Rice ascorbate peroxidase gene family encodes functionally diverse isoforms localized in different subcellular compartments

Planta

Volumn 224, Issue 2, 2006, Pages 300-314

  Teixeira, Felipe Karam ^a   Menezes Benavente, Larissa ^a,c   Galvão, Vinícius Costa ^a   Margis, Rogério ^b   Margis Pinheiro, Márcia ^a,b  

^a FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^b FEDERAL UNIVERSITY OF RIO GRANDE DO SUL   (Brazil)

^c NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

Antioxidant metabolism; Ascorbate peroxidase; BY 2 tobacco cells; Green fluorescent protein; Oryza

Indexed keywords

ASCORBATE PEROXIDASE; HYBRID PROTEIN; INORGANIC SALT; ISOENZYME; MESSENGER RNA; PEROXIDASE;

ARTICLE; CELL FRACTIONATION; CYTOLOGY; DRUG EFFECT; ENZYMOLOGY; FLOWER; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; NORTHERN BLOTTING; PLANT LEAF; PLANT STEM; PROTEIN TRANSPORT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RICE; SEEDLING; SOUTHERN BLOTTING; TOBACCO; TRANSGENIC PLANT;

BLOTTING, NORTHERN; BLOTTING, SOUTHERN; FLOWERS; GENE EXPRESSION REGULATION, PLANT; ISOENZYMES; ORYZA SATIVA; PEROXIDASES; PLANT LEAVES; PLANT STEMS; PLANTS, GENETICALLY MODIFIED; PROTEIN TRANSPORT; RECOMBINANT FUSION PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SALTS; SEEDLING; SUBCELLULAR FRACTIONS; TOBACCO;

NICOTIANA TABACUM; ORYZA SATIVA;

EID: 33745355254     PISSN: 00320935     EISSN: 14322048     Source Type: Journal    
DOI: 10.1007/s00425-005-0214-8     Document Type: Article

References (71)

1. Agrawal GK, Jwa N, Iwahashi H, Rakwal R (2003) Importance of ascorbate peroxidases OsAPx1 and OsAPx2 in the rice pathogen response pathway and growth and reproduction revealed by their transcriptional profiling. Gene 322:93-103
2. Alscher RG, Donahue JL, Cramer CL (1997) Reactive oxygen species and antioxidants: relationships in green cells. Physiol Plant 100:224-233
3. Asada K (1999) The water-water cycle in chloroplasts: scavenging of active oxygen and dissipation of excess photons. Annu Rev Plant Physiol Plant Mol Biol 50:601-639
4. Causse MA et al (1994) Saturated molecular map of the rice genome based on an interspecific backcross population. Genetics 138:1251-1274
5. Chang CC, Ball L, Fryer MJ, Baker N, Karpinski S, Mullineaux PM (2004) Induction of ASCORBATE PEROXIDASE 2 expression in wounded Arabidopsis leaves does not involve known wound-signalling pathways but is associated with changes in photosynthesis. Plant J 38:499-511
6. Chew O, Whelan J (2004) Just read the message: a model for sorting of proteins between mitochondria and chloroplasts. Trends Plant Sci 9:318-319
7. Chew O, Rudhe C, Glaser E, Whelan J (2003a) Characterization of the targeting signal of dual-targeted pea glutathione reductase. Plant Mol Biol 53:341-356
8. Chew O, Whelan J, Millar H (2003b) Molecular definition of the ascorbate-glutathione cycle in Arabidopsis mitochondria reveals dual targeting of antioxidant defenses in plants. J Biol Chem 278:46869-46877
9. Church GM, Gilbert W (1984) Genomic sequencing. Proc Natl Acad Sci 81:1991-1995
10. Danna CH, Bartoli CG, Sacco F, Ingala LR, Santa-María GE, Guiamet JJ, Ugalde RA (2003) Thylakoid-bound ascorbate peroxidase mutant exhibits impaired electron transport and photosynthetic activity. Plant Physiol 132:2116-2125
11. 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 response. Cell Mol Life Sci 57:779-795
12. Davletova S, Rizhsky L, Liang H, Shengqiang Z, Oliver DJ, Coutu J, Shulaev V, Schlauch K, Mittler R (2005) Cytosolic ascorbate peroxidase 1 is a central component of the reactive oxygen gene network of arabidopsis. Plant Cell 17:268-281
13. De Leonardis S, Dipierro N, Dipierro S (2000) Purification and characterization of an ascorbate peroxidase from potato tuber mitochondria. Plant Physiol Biochem 38:773-779
14. Feinberg AP, Vogelstein B (1983). A technique for radiolabelling DNA restriction endonuclease fragments to high specific affinity. Anal Biochem 132:6-13
15. van der Fits L, Deakin E, Hoge H, Memelink J (2000) The ternary transformation system: constitutive virG on a compatible plasmid dramatically increases Agrobacterium-mediated plant transformation. Plant Mol Biol 43:495-502
16. Fourcroy P, Vansuyt G, Kushnir S, Inzé D, Briat J (2004) Iron-regulated expression of a cytosolic ascorbate peroxidase encoded by the APX1 gene in arabidopsis seedlings. Plant Physiol 134:605-613
17. Fridovich I (1998) Oxygen toxicity: a radical explanation. J Exp Bot 201:1203-1209
18. Fryer MJ, Ball L, Oxborough K, Karpinski S, Mullineaux PM, Baker NR (2003) Control of Ascorbate Peroxidase 2 expression by hydrogen peroxide and leaf water status during excess light stress reveals a functional organization of Arabidopsis leaves. Plant J 33:691-705
19. Furlani AMC, Furlani PR (1998) Composição e pH de soluções nutritivas para estudos fisiológicos e de seleção de plantas em condições nutricionais adversas. Technical bulletin 121, Instituto Agronômico de Campinas pp 1-34
20. Gadea J, Conejero V, Vera P (1999) Developmental regulation of a cytosolic ascorbate peroxidase gene from tomato plants. Mol Gen Genet 262:212-219
21. Halliwell B, Gutteridge JM (1999) Free radicals in biology and medicine. Oxford University Press, New York p 936
22. Höfgen R, Willmitzer L (1988) Storage of competent cells for Agrobacterium transformation. Nucleic Acids Res 16:9877
23. Ishikawa T, Sakai K, Takeda T, Shigeoka S (1995) Cloning and expression of cDNA encoding a new type of ascorbate peroxidase in spinach. FEBS Lett 367:28-32
24. Ishikawa T, Sakai K, Yoshimura K, Takeda T, Shigeoka S (1996) cDNAs encoding spinach stromal and thylakoid-bound ascorbate peroxidase, differing in the presence or absence of their 3′-coding regions. FEBS Lett 384:289-293
25. Ishikawa T, Yoshimura K, Sakai K, Tamoi M, Takeda T, Shigeoka S (1998) Molecular characterization and physiological role of a glyoxysome-bound ascorbate peroxidase from spinach. Plant Cell Physiol 39:23-34
26. 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
27. Jiménez A, Hernández JA, Pastori G, del Río LA, Sevilla F (1998) Role of the ascorbate-glutathione cycle of mitochondria and peroxisomes in the senescence of pea leaves. Plant Physiol 118:1327-1335
28. Kamada T, Nito K, Hayashi H, Mano S, Hayashi M, Nishimura M (2003) Functional differentiation of peroxisomes revealed by expression profiles of peroxisomal genes in Arabidopsis thaliana. Plant Cell Physiol 44:1275-1289
29. Karimi M, Inzé D, Depicker A (2002) GATEWAY™ vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci 7:193-195
30. Karpinski S, Escobar C, Karpinska B, Creissen G, Mullineaux PM (1997) Photosynthetic electron transport regulates the expression of cytosolic ascorbate peroxidase genes in arabidopsis during excess light stress. Plant Cell 9:627-640
31. Kato K, Matsumoto T, Koiwai S, Mizusaki S, Nishida K, Nogushi M, Tamaki E (1972) Liquid suspension culture of tobacco cells. In: Terui G (ed) Ferment technology today. Society of Fermentation Technology, Osaka, pp 689-695
32. Kunce CM, Trelease RN, Turley RB (1988) Purification and biosynthesis of cottonseed (Gossypium hirsutum L). Biochem J 251:147-155
33. Lee HD, Kim YS, Lee CB (2001) The inductive responses of the antioxidant enzymes by salt stress in the rice (Oryza sativa L.). J Plant Physiol 158:737-745
34. Lisenbee CS, Heinze M, Trelease RN (2003a) Peroxisomal ascorbate peroxidase resides within a subdomain of rough endoplasmic reticulum in wild-type arabidopsis cells. Plant Physiol 132:870-882
35. Lisenbee CS, Karnik SK, Trelease RN (2003b) Overexpression and mislocalization of a tail-anchored GFP redefines the identity of peroxisomal ER. Traffic 4:491-501
36. -ΔΔCt method. Methods 25:402-408
37. Madhusudhan R, Ishikawa T, Sawa Y, Shigeoka S, Shibata H (2003) Characterization of an ascorbate peroxidase in plastids of tobacco BY-2 cells. Physiol Plant 117:550-557
38. Mano S, Yamaguchi K, Hayashi M, Nishimura M (1997) Stromal and thylakoid-bound ascorbate peroxidases are produced by alternative splicing in pumpkin. FEBS Lett 413:21-26
39. Margis-Pinheiro M, Zhou XR, Zhu QH, Dennis ES, Upadhyaya NM (2005) Isolation and characterization of a Ds-tagged rice (Oryza sativa L.) GA-responsive dwarf mutant defective in an early step of the gibberellin biosynthesis pathway. Plant Cell Rep 23:819-33
40. Menezes-Benavente L, Kernodle SP, Margis-Pinheiro M, Scandalios JG (2004a) Salt-induced antioxidant metabolism defenses in maize (Zea mays L.) seedlings. Redox Rep 9:29-36
41. Menezes-Benavente L, Teixeira FK, Kamei CL, Margis-Pinheiro M (2004b) Salt stress induces expression of genes encoding antioxidant enzymes in seedlings of a Brazilian indica rice (Oryza sativa L.). Plant Sci 166:323-331
42. Mittler R, Feng X, Cohen M (1998) Post-transcriptional suppression of cytosolic ascorbate peroxidase expression during pathogen-induced programmed cell death in tobacco. Plant Cell 10:461-473
43. Mittler R, Vanderauwera S, Gallery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490-498
44. Mittova V, Guy M, Tal M, Volokita M (2004a) Salinity up-regulates the antioxidative system in root mitochondria and peroxisomes of the wild salt-tolerant tomato species Lycopersicon pennellii. J Exp Bot 55:1105-1113
45. Mittova V, Theodoulou FL, Kiddle G, Volokita M, Tal M, Foyer CH, Guy M (2004b) Comparison of mitochondrial ascorbate peroxidase in the cultivated tomato, Lycopersicon esculentum, and its wild, salt-tolerant relative, L. pennellii - a role for matrix isoforms in protection against oxidative damage. Plant Cell Environ 27:237-250
46. Miyake C, Cao WH, Asada K (1993) Purification and molecular properties of thylakoid-bound acorbate peroxidase in spinach chloroplasts. Plant Cell Physiol 34:881-889
47. Mullen RT, Trelease RN (2000) The sorting signals for peroxisomal membrane-bound ascorbate peroxidase are within its C-terminal tail. J Biol Chem 275:16337-16344
48. Mullen RT, Lisenbee CS, Miernyk JA, Trelease RN (1999) Peroxisomal membrane ascorbate peroxidase is sorted to a membranous network that resembles a subdomain of the endoplasmic reticulum. Plant Cell 11:2167-2185
49. Mullineaux P, Karpinski S (2002) Signal transduction in response to excess light: getting out of the chloroplast. Curr Opin Plant Biol 5:43-48
50. Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Plant Physiol 15:473-497
51. Nishimura M, Hayashi M, Kato A, Yamaguchi H, Mano S (1996) Functional transformation of microbodies in higher plant cells. Cell Struct Funct 21:387-393
52. Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Physiol Plant Mol Biol 49:249-79
53. Obara K, Sumi K, Fukuda H (2002) The use of multiple transcription starts causes the dual targeting of Arabidopsis putative mondehydroascorbate reductase to both mitochondria and chloroplasts. Plant Cell Physiol 43:697-705
54. Orozco-Cárdenas ML, Narváez-Vasquéz J, Ryan CA (2001) Hydrogen peroxide acts as a second messenger for the induction of defense genes in tomato plants in response to wounding, systemin, and methyl-jasmonate. Plant Cell 13:179-191
55. Pnueli L, Liang H, Rozenberg M, Mittler R (2003) Growth suppression, altered stomatal responses, and augmented induction of heat shock protein in cytosolic ascobate peroxidase (Apx1)-deficient Arabidopsis plants. Plant J 34:187-203
56. Ragueh F, Fescure N, Roby D, Marco Y (1989) Gene expression in Nicotiana tabacum in response to compatible and incompatible isolates of Pseudomonas solonaciarum. Physiol Mol Plant Pathol 35:23-33
57. Rizhsky L, Davletova S, Liang H, Mittler R (2004) The zing finger protein Zat12 is required for cytosolic ascorbate peroxidase 1 expression during oxidative stress in Arabidopsis. J Biol Chem 279:11736-11743
58. Sato Y, Murakami T, Funatsuki H, Matsuba S, Saruyama H, Tanida M (2001) Heat shock-mediated APX gene expression and protection against chilling injury in rice seedlings. J Exp Bot 52:145-151
59. 4 treatments trigger distinct oxidative defense mechanisms in Nicotiana plumbaginifolia L. Plant Cell Environ 22:387-396
60. Scandalios JG (2002) The rise of ROS. Trends Biochem Sci 27:483-486
61. Shigeoka S, Nakano Y, Kitaoka S (1980) Metabolism of hydrogen peroxide in Euglena gracilis Z by L-ascorbic acid peroxidase. Biochem J 186:377-380
62. Shigeoka S, Ishikawa T, Tamoi M, Miyagawa Y, Takeda T, Yabuta Y, Yoshimura K (2002) Regulation and function of ascorbate peroxidase isoenzymes. J Exp Bot 53:1305-1319
63. Silva-Filho MC (2003) One ticket for multiple destinations: dual targeting of proteins to distinct subcellular locations. Curr Opin Plant Biol 6:589-595
64. Teixeira FK, Menezes-Benavente L, Margis R, Margis-Pinheiro M (2004) Analysis of the molecular evolutionary history of the ascorbate peroxidase gene family: inferences from the rice genome. J Mol Evol 59:761-770
65. Vandenabeele S, Van Der Kelen K, Dat J, Gadjev I, Boonefaes T, Morsa S, Rottiers P, Slooten L, Van Montagu M, Zabeau M, Inzé D, Van Breusegem F (2003) A comprehensive analysis of hydrogen peroxide-induced gene expression in tobacco. Proc Natl Acad Sci USA 100:16113-16118
66. Yabuta Y, Motoki T, Yoshimura K, Takeda T, Ishikawa, Shigeoka S (2002) Thylakoid membrane-bound ascorbate peroxidase is a limiting factor of antioxidative systems under photooxidative stress. Plant J 32:915-925
67. Yoshimura K, Yabuta Y, Ishikawa T, Shigeoka S (2000) Expression of spinach ascorbate peroxidase isoenzymes in response to oxidative stresses. Plant Physiol 123:223-233
68. Yoshimura K, Yabuta Y, Ishikawa T, Shigeoka S (2002) Identification of a cis element for tissue-specific alternative splicing of chloroplast ascorbate peroxidase pre-mRNA in higher plants. J Biol Chem 277:40623-40632
69. Zhang H, Wang J, Nickel U, Allen RD, Goodman HM (1997) Cloning and expression of an Arabidopsis gene encoding a putative peroxisomal ascorbate peroxidase. Plant Mol Biol 34:967-971
70. Zhu JK (2001) Plant salt tolerance. Trends Plant Sci 6:66-67
71. Zottini M, Formentin E, Scattolin M, Carimi F, Lo Schiavo F, Terzi M (2002) Nitric oxide affects plant mitochondrial functionality in vivo. FEBS Lett 515:75-78