Mitochondrial and peroxisomal manganese superoxide dismutase: Differential expression during leaf senescence

Journal of Experimental Botany

Volumn 54, Issue 384, 2003, Pages 923-933

  Del Río, Luis A ^b   Sandalio, Luisa M ^b   Altomare, Deborah A ^a,c   Zilinskas, Barbara A ^a  

^a RUTGERS UNIVERSITY   (United States)

^b CSIC   (Spain)

^c FOX CHASE CANCER CENTER   (United States)

Author keywords

Differential expression; Immunocytochemical localization; Manganese superoxide dismutase; Mitochondria; Peroxisomes; Pisum sativum L.; Senescence; Superoxide dismutase

Indexed keywords

ANTIBODIES; DNA; ELECTROPHORESIS; GENETIC ENGINEERING; PLANTS (BOTANY);

MITOCHONDRIA;

ENZYMES;

APOPTOSIS; BLOTTING, NORTHERN; BLOTTING, WESTERN; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, PLANT; MICROSCOPY, IMMUNOELECTRON; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; PEAS; PEROXISOMES; PLANT LEAVES; SUPEROXIDE DISMUTASE;

PISUM; PISUM SATIVUM;

EID: 0242585515     PISSN: 00220957     EISSN: None     Source Type: Journal    
DOI: 10.1093/jxb/erg091     Document Type: Article

References (74)

1. Alscher RG, Ertuk N, Heath LS. 2002. Role of superoxide dismutases (SODs) in controlling oxidative stress in plants. Journal of Experimental Botany 53, 1331-1341.
2. Altomare DA. 1992. Copper/zinc- and manganese-superoxide dismutases in pea: molecular cloning of cDNAs and regulation of superoxide dismutase gene expression. PhD thesis. Rutgers University, New Brunswick, NJ, 170 pp. MSU Dissertation Abstracts 54, no. 03B: 1224.
3. Bannister JV, Bannister WH, Rotilio G. 1987. Aspects of the structure, function and applications of superoxide dismutase. Critical Revews in Biochemistry 22, 111-180.
4. Baum JA, Scandalios JG. 1981. Isolation and characterization of the cytosolic and mitochondrial superoxide dismutases of maize. Archives of Biochemistry and Biophysics 206, 249-264.
5. Beauchamp C, Fridovich I. 1971. Superoxide dismutase. Improved assays and an assay applicable to acrylamide gels. Analytical Biochemistry 44, 276-287.
6. Bolwell GP. 1999. Role of reactive oxygen species and NO in plant defence responses. Current Opinion in Plant Biology 2, 287-294.
7. Bowler C, Van Montagu M, Inzé D. 1992. Superoxide dismutase and stress tolerance. Annual Review of Plant Physiology and Plant Molecular Biology 43, 83-116.
8. Bradford MM. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248-254.
9. Bueno P, Varela J, Giménez-Gallego G, del Río LA. 1995. Peroxisomal copper,zinc superoxide dismutase: characterization of the isoenzyme from water-melon cotyledons. Plant Physiology 108, 1151-1160.
10. Bunkelmann JR, Trelease RN. 1996. Ascorbate peroxidase: a prominent membrane protein in oilseed glyoxysomes. Plant Physiology 110, 589-598.
11. Casano LM, Martín M, Sabater B. 1994. Sensitivity of superoxide dismutase transcript levels and activities to oxidative stress is lower in mature-senescent than in young barley leaves. Plant Physiology 106, 1033-1039.
12. Chomczynski P, Sacchi N. 1987. Single-step method of RNA isolation by guanidinium thiocyanate-phenol-chloroform extraction. Analytical Biochemistry 162, 156-159.
13. Corpas FJ, Barroso JB, del Río LA. 2001. Peroxisomes as a source of reactive oxygen species and nitric oxide signal molecules in plant cells. Trends in Plant Science 6, 145-150.
14. Corpas FJ, Bunkelmann JR, Trelease RN. 1994. Identification and immunochemical characterization of a family of peroxisome membrane proteins (PMPs) in oilseed glyoxysomes. European Journal of Cell Biology 65, 280-290.
15. Corpas FJ, Palma JM, del Río LA. 1993. Evidence for the presence of proteolytic activity in peroxisomes. European Journal of Cell Biology 61, 81-85.
16. Corpas FJ, Sandalio LM, del Río LA, Trelease RN. 1998. Copper-zinc superoxide dismutase is a constituent enzyme of the matrix of peroxisomes in the cotyledons of oilseed plants. New Phytologist 138, 307-314.
17. Dat J, Vandenabeele S, Vranová E, Van Montagu M, Inzé D, Van Breusegem F. 2000. Dual action of the active oxygen species during plant stress responses. Cellular and Molecular Life Sciences 57, 779-795.
18. del Río LA, Corpas FJ, Sandalio LM, Palma JM, Gómez M, Barroso JB. 2002. Reactive oxygen species, antioxidant systems and nitric oxide in peroxisomes. Journal of Experimental Botany 53, 1255-1272.
19. del Río LA, Lyon DS, Olah I, Glick B, Salin ML. 1983. Immunocytochemical evidence for a peroxisomal localization of manganese superoxide dismutase in leaf protoplasts from a higher plant. Planta 158, 216-224.
20. del Río LA, Palma JM, Sandalio LM, Corpas FJ, Pastori GM, Bueno P, López-Huertas E. 1996. Peroxisomes as a source of superoxide and hydrogen peroxide in stressed plants. Biochemical Society Transactions 24, 434-438.
21. del Río LA, Pastori GM, Palma JM, Sandalio LM, Sevilla F, Corpas FJ, Jiménez A, López-Huertas E, Hernández JA. 1998. The activated oxygen role of peroxisomes in senescence. Plant Physiology 116, 1195-1200.
22. del Río LA, Sandalio LM, Palma JM, Bueno P, Corpas FJ. 1992. Metabolism of oxygen radicals in peroxisomes and cellular implications. Free Radical Biology and Medicine 13, 557-580.
23. del Río LA, Sandalio LM, Yánez J, Gómez M. 1985. Induction of a manganese-containing superoxide dismutase in leaves of Pisum sativum L. by high nutrient levels of zinc and manganese. Journal of Inorganic Biochemistry 24, 25-34.
24. del Río LA, Sevilla F, Gómez M, Yáñez J, López-Gorgé J. 1978. Superoxide dismutase: an enzyme system for the study of micronutrient interactions in plants. Planta 140, 221-225.
25. 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 Radical Research Communications 12-13, 819-827.
26. Distefano S, Palma JM, Gómez M, del Río LA. 1997. Characterization of endoproteases from plant peroxisomes. Biochemical Journal 327, 399-405.
27. Distefano S, Palma JM, McCarthy I, del Río LA. 1999. Proteolytic cleavage of plant proteins by peroxisomal endoproteases from senescent pea leaves. Planta 209, 308-313.
28. Duke MV, Salin ML. 1983. Isoenzymes of Cu,Zn-SOD from Pisum sativum. Phytochemistry 22, 2369-2373.
29. Edwards EA, Enard C, Creissen GP, Mullineaux PM. 1994. Synthesis and properties of glutathione reductase in stressed peas. Planta 192, 37-143.
30. Fernández VM, Sevilla F, López-Gorgé J, del Río LA. 1982. Evidence for manganese(III) binding to the mangano superoxide dismutase from a higher plant (Pisum sativum L.). Journal of Inorganic Biochemistry 16, 79-84.
31. Fridovich I. 1995. Superoxide radical and superoxide dismutases. Annual Review of Biochemistry 64, 97-112.
32. Friedman KD, Rosen NL, Newman PJ, Montgomery RR. 1990. Screening of λgtII4 libraries. In: Innis MA, Gelfand DHñ, Sninsky JJ, White TJ, eds. PCR protocols. New York: Academic Press, 253-258.
33. Gantt JS, Key JL. 1986. Isolation of nuclear encoded plastid ribosomal protein cDNAs. Molecular and General Genetics 202, 186-193.
34. Grant JJ, Loake GJ. 2000. Role of reactive oxygen intermediates and cognate redox signalling in plant disease resistance. Plant Physiology 124, 21-29.
35. Halliwell B, Gutteridge JMC. 2000. Free radicals in biology and medicine, 3rd edn. Oxford, UK: Oxford University Press.
36. Harris CA, Andryuk PJ, Cline S, Chan HK, Natarajan A, Siekierka JJ, Goldstein G. 1994. Three distinct human thymopoietins are derived from alternatively spliced mRNAs. Proceedings of the National Academy of Sciences, USA 91, 6283-6287.
37. Jacob C, Courbot M, Brun A, Steinman HW, Jacquot J-P, Botton B, Chalot M. 2001. Molecular cloning, characterization and regulation by cadmium of a superoxide dismutase from the ectomycorrhizal fungus Paxillus involutus. European Journal of Biochemistry 268, 3223-3232.
38. Jiménez A, Herńandez JA, Pastori GM, del Río LA, Sevilla F. 1998. Role of the ascorbate-glutathione cycle of mitochondria and peroxisomes in the senescence of pea leaves. Plant Physiology 118, 1327-1335.
39. Kar M, Feierabend J. 1984. Metabolism of activated oxygen in detached wheat and rye leaves and its relevance to the initiation of senescence. Planta 160, 385-391.
40. 2. Physiologia Plantarum 85, 689-696.
41. Kröniger W, Rennenberg H, Tadros MH, Polle A. 1995. Purification and properties of manganese superoxide dismutase from Norway spruce (Picea abies L. Karst). Plant and Cell Physiology 36, 191-196.
42. Laemmli UK. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
43. Larsson L-I. 1988. Immunocytochemistry: theory and practice. Boca Raton, FL: CRC Press.
44. López-Huertas E, Baker A. 1999. Peroxisome biogenesis. In: Broome-Smith JK, Baumberg S, Stirling CJ, Ward FB, eds, Transport of molecules across microbial membranes. Society for General Microbiology. Cambridge: Cambridge University Press, 204-238.
45. López-Huertas E, Sandalio LM, del Río LA. 1995. Integral membrane polypeptides of pea leaf peroxisomes: characterization and response to plant stress. Plant Physiology and Biochemistry 33, 295-302.
46. Mano S, Yamaguchi K, Hayashi M, Nishimura M. 1997. Stromal and thylakoid-bound ascorbate peroxidases are produced by alternative splicing in pumpkin. FEBS Letters 413, 21-26.
47. Mano S, Hayashi M, Nishimura M. 1999. Light regulates alternative splicing of hydroxypyruvate reductase in pumpkin. The Plant Journal 17, 309-320.
48. 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 and Environment 24, 1065-1073.
49. Mittler R, Zilinskas BA. 1994. Regulation of pea cytosolic ascorbate peroxidase and other antioxidant enzymes during the progression of drought stress and following recovery from drought. The Plant Journal 5, 397-405.
50. Mullen RT, Trelease RN. 1996. Biogenesis and membrane properties of peroxisomes: does the boundary membrane serve and protect? Trends in Plant Science 1, 389-394.
51. Nishimura M, Akhmedov YD, Akazawa T. 1983. Molecular structure and subcellular localization of spinach leaf glycolate oxidase. Photosynthesis Research 4, 99-109.
52. Noctor G, Foyer CH. 1998. Ascorbate and glutathione: keeping active oxygen under control. Annual Review of Plant Physiology and Plant Molecular Biology 49, 249-279.
53. Palma JM, Sandalio LM, del Río LA. 1986. Manganese superoxide dismutase and higher plant chloroplasts: a reappraisal of a controverted cellular localization. Journal of Plant Physiology 125, 427-439.
54. Palma JM, López-Huertas E, Corpas F J, Sandalio LM, Gómez M, del Río LA. 1998. Peroxisomal manganese superoxide dismutase: purification and properties of the isozyme from pea leaves. Physiologia Plantarum 104, 720-726.
55. Pastori GM, del Río LA. 1994a. An activated-oxygen-mediated role for peroxisomes in the mechanism of senescence of Pisum sativum L. leaves. Planta 193, 385-391.
56. Pastori GM, del Río LA. 1994b. Activated oxygen species and superoxide dismutase activity in peroxisomes from senescent pea leaves. Proceedings of the Royal Society of Edinburgh 102B, 505-509.
57. Pastori GM, del Río LA. 1997. Natural senescence of pea leaves: an activated oxygen-mediated function for peroxisomes. Plant Physiology 113, 411-418.
58. Romero-Puertas MC, Sandalio LM, Palma JM, Gómez M, del Río LA. 2002. Cadmium causes the oxidative modification of proteins in pea plants. Plant, Cell and Environment 25, 677-686.
59. 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. Journal of Experimental Botany 52, 2115-2126.
60. Sandalio LM, López-Huertas E, Bueno P, del Río LA. 1997. Immunocytochemical localization of copper,zinc superoxide dismutase in peroxisomes from watermelon (Citrullus vulgaris Schrad.) cotyledons. Free Radical Research 26, 187-194.
61. Sandalio LM, Palma JM, del Río LA. 1987. Localization of manganese superoxide dismutase in peroxisomes isolated from Pisum sativum L. Plant Science 51, 1-8.
62. 2-induced oxidative stress in Populusxcanescens roots. Plant Physiology and Biochemistry 40, 577-584.
63. Sevilla F, López-Gorgé J, Gómez M, del Río LA. 1980a. Manganese superoxide dismutase from a higher plant: purification of a new Mn-containing enzyme. Planta 150, 153-157.
64. Sevilla F, López-Gorgé J, del Río LA. 1980b. Preliminary characterization of a Mn-containing superoxide dismutase from a higher plant (Pisum sativum L.). In: Bannister JV, Hill HAO, eds. Chemical and biochemical aspects of superoxide and superoxide dismutase. North-Holland, New York: Elsevier, 185-195.
65. Sevilla F, López-Gorgé J, del Río LA. 1982. Characterization of a manganese superoxide dismutase from the higher plant Pisum sativum L. Plant Physiology 70, 1321-1326.
66. Srinivasan M, Edman CF, Schulman H. 1994. Alternative splicing introduces a nuclear localization signal that targets multifunctional CaM kinase to the nucleus. Journal of Cell Biology 126, 839-852.
67. Steinman HM. 1982. Superoxide dismutases: protein chemistry and structure-function relationships. In: Oberley LW, ed. Superoxide dismutase, Vol. 1. Boca Ratón, FL: CRC Press, 11-68.
68. Streller S, Krömer S, Wingsle G. 1994. Isolation and purification of mitochondrial Mn-superoxide dismutase from the gymnosperm Pinus sylvestris L. Plant and Cell Physiolology 35, 859-867.
69. Thompson JE, Ledge RL, Barber RF. 1987. The role of free radicals in senescence and wounding. New Phytologist 105, 317-344.
70. Van Camp W, Hérouart D, Willekens H, Takahashi H, Saito K, Van Montagu M, Inzé D. 1996. Tissue-specific activity of two manganese superoxide dismutase promoters in transgenic tobacco. Plant Physiology 112, 525-535.
71. 2 and NO: redox signals in disease resistance. Trends in Plant Science 3, 330-334.
72. White JA, Scandalios JG. 1988. Isolation and characterization of a cDNA for mitochondrial manganese superoxide dismutase (SOD-3) of maize and its relation to other manganese superoxide dismutases. Biochimica et Biophysica Acta 951, 61-70.
73. Wong-Vega L, Burke JJ, Allen RD. 1991. Isolation and sequence analyis of a cDNA that encodes pea manganese superoxide dismutase. Plant Molecular Biology 17, 1271-1274.
74. Zhu D, Scandalios JG. 1993. Maize mitochondrial manganese superoxide dismutases are encoded by a differentially expressed multigene family. Proceedings of the National Academy of Sciences, USA 90, 9310-9314.