Nacional de Mar del Plata-Consejo Nacional de Investigaciones Científicas y Técnicas, Mar del Plata, Argentina
Search for more papers by this authorMacarena Nocioni
Instituto de Investigaciones Biológicas, Facultad de Ciencias Exactas y Naturales, Universidad Nacional de Mar del Plata-Consejo Nacional de Investigaciones Científicas y Técnicas, Mar del Plata, Argentina
Search for more papers by this authorValeria Dávila
Laboratorio de Zoonosis Parasitarias, Facultad de Ciencias Exactas y Naturales, Universidad Nacional de Mar del Plata, Mar del Plata, Argentina
Search for more papers by this authorRaúl Cassia,
Melina Amenta,
María Belén Fernández,
Macarena Nocioni,
Valeria Dávila,
Raúl Cassia
Instituto de Investigaciones Biológicas, Facultad de Ciencias Exactas y Naturales, Universidad Nacional de Mar del Plata-Consejo Nacional de Investigaciones Científicas y Técnicas, Mar del Plata, Argentina
Search for more papers by this authorMelina Amenta
Laboratorio de Bioquímica Vegetal y Microbiana, Facultad de Cs. Agrarias, Universidad Nacional de Mar del Plata, Balcarce, Argentina
Search for more papers by this authorMaría Belén Fernández
Instituto de Investigaciones Biológicas, Facultad de Ciencias Exactas y Naturales, Universidad Nacional de Mar del Plata-Consejo Nacional de Investigaciones Científicas y Técnicas, Mar del Plata, Argentina
Search for more papers by this authorMacarena Nocioni
Instituto de Investigaciones Biológicas, Facultad de Ciencias Exactas y Naturales, Universidad Nacional de Mar del Plata-Consejo Nacional de Investigaciones Científicas y Técnicas, Mar del Plata, Argentina
Search for more papers by this authorValeria Dávila
Laboratorio de Zoonosis Parasitarias, Facultad de Ciencias Exactas y Naturales, Universidad Nacional de Mar del Plata, Mar del Plata, Argentina
Search for more papers by this authorBook Editor(s):Mirza Hasanuzzaman,
Vasileios Fotopoulos,
Kamrun Nahar,
Masayuki Fujita,
Mirza 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
The evidence presented here highlights the role of the nitric oxide (NO) as anti-stress molecule, capable to handling with UV-B-induced changes in the redox state of cell. Our model proposes that the UV-B perception triggers an increase in abscisic acid (ABA) concentration, which increases H2O2 and induces NO. In parallel, UV-B activates the UV-B receptor UVR8. UVR8 is stabilized by endogenous NO and activates the HY5 transcription factor. HY5 may regulate the expression and activity of nitrate reductase, inducing NO increase. NO reduces ROS levels by its scavenger activity. Likewise, HY5 also up-regulates the expression of CHS and CHI. That results in an increase of flavonoid and anthocyanin content, which are capable of absorbing UV-B radiation and scavenge ROS. Moreover, NO may also regulates the activity of the antioxidant system (AS) by posttranslational modifications of antioxidants enzymes as catalases, peroxidases, oxidases, and reductases.
References
- Allen, D.J., Mckee, I.F., Farage, P.K., and Baker, N.R. (1997). Analysis of limitations to CO2 assimilation on exposure of leaves of two Brassica napus cultivars. Plant, Cell and Environment 20: 633–640.
- An, L., Liu, Y., Zhang, M. et al. (2005). Effects of nitric oxide on growth of maize seedling leaves in the presence or absence of ultraviolet-B radiation. Journal of Plant Physiology 162: 317–326.
- Bai, X., Yang, L., Tian, M. et al. (2011). Nitric oxide enhances desiccation tolerance of recalcitrant Antiaris toxicaria seeds via protein S-nitrosylation and carbonylation. PLoS One 6: e20714. https://doi.org/10.1371/journal.pone.0020714.
- Bais, A.F., McKenzie, R.L., Bernhard, G. et al. (2015). Ozone depletion and climate change: impacts on UV radiation. Photochemical and Photobiological Sciences 14: 19–52.
- Ballaré, C.L., Caldwell, M.M., Flint, S.D. et al. (2011). Effects of solar ultraviolet radiation on terrestrial ecosystems. Patterns, mechanisms, and interactions with climate change. Photochemical and Photobiological Sciences 10: 226–241.
- Begara-Morales, J.C., Sanchez-Calvo, B., Chaki, M. et al. (2014). Dual regulation of cytosolic ascorbate peroxidase (APX) by tyrosine nitration and S-nitrosylation. Journal of Experimental Botany 65: 527–538.
- Beligni, M.V. and Lamattina, L. (1999). Nitric oxide protects against cellular damage produced by methylviologen herbicides in potato plants. Nitric Oxide 3: 199–208.
- Beligni, M.V. and 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.
- Berli, F.J. and Bottini, R. (2013). UV-B and abscisic acid effects on grape berry maturation and quality. Journal of Berry Research 3: 1–14.
- Binkert, M., Crocco, C.D., Ekundayo, B. et al. (2015). Revisiting chromatin binding of the Arabidopsis UV-B photoreceptor UVR8. BMC Plant Biology 16: 42.
- Brown, G.C. (1995). Reversible binding and inhibition of catalase by nitric oxide. European Journal of Biochemistry 232: 188–191.
- Brown, B.A., Cloix, C., Jiang, G.H. et al. (2005). A UV-B-specific signaling component orchestrates plant UV protection. Proceedings of the National Academy of Sciences of the United States of America 102: 18225–18230.
- Brown, B.A. and Jenkins, G.I. (2008). UV-B signaling pathways with different fluence-rate response profiles are distinguished in mature Arabidopsis leaf tissue by requirement for UVR8, HY5, and HYH. Plant Physiology 146: 576–588.
- Camejo, D., Romero-Puertas, M., del, C. et al. (2013). Salinity-induced changes in S-nitrosylation of pea mitochondrial proteins. Journal of Proteomics 79: 87–99.
- Cassia, R., Nocioni, M., Correa- Aragunde, N., and Lamattina, L. (2018). Climate change and the impact of greenhouse gasses: CO2 and NO, friends and foes of plant oxidative stress. Frontiers in Plant Science 9: 273. https://doi.org/10.3389/fpls.2018.00273.
- Chen, Y.Y., Chu, H.M., Pan, K.T. et al. (2008). Cysteine S-nitrosylation protects protein-tyrosine phosphatase 1B against oxidation-induced permanent inactivation. The Journal of Biological Chemistry 283: 35265–35272.
- Chen, M., Zhang, W.H., Lv, Z.W. et al. (2013). Abscisic acid is involved in the response of Arabidopsis mutant sad2-1 to ultraviolet-B radiation by enhancing antioxidant enzymes. South African Journal of Botany 85: 79–86.
- Cheng, T., Chen, J., Ef, A.A. et al. (2015). Quantitative proteomics analysis reveals that S-nitrosoglutathione reductase (GSNOR) and nitric oxide signaling enhance poplar defense against chilling stress. Planta 242: 1361–1390.
- Choudhury, F.K., Rivero, R.M., Blumwald, E., and Mittler, R. (2017). Reactive oxygen species, abiotic stress and stress combination. The Plant Journal 90: 856–867.
- Christie, J.M., Arvai, A.S., Baxter, K.J. et al. (2012). Plant UVR8 photoreceptor senses UV-B by tryptophan-mediated disruption of cross-dimer salt bridges. Science 335: 1492–1496.
- Clark, D., Durner, J., Navarre, D.A., and Klessig, D.F. (2000). Nitric oxide inhibition of tobacco catalase and ascorbate peroxidase. Molecular Plant-Microbe Interactions 13: 1380–1384.
- Cordero, R.R., Damiani, A., Seckmeyer, G. et al. (2016). The solar spectrum in the Atacama Desert. Scientific Reports 6: 22457.
- Corpas, F.J., Alche, J.D., and Barroso, J.B. (2013). Current overview of S-nitrosoglutathione (GSNO) in higher plants. Frontiers in Plant Science 4: 126. https://doi.org/10.3389/fpls.2013.00126.
- Correa-Aragunde, N., Foresi, N., Delledonne, M., and Lamattina, L. (2013). Auxin induces redox regulation of ascorbate peroxidase 1 activity by S-nitrosylation/denitrosylation balance resulting in changes of root growth pattern in Arabidopsis . Journal of Experimental Botany 64: 3339–3349.
- de Pinto, M.C., Locato, V., Sgobba, A. et al. (2013). S-nitrosylation of ascorbate peroxidase is part of programmed cell death signaling in tobacco Bright Yellow-2 cells. Plant Physiology 163: 1766–1775.
- Delledonne, M. (2005). NO news is good news for plants. Current Opinion in Plant Biology 8: 390–396.
- Dotto, M. and Casati, P. (2017). Developmental reprogramming by UV-B radiation in plants. Plant Science 264: 96–101.
- Fancy, N.N., Bahlmann, A.K., and Loake, G.J. (2017). Nitric oxide function in plant abiotic stress. Plant, Cell and Environment 40: 462–472.
- 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.
- Favory, J.J., Stec, A., Gruber, H. et al. (2009). Interaction of COP1 and UVR8 regulates UV-B-induced photomorphogenesis and stress acclimation in Arabidopsis . EMBO Journal 28: 591–601.
- Fernandez, M.B., Tossi, V., Lamattina, L., and Cassia, R. (2016). A comprehensive phylogeny reveals functional conservation of the UV-B photoreceptor UVR8 from green algae to higher plants. Frontiers in Plant Science 7: 1698.
- Foyer, C.H. and Noctorm, G. (2011). Ascorbate and glutathione: the heart of the redox hub. Plant Physiology 155: 2–18.
- Frungillo, L., Skelly, M.J., Loake, G.J. et al. (2014). S-nitrosothiols regulate nitric oxide production and storage in plants through the nitrogen assimilation pathway. Nature Communications 5: 5401.
- Garcia-Mata, C. and Lamattina, L. (2001). Nitric oxide induces stomatal closure and enhances the adaptive plant responses against drought stress. Plant Physiology 126: 1196–1204.
- Garcia-Mata, C. and Lamattina, L. (2002). Nitric oxide and abscisic acid cross talk in guard cells. Plant Physiology 128: 790–792.
- Gonzalez Besteiro, M.A., Bartels, S., Albert, A., and Ulm, R. (2011). Arabidopsis MAP kinase phosphatase 1 and its target MAP kinases 3 and 6 antagonistically determine UV-B stress tolerance, independent of the UVR8 photoreceptor pathway. Plant Journal 68: 727–737.
- Han, C., Liu, Q., and Yang, Y. (2009). Short-term effects of experimental warming and enhanced ultraviolet-B radiation on photosynthesis and antioxidant defense of Picea asperata seedlings. Plant Growth Regulation 58: 153–162.
- He, J.M., Ma, X.G., Zhang, Y. et al. (2013). Role and interrelationship of Gα protein, hydrogen peroxide, and nitric oxide in ultraviolet B-induced stomatal closure in Arabidopsis leaves. Plant Physiology 161: 1570–1583.
- He, J., Yue, X., Wang, R., and Zhang, Y. (2011a). Ethylene mediates UV-B-induced stomatal closure via peroxidase-dependent hydrogen peroxide synthesis in Vicia faba L. Journal of Experimental Botany 62: 2657–2666.
- He, J., Yue, X., Wang, R., and Zhang, Y. (2011b). UV-B-induced stomatal closure via ethylene-dependent NO generation in Vicia faba L. Functional Plant Biology 38: 293–302.
- Heijde, M. and Ulm, R. (2012). UV-B photoreceptor-mediated signalling in plants. Trends in Plant Science 17: 230–237.
- Hideg, E. and Vass, I. (1996). UV-B induced free radical production in plant leaves and isolated thylakoid membranes. Plant Science 115: 251–260.
- Holzmeister, C., Gaupels, F., Geerlof, A. et al. (2015). Differential inhibition of Arabidopsis superoxide dismutases by peroxynitrite-mediated tyrosine nitration. Journal of Experimental Botany 66: 989–999.
- Hood, L.L. and Soukharev, B.E. (2012). The lower-stratospheric response to 11-Yr solar forcing: coupling to the troposphere–ocean response. Journal of the Atmospheric Sciences 69: 1841–1864.
- Hu, J., Huang, X., Chen, L. et al. (2015). Site-specific nitrosoproteomic identification of endogenously S-nitrosylated proteins in Arabidopsis . Plant Physiology 167: 1731–1746.
- Huang, X., Yang, P., Ouyang, X. et al. (2014). Photoactivated UVR8-COP1 module determines photomorphogenic UV-B signaling output in Arabidopsis . PLoS Genetics 10: e1004218. https://doi.org/10.1371/journal.pgen.1004218.
- Jenkins, G.I. (2009). Signal transduction in responses to UV-B radiation. Annual Review of Plant Biology 60: 407–431.
- Jonassen, E.M., Lea, U.S., and Lillo, C. (2008). HY5 and HYH are positive regulators of nitrate reductase in seedlings and rosette stage plants. Planta 227: 559–564.
- Jonassen, E.M., Sevin, D.C., and Lillo, C. (2009). The bZIP transcription factors HY5 and HYH are positive regulators of the main nitrate reductase gene in Arabidopsis leaves, NIA2, but negative regulators of the nitrate uptake gene NRT1.1. Journal of Plant Physiology 166: 2071–2076.
- Kaiserli, E. and Jenkins, G.I. (2007). UV-B promotes rapid nuclear translocation of the Arabidopsis UV-B specific signaling component UVR8 and activates its function in the nucleus. Plant Cell 19: 2662–2673.
- Kliebenstein, D.J., Lim, J.E., Landry, L.G., and Last, R.L. (2002). Arabidopsis UVR8 regulates ultraviolet-B signal transduction and tolerance and contains sequence similarity to human regulator of chromatin condensation 1. Plant Physiology 130: 234–243.
- Kohr, M.J., Aponte, A.M., Sun, J. et al. (2011). Characterization of potential S-nitrosylation sites in the myocardium. American Journal of Physiology. Heart and Circulatory Physiology 300: H1327–H1335.
- Kohr, M.J., Murphy, E., and Steenbergen, C. (2014). Glyceraldehyde-3-phosphate dehydrogenase acts as a mitochondrial trans-S-nitrosylase in the heart. PLoS One 9: e111448. https://doi.org/10.1371/journal.pone.0111448.
- Lamattina, L., Garcia-Mata, C., Graziano, M., and Pagnussat, G. (2003). Nitric oxide: the versatility of an extensive signal molecule. Annual Review of Plant Biology 54: 109–136.
-
Lamattina, L. and Polacco, J.C. (2007). Nitric Oxide in Plant Growth, Development and Stress Physiology. Heidelberg: Springer.
10.1007/11563280 Google Scholar
- Leitner, M., Vandelle, E., Gaupels, F. et al. (2009). NO signals in the haze: nitric oxide signalling in plant defence. Current Opinion in Plant Biology 12: 451–458.
- Li, F., Sonveaux, P., Rabbani, Z.N. et al. (2007). Regulation of HIF-1alpha stability through S-nitrosylation. Molecular Cell 26: 63–74.
- Lindermayr, C. and Durner, J. (2009). S-nitrosylation in plants: pattern and function. Journal of Proteomics 73: 1–9.
- Liu, L., Gregan, S., Winefield, C., and Jordan, B. (2015). From UVR8 to flavonol synthase: UV-B-induced gene expression in Sauvignon blanc grape berry. Plant, Cell and Environment 38: 905–919.
- Lu, S., Su, W., Li, H., and Guo, Z. (2009). Abscisic acid improves drought tolerance of triploid bermudagrass and involves H2O2- and NO-induced antioxidant enzyme activities. Plant Physiology and Biochemistry 47: 132–138.
- Mackerness, S.A.-H.S., John, C.F., Jordan, B., and Thomas, B. (2001). Early signaling components in ultraviolet-B responses: distinct roles for different reactive oxygen species and nitric oxide. FEBS Letters 489: 237–242.
- Mao, K., Wang, L., Li, Y.Y., and Wu, R. (2015). Molecular cloning and functional analysis of UV RESISTANCE LOCUS 8 (PeUVR8) from Populus euphratica . PLoS One 10: e0132390. https://doi.org/10.1371/journal.pone.0132390.
- Marino, D., Dunand, C., Puppo, A., and Pauly, N. (2012). A burst of plant NADPH oxidases. Trends in Plant Science 17: 9–15.
- Moreno, J., Peñarrubia, L., and García-Ferris, C. (1995). The mechanism of redox regulation of ribulose-1,5-bisphosphate carboxylase/oxygenase turnover. Plant Physiology and Biochemistry 33: 121–127.
- Muller-Xing, R., Xing, Q., and Goodrich, J. (2014). Footprints of the sun: memory of UV and light stress in plants. Frontiers in Plant Science 5: 474. https://doi.org/10.3389/fpls.2014.00474.
- Nawkar, G.M., Maibam, P., Park, J.H. et al. (2013). UV-induced cell death in plants. International Journal of Molecular Sciences 14: 1608–1628.
- O'Hara, A. and Jenkins, G.I. (2012). In vivo function of tryptophans in the Arabidopsis UV-B photoreceptor UVR8. Plant Cell 24: 3755–3766.
- Ortega-Galisteo, A.P., Rodriguez-Serrano, M., Pazmino, D.M. et al. (2012). S-Nitrosylated proteins in pea (Pisum sativum L.) leaf peroxisomes: changes under abiotic stress. Journal of Experimental Botany 63: 2089–2103.
- Penarrubia, L. and Moreno, J. (1990). Increased susceptibility of ribulose-1,5-bisphosphate carboxylase/oxygenase to proteolytic degradation caused by oxidative treatments. Archives of Biochemistry and Biophysics 281: 319–323.
- Petrov, V., Hille, J., Mueller-Roeber, B., and Gechev, T.S. (2015). ROS-mediated abiotic stress-induced programmed cell death in plants. Frontiers in Plant Science 6: 69. https://doi.org/10.3389/fpls.2015.00069.
- Pietta, P.G. (2000). Flavonoids as antioxidants. Journal of Natural Products 63: 1035–1042.
- Popov, V.N., Simonian, R.A., Skulachev, V.P., and Starkov, A.A. (1997). Inhibition of the alternative oxidase stimulates H2O2 production in plant mitochondria. FEBS Letters 415: 87–90.
- Qian, C., Mao, W., Liu, Y. et al. (2016). Dual-source nuclear monomers of UV-B light receptor direct photomorphogenesis in Arabidopsis . Molecular Plant 9: 1671–1674.
- Qu, Y., Feng, H., Wang, Y. et al. (2006). Nitric oxide functions as a signal in ultraviolet-B induced inhibition of pea stems elongation. Plant Science 170: 994–1000.
- Rakitin, V.Y., Karyagin, V.V., Rakitina, T.Y. et al. (2008). UV-B stress-induced ABA production in Arabidopsis thaliana mutants defective in ethylene signal transduction pathway. Russian Journal of Plant Physiology 55: 854–856.
- Rao, M.V., Paliyath, G., and Ormrod, D.P. (1996). Ultraviolet-B- and ozone-induced biochemical changes in antioxidant enzymes of Arabidopsis thaliana . Plant Physiology 110: 125–136.
- Rizzini, L., Favory, J.J., Cloix, C. et al. (2011). Perception of UV-B by the Arabidopsis UVR8 protein. Science 332: 103–106.
- Romero-Puertas, M.C., Laxa, M., Mattè, A. et al. (2007). S-nitrosylation of peroxiredoxin II E promotes peroxynitrite-mediated tyrosine nitration. Plant Cell 19: 4120–4130.
- Santa-Cruz, D.M., Pacienza, N.A., Zilli, C.G. et al. (2014). Nitric oxide induces specific isoforms of antioxidant enzymes in soybean leaves subjected to enhanced ultraviolet-B radiation. Journal of Photochemistry and Photobiology B: Biology 141: 202–209.
- Sharma, P., HJha, A.B., Dubey, R.S., and Pessarakli, M. (2012). Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. Journal of Botany 2012: 1–26.
- Shi, S., Wang, G., Wang, Y., and Zhang, L. (2005). Protective effect of nitric oxide against oxidative stress under ultraviolet-B radiation. Nitric Oxide 13: 1–9.
- Singh, R., Hogg, N., Goss, S. et al. (1999). Mechanism of superoxide dismutase/H2O2-mediated nitric oxide release from S-nitrosoglutathione–role of glutamate. Archives of Biochemistry and Biophysics 372: 8–15.
- Song, C.J., Steinebrunner, I., Wang, X. et al. (2006). Extracellular ATP induces the accumulation of superoxide via NADPH oxidases in Arabidopsis . Plant Physiology 140: 1222–1232.
- Stapleton, A.E. and Walbot, V. (1994). Flavonoids can protect maize DNA from the induction of ultraviolet radiation damage. Plant Physiology 105: 881–889.
- Strid, A., Chow, W.S., and Anderson, J.M. (1994). UV-B damage and protection at the molecular level in plants. Photosynthesis Research 39: 475–489.
- Tong, H., Leasure, C.D., Hou, X. et al. (2008). Role of root UV-B sensing in Arabidopsis early seedling development. Proceedings of the National Academy of Sciences of the United States of America 105: 21039–21044.
- Uchida, A., Jagendorf, A.T., Hibino, T. et al. (2002). Effect of hydrogen peroxide and nitric oxide on both salt and heat stress tolerance in rice. Plant Science 163: 515–523.
- Vishwakarma, K., Upadhyay, N., Kumar, N. et al. (2017). Abscisic acid signaling and abiotic stress tolerance in plants: a review on current knowledge and future prospects. Frontiers in Plant Science 8: 161. https://doi.org/10.3389/fpls.2017.00161.
- Willing, E.M., Piofczyk, T., Albert, A. et al. (2016). UVR2 ensures transgenerational genome stability under simulated natural UV-B in Arabidopsis thaliana . Nature Communications 7: 13522. https://doi.org/10.1038/ncomms13522.
- Wilson, I.D., Neill, S.J., and Hancock, J.T. (2008). Nitric oxide synthesis and signalling in plants. Plant, Cell and Environment 31: 622–631.
- Wu, D., Hu, Q., Yan, Z. et al. (2012). Structural basis of ultraviolet-B perception by UVR8. Nature 484: 214–219.
- Wu, Q., Su, N., Zhang, X. et al. (2016). Hydrogen peroxide, nitric oxide and UV RESISTANCE LOCUS8 interact to mediate UV-B-induced anthocyanin biosynthesis in radish sprouts. Scientific Reports 6: 29164.
- Yang, Y., Liang, T., Zhang, L. et al. (2018). UVR8 interacts with WRKY36 to regulate HY5 transcription and hypocotyl elongation in Arabidopsis . Nature Plants 4: 98–107.
- Yang, X., Montano, S., and Ren, Z. (2016). How does photoreceptor UVR8 perceive a UV- B signal? Photochemistry and Photobiology 91: 993–1003.
- Yang, H., Mu, J., Chen, L. et al. (2015). S-nitrosylation positively regulates ascorbate peroxidase activity during plant stress responses. Plant Physiology 167: 1604–1615.
- Yokawa, K., Kagenishi, T., and Baluska, F. (2016). UV-B induced generation of reactive oxygen species promotes formation of BFA-induced compartments in cells of Arabidopsis root apices. Frontiers in Plant Science 6: 1162. https://doi.org/10.3389/fpls.2015.01162.
- Yun, B.W., Feechan, A., Yin, M. et al. (2011). S-nitrosylation of NADPH oxidase regulates cell death in plant immunity. Nature 478: 264–268.
- Zeier, J., Delledonne, M., Mishina, T. et al. (2004). Genetic elucidation of nitric oxide signaling in incompatible plant-pathogen interactions. Plant Physiology 136: 2875–2886.
- Zhang, M., An, L., Feng, H. et al. (2003). The cascade mechanisms of nitric oxide as a second messenger of ultraviolet B in inhibiting mesocotyl elongations. Photochemistry and Photobiology 77: 219–225.
- Zhang, S.G., Han, S.Y., Yang, W.H. et al. (2009). Changes in H2O2 content and antioxidant enzyme gene expression during the somatic embryogenesis of Larix leptolepis . Plant Cell, Tissue and Organ Culture 100: 21. https://doi.org/10.1007/s11240-009-9612-0.
- Zhao, C., Mao, K., You, C.X. et al. (2016). Molecular cloning and functional analysis of a UV-B photoreceptor gene, MdUVR8 (UV Resistance Locus 8), from apple. Plant Science 247: 115–126.
- Zhao, L., Zhang, F., Guo, J. et al. (2004). Nitric oxide functions as a signal in salt resistance in the calluses from two ecotypes of reed. Plant Physiology 134: 849–857.
- Zhu, Y., Ge, X.M., Wu, M.M. et al. (2014). The role and interactions of cytosolic alkalization and hydrogen peroxide in ultraviolet B-induced stomatal closure in Arabidopsis . Plant Science 215: 84–90.
