Cellular response of pea plants to cadmium toxicity: Cross talk between reactive oxygen species, nitric oxide, and calcium

Plant Physiology

Volumn 150, Issue 1, 2009, Pages 229-243

  Rodríguez Serrano, María ^a,b   Romero Puertas, María C ^a   Pazmino, Diana M ^a   Testillano, Pilar S ^b   Risueno, María C ^b   Del Río, Luis A ^a   Sandalio, Luisa M ^a  

^a CSIC   (Spain)

^b CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

PISUM SATIVUM;

EID: 66149143498     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.108.131524     Document Type: Article

References (126)

1. Alvarez ME (2000) Salicylic acid in the machinery of hypersensitive cell death and disease resistance. Plant Mol Biol 44: 429-442
2. Azevedo H, Pinto CGG, Santos C (2005) Cd effects in sunflower: nutritional imbalances in plants and calluses. J Plant Nutr 28: 2221-2231
3. Azpilicueta CE, Benavides MP, Tomaro ML, Gallego SM (2007) Mechanism of CATA3 induction by Cd in sunflower leaves. Plant Physiol Biochem 45: 589-595
4. Bailey-Serres J, Mittler R (2006) The roles of reactive oxygen species in plant cells. Plant Physiol 141: 311
5. Barroso JB, Corpas FJ, Carreras A, Rodriguez-Serrano M, Esteban FJ, Fernandez-Ocana A, Chaki M, Romero-Puertas MC, Valderrama R, Sandalio LM, et al (2006) Localization of S-nitrosoglutathione and expression of S-nitrosoglutathione reductase in pea plants under Cd stress. J Exp Bot 57: 1785-1794
6. Bartha B, Kolbert Z, Erdei L (2005) Nitric oxide production induced by heavy metals in Brassica juncea L. Czern. and Pisum sativum L. Acta Biologica Szegediensis 49: 9-12
7. Békésiová B, Hras?ka S, Libantová J, Moravcikova J, Matuss?iková I (2008) Heavy-metal stress induced accumulation of chitinase isoforms in plants. Mol Biol Rep 35: 579-588
8. Benavides MP, Gallego SM, Tomaro M(2005) Cadmium toxicity in plants. Braz J Plant Physiol 17: 21-34
9. Broekaert W, Lee H, Kush A, Chua NH, Raikhel NV (1990) Woundinduced accumulation of mRNA containing a hevein sequence in laticifers of rubber tree (Hevea brasiliensis). Proc Natl Acad Sci USA 87: 7633-7637
10. Cardinaels C, Put C, Van Asche F, Clijsters H (1984) The superoxide dismutase as a biochemical indicator, discriminating between zinc and cadmium toxicity. Biol Plant 40: 131-135
11. Cheong YH, Chang HS, Gupta CR, Wang X, Zhu T, Luan S (2002) Transcriptional profiling reveals novel interactions between wounding, pathogen, abiotic stress, and hormonal responses in Arabidopsis. Plant Physiol 129: 661-677
12. ChoiHW, KimYJ, Lee SC, Hong JK,Hwang BK(2007) Hydrogen peroxide generation by the pepper extracellular peroxidase CaPO2 activates local and systemic cell death and defense response to bacterial pathogens. Plant Physiol 145: 890-904
13. Chomczynski P, Sacchi N (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162: 156-159
14. Chung SY, Lee KA, Oh KJ, Cho TJ (2005) Molecular characterization of PR4 gene in Chinese cabbage. Integr Biosci 9: 239-244
15. Clark D, Durner J, Navarre DA, Klessig DF (2000) Nitric oxide inhibition of tobacco catalase and ascorbate peroxidase. Mol Plant Microbe Interact 13: 1380-1384
16. Clemens S (2006) Toxic metal accumulation, responses to exposure and mechanisms of tolerance in plants. Biochimie 88: 1707-1719
17. Corpas FJ, Barroso JB, Carreras A, Quirós M, León A, Romero-Puertas MC, Esteban FJ, Valderrama R, Palma JM, Sandalio LM, et al (2004) Cellular and subcellular localization of endogenous nitric oxide in young and senescent pea plants. Plant Physiol 136: 2722-2733
18. Corpas FJ, Barroso JB, Carreras A, Valderrama R, Palma JM, León AM, Sandalio LM, del Río LA (2006) Constitutive arginine-dependent nitric oxide synthase activity in different organs of pea seedlings during plant development. Planta 224: 246-254
19. Dana MM, Pintor-Toro JA, Cubero B (2006) Transgenic tobacco plants overexpressing chitinases of fungal origin show enhanced resistance to biotic and abiotic stress agents. Plant Physiol 142: 722-730
20. Delledonne M, Zeier J, Marocco A, Lamb C (2001) Signal interactions between nitric oxide and reactive oxygen intermediates in the plant hypersensitive disease resistance response. Proc Natl Acad Sci USA 98: 13454-13459
21. del Río LA, Corpas FJ, Barroso JB (2004) Nitric oxide and nitric oxide synthase activity in plants. Phytochemistry 65: 783-792
22. del Río LA, Sevilla F, Sandalio LM, Palma JM(1991) Nutritional effect and expression of SODs: induction and gene expression; diagnostics; prospective protection against oxygen toxicity. Free Radic Res Commun 12-13: 819-827
23. Demontis MP, VaroniMV, Volpe AR, Emanueli C, Madeddu P (1998) Role of nitric oxide synthase inhibition in the acute hypertensive response to intracerebroventrical cadmium. Br J Pharmacol 123: 129-135
24. de Pinto MC, Tommasi F, De Gara L (2002) Changes in the antioxidant systems as part of the signalling pathway responsible for the programmed cell death activated by nitric oxide and reactive oxygen species in tobacco Bright-Yellow 2 cells. Plant Physiol 130: 698-708
25. DeRocher A, Vierling E (1995) Cytoplasmic HSP70 homologues of pea: differential expression in vegetative and embryonic organs. Plant Mol Biol 27: 441-456
26. Devoto A, Turner JG (2005) Jasmonate-regulated Arabidopsis stress signalling network. Physiol Plant 123: 161-172
27. Dixit V, Pandey V, Shymar R (2001) Differential antioxidative responses to cadmium in roots and leaves of pea (Pisum sativum L. cv Azard). J Exp Bot 52: 1101-1109
28. Durner J, Wendehenne D, Klessig DF (1998) Defense gene induction in tobacco by nitric oxide, cyclic GMP, and cyclic ADP-ribose. Proc Natl Acad Sci USA 95: 10328-10333
29. Fricker MD, Meyer AJ (2001) Confocal imaging of metabolism in vivo: pitfalls and possibilities. J Exp Bot 52: 631-640
30. Gabaldón C, Gómez LV, Pedreño MA, Ros Barceló A (2005) Nitric oxide production by the differentiating xylem of Zinnia elegans. New Phytol 165: 121-130
31. Gallego SM, Benavides MP, Tomaro ML (1996) Effect of heavy metal ion excess on sunflower leaves: evidence for involvement of oxidative stress. Plant Sci 121: 151-159
32. García-Mata C, Lamattina L (2002) Nitric oxide and abscisic acid cross talk in guard cells. Plant Physiol 128: 790-792
33. Garnier L, Simon-Plas F, Thuleau P, Agnel JP, Blein JP, Ranjeva R, Montillet JL (2006) Cd affects tobacco cells by a series of three waves of reactive oxygen species that contribute to cytotoxicity. Plant Cell Environ 29: 1956-1969
34. Garrido I, Espinosa F, Córdoba-Pedregosa MC, González-Reyes JA, Alvarez-Tinaut MC (2003) Redox-related peroxidative responses evoked bymethyl-jasmonate in axenically cultured aeroponic sunflower (Helianthus annuus L.). Protoplasma 221: 79-91
35. Gomes-Junior RA, Moldes CA, Delite FS, Pompeu GB, Gratao PL, Mazzafera P, Lea PJ, Azevedo RA (2006) Antioxidant metabolism of coffee cell suspension cultures in response to cadmium. Chemosphere 65: 1330-1337
36. Gould KS, Lamotte O, Klinguer A, Pugin A, Wedehenne D (2003) Nitric oxide production in tobacco leaf cells: a generalized stress response? Plant Cell Environ 26: 1851-1862
37. Grün S, Lindermayr C, Sell S, Durner J (2006) Nitric oxide and gene regulation in plants. J Exp Bot 57: 507-516
38. Guo H, Ecker JR (2004) The ethylene signaling pathway: new insights. Curr Opin Plant Biol 7: 40-49
39. Gussarson M, Asp H, Adalsteinsson S, Jensén P (1996) Enhancement of Cd effects on growth and nutrient composition of birch (Betula pendula) by buthionine sulphoxinine (BSO). J Exp Bot 47: 211-215
40. Hernández LE, Lozano-Todróguez E, Gárate A, Carpena-Ruíz R (1998) Influence of Cd on the uptake, tissue accumulation and subcellular distribution of manganese in pea seedlings. Plant Sci 132: 139-151
41. Howarth JR, Domínguez-Solís JR, Gutiérrez- Alcalá G, Wray JL, Romero LC, Gotor C (2003) The serine acetyltransferase gene family in Arabidopsis thaliana and the regulation of its expression by cadmium. Plant Mol Biol 51: 589-598
42. Ignarro LJ (2002) Nitric oxide as a unique signaling molecule in the vascular system: a historical overview. J Physiol Pharmacol 53: 503-514
43. Illés? P, Schlicht M, Pavlovkin J, Lichtscheidl I, Balus?ka F, Ovecka M (2006) Aluminium toxicity in plants: internalization of aluminium into cells of the transition zone in Arabidopsis root apices related to changes in plasma membrane potential, endosomal behavior, and nitric oxide production. J Exp Bot 57: 4201-4213
44. Jiménez A, Hernández JA, del Río LA, Sevilla F (1997) Evidence for the presence of the ascorbate-glutathione cycle in mitochondria and peroxisomes of pea leaves. Plant Physiol 114: 275-284
45. Kasprzewska A (2003) Plant chitinases: regulation and function. Cell Mol Biol Lett 8: 809-824
46. Kim Y, Yang YY, Lee Y (2002) Pb and Cd uptake in rice toots. Physiol Plant 116: 368-372
47. Kinraide TB (1998) Three mechanisms for the calcium alleviation of mineral toxicities. Plant Physiol 118: 513-520
48. Kinraide TB, Parker DR (1987) Cation amelioration of aluminium toxicity in wheat. Plant Physiol 83: 546-551
49. Kinraide TB, Perler JF, Parker DR (2004) Relative effectiveness of calcium and magnesium in the alleviation of rhizotoxicity in wheat induced by copper, zinc, aluminum, sodium, and low pH. Plant Soil 259: 201-208
50. Kopyra M, Gwózdz EA (2003) Nitric oxide stimulates seed germination and counteracts the inhibitory effect of heavy metals and salinity on root growth of Lupinus luteus. Plant Physiol Biochem 41: 1011-1017
51. Kopyra M, Stachín-Wilk M, Gwóždž EA (2006) Effect of exogenous nitric oxide on the antioxidant capacity of cadmium-treated soybean cell suspension. Acta Physiol Plant 28: 525-536
52. Laspina NV, Groppa MD, Tomaro ML, Benavides MP (2005) Nitric oxide protects sunflower leaves against Cd-induced oxidative stress. Plant Sci 169: 323-330
53. Lee SC, Hwang BK (2003) Identification of the pepper SAR8.2 gene as a molecular marker for pathogen infection, abiotic elicitors and environmental stresses in Capsicum annuum. Planta 216: 387-396
54. Leshem YY (1996) Nitric oxide in biological systems. Plant Growth Regul 18: 155-159
55. Leshem YY (2000) Nitric Oxide in Plants: Occurrence, Function and Use. Kluwer Academic Press, Dordrecht, The Netherlands Leshem YY, Haramaty E (1996) The characterization and contrasting effects of the nitric-oxide free radical in vegetative stress and senescence of Pisum sativum Linn. foliage. J Plant Physiol 148: 258-263
56. Lindermayr C, Saalbach G, Bahnweg G, Durner J (2006) Differential inhibition of Arabidopsis methionine adenosyltransferases by protein S-nitrosylation. J Biol Chem 281: 4285-4291
57. Lozano-Rodriguez E, Hernández LE, Bonay P, Carpena-Ruiz RO (1997) Distribution of Cd in shoot and root tissues of maize and pea plants: physiological disturbances. J Exp Bot 48: 123-128
58. Lu YT, Harrington HM (1994) Isolation of tobacco cDNA clones encoding calmodulin-binding proteins and characterization of a known calmodulin-binding domain. Plant Physiol Biochem 32: 413-422
59. Ma CH, Haslbeck M, Babujee L, Jahn O, Reumann S (2006) Identification and characterization of a stress-inducible and a constitutive small heatshock protein targeted to the matrix of plant peroxisomes. Plant Physiol 141: 47-60
60. Magalhaes JR, Pedroso MC, Durzan D (1999) Nitric oxide, apoptosis and plant stress. Physiol Mol Biol Plant 5: 115-125
61. Maksymiec W, Malgorzata W, Krupa Z (2007) Variation in oxidative stress and photochemical activity in Arabidopsis thaliana leaves subjected to Cd and excess copper in the presence or absence of jasmonate and ascorbate. Chemosphere 66: 421-427
62. Marone M, Mozzetti S, De Ritis D, Pierelli L, Scambia G (2001) Semiquantitative RT-PCR analysis to assess the expression levels of multiple transcripts from the same sample. Biol Proced Online 3: 19-25
63. Massonneau A, Coronado MJ, Audran A, Bagniewska-Zadworna A, Mol R, Testillano PS, Goralski G, Dumas C, Risueñ oMC,Matthys-Rochon E (2005) Multicellular structures that develop during in vitro maize pollen embryogenesis express both endosperm- and embryo-specific genes: which is which? Eur J Cell Biol 84: 663-675
64. McCarthy I, Romero-Puertas MC, Palma JM, Sandalio LM, Corpas FJ, Gómez M, del Río LA (2001) Cadmium induces senescence symptoms in leaf peroxisomes of pea plants. Plant Cell Environ 24: 1065-1073
65. McDowell JM, Dangl JL (2000) Signal transduction in the plant immune response. Trends Biochem Sci 25: 79-82
66. Metwally A, Finkemeier I, Georgi M, Dietz KJ (2003) Salicylic acid alleviates the cadmium toxicity in barley seedling. Plant Physiol 132: 272-281
67. Miller G, Mittler R (2006) Could heat shock transcription factors function as hydrogen peroxide sensor in plants? Ann Bot (Lond) 98: 279-288
68. Milone MT, Sgherri C, Clijsters H, Navarri-Izzo F (2003) Antioxidant responses of wheat treated with realistic concentration of cadmium. Environ Exp Bot 50: 265-276
69. Moncada S, Palmer RM, Higgs EA (1991) Nitric oxide: physiology, pathophysiology, and pharmacology. Pharmacol Rev 43: 109-142
70. Neill S, Bright J, Desikan R, Hanckock J, Harrison J,Wilson I (2008) Nitric oxide evolution and perception. J Exp Bot 59: 25-35
71. Neill SJ, Desikan R, Clarke A, Hancock JT (2002) Nitric oxide is a novel component of abscisic acid signalling in stomatal guard cells. Plant Physiol 128: 13-16
72. Nocito FF, Lancilli C, Crema B, Fourcroy P,Davidian JC, Sacchi GA(2006) Heavy metal stress and sulfate uptake in maize roots. Plant Physiol 141: 1138-1148
73. Noctor G, Arisi A, Jouanin L, Renneberger H, Foyer C (1998) Glutathione: biosynthesis, metabolism and relationship to stress tolerance explored in transformed plants. J Exp Bot 49: 623-647
74. Obregón P, Marín R, Sanz A, Castresana C (2001) Activation of defencerelated genes during senescence: a correlation between gene expression and cellular damage. Plant Mol Biol 46: 67-77
75. Ogawa K, Kanematsu S, Asada K (1997) Generation of superoxide anion and localization of CuZn-superoxide dismutase in the vascular tissue of spinach hypocotyls: their association with lignification. Plant Cell Physiol 38: 1118-1126
76. Olmos E, Martinez-Solano JR, Piqueras A, Hellin E (2003) Early steps in the oxidative burst induced by cadmium in cultured tobacco cells (BY-2 line). J Exp Bot 54: 291-301
77. Orozco-Cardenas M, Ryan CA (1999) Hydrogen peroxide is generated systemically in plant leaves by wounding and systemin via the octadecanoid pathway. Proc Natl Acad Sci USA 96: 6553-6557
78. Ortega-Villasante C, Rellán-Á lvarez ZZ, Del Campo FF, Carpena-Ruiz RO, Hernandez LE (2005) Cellular damage induced by Cd and mercury in Medicago sativa. J Exp Bot 56: 2239-2251
79. Pedroso MC, Durzan DJ (2000) Effect of different gravity environments of DNA fragmentation and cell death in Kalanchoë leaves. Ann Bot (Lond) 86: 983-994
80. Pinto AP, Mota AM, De Varennes A, Pinto FC (2004) Influence of organic matter on the uptake of cadmium, zinc, copper and iron by sorghum plants. Sci Total Environ 326: 239-274
81. Rakwal R, Yang G, Komatsu S (2004) Chitinase induced by jasmonic acid, methyl jasmonate, ethylene and protein phosphatase inhibitors in rice. Mol Biol Rep 31: 113-119
82. Rentel MC, Knight MR (2004) Oxidative stress-induced calcium signaling in Arabidopsis. Plant Physiol 135: 1471-1479
83. Ribeiro EA, Cunha FQ, Tamashiro WMSC, Martins IS (1999) Growth phase-dependent subcellular localization of nitric oxide synthase in maize cells. FEBS Lett 445: 283-286
84. 2+ toxicity during the early phases of radish (Raphanus sativus L.) seed germination. Plant Cell Environ 20: 600-608
85. Roberts DM, Harmon AC (1993) Calcium-modulated proteins: targets of intracellular calcium signals in higher-plants. Annu Rev Plant Physiol Plant Mol Biol 43: 375-414
86. Rockel P, Strube F, Rockel A, Wildt J, Kaiser WM (2002) Regulation of nitric oxide (NO) production by plant nitrate reductase in vivo and in vitro. J Exp Bot 53: 103-110
87. Rodríguez-Serrano M, Romero-Puertas MC, Zabalza A, Corpas FJ, Gómez M, del Río LA, Sandalio LM (2006) Cadmium effect on oxidative metabolism of pea (Pisum sativum L.) roots: imaging of reactive oxygen species and nitric oxide accumulation in vivo. Plant Cell Environ 29: 1532-1544
88. Rogers EE, Eide DJ, Guerinot ML (2000) Altered selectivity in an Arabidopsis metal transporter. Proc Natl Acad Sci USA 97: 12356-12360
89. Romero-Puertas MC, Corpas FJ, Rodriguez-Serrano M, Gomez M, del Río LA, Sandalio LM (2007) Differential expression and regulation of antioxidative enzymes by Cd in pea plants. J Plant Physiol 164: 1346-1357
90. Romero-Puertas MC, Delledonne M (2003) Nitric oxide signalling in plant-pathogen interactions. IUBMB Life 55: 579-583
91. Romero-Puertas MC, McCarthy I, Sandalio LM, Palma JM, Corpas FJ, Gómez M, del Río LA (1999) Cadmium toxicity and oxidative metabolism in pea leaf peroxisomes. Free Radic Res (Suppl) 31: 25-31
92. Romero-Puertas MC, Palma JM, Gómez M, del Río LA, Sandalio LM (2002) Cadmium causes the oxidative modification of proteins in pea plants. Plant Cell Environ 25: 677-686
93. 2 in pea leaves. Plant Cell Environ 27: 1122-1134
94. - generating system from the lignifying xylem of Zinnia elegans. Free Radic Res (Suppl) 31: S147-S154
95. alt DE, Prince RC, Pickering IJ, Raskin I (1995) Mechanism of cadmium mobility and accumulation in Indian mustard. Plant Physiol 109: 1427-1433
96. Sandalio LM, Dalurzo HC, Gómez M, Romero-Puertas MC, del Río LA (2001) Cadmium-induced changes in the growth and oxidative metabolism of pea plants. J Exp Bot 52: 2115-2126
97. Sandalio LM, Rodríguez-Serrano M, Romero-Puertas M, del Río LA (2008) Imaging of reactive oxygen species and NO in vivo in plant tissues. Methods Enzymol 440: 399-409
98. Sanitá di Toppi L, Gabbrielli R (1999) Response to cadmium in higher plants. Environ Exp Bot 41: 105-130
99. Sävestrand H, Brosché M, Ä ngehagen M, Strid A (2000) Molecular markers for ozone stress isolated by suppression subtractive hybridization: specificity of gene expression and identification of a novel stressregulated gene. Plant Cell Environ 23: 689-700
100. Schickler H, Caspi H (1999) Response of antioxidative enzymes to nickel and cadmium stress in hyperaccumulator plants of the genus Alyssum. Physiol Plant 105: 39-44
101. Schmitz-Eiberger M, Haefs R, Noga G (2002) Calcium deficiency: influence in the antioxidative defense system in tomato plants. J Plant Physiol 159: 733-742
102. Schü tzendü bel A, Schwanz P, Terchmann T, Grossk Langeenfeld-Heyger R, Godbold DL, Polle A (2001) Cadmium-induced changes in antioxidative systems, hydrogen peroxide content, and differentiation in Scots pine roots. Plant Physiol 75: 887-898
103. Shaw BP (1995) Effect of mercury and cadmium on the activities of antioxidative enzymes in the seedling of Phaseolus aureus. Biol Plant 37: 587-596
104. Shukla UC, Singh J, Joshi PC, Kakkar P (2003) Effect of bioaccumulation of cadmium on biomass productivity, essential trace elements, chlorophyll biosynthesis, and macromolecules of wheat seedlings. Biol Trace Elem Res 92: 257-274
105. Somashekaraiah BV, Padmaja K, Prasad ARK (1992) Phytotoxicity of cadmium ions on germinating seedlings of mung bean (Phaseolus vulgaris): involvement of lipid peroxides in chlorophyll degradation. Physiol Plant 85: 85-89
106. Stoch SJ, Bagchi D (1995) Oxidative mechanism in the toxicity of metal ions. Free Radic Biol Med 18: 321-336
107. Stressmann M, Kitao S, Griffith M,Moresoli C, Bravo LA,Marangoni AG (2004) Calcium interacts with antifreeze proteins and chitinase from cold-acclimated winter rye. Plant Physiol 135: 364-376
108. Sunkar R, Kapoor A, Zhu JK (2006) Posttranscriptional induction of two Cu/Zn superoxide dismutase genes in Arabidopsis is mediated by downregulation of miR398 and important for oxidative stress tolerance. Plant Cell 18: 2051-2065
109. Suzuki N (2005) Alleviation by calcium of cadmium-induced root growth inhibition in Arabidopsis seedling. Plant Biotechnol 22: 19-25
110. Suzuki N, Koizumi N, Sano H (2001) Screening of cadmium-responsive genes in Arabidopsis thaliana. Plant Cell Environ 24: 1177-1188
111. Tateishi Y, Umenura Y, Muneharu E (2001) A basic class I chitinase expression in winged bean is up-regulated by osmotic stress. Biosci Biotechnol Biochem 65: 1663-1668
112. Thomma B, Penninckx I, Broekaert WF, Cammue BP (2001) The complexity of disease signalling in Arabidopsis. Curr Opin Immunol 13: 63-68
113. Tian QY, Sun DH, Zhao MG, Zhang WH (2007) Inhibition of nitric oxide synthase (NOS) underlies aluminium-induced inhibition of root elongation in Hibiscus moscheutos. New Phytol 174: 322-331
114. Tsyganov VE, Belimov AA, Borisov AY, Safronova VI, Georgi M, Dietz KJ, Tikhonovich IA (2007) A chemically induced new pea (Pisum sativum) mutant SGECdt with increased tolerance to, and accumulation of, cadmium. Ann Bot (Lond) 99: 227-237
115. Vigliocco A, Bonamico B, Alemano S, Miersch O, Abdala G (2002) Stimulation of jasmonic acid production in Zea Mays L. infected by the maize rough dwarf virus - Río Cuarto. Reversion of symptoms by salicylic acid. Biocell 26: 369-374
116. Vitó ria AP, Lea PJ, Azevedo RA (2001) Antioxidant enzymes responses to cadmium in radish tissues. Phytochemistry 57: 701-710
117. Wang JW, Wu JY (2005) Nitric oxide is involved in methyl jasmonateinduced defense responses and secondary metabolism activities of Taxus cells. Plant Cell Physiol 46: 923-930
118. WangW, Vinocur B, Shoseyov O, Altman A (2004) Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci 9: 244-252
119. Wasternack C, Parthier B (1997) Jasmonate-signalled plant gene expression. Trends Plant Sci 2: 302-307
120. Wu CT, Bradford KJ (2003) Class I chitinase and b-1-3-glucanase are differentially regulated by wounding, methyl jasmonate, ethylene, and gibberellin in tomato seeds and leaves. Plant Physiol 113: 263-273
121. Wubben JP, Lawrence CB, de Wit PJGM (1996) Differential induction of chitinase and 1,3-b-glucanase gene expression in tomato by Cladosporium fulvum and its race-specific elicitors. Physiol Plant Pathol 48: 105-116
122. Xiang C, Oliver DJ (1998) Glutathione metabolic genes coordinately respond to heavy metals and jasmonic acid in Arabidopsis. Plant Cell 10: 1539-1550
123. Yang T, Poovaiah BW (2002) Hydrogen peroxide homeostasis: activation of plant catalase by calcium/calmodulin. Proc Natl Acad Sci USA 19: 4097-4102
124. ZangH, Jiang Y, He Z, MaM(2005) Cadmium accumulation and oxidative burst in garlic (Allium sativum). J Plant Physiol 162: 977-984
125. Zemojtel T, Fröhlich A, Palmieri MC, Kolanczyk M, Mikula I, Wyrwicz LS, Wanker EE, Mundlos S, Vingron M, Martasek P, et al (2006) Plant nitric oxide synthase: a never-ending story? Trends Plant Sci 11: 524-528
126. Zenk MH (1996) Heavy metal detoxification in higher plants: a review. Gene 179: 21-30