TY  - JOUR
T1  - The Role of the Relationship between Hydrogen Peroxide and Nitric Oxide in Plant Tolerance to Abiotic Stresses
TT  - Hidrojen Peroksit ve Nitrik Oksit İlişkisinin Bitkilerde Abiyotik Stres Toleransındaki Rolü
AU  - Öcal Özdamar, Fahriye
AU  - Baysal Furtana, Gökçen
AU  - Ellialtıoğlu, Şeküre
AU  - Tıpırdamaz, Rukiye
PY  - 2016
DA  - August
DO  - 10.21566/tbmaed.45530
JF  - Tarla Bitkileri Merkez Araştırma Enstitüsü Dergisi
PB  - Tarla Bitkileri Merkez Araştırma Enstitüsü
WT  - DergiPark
SN  - 1302-4310
SP  - 0
EP  - 0
VL  - 25
IS  - 1
LA  - en
AB  - Hydrogen peroxide (H2O2)and Nitric oxide (NO) are signalling molecules that play an important role in different organisms. Even though intensive research in the past two decades, knowledge about the role of these two molecules interact with each other in abiotic stress tolerance and the relationship with biological processes aren’t completely elucidated yet. In this paper, H2O2 and NO cross-talk and possible role in plant responses to abiotic stresses such as drought, salinity, extreme temperatures, UV irradiation and heavy metals at the level of biosynthesis and gene expression and protein activities are investigated in light of recent literature. In addition, the cross-talk between H2O2 and NO with other signalling pathways in the regulation of abiotic stress responses in plants is also discussed.
KW  - Abiotic stress; nitric oxide; hydrogen peroxide; signaling
N2  - Hidrojen peroksit (H2O2)ve Nitrik oksit (NO), çeşitli organizmalarda önemli etkileri bulunan sinyal iletim molekülleridir. Son 20 yıldır yapılan yoğun çalışmalara rağmen, abiyotik stres toleransında bu iki molekülün birbirleriyle olan etkileşimlerinin rolü ve oluşturdukları sinyallerin biyolojik süreçlerle ilişkileri konusundaki bilgiler günümüzde de sınırlı düzeydedir. Bu makalede bitkilerin kuraklık, tuzluluk, aşırı sıcaklık, UV ışığı ve ağır metaller gibi abiyotik strese tepkide H2O2 ve NO etkileşiminin muhtemel rolleri ve biyosentez, gen ifadesi ve protein aktiviteleri düzeyinde son literatür verileri ışığında araştırılmıştır. Ayrıca bitkilerde abiyotik stres yanıtlarında yer alan diğer sinyal iletim yolakları ile H2O2 ve NO’nun arasındaki etkileşimler tartışılmıştır.
CR  - Abogadallah G.M., 2010. Antioxidative defense under salt stress. Plant Signalling Behaviour, 5: 369–374
CR  - Avsian-Kretchmer O., Gueta-Dahan Y., Lev-Yadun S., Gollop R. and Ben-Hayyim G., 2004. The salt-stress signal transduction pathway that activates the gpx1 pro-moter is mediated by intracellular H2O2, different from the pathway induced byextracellular H2O2 Plant Physiology, 135: 1685–1696
CR  - Bajguz A. and Hayat S., 2009. Effects of brassinosteroids on the plant responses to environmental stresses. Plant Physiology and Biochemistry, 47: 1–8
CR  - Banti V., Mafessoni, F., Loreti E., Alpi A. and Perata P., 2010. The heat-inducible transcription factor HsfA2 enhances anoxia tolerance in Arabidopsis. Plant Physiology, 152: 1471–1483
CR  - Beligni M. V. and Lamattina L. 1999. Is nitric oxide toxic or protective? Trends in Plant Science, 4: 299–300
CR  - Besson-Bard A., Courtois C. and Gauthier A., Nitric Oxide in Plants: Production and cross-talk with Ca2+ signalling, Plant Molecular Biology, 1: 218-228
CR  - Bethke P. C., Badger M.R. and Jones R. L. 2004. Apoplastic synthesis of nitric oxide by plant tissues. Plant Cell, 16: 332–341
CR  - Blokhina O. and Fagerstedt KV., 2010. Reactive oxygen species and nitric oxide in plant mitochondria: origin and redundant regulatory systems. Physiologia Plantarum, 138:447–462
CR  - Bouchard J.N. and Yamasaki H., 2009. Implication of nitric oxide in the heat-stress-induced cell death of the symbiotic alga Symbiodinium microadriaticum Marine Biology 156: 2209–2220
CR  - Bright J., Desikan R., Hancock J.T., Weir I.S., Neill, S.J., 2006. ABA-induced NO generation and stomatal closure in Arabidopsis are dependent on H2O2 synthesis. The Plant Journal. 4: 113–122
CR  - Broniowska K. A., Diers A.R. and Hogg N., 2013. S - Nitrosoglutathione. Biochimica et Biophysica Acta, 1830: 3173–3181
CR  - Büyük I., Soydam-Aydın S. ve Aras S., 2012. Bitkilerin Tuz Stresine Verdiği Moleküler Cevaplar, Türk Hijyen ve Deneysel Biyoloji Dergisi, 69 (2): 97-110
CR  - Clarke A., Desikan R., Hurst R.D., Hancock, J.T. and Neill, S.J., 2000. NO way back: nitric oxide and programmed cell death in Arabidopsis thaliana suspension cultures. The Plant Journal, 24: 667–677
CR  - Cooney R.V., Harwood P.J., Custer L.J. and Franke A.A. 1994. Light mediated conversion of nitrogen dioxide to nitric oxide by carotenoids. Environ Health Perspectives, 102:460–462
CR  - Corpas F.J., Barroso J.B. and Carreras A., 2004. Cellular and subcellular localization of endogenous nitric oxide in young and senescent pea plants. Plant Physiology, 136:2722–2733
CR  - Cui X.M., Zhang Y.K., Wu X.B. and Liu C.S., 2010. The investigation of the alleviated effect of copper toxicity by exogenous nitric oxide in tomato plants. Plant Soil and Environment, 56: 274–281
CR  - Cui J., Zhou Y., Ding J., Xia X., Shi K., Chen S., Asami T., Chen Z. and Yu, J., 2011. Role of nitric oxide in hydrogen peroxide-dependent induction of abiotic stress tolerance by brassinosteroids in cucumber. Plant Cell and Environment, 34: 347–358
CR  - Del Rìo L.A., Corpas F.J. and Barroso J.B., 2004. Nitric oxide and nitric oxide synthase activity in plants. Phytochemistry 65: 783–792
CR  - Delledonne M., Xia Y.J., Dixon R.A. and Lamb, C., 1998. Nitric oxide functions as a signaling in plant disease resistance. Nature, 39: 585–588
CR  - Delledonne M., 2005. NO news is good news for plants. Current Opinion in Plant Biology, 8: 390–396
CR  - Desikan R., Mackerness S.A-H., Hancock J.T. and Neill S.J., 2001a. Regulation of the Arabidopsis transcriptome by oxidative stress. Plant Physiology, 127:159–172
CR  - Desikan R., Hancock J.T., Ichimura K., Shinozaki K. and Neill S.J., 2001b. Harpin induces activation of the Arabidopsis mitogen-activated protein kinases AtMPK4 and AtMPK6. Plant Physiology, 126: 1579–1587
CR  - Desikan R., Cheung M.K., Bright J., Henson D., Hancock J.T. and Neill S.J., 2004. ABA, hydrogen peroxide and nitric oxide signaling in stomatal guard cell. Journal of Experimental Botany, 395: 205–212
CR  - Desikan R., Hancock J.T., Bright J., Harrison J., Weir I., Hooley R. and Neill S.J., 2005. A role for ETR1 in hydrogen peroxide signaling in stomatal guard cells. Plant Physiology, 137: 831–834
CR  - Desikan R., Last K., Harrett-Williams R., Tagliavia C., Harter, K., Hooley, R., Hancock J.T. and Neill S.J., 2006. Ethylene-induced stomatal closure in Arabidopsis occurs via AtrbohF-mediated hydrogen peroxide synthesis. The Plant Journal, 47: 907–916
CR  - Esim N. and Atıcı Ö., 2015, Effects of exogenous nitiric oxide and salicylic acid on chilling-induced oxidative stress in wheat (Triticum aestivum), Frontiers in Life Science, 8(2): 124-130
CR  - Esim N. and Atıcı Ö., 2014. Nitric oxide improves chilling tolerance of maize by affecting apoplastic antioksidative enzymes in leaves, Plant Growth Regulation, 72: 29-38
CR  - Esim N., Atıcı Ö. and Mutlu S., 2014. Effects of exogenous nitric oxide in wheat seedlings under chilling stress, Toxicology and Industrial Health, 30(3): 268-274
CR  - Esim N. and Atıcı Ö., 2013, Nitric oxide alleviates boron toxicity by reducing oxidative damage and growth inhibition in maize seedlings, Australian Journal of Crop Sciences, 7(8): 1085-1092
CR  - Fan H., Guo S., Jiao Y., Zhang R. and Li J., 2007. Effects of exogenous nitric oxide on growth, active oxygen species metabolism, and photosynthetic characteristics in cucumber seedlings under NaCl stress. Frontiers of Agriculture in China 1: 308–314
CR  - Foyer C.H. and Noctor, 2011. Ascorbate and glutathione: the heart of the redox hub. Plant Physiology, 155: 2-18
CR  - Gould K.S., Lamotte O., Klinguer A., Pugin A. and Wendehenne D., 2003. Nitric oxide production in tobacco leaf cells: a generalized stress response? Plant Cell & Environment, 26: 1851–1862
CR  - Grant J.J., Yun B.-W. and Loake G.J., 2000. Oxidative burst and cognate redox signaling reported by luciferase imaging: identification of a signal network that functions independently of ethylene, SA and Me-JA but is dependent on MAPKK activity. The Plant Journal, 24: 569–582
CR  - Gropa M.D., Rosales E.P., Lannone M.F. and Benavides M.P., 2008. Nitric oxide, polyamines and Cd induced phytotoxicity in wheat roots. Phytochemistry, 69: 2609–2615
CR  - Guo H. and Ecker J.R., 2004. The ethylene signaling pathway: new insights. Current Opinion in Plant Biology, 7: 40–49
CR  - Guo F.Q., Okamoto M. and Crawford N.M., 2003. Identification of a plant nitric oxide synthase gene involved in hormonal signaling. Science, 302, 100–103
CR  - Halliwell B., 1984. Toxic effects of oxygen in plant tissues, In: Chloroplast Metabolism, The structure and function of chloroplasts in green leaf cells. Oxford Press, Oxford, 180-206
CR  - Halliwell B. and Gutteridge J.M.C. 2007. Free Radicals in Biology and Medicine. 4th ed., Oxford University Press, Oxford
CR  - Hancock J.T., Henson D., Nyirendam M., Desikan R., Harrison J., Lewis M., Hughes J. and Nefill S.J., 2005. Proteomic identification of glyceraldehyde 3-phosphate dehydrogenase as an inhibitory target of hydrogen peroxide in Arabidopsis. Plant Physiology and Biochemistry, 43: 828–835
CR  - Hao G.P., Xing Y. and Zhang J.H., 2008. Role of nitric oxide dependence on nitric oxide synthase-like activity in the water stress signalling of maize seedling. Journal of Integrative Plant Biology, 50: 435–442
CR  - He J.M., Xu H., She X.P., Song X.G. and Zhao W.M., 2005. The role and the interrelationship of hydrogen peroxide and nitric oxide in the UV-B-induced stomatal closure in broad bean. Functional Plant Biology, 32: 237–247
CR  - He J.M., Yue X.Z., Wang R.B. 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
CR  - He J.M., Zhang Z., Wang R.B. and Chen Y.P., 2011b. UV-B-induced stomatal clo-sure via ethylene-dependent NO generation in Vicia faba, Functional Plant Biology 38,293–302
CR  - Henry Y. A., Ducastel B. and Guissani A., 1996. Basic chemistry of nitric oxide and related nitrogen oxides. In: Nitric oxide research from chemistry to biology. Springer, USAHsu Y.T., Kao C.H., 2004. Cadmium toxicity is reduced by nitric oxide in rice leaves. Plant Growth Regulation, 42: 227–238
CR  - Hsu Y.T. and Kao C.H., 2004. Cadmium toxicity is reduced by nitric oxide in rice leaves Plant Growth Regulation., 42: 227–238
CR  - Hu K.D., Hu L.Y., Li Y.H., Zhang F.Q., Zhang H., 2007. Protective roles of nitric oxide on germination and antioxidant metabolism in wheat seeds under copper stress. Plant Growth Regulation, 53: 173–183
CR  - Huang X., von Rad, U. and Durner, J., 2002. Nitric oxide induces transcriptional activation of the nitric oxide-tolerant alternative oxidase in Arabidopsis suspension cells. Planta 215, 914–923
CR  - Jasid S., Simontacchi M., Bartoli C.G. and Puntarulo S., 2006. Chloroplasts as a nitric oxide cellular source. Effect of reactive nitrogen species on chloroplastic lipidsand proteins. Plant Physiology, 142: 1246-1255
CR  - Jubany-Marí T., Munne B.S. and Alegre L., 2010. Redox regulation of water stress responses in field-grown plants. Role of hydrogen peroxide and ascorbate. Plant Physiology and Biochemistry, 48: 351–358
CR  - Kagale S., Divi U.K., Krochko J.E., Keller W.A. and Krishna P., 2007. Brassinosteroid confers tolerance in Arabidopsis thaliana and Brassica napus to a range of abiotic stresses. Planta, 225: 353–364
CR  - Kaya C., Sönmez O., Ashraf M., Polat T., Tuna L. and Aydemir S., 2015. Exogenous application of nitric oxide and thiourea regulates on growth and some key physiological processes in maize (Zea mays L.) plants under saline stress. Soil-Water Journal, Special Issue: 61-66
CR  - Khan M.N., Mobin M., Mohammad F. and Corpas F.J., Nitric oxide action in abiotic stress responses in plants. 2015, Springer International Publishing Switzerland. 100-102
CR  - Klatt P. and Lamas S. 2000. Regulation of protein function by S-gluthiolation in response to oxidative and nitrosative stress, European Journal of Biochemistry, 267: 4928- 4944
CR  - Kolbert Z., Bartha B. and Erdei L., 2005. Generation of nitric oxide in roots of Pisum sativum, Triticum aestivum and Petroselinum crispum plants under osmotic and drought stress. Acta Biologica Szegediensis, 49: 13–16
CR  - Königshofer H., Tromballa H.W. and Löppert H.G., 2008. Early events in signaling high-temperature stress in tobacco BY2 cells involve alterations in membranefluidity and enhanced hydrogen peroxide production. Plant Cell and Environment, 31: 1771–1780
CR  - Kopyra M. and Gwó´zd´z E.A., 2003. Nitric oxide stimulates seed germination and coun-teracts the inhibitory effect of heavy metals and salinity on root growth of Lupinus luteus. Plant Physiology and Biochemistry, 41: 1011–1017
CR  - Kopyra M., Stachon-Wilk M. and Gwó´zd´z E.A., 2006. Effects of exogenous nitric oxide on the antioxidant capacity of cadmium-treated soybean cell suspension. Acta Physiologiae Plantarum, 28: 525–536
CR  - Kumar D. and Klessig D.F., 2000. Differential induction of tobacco MAP kinases by the defense signals nitric oxide, salicylic acid, ethylene, and jasmonic acid. Molecular Plant-Microbe Interactions Journal, 13: 347–351
CR  - Larkindale J. and Knight M.R., 2002. Protection against heat stress-induced oxidative damage in Arabidopsis involves calcium, abscisic acid, ethylene, and salicylic acid. Plant Physiology, 128: 682–695
CR  - Leshem Y.Y. and Haramaty E., 1996. The characterization and contrasting effects of the nitric oxide free radical in vegetative stress and senescence of Pisum sativum Linn. foliage. Journal of Plant Physiology, 148: 258–263
CR  - Li Q.Y., Niu H.B., Yin J., Wang M.B., Shao H.B., Deng D.Z., Chen X.X., Ren J.P. and Li, Y.C., 2008. Protective role of exogenous nitric oxide against oxidative-stress induced by salt stress in barley (Hordeum vulgare). Colloids and Surfaces Biointerfaces, 65: 220-225
CR  - Liao W., Huang G., Yu J. and Zhang M., 2012. Nitric oxide and hydrogen peroxide alleviate drought stress in marigold explants and promote its adventitious root development. Plant Physiology and Biochemistry, 58: 6–15
CR  - Lin Y.F. and Aarts M.G., 2012. The molecular mechanism of zinc and cadmium stress response in plants. Cellular and Molecular Life Sciences, 69: 3187–3206
CR  - Lindermayr C., Saalbach G. and Durner J., 2005. Proteomic identification of S-nitrosylated proteins in Arabidopsis. Plant Physiology, 137: 921–930
CR  - Liu H., Lau E., Lam M.P.Y., Chu H., Li, S., Huang G., Guo P., Wang J., Jiang L., Chu I.K., Lo C. and Tao Y., 2010a. OsNOA1/RIF1 is a functional homolog of AtNOA1/RIF1: implication for a highly conserved plant cGTPase essential for chloroplast func-tion. New Phytologist, 187: 83–105
CR  - Liu Y., Ye N., Liu R., Chen M. and Zhang J., 2010b. H2O2 mediates the regulation of ABA catabolism and GA biosynthesis in Arabidopsis seed dormancy and germination. Journal of Experimental Botany, 61: 2979–2990
CR  - 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, 7: 132–138
CR  - Lum H.K., Butt Y.K.C. and Lo S.C.L., 2002. Hydrogen peroxide induces a rapid production of nitric oxide in mung bean (Phaseolus aureus). Nitric Oxide, 6: 205–213
CR  - Ma F., Lu R., Liu H., Shi B., Zhang J., Tan, M., Zhang, A. and Jiang, M., 2012. Nitric oxide-activated calcium/calmodulin-dependent protein kinase regulates the abscisic acid-induced antioxidant defence in maize. Journal of Experimental Botany, 63: 4835–4847
CR  - Malik S. I., Hussain A., Yun B.W., Spoel S.H. and Loake G.J., 2011. GSNOR-mediated denitrosylation in the plant defence response. Plant Science, 181: 540–544
CR  - Mazid M., Khan T.A. and Mohammad F., 2011. Role of nitric oxide in regulation of H2O2 mediating tolerance of plants to abiotic stress: a synergistic signaling approach. Journal of Stress Physiology & Biochemistry, 7: 34–74
CR  - Mittler R., Vanderauwera S., Gollery M. and Van Breusegem F., 2004. Reactive oxygen gene network of plants. Trends in Plant Science, 9: 490–498
CR  - Mittler, R., 2002. Oxidative Stress, Antioxidants and Stress Tolerance, Trends in Plant Science, 7: 405-410
CR  - Molassiotis A. and Fotopoulo V., 2011. Oxidative and nitrosative signaling in plants,two branches in the same tree? Plant Signalling Behaviour, 6: 210–214
CR  - Mutlu F. and Yürekli F., 2015. Analysis of interactions of nitric oxide and polyamine under cadmium stress in wheat. Turkish Journal of Botany, 39: 778-785
CR  - Navarre D.A., Wendehenne D., Durner J., Noad R. and Klessig D.F., 2000. Nitric oxide modulates the activity of tobacco aconitase. Plant Physiology, 122: 573–582
CR  - Neill S.J., Desikan R., Clarke A. and Hancock J.T., 2002a. Nitric oxide is a novel component of abscisic acid signaling in stomatal guard cells. Plant Physiology, 128: 13–16
CR  - Neill S.J., Desikan R. and Clarke A., 2002b. Hydrogen peroxide and nitric oxide as signaling molecules in plants. Journal of Experimental Botany, 53: 1237–1242
CR  - Neill S., Desikan R. and Hancock J.T., 2002c. Hydrogen peroxide signalling. Current Opinion in Plant Biology, 5(5): 388-395.
CR  - Neill S., Desikan R. and Hancock J.T., 2003. Nitric oxide signalling in plants. New Phytologist, 159: 11–35
CR  - Pasqualini S., Meier S., Gehring C., Madeo L., Fornaciari M., Romanoand B. and Ederli L., 2009. Ozone and nitric oxide induce cGMP-dependent and independent transcription of defence genes in tobacco. New Phytologist, 181: 860–870
CR  - Qiao W.H., Xiao S.H., Yu L. and Fan L.M., 2009. Expression of a rice gene OsNOA1 re-establishes nitric oxide synthesis and stress-related gene expression for salttolerance in Arabidopsis nitric oxide-associated 1 mutant Atnoa1. Environmental and Experimental Botany, 65: 90–98
CR  - Qiao W., Li C. and Fan L-M., 2014. Cross-talk between nitric oxide and hydrogen peroxide in plant responses to abiotic stresses, Environmental and Experimental Botany, 100: 84-93
CR  - Rockel P., Strube F., Rockel A., Wildt J. and Kaiser, W.M., 2002. Regulation of Nitric Oxide (NO) Production by Plant Nitrate Reductase in vivo and in vitro, Journal of Experimental Botany, (53):103-110
CR  - Sang J., Zhang A., Lin F., Tan M. and Jiang M., 2008. Cross-talk between calcium-calmodulin and nitric oxide in abscisic acid signaling in leaves of maize plants. Cell Research, 18: 577–588
CR  - Santa-Cruz D.M., Pacienza N.A., Polizio A.H. and Balestrasse K.B., Tomaro M.L.,Yannarelli G.G., 2010. Nitric oxide synthase-like dependent NO production enhances heme oxygenase up-regulation in ultraviolet–B-irradiated soybean plants. Phytochemistry, 71: 1700–1707
CR  - Shi S., Wang G., Wang Y., Zhang L. and Zhang L., 2005. Protective effect of nitric oxide against oxidative stress under ultraviolet-B radiation. Nitric Oxide, 13: 1–9
CR  - Singh H.P., Batish D.R., Kaur G., Arora K. and Kohli R.K., 2008. Nitric oxide (as sodium nitroprusside) supplementation ameliorates Cd toxicity in hydroponically grown wheat roots. Environmental and Experimental Botany, 63: 158–167
CR  - Ślesak I., Libik M., Karpinska B., Karpinski S. and Miszalski Z., 2007. The Role of Hydrogen Peroxide in Regulation of Plant Metabolism and Cellular Signalling in Response to Environmental Stresses. Acta Biochimica Polonica, 54: 39-50
CR  - Smykowski A., Zimmermann P. and Zentgraf U., 2010. G-Box binding factor 1 reduces CATALASE 2 expression and regulates the onset of leaf senescence in Arabidopsis. Plant Physiology, 153: 1321–1331
CR  - Song L., Ding W., Zhao M., Sun B. and Zhang L., 2006. Nitric oxide protects against oxidative stress under heat stress in the calluses from two ecotypes of reed. Plant Science, 171: 449–458
CR  - Suzuki N. and Mittler R., 2006. Reactive oxygen species and temperature stresses: adelicate balance between signalling and destruction. Physiologia Plantarum, 126: 45–51
CR  - Tanou, G., Molassiotis, A. and, Diamantidis, G., 2009a. Induction of reactive oxygen species and necrotic death-like destruction in strawberry leaves by salinity. Environmental and Experimental Botany, 65: 270–281
CR  - Tanou G., Job C., Rajjou L., Arc E., Belghazi M., Diamantidis G., Molassiotis A. and Job D., 2009b. Proteomics reveals the overlapping roles of hydrogen peroxide and nitric oxide in the acclimation of citrus plants to salinity. The Plant Journal, 60: 795–804
CR  - Tian Q.Y., Sun D.H., Zhao M.G. and Zhang W.H., 2006. Inhibition of nitric oxide synthase (NOS) underlies aluminum-induced inhibition of root elongation in Hibiscus moscheutos. New Phytologist, 174: 322–331
CR  - Tossi V., Lamattina L. and Cassia R., 2009. An increase in the concentration of abscisic acid is critical for nitric oxide mediated plant adaptive responses to UV-B irradiation. New Phytologist, 181: 871–879
CR  - Uchida A., Jagendorf A.T., Hibino T., Takabe T. and Takabe T., 2002. Effects of hydrogen peroxide and nitric oxide on both salt and heat stress tolerance in rice. Plant Science, 163: 515–523
CR  - Unsal NP. and Arısan D., 2009. Nitric Oxide Signalling in Plants, The Botanical Review, 75 (2): 203-229
CR  - Verma K., Mehta S.K. and Shekhawat G.S., 2013. Nitric oxide (NO) counteracts cadmium induced cytotoxic processes mediated by reactive oxygen species (ROS) in Brassica juncea: cross-talk between ROS, NO and antioxidant responses. Biometals, 26: 255–269
CR  - Volkov R.A., Panchuk I.I. and Mullineaux P.M., Schöffl F., 2006. Heat stress-induced H2O2 is required for effective expression of heat shock genes in Arabidopsis. Plant Molecular Biology, 61: 733–746
CR  - Vraová E., Inzé D. and Van Breusegem F., 2002. Signal transduction during oxidative stress. Journal of Experimental Botany, 53: 1227–1236
CR  - Wahid A., Perveen M., Geelani S. and Basra S.M.A., 2007. Pretreatment of seed with H2O2 improves salt tolerance of wheat seedlings by alleviation of oxidative damage and expression of stress proteins. Journal of Plant Physiology, 164: 283–294
CR  - Wang Y.S. and Yang Z.M., 2005. Nitric oxide reduces aluminum toxicity by preventingoxidative stress in the roots of Cassia tora L. Plant Cell Physiology, 46: 1915–1923
CR  - Wang Y., Feng H., Qu Y., Cheng J., Zhao Z., Zhang M., Wang X. and An L., 2006. The relationship between reactive oxygen species and nitric oxide in ultraviolet-B-induced ethylene production in leaves of maize seedlings. Environmental and Experimental Botany, 57: 51–61
CR  - Wang H., Liang X., Wan Q., Wang X. and Bi Y., 2009. Ethylene and nitric oxide are involved in maintaining ion homeostasis in Arabidopsis callus under salt stress. Planta, 230: 293–307
CR  - Wang L., Yang L., Yang F., Li X., Song Y., Wang X. and Hu X., 2010a. Involvements of H2O2 and metallothionein in NO-mediated tomato tolerance to copper toxicity. Journal of Plant Physiology, 167: 1298–1306
CR  - Wang P., Du Y., Li Y., Ren D. and, Song C., 2010b. Hydrogen peroxide-mediated activation of MAP kinase 6 modulates nitric oxide biosynthesis and signal transduction in Arabidopsis. Plant Cell, 22: 2981–2998
CR  - Wang Y., Ries A., Wu K., Yang A. and Crawford N.M., 2010c. The Arabidopsis pro-hibitin gene phb3 functions in nitric oxide-mediated responses and in hydrogen peroxide-induced nitric oxide accumulation. Plant Cell, 22: 249–259
CR  - Wang Y., Lin A., Loake G.J. and Chu C., 2013. H2O2-induced leaf cell death and thecrosstalk of reactive nitric/oxygen species. Journal of Integrative Plant Biology, 55: 202–208
CR  - Wendehenne D, Gould K. and Lamotte O., 2004. Nitric oxide is a essential component of biotic and abiotic stress-induced signaling pathways in plants. In: Magalhaes JR (ed) Nitric oxide signaling in higher plants. Studium Press, Houston, 55–64
CR  - Xia X.J., Wang,Y.J., Zhou,Y.H., Tao,Y., Mao W.H., Shi K., Asami T., Chen Z. and Yu J.Q., 2009. Reactive oxygen species are involved in brassinosteroid-induced stress tolerance in cucumber. Plant Physiology, 150: 801–814
CR  - Xiong J., An L., Lu H. and Zhu C., 2009. Exogenous nitric oxide enhances cadmium tolerance of rice by increasing pectin and hemicelluloses contents in root cellwall. Planta, 230: 755–765
CR  - Xiong J., Fu, G., Tao, L. and Zhu, C., 2010. Roles of nitric oxide in alleviating heavy metal toxicity in plants. Archives of Biochemistry and Biophysics.497: 13–20
CR  - Xuan Y., Zhou S., Wang L., Cheng Y. and Zhao L., 2010. Nitric oxide functions as a signal and acts upstream of AtCaM3 in thermotolerance in Arabidopsis seedlings. Plant Physiology, 153: 1895-1906
CR  - Zago E., Morsa S., Dat J.F., Alard P., Ferrarini A., Inze D., Delledonne M. and Breusegem F.V., 2006. Nitric oxide and hydrogen peroxide-responsive gene regulation during cell death induction in tobacco. Plant Physiology, 141: 404–411
CR  - Zhang Y., Wang L., Liu Y., Zhang Q., Wei Q. and Zhang W., 2006. Nitric oxide enhances salt tolerance in maize seedlings through increasing activities of proton-pumpand Na+/H+ antiport in the tonoplast. Planta, 224: 545–555
CR  - Zhang A., Jiang M., Zhang J., Ding H., Xu S., Hu X. and Tan M., 2007. Nitric oxide induced by hydrogen peroxide mediates abscisic acid-induced activation of the mitogen activated protein kinase cascade involved in antioxidant defense in maize leaves. New Phytologist, 175: 36–50
CR  - Zhang H., Li, Y.H., Hu, L.Y., Wang, S.H., Zhang F.Q. and Hu K.D., 2008. Effects of exoge-nous nitric oxide donor on antioxidant metabolism in wheat leaves under aluminum stress. Russian Journal of Plant Physiology, 55: 469–474
CR  - Zhang Y., Tan J., Guo Z., Lu S., He S., Shu, W. and Zhou, B., 2009. Increased abscisic acid levels in transgenic tobacco over-expressing 9 cis-epoxycarotenoid dioxygenase influence H2O2 and NO production and antioxidant defences. Plant Cell and Environment, 32: 509–519
CR  - Zhang A., Zhang J., Zhang J., Ye N., Zhang H., Tan M. and Jiang M., 2011. Nitric oxide mediates brassinosteroid-induced ABA biosynthesis involved in oxidative stress tolerance in maize leaves. Plant Cell Physiology, 52: 181–192
CR  - Zhao L., Zhang F., Guo J., Yang Y., Li B. and Zhang L., 2004. Nitric oxide functions as asignal in salt resistance in the calluses from two ecotypes of reed. Plant Physiology, 134: 849–857
CR  - Zhao M., Zhao X., Wu Y. and Zhang L., 2006. Enhanced sensitivity to oxidative stress in Arabidopsis nitric oxide synthase mutant. Journal of Plant Physiology, 164: 737–745
CR  - Zhao M.G., Tian Q.Y. and Zhang W.H., 2007. Nitric oxide synthase dependent nitric oxide production is associated with salt tolerance in Arabidopsis. Plant Physiology, 144: 206–217
CR  - Zhao M.G., Chen L., Zhang L.L. and Zhang W.H., 2009. Nitric reductase dependent nitric oxide production is involved in cold acclimation and freezing tolerance in Arabidopsis. Plant Physiology, 151: 755–767
UR  - https://doi.org/10.21566/tbmaed.45530
L1  - https://dergipark.org.tr/tr/download/article-file/220263
ER  -