Functional role of nitric oxide under abiotic stress conditions

Nitric Oxide Action in Abiotic Stress Responses in Plants

Volumn , Issue , 2015, Pages 21-41

  Tufan Oz, Mehmet ^a   Eyidogan, Fusun ^b   Yucel, Meral ^c   Öktem, Hüseyin Avni ^d  

^a UNIVERSITY OF FLORIDA   (United States)

^b BASKENT UNIVERSITY   (Turkey)

^c MIDDLE EAST TECHNICAL UNIVERSITY   (Turkey)

^d KONYA FOOD AND AGRICULTURE UNIVERSITY   (Turkey)

Author keywords

Nitrosative stress; Oxidative stress; Phytohormone; Signalling

Indexed keywords

EID: 84943793365     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-3-319-17804-2_2     Document Type: Chapter

References (139)

1. Abat JK, Deswal R (2009) 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 9:4368-4380.
2. Aftab T, Khan MM, Naeem M et al (2012) Exogenous nitric oxide donor protects Artemisia annua from oxidative stress generated by boron and aluminium toxicity. Ecotoxicol Environ Saf 80:60-68.
3. Ahlfors R, Brosche M, Kollist H, Kangasjarvi J (2009) Nitric oxide modulates ozone induced cell death, hormone biosynthesis and gene expression in Arabidopsis thaliana.Plant J 58:1-12.
4. Airaki M, Leterrier M, Mateos RM et al (2012) Metabolism of reactive oxygen species and reactive nitrogen species in pepper (Capsicum annuum L.) plants under low temperature stress. Plant Cell Environ 35:281-295.
5. An L, Liu Y, Zhang M et al (2005) Effect of nitric oxide on growth of maize seedling leaves in presence or absence of ultraviolet-B radiation. J Plant Physiol 162:317-326.
6. Arasimowicz-Jelonek M, Floryszak-Wieczorek J, Gwozdz EA (2011) The message of nitric oxide in cadmium challenged plants. Plant Sci 181:612-620.
7. Arasimowicz-Jelonek M, Floryszak-Wieczorek J, Deckert J et al (2012) Nitric oxide implication in cadmium-induced programmed cell death in roots and signalling response of yellow lupine plants. Plant Physiol Biochem 58:124-134.
8. Arnaud N, Murgia I, Boucherez J et al (2006) An iron-induced nitric oxide burst precedes ubiq-uitin-dependent protein degradation for Arabidopsis AtFer1 ferritin gene expression. J Biol Chem 281:23579-23588.
9. Barroso JB, Corpas FJ, Carreras A et al (2006) Localization of S-nitrosoglutathione and expression of S-nitrosoglutathione reductase in pea plants under cadmium stress. J Exp Bot 57:1785-1793.
10. Benavides MP, Gallego SM, Tomaro ML (2005) Cadmium toxicity in plants. Braz J Plant Physiol 17:21-34.
11. Benzarti S, Mohri S, Ono Y (2008) Plant response to heavy metal toxicity: Comparative study between the hyperaccumulator Thlaspicaerulescens (ecotype Ganges) and nonaccumulator plants: Lettuce, radish, and alfalfa. Environ Toxicol 23:607-616.
12. Besson-Bard A, Pugin A, Wendehenne D (2008a) New insights into nitric oxide signalling in plants. Ann Rev Plant Biol 59:21-39.
13. Besson-Bard A, Courtois C, Gauthier A et al (2008b) Nitric oxide in plants: Production and cross-talk with Ca2+ signalling. Mol Plant 1:218-228.
14. Besson-Bard A, Gravot A, Richaud P et al (2009) Nitric oxide contributes to cadmium toxicity inArabidopsis by promoting cadmium accumulation in roots and by up-regulating genes related to iron uptake. Plant Physiol 149:1302-1315.
15. Boyarshinov AV, Asafova EV (2011) Stress responses of wheat leaves to dehydration: Participation of endogenous NO and effect of sodium nitroprusside. Russ J Plant Physiol 58:1034-1039.
16. Botrel A, Magne C, Kaiser WM (1996) Nitrate reduction, nitrite reduction and ammonium assimilation in barley roots in response to anoxia. Plant Physiol Biochem 34:645-652.
17. Bright J, Desikan R, Hancock JT et al (2006) ABA-induced NO generation and stomatal closure in Arabidopsis are dependent on H2O2synthesis. Plant J 45:113-122.
18. Cantrel C, Vazquez T, Puyaubert J et al (2011) Nitric oxide participates in cold-responsive phosphosphingolipid formation and gene expression in Arabidopsis thaliana.New Phytol 189:415-427.
19. Chaki M, Valderrama R, Fernández-Ocana A et al (2011) Mechanical wounding induces a nitro-sative stress by down-regulation of GSNO reductase and an increase in S-nitrosothiols in sunflower (Helianthus annuus) seedlings. J Exp Bot 62:1803-1813.
20. Corpas FJ, Carreras A, Valderrama R et al (2007) Reactive nitrogen species and nitrosative stress in plants. Plant Stress 1:37-41.
21. Corpas FJ, Palma JM, Sandalio LM et al (2008) Metabolism of reactive nitrogen species in pea plants under abiotic stress conditions. Plant Cell Physiol 49:1711-1722.
22. Corpas FJ, Leterrier M, Valderrama R et al (2011) Nitric oxide imbalance provokes a nitrosative response in plants under abiotic stress. Plant Sci 181:604-611.
23. Dat JF, Capelli N, Folzer H et al (2004) Sensing and signalling during plant flooding. Plant Physiol Biochem 42:273-282.
24. David A, Yadav S, Bhatla SC (2010) Sodium chloride stress induces nitric oxide accumulation in root tips and oil body surface accompanying slower oleosin degradation in sunflower seedlings. Physiol Plant 140:342-354.
25. De Michele R, Vurro E, Rigo C et al (2009) Nitric oxide is involved in cadmium-induced programmed cell death in Arabidopsis suspension cultures. Plant Physiol 150:217-228.
26. Distefano AM, Garcia-Mata C, Lamattina L, Laxalt AM (2008) Nitric oxide-induced phospha-tidic acid accumulation: A role for phospholipases C and D in stomatal closure. Plant Cell Environ 31:187-194.
27. Dordas C, Rivoal J, Hill RD (2003) Plant haemoglobins, nitric oxide and hypoxic stress. Ann Bot 91:173-178.
28. Durner J, Wendehenne D, Klessig D (1998) Defense gene induction in tobacco by nitric oxide, cyclic GMP, and cyclic ADP-Ribose. Proc Natl Acad Sci USA 95:10328-1033.
29. Ederli L, Morettini R, Borgogni A et al (2006) Interaction between nitric oxide and ethylene in the induction of alternative oxidase in ozone-treated tobacco plants. Plant Physiol 142:595-608.
30. Ederli L, Meier S, Borgogni A et al (2008) cGMP in ozone and NO-dependent responses. Plant Signal Behav 3:36-37.
31. Fan HF, Du CX, Guo SR (2013) Nitric oxide enhances salt tolerance in cucumber seedlings by regulating free polyamine content. Environ Exp Bot 86:52-59.
32. Farooq M, Basra SMA, Wahid A, Rehman H (2009) Exogenously applied nitric oxide enhances the drought tolerance in fine grain aromatic rice (Oryza sativa L.). J Agron Crop Sci 195:254-261.
33. Frohnmeyer H, Staiger D (2003) Ultraviolet-B radiation-mediated responses in plants. Balancing damage and protection. Plant Physiol 133:1420-1428.
34. Garcia-Mata C, Lamattina L (2001) Nitric oxide induces stomatal closure and enhances the adaptive plant responses against drought stress. Plant Physiol 126:1196-1204.
35. Garcia-Mata C, Lamattina L (2002) Nitric oxide and abscisic acid cross talk in guard cells. Plant Physiol 128:790-792.
36. Gould KS, Lamotte O, Klinguer A et al (2003) Nitric oxide production in tobacco leaf cells: A generalized stress response? Plant Cell Environ 26:1851-1862.
37. Groppa MD, Rosales EP, Iannone MF, Benavides MP (2008) Nitric oxide, polyamines and Cd-induced phytotoxicity in wheat roots. Phytochemistry 69:2609-2615.
38. Guo FQ, Okamoto M, Crawford NM (2003) Identification of a plant nitric oxide synthase gene involved in hormonal signalling. Science 302:100-103.
39. Gupta DK, Srivastava S, Huang H et al (2011) Arsenic tolerance and detoxification mechanisms in plants. In: Sherameti I, Varma A (eds) Detoxification of heavy metals. Soil biology. Springer, Heidelberg.
40. Gupta DK, Inouhe M, Rodríguez-Serrano M et al (2013) Oxidative stress and arsenic toxicity: Role of NADPH oxidases. Chemosphere 90:1987-1996.
41. Hall JL (2002) Cellular mechanisms for heavy metal detoxification and tolerance. J Exp Bot 53:1-11.
42. Hao GP, Xing Y, Zhang JH (2008) Role of nitric oxide dependence on nitric oxide synthase-like activity in the water stress signalling of maize seedling. J Integr Plant Biol 50:435-442.
43. Hao G, Du X, Zhao F et al (2009) Role of nitric oxide in UV-B-induced activation of PAL and stimulation of flavonoid biosynthesis in Ginkgo biloba callus. Plant Cell Tissue Organ Cult 97:175-185.
44. Hayat S, Yadav S, Wani AS et al (2012) Impact of sodium nitroprusside on nitrate reductase, proline content, and antioxidant system in tomato under salinity stress. Hortic Environ Biotechnol 53:362-367.
45. He HY, Zhan J, He LF, Gu MH (2012a) Nitric oxide signalling in aluminum stress in plants. Protoplasma 249:483-492.
46. He HY, He LF, Gu MH, Li XF (2012b) Nitric oxide improves aluminum tolerance by regulating hormonal equilibrium in the root apices of rye and wheat. Plant Sci 183:123-130.
47. Hossain KK, Nakamura T, Yamasaki H (2011) Effect of nitric oxide on leaf non-photochemical quenching of fluorescence under heat stress conditions. Russ J Plant Physiol 58:629-633.
48. Hsu YT, Kao CH (2004) Cadmium toxicity is reduced by nitric oxide in rice leaves. Plant Growth Regul 42:227-238.
49. Huang X, Stettmaier K, Michel C et al (2004) Nitric oxide is induced by wounding and influences jasmonic acid signalling in Arabidopsis thaliana.Planta 218:938-946.
50. Igamberdiev AU, Baron K, Manac’h-Little N et al (2005) Thehaemoglobin/nitric oxide cycle: Involvement in flooding stress and effects on hormone signalling. Ann Bot 96:557-564.
51. Ismail GSM (2012) Protective role of nitric oxide against arsenic-induced damages in germinating mung bean seeds. Acta Physiol Plant 34:1303-1311.
52. Jhanji S, Setia RC, Kaur N et al (2012) Role of nitric oxide in cadmium-induced stress on growth, photosynthetic components and yield of Brassica napus L. J Environ Biol 33:1027-1032.
53. Jin JW, Xu YF, Huang YF (2010) Protective effect of nitric oxide against arsenic-induced oxidative damage in tall fescue leaves. African J Biotech 9:1619-1627.
54. Karpets YV, Kolupaev YE, Yastreb TO (2011) Effect of sodium nitroprusside on heat resistance of wheat coleoptiles: Dependence on the formation and scavenging of reactive oxygen species. Russ J Plant Physiol 58:1027-1033.
55. Karpets YV, Kolupaev E, Yastreb TO, Dmitriev OP (2012) Possible pathways of heat resistance induction in plant cells by exogenous nitrogen oxide. Cytol Genetics 46:354-359.
56. Khan MN, Siddiqui MH, Mohammad F, Naeem M (2012) Interactive role of nitric oxide and calcium chloride in enhancing tolerance to salt stress. Nitric Oxide-Biol Chem 27:210-218.
57. Kopyra M, Stachon-Wilk M, Gwozdz EA (2006) Effects of exogenous nitric oxide on the antioxidant capacity of cadmium-treated soybean cell suspension. Acta Physiol Plant 28:525-536.
58. Kotak S, Larkindale J, Lee U, von Koskull-Doring P, Vierling E, Scharf KD (2007) Complexity of the heat stress response in plants. Curr Opin Plant Biol 10:310-316.
59. Krasylenko YA, Yemets AI, Sheremet YA, Blume YB (2012) Nitric oxide as a critical factor for perception of UV-B irradiation by microtubules in Arabidopsis. Physiol Plant 145:505-515.
60. Kulik A, Anielska-Mazur A, Bucholc M et al (2012) SNF1-related protein kinases type 2 are involved in plant responses to cadmium stress. Plant Physiol 160:868-883.
61. Lamattina L, Garcia-Mata C, Graziano M, Pagnussat G (2003) Nitric oxide: The versatility of an extensive signal molecule. Annu Rev Plant Biol 54:109-136.
62. Lanteri ML, Laxalt AM, Lamattina L (2008) Nitric oxide triggers phosphatidic acid accumulation via phospholipase D during auxin induced adventitious root formation in cucumber. Plant Physiol 147:188-198.
63. Laspina NV, Groppa MD, Tomaro ML, Benavides MP (2005) Nitric oxide protects sunflower leaves against Cd-induced oxidative stress. Plant Sci 169:323-330.
64. Laxalt AM, Raho N, Ten HA, Lamattina L (2007) Nitric oxide is critical for inducing phospha-tidic acid accumulation in xylanase-elicited tomato cells. J Biol Chem 282:21160-21168.
65. Lee U, Wie C, Fernández BO 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.
66. Lei Y, Yin C, Li C (2007) Adaptive responses of Populus przewalskii to drought stress and SNP application. Acta Physiol Plant 29:519-526.
67. Leterrier M, Airaki M, Palma JM et al (2012) Arsenic triggers the nitric oxide (NO) and S-nitrosoglutathione (GSNO) metabolism in Arabidopsis.Environ Pollut 166:136-143.
68. Locato V, Gadaleta C, De Gara L, De Pinto MC (2008) Production of reactive species and modulation of antioxidant network in response to heat shock: A critical balance for cell fate. Plant Cell Environ 31:1606-1619.
69. Ma JF, Shen R, Zhao Z et al (2002) Response of rice to Al stress and identification of quantitative trait loci for Al tolerance. Plant Cell Physiol 43:652-659.
70. Mackerness SAH, John CF, Jordan B, Thomas B (2001) Early signalling components in ultravi-olet-B responses: Distinct roles for different reactive oxygen species and nitric oxide. Febs Lett 489:237-242.
71. Mahalingam R, Jambunathan N, Gunjan SK et al (2006) Analysis of oxidative signalling induced by ozone in Arabidopsis thaliana.Plant Cell Environ 29:1357-1371.
72. Moreau M, Lee GI, Wang Y et al (2008) AtNOS/AtNOA1 is a functional Arabidopsis thaliana cGTPase and not a nitric oxide synthase. J Biol Chem 283:32957-32967.
73. Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651-681.
74. Nasibi F, Kalantari KM (2009) Influence of nitric oxide in protection of tomato seedling against oxidative stress induced by osmotic stress. Acta Physiol Plant 31:1037-1044.
75. Neill SJ, Desikan R, Hancock JT (2003) Nitric oxide signalling in plants. New Phytol 159:11-35.
76. Neill S (2007) Interactions between abscisic acid, hydrogen peroxide and nitric oxide mediate survival responses during water stress. New Phytol 175:4-6.
77. Neill S, Barroso R, Bright J, Desikan R, Hancock J, Harrison J, Morris P, Ribeiro D, Wilson J (2008) Nitric oxide, stomatal closure, and abiotic stress. J Exp Bot 59:165-176.
78. Ortega-Galisteo AP, Rodríguez-Serrano M, Pazmiño D et al (2012) S-nitrosylated proteins in pea (Pisum sativum L.) leaf peroxisomes: Changes under abiotic stress. J Exp Bot 63:2089-2103.
79. Pasqualini S, Meier S, Gehring C et al (2009) Ozone and nitric oxide induce cGMP-dependent and -independent transcription of defence genes in tobacco. New Phytol 181:860-870.
80. Pasqualini S, Reale L, Calderini O et al (2012) Involvement of protein kinases and calcium in the NO-signalling cascade for defence-gene induction in ozonated tobacco plants. J Exp Bot 63:4485-4496.
81. Patakas AA, Zotos A, Beis AS (2010) Production, localisation and possible roles of nitric oxide in drought-stressed grapevines. Aust J Grape Wine R 16:203-209.
82. Qu HY, Feng YB, Wang MX et al (2006) Nitric oxide functions as a signal in ultraviolet-B induced inhibition of pea stems elongation. Plant Sci 170:994-1000.
83. Rao MV, Davis KR (2001) The physiology of ozone induced cell death. Planta 213:682-690.
84. Rao KP, Vani G, Kumar K et al (2011) Arsenic stress activates MAP kinase in rice roots and leaves. Arch Biochem Biophys 506:73-82.
85. Rascio N, Navari-Izzo F (2011) Heavy metal hyperaccumulating plants: How and why do they do it? And what makes them so interesting? Plant Sci 180:169-181.
86. Rockel P, Strube F, Rockel A et al (2002) Regulation of nitric oxide (NO) production by plant nitrate reductase in vivo and in vitro. J Exp Bot 53:1-7.
87. Rodríguez-Serrano M, Romero-Puertas MC, Pazmiño DM et al (2009) Cellular response of pea plants to cadmium toxicity: Cross talk between reactive oxygen species, nitric oxide, and calcium. Plant Physiol 150:229-243.
88. Sairam RK, Kumutha D, Ezhilmathi K et al (2008) Physiology and biochemistry of water logging tolerance in plants. Biol Plant 52:401-412.
89. Sang J, Jiang M, Lin F et al (2008) Nitric oxide reduced hydrogen peroxide accumulation involved in water stress induced subcellular antioxidant defense in maize plants. J Integr Plant Biol 50:231-243.
90. Sanchez C, Gates AJ, Meakin GE et al (2010) Production of nitric oxide and nitrosylleghemo-globin complexes in soybean nodules in response to flooding. Mol Plant Microbe Interact 23:702-711.
91. Schilmiller AL, Howe GA (2005) Systemic signalling in the wound response. Curr Opin Plant Biol 8:369-377.
92. Seki M, Narusaka M, Ishida J et al (2002) Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray. Plant J31:279-292.
93. Sharma P, Sharma N, Deswal R (2005) The molecular biology of the low-temperature response in plants. Bioessays 27:1048-1059.
94. Sharma I (2012) Arsenic induced oxidative stress in plants. Biologia 67:447-453.
95. Shi SY, Wang G, Wang YD et al (2005) Protective effect of nitric oxide against oxidative stress under ultraviolet-B radiation. Nitric Oxide-Biol Chem 13:1-9.
96. Shi HT, Li RJ, Cai W et al (2012) Increasing nitric oxide content in Arabidopsis thaliana by expressing rat neuronal nitric oxide synthase resulted in enhanced stress tolerance. Plant Cell Physiol 53:344-357.
97. Shimoda Y, Nagata M, Suzuki A et al (2005) Symbiotic Rhizobium and nitric oxide induce gene expression of non-symbiotic hemoglobin in Lotus japonicus. Plant Cell Physiol 46:99-107.
98. Shinozaki K, Yamaguchi-Shinozaki K, Seki M (2003) Regulatory network of gene expression in the drought and cold stress responses. Curr Opin Plant Biol 6:410-417.
99. Singh HP, Kaur S, Batish DR et al (2009) Nitric oxide alleviates arsenic toxicity by reducing oxidative damage in the roots of Oryza sativa (rice). Nitric Oxide 20:289-297.
100. Song LL, Ding W, Zhao MG et al (2006) Nitric oxide protects against oxidative stress under heat stress in the calluses from two ecotypes of reed. Plant Sci 171:449-458.
101. Srivastava S, Dubey RS (2012) Nitric oxide alleviates manganese toxicity by preventing oxidative stress in excised rice leaves. Acta Physiol Plant 34:819-825.
102. Tanou G, Job C, Rajjou L et al (2009) Proteomics reveals the overlapping roles of hydrogen peroxide and nitric oxide in the acclimation of citrus plants to salinity. Plant J 60:795-804.
103. Tanou G, Filippou P, Belghazi M et al (2012) Oxidative and nitrosative-based signalling and associated post-translational modifications orchestrate the acclimation of citrus plants to salinity stress. Plant J 72:585-599.
104. Tewari RK, Hahn EJ, Paek KY (2008) Modulation of copper toxicity-induced oxidative damage by nitric oxide supply in the adventitious roots of Panax ginseng. Plant Cell Rep 27:171-181.
105. Thapa G, Sadhukhan A, Panda SK, Sahoo L (2012) Molecular mechanistic model of plant heavy metal tolerance. Biometals 25:489-505.
106. Tian X, Lei Y (2007) Physiological responses of wheat seedlings to drought and UV-B radiation. Effect of exogenous sodium nitroprusside application.Russ. J Plant Physiol 54:676-682.
107. Tian QY, Sun DH, Zhao MG, Zhang WH (2007) Inhibition of nitric oxide synthase (NOS) underlies aluminum-induced inhibition of root elongation in Hibiscus moscheutos. New Phytol 174:322-331.
108. Tossi V, Cassia R, Lamattina L (2009a) Apocynin-induced nitric oxide production confers antioxidant protection in maize leaves. J Plant Physiol 166:1336-1341.
109. ossi V, Lamattina L, Cassia R (2009b) An increase in the concentration of abscisic acid is critical for nitric oxide-mediated plant adaptive responses to UV-B irradiation. New Phytol 181:871-879.
110. Tossi V, Cassia R, Bruzzone S et al (2012a) ABA says NO to UV-B: A universal response? Trends Plant Sci 17:510-517.
111. Tossi V, Lombardo C, Cassi R, Lamattina L (2012b) Nitric oxide and flavonoids are systemically induced by UV-B in maize leaves. Plant Sci 193 -194:103-109.
112. chida A, Jagendorf AT, Hibino T et al (2002) Effects of hydrogen peroxide and nitric oxide on both salt and heat stress tolerance in rice. Plant Sci 163:515-523.
113. Verbruggen N, Hermans C, Schat H (2009) Mechanisms to cope with arsenic or cadmium excess in plants. Curr Opin Plant Biol 12:1-9.
114. Wang R, Guegler K, LaBrie ST, Crawford NM (2000) Genomic analysis of a nutrient response in Arabidopsis reveals diverse expression patterns and novel metabolic and potential regulatory genes induced by nitrate. Plant Cell 12:1491-1510.
115. Wang HH, Huang JJ, Bi YR (2010) Nitrate reductase-dependent nitric oxide production is involved in aluminum tolerance in red kidney bean roots. Plant Sci 179:281-288.
116. Wang YH, Li XC, Zhu-Ge Q et al (2012) Nitric oxide participates in cold-inhibited Camellia sinensis pollen germination and tube growth partly via cGMP in vitro. Plos ONE 7:1-11.
117. Wang QH, Liang X, Dong YJ et al (2013) Effects of exogenous nitric oxide on cadmium toxicity, element contents and antioxidative system in perennial ryegrass. Plant Growth Regul 69:11-20.
118. Wawer I, Bucholc M, Astier J et al (2010) Regulation of Nicotianatabacum osmotic stress-activated protein kinase and its cellular partner GAPDH by nitric oxide in response to salinity. Biochem J 429:73-83.
119. Wimalasekera R, Tebartz F, Scherer GF (2011) Polyamines, polyamine oxidases and nitric oxide in development, abiotic and biotic stresses. Plant Sci 181:593-603.
120. Winfield MO, Lu C, Wilson ID et al (2010) Plant responses to cold: Transcriptome analysis of wheat. Plant Biotechnol J8:749-771.
121. Wu XX, Zhu WM, Zhang H et al (2011) Exogenous nitric oxide protects against salt-induced oxidative stress in the leaves from two genotypes of tomato (Lycopersicom esculentum Mill.). Acta Physiol Plant 33:1199-1209.
122. Xiong J, An L, Lu H, Zhu C (2009) Exogenous nitric oxide enhances cadmium tolerance of rice by increasing pectin and hemicellulose contents in root cell wall. Planta 230:755-765.
123. Xiong J, Fu G, Tao L, Zhu C (2010) Roles of nitric oxide in alleviating heavy metal toxicity in plants. Arch Biochem Biophys 497:13-20.
124. Xu J, Yin H, Li Y, Liu X (2010) Nitric oxide is associated with long-term zinc tolerance in Solanum nigrum.Plant Physiol 154:1319-1334.
125. Xua M, Zhub Y, Dongb J et al (2012) Ozone induces flavonol production of Ginkgo biloba cells dependently on nitrate reductase-mediated nitric oxide signalling. Environ Exp Bot 75:114-119.
126. Yamasaki H, Sakihama Y, Takahashi S (1999) An alternative pathway of nitric oxide production: New features of an old enzyme. Trends Plant Sci 4:128-129.
127. Yang LT, Qi YP, Chen LS et al (2012) Nitric oxide protects sour pummelo (Citrus grandis) seedlings against aluminum-induced inhibition of growth and photosynthesis. Environ Exp Bot 82:1-13.
128. Ye Y, Li Z, Xing D (2013) Nitric oxide promotes MPK6-mediated caspase-3-like activation in cadmium-induced Arabidopsis thaliana programmed cell death. Plant Cell Environ 36:1-15.
129. Yu Q, Sun L, Jin H et al (2012) Lead-induced nitric oxide generation plays a critical role in lead uptake by Pogonatherum crinitum root cells. Plant Cell Physiol 53:1728-1736.
130. Yung BW, Feechan A, Yin M et al (2011) S-nitrosylation of NADPH oxidase regulates cell death in plant immunity. Nature 478:264-268.
131. Zago E, Morsa S, Dat JF et al (2006) Nitric oxide- and hydrogen peroxide-responsive gene regulation during cell death induction in tobacco. Plant Physiol 141:404-411.
132. Zhao Z, Chen G, Zhang C (2001) Interaction between reactive oxygen species and nitric oxide in drought-induced abscisic acid synthesis in root tips of wheat seedlings. Austr J Plant Physiol 28:1055-1061.
133. Zhao LQ, Zhang F, Guo JK et al (2004) Nitric oxide functions as a signal in salt resistance in the calluses from two ecotypes of reed. Plant Physiol 134:849-857.
134. Zhao MG, Tian QY, Zhang WH (2007) Nitric oxide synthase dependent nitric oxide production is associated with salt tolerance in Arabidopsis.Plant Physiol 144:206-217.
135. Zhao MG, Chen L, Zhang LL, Zhang WH (2009) Nitric reductase-dependent nitric oxide production is involved in cold acclimation and freezing tolerance in Arabidopsis. Plant Physiol 151:755-767.
136. Zhao R, Sheng J, Lv S, Zheng Y et al (2011) Nitric oxide participates in the regulation of LeCBF1 gene expression and improves cold tolerance in harvested tomato fruit. Postharvest Biol Technol 62:121-126.
137. Zhang YY, Wang LL, Liu YL et al (2006) Nitric oxide enhances salt tolerance in maize seedlings through increasing activities of proton-pump and Na+/H+ antiport in the tonoplast. Planta 224:545-555.
138. Zhang M, Dong J-F, Jin HH et al (2011) Ultraviolet-B-induced flavonoid accumulation in Betula pendula leaves is dependent upon nitrate reductase-mediated nitric oxide signalling. Tree Physiol 31:798-807.
139. Zhu J, Dong CH, Zhu JK (2007) Interplay between cold responsive gene regulation, metabolism and RNA processing during plant cold acclimation. Curr Opin Plant Biol 10:290-295.