Differential expression and regulation of antioxidative enzymes by cadmium in pea plants

Journal of Plant Physiology

Volumn 164, Issue 10, 2007, Pages 1346-1357

  Romero Puertas, María C ^a   Corpas, Francisco J ^a   Rodríguez Serrano, María ^a   Gómez, Manuel ^a   del Río, Luis A ^a   Sandalio, Luisa M ^a  

^a CSIC   (Spain)

Author keywords

Antioxidants; Cadmium; Oxidative stress; ROS; Signal transduction

Indexed keywords

CADMIUM; GENE EXPRESSION; METABOLISM; OXIDATIVE STRESS; PLANTS (BOTANY); SIGNAL TRANSDUCTION;

ASCORBIC ACID (ASC); CATALASE (CAT); MONODEHYDROASCORBATE REDUCTASE (MDHAR); REACTIVE OXYGEN SPECIES (ROS) METABOLISM;

ENZYMES;

PISUM SATIVUM;

EID: 34548719870     PISSN: 01761617     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jplph.2006.06.018     Document Type: Article

References (74)

1. Aebi H. Catalase in vitro. Methods Enzymol 105 (1984) 121-126
2. Asada K. Radical production and scavenging in the chloroplast. In: Barker N.R. (Ed). Photosynthesis and the environment (1996), Kluwer, Dordrecht, The Netherlands 123-320
3. Beauchamp C., and Fridovich I. Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44 (1971) 276-287
4. Ben Rejeb I., Lenne C., Leblanc N., Julien J., Ammar S., Bouzid S., et al. Iron-superoxide dismutase and monodehydroascorbate reductase transcripts accumulate in response to internode rubbing in tomato. CR Biol 327 (2004) 679-686
5. Bueno P., Varela J., Giménez-Gallego G., and del Río L.A. Peroxisomal copper,zinc superoxide dismutase: characterization of the isoenzyme from watermelon (Citrullus vulgaris Schrad.) cotyledons. Plant Physiol 108 (1995) 1151-1160
6. Bunkelmann R., and Trelease R.N. Ascorbate peroxidase. A prominent membrane protein in oilseed glyoxysomes. Plant Physiol 110 (1996) 589-598
7. Chaoui A., Mazhoudi S., Ghorbal M.H., and El Ferjani E. Cadmium and zinc induction of lipid peroxidation and effects on antioxidant enzyme activities in bean (Phaseolus vulgaris L.). Plant Sci 127 (1997) 139-147
8. Church G., and Gilbert W. Genomic sequencing. Proc Natl Acad Sci USA 81 (1984) 1991-1995
9. Clark D., Durner J., Navarre D.A., and Klessig D.F. Nitric oxide inhibition of tobacco catalase and ascorbate peroxidase. Mol Plant Microbe Interact 13 (2000) 1380-1384
10. Corpas F.J., and Trelease R.N. Differential expression of ascorbate peroxidase and a putative molecular chaperone in the boundary membrane of differentiating cucumber seedling peroxisomes. J Plant Physiol 154 (1998) 332-338
11. Corpas F., Palma J.M., Sandalio L.M., Lopez-Huertas E., Romero-Puertas M.C., Barroso J.B., et al. Purification of catalase from pea leaf peroxisomes: identification of five different isoforms. Free Rad Res 31 Suppl (1999) 235-241
12. Distefano S., Palma J., McCarthy I., and del Río L.A. Proteolytic cleavage of plant proteins by peroxisomal endoproteases from senescent pea leaves. Planta 209 (1999) 308-313
13. Dixit V., Pandey V., and Shymar R. Differential antioxidative responses to cadmium in roots and leaves of pea (Pisum sativum L. cv Azard). J Exp Bot 52 (2001) 1101-1109
14. Edwards E.A., Rawsthone S., and Mullineaux P. Subcellular distribution of multiple forms of glutathione reductase in leaves of pea (Pisum sativum L.). Planta 180 (1990) 278-284
15. Finkemeier I., Kluge C., Metwally A., Georgi M., Grotjohann N., and Dietz K.-J. Alterations in Cd-induced gene expression under nitrogen deficiency in Hordeum vulgare. Plant Cell Environ 26 (2003) 821-833
16. Foyer C.H., and Noctor G. Redox sensing and signaling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria. Physiol Plant 119 (2003) 355-364
17. Foyer C.H., and Rennenberg H. Regulation of glutathione synthesis and its role in abiotic and biotic stress. In: Brunold C., et al. (Ed). Sulfur nutrition and sulfur assimilation in higher Plants (2000), Paul Haupt, Bern, Switzerland 127-153
18. Gallego S.M., Benavides M.P., and Tomaro M.L. Effect of heavy metal ion excess on sunflower leaves: evidence for involvement of oxidative stress. Plant Sci 121 (1996) 151-159
19. Guan L.M., and Scandalios J. Catalase transcript accumulation in response to dehydration and osmotic stress in leaves of maize viviparous mutants. Redox Rep 5 (2000) 377-383
20. Halliwell B., and Gutteridge J.M.C. In: Free radicals in biology and medicine, 3rd ed (2000), Clarendon Press, Oxford
21. Harada E., Yamaguchi Y., Koizumi N., and Sano H. Cadmium stress induces production of thiol compounds and transcripts for enzymes involved in sulfur assimilation pathways in Arabidopsis. J Plant Physiol 159 (2002) 445-448
22. Hendry G.A.F., Baker A.J.M., and Ewart C.F. Cadmium tolerance and toxicity, oxygen radical processes and molecular damage in cadmium-tolerant and cadmium-sensitive clones of Holcus lanatus L. Acta Bot Neerl 41 (1992) 271-281
23. Howden R., Andersen C.R., Goldsbrough P.B., and Cobbett C. A cadmium-sensitive, glutathione-deficiente mutant of Arabidopsis thaliana. Plant Physiol 107 (1995) 1067-1073
24. Huang X., Kiefer E., Von Rad U., Ernst D., Foissner I., and Durner J. Nitric oxide burst and nitric oxide-dependent gene induction in plants. Plant Physiol Biochem 40 (2002) 625-632
25. Isin R., and Allen S.H. Isolation and characterization of a pea catalase cDNA. Plant Mol Biol 17 (1991) 1263-1265
26. Isin S.H., Burke J.J., and Allen R.D. Sequence divergence of pea Cu/Zn superoxide dismutase II cDNAs. Plant Mol Biol 15 (1990) 789-791
27. Jiang M., and Zhang J. Cross-talk between calcium and reactive oxygen species originated from NADPH oxidase in abscisic acid-induced antioxidant defence in leaves of maize seedlings. Plant Cell Environ 26 (2003) 929-939
28. Jiménez A., Hernández J.A., del Río L.A., and Sevilla F. Evidence for the presence of the ascorbate-glutathione cycle in mitochondria and peroxisomes of pea leaves. Plant Physiol 114 (1997) 275-284
29. Jonak C., and Nakagami H. Heavy metal stress. Activation of distinct mitogen-activated protein kinase pathways by copper and cadmium. Hirt Plant Physiol 136 (2004) 3276-3283
30. Knight H., and Knight M.R. Abiotic stress signalling pathways: specificity and cross-talk. Trends Plant Sci 6 (2001) 262-267
31. Lee S., and Leusteck T. The effect of cadmium on sulfate assimilation enzymes in Brassica juncea. Plant Sci 141 (1999) 201-207
32. León A.M., Palma J.M., Corpas F.J., Gómez M., Romero-Puertas M.C., Chatterjee D., et al. Antioxidative enzymes in cultivars of pepper plants with different sensitivity to cadmium. Plant Physiol Biochem 40 (2002) 813-820
33. Leterrier M., Corpas F.J., Barroso J.B., Sandalio L.M., and del Rio L.A. Peroxisomal monodehydroascorbate reductase. Genomic clone characterization and functional analysis under environmental stress conditions. Plant Physiol 138 (2005) 2111-2123
34. Lozano-Rodríguez E., Hernández L.E., Bonay P., and Carpena-Ruiz R. Distribution of Cd in pea and maize tissues. Physiological disturbances. J Exp Bot 48 (1997) 123-128
35. May M.J., Vernoux T., Leaver C., Van Montagni M., and Inzé D. Glutathione homeostasis in plants: implications for environmental sensing and plant development. J Exp Bot 49 (1998) 649-667
36. McCarthy I., Romero-Puertas M.C., Palma J.M., Sandalio L.M., Corpas F.J., Gómez M., et al. Cadmium induces senescence symptoms in leaf peroxisomes of pea plants. Plants Cell Environ 24 (2001) 1065-1073
37. Metwally A., Finkemeier I., Georgi M., and Dietz K.-J. Salicylic acid alleviates the cadmium toxicity in barley seedlings. Plant Physiol 132 (2003) 272-281
38. Mithöfer A., Schulze B., and Boland W. Biotic and heavy metal stress response in plants: evidence for common signals. FEBS Lett 66 (2004) 1-5
39. Mohan B.S., and Hosetti B.B. Potential phytotoxicity of lead and cadmium to Lemna minor grown in sewage stabilization pods. Environ Pol 98 (1997) 233-238
40. Murthy S.S., and Zilinskas B.A. Molecular cloning and characterization of a cDNA encoding pea monodehydroascorbate reductase. J Biol Chem 269 (1994) 31129-31133
41. Nocito F.F., Pirovano L., Cocucci M., and Sacchi G.A. Cadmium-induced sulfate uptake in maize roots. Plant Physiol 129 (2002) 1872-1879
42. Noctor G., and Foyer C. Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49 (1998) 249-279
43. Patra J., Lenka M., and Panda B. Tolerance and co-tolerance of the grass Chloris barbata Sw. to mercury, cadmium and zinc. New Phytol 128 (1994) 165-171
44. Poschenrieder Ch., and Barceló J. Water relations in heavy metal stressed plants. In: Prasad M.N.V., and Hagemeyer J. (Eds). Heavy metal stress in plants. From molecules to ecosystems (1999), Springer, Heidelberg 207-230
45. Prasad M.N.V. Cadmium toxicity and tolerance in vascular plants. Environ Exp Bot 35 (1995) 525-545
46. Price A.H., Taylor A., Ripley S., Griffiths A., Trewavas A.J., and Knight M.R. Oxidative signals in tobacco increase cytosolic calcium. Plant Cell 6 (1994) 1301-1310
47. del Río L., Sandalio L.M., Altomare D.A., and Zilinskas B.A. Mitochondrial and peroxisomal manganese superoxide dismutase: differential expression during leaf senescence. J Exp Bot 54 (2003) 923-933
48. del Río L.A., Sevilla F., Sandalio L.M., and Palma J.M. Nutritional effect and expression of SODs: induction and gene expression; diagnostics; prospective protection against oxygen toxicity. Free Rad Res Commun 12-13 (1991) 819-823
49. Rodríguez-Serrano M., Romero-Puertas M.C., Zabalza A., Corpas F.J., Gómez M., del Río L.A., et al. 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 (2006) 1532-1544
50. Romero-Puertas M.C., McCarthy I., Sandalio L.M., Palma J.M., Corpas F.J., Gómez M., et al. Cadmium toxicity and oxidative metabolism of pea leaf peroxisomes. Free Rad Res 31 Suppl (1999) 25-32
51. Romero-Puertas M., Palma J.M., Gómez M., del Río L.A., and Sandalio L.M. Cadmium causes the oxidative modification of proteins in pea plants. Plant Cell Environ 25 (2002) 677-686
52. Romero-Puertas M.C., Rodriguez-Serrano M., Corpas F.J., Gómez M., del Rio L.A., and Sandalio L.M. Cadmium-induced subcellular accumulation of O2. - and H2O2 in pea leaves. Plant Cell Environ 27 (2004) 1122-1134
53. Sambrook J., Fritsch E.F., Maniatis T., and Harbor N.Y. Molecular cloning: a laboratory manual, 2nd ed (1989), Cold Spring Harbor Laboratory Press, New York
54. Sandalio L., Dalurzo H.C., Gómez M., Romero-Puertas M., and del Río L.A. Cadmium-induced changes in the growth and oxidative metabolism of pea plants. J Exp Bot 52 (2001) 2115-2126
55. Sandalio L.M., and del Río L.A. Localization of superoxide dismutase in glyoxysomes from Citrullus vulgaris. Functional implications in cellular metabolism. J Plant Physiol 127 (1987) 395-409
56. Schickler H., and Caspi H. Response of antioxidative enzymes to nickel and cadmium stress in hyperaccumulator plants of the generus Alyssum. Physiol Plant 105 (1999) 39-44
57. Schützendübel A., Schwanz P., Teichmann T., Gross K., Langenfeld-Heyser R., Godbold D.L., and Polle A. Cadmium-induced changes in antioxidative systems, hydrogen peroxide content, and differentiation in Scots pine roots. Plant Physiol 75 (2001) 887-898
58. Sgherri C., Cosi E., and Navari-Izzo F. Phenols and antioxidative status of Raphanus sativus grown in copper excess. Physiol Plant 118 (2003) 21-28
59. Shaw B.P. Effect of mercury and cadmium on the activities of antioxidative enzymes in the seedlings of Phaseolus aureus. Biol Plant 37 (1995) 587-596
60. Shigeoka S., Ishikawa T., Tamoi M., Miyagawa Y., Takeda T., Yabuta Y., et al. Regulation and function of ascorbate peroxidase isoenzymes. J Exp Bot 53 (2002) 1305-1319
61. Somashekaraiah B.V., Padmaja K., and Prasad A.R.K. Phytotoxicity of cadmium ions on germinating seedlings of mung bean (Phaseolus vulgaris): involvement of lipid peroxides in chlorophyll degradation. Physiol Plant 85 (1992) 85-89
62. Stevens R., Creissen G., and Mullineaux P.M. Cloning and characterization of a cytosolic glutathione reductase cDNA from pea (Pisum sativum L.) and its expression in response to stress. Plant Mol Biol 35 (1997) 641-664
63. Streb P., Michael-Knauf A., and Feierabend J. Preferential photoinactivation of catalase and photoinhibition of photosystem II are common early symptoms under various osmotic and chemical stress conditions. Physiol Plant 88 (1993) 590-598
64. Suzuki N., Koizumi N., and Sano H. Screening off cadmium-responsive genes in Arabidopsis thaliana. Plant Cell Environ 24 (2001) 1177-1188
65. Wagner G.J. Accumulation of cadmium in crop plants and its consequences to human health. Adv Agron 51 (1993) 173-212
66. Wingsle G., and Karpinski S. Differential redox regulation by glutathione of glutathione reductase and CuZn-superoxide dismutase gene expression in Pinus sylvestris L needle. Planta 198 (1996) 151-157
67. Xiang C., and Oliver D.J. Glutathione metabolic genes coordinately respond to heavy metals and jasmonic acid in Arabidopsis. Plant Cell 10 (1998) 1539-1550
68. Yamaguchi J., and Nishimura M. Purification of glyoxysomal catalase and immunochemical comparison of glyoxysomal and leaf peroxisomal catalase in germinating pumpkin cotyledons. Plant Physiol 74 (1984) 261-267
69. Yang T., and Poovaiah B.W. Hydrogen peroxide homeostasis: activation of plant catalase by calcium/calmodulin. Proc Natl Acad Sci USA 99 (2002) 4097-4102
70. Ye B., and Gressel J. Transient, oxidant-induced antioxidant transcript and enzyme levels correlate with greater oxidant-resistance in paraquat-resistant Conyza bonariensis. Planta 211 (2000) 50-61
71. Yeh C.M., Hsiao L.J., and Huang H.J. Cadmium activates a mitogen-activated protein kinase gene and MBP kinases in rice. Plant Cell Physiol 45 (2004) 1306-1312
72. Yoon H., Lee H., Lee I.A., Kim K.Y., and Jo J. Molecular cloning of the monodehydroascorbate reductase gene from Brassica campestris and analysis of its mRNA level in response to oxidative stress. Biochim Biophys Acta 1658 (2004) 181-186
73. Zenk M.H. Heavy metal detoxification in higher plants - a review. Gene 179 (1996) 21-30
74. Zhu Y.L., Pilon-Smits E.A.H., Tarun A.S., Weber S., Jouanin L., and Terry N. Cadmium tolerance and accumulation in Indian mustard is enhanced by overexpressing g-glutamylcysteine synthetase. Plant Physiol 121 (1999) 1169-1177