Enhanced sensitivity and characterization of photosystem II in transgenic tobacco plants with decreased chloroplast glutathione reductase under chilling stress

Biochimica et Biophysica Acta - Bioenergetics

Volumn 1817, Issue 11, 2012, Pages 1979-1991

  Ding, Shunhua ^a   Lei, Ming ^a   Lu, Qingtao ^a   Zhang, Aihong ^a   Yin, Yan ^a   Wen, Xiaogang ^a   Zhang, Lixin ^a   Lu, Congming ^a  

^a INSTITUTE OF BOTANY   (China)

Author keywords

Chilling stress; Chlorophyll fluorescence; Glutathione reductase; Photosystem II; Thermoluminescence; Transformed tobacco (Nicotiana tabacum)

Indexed keywords

ASCORBIC ACID; DEHYDROASCORBIC ACID; GLUTATHIONE; GLUTATHIONE REDUCTASE; HYDROGEN PEROXIDE;

ARTICLE; BIOACCUMULATION; CHILLING STRESS; CHLOROPLAST; CONTROLLED STUDY; ELECTRON TRANSPORT; ENZYME ACTIVITY; ENZYME ASSAY; FLUORESCENCE; IMMUNOBLOTTING; MOLECULAR STABILITY; NONHUMAN; OXIDATION REDUCTION POTENTIAL; OXIDATIVE STRESS; PHOTOSYNTHESIS; PHOTOSYSTEM II; PRIORITY JOURNAL; RECYCLING; RNA INTERFERENCE; TEMPERATURE SENSITIVITY; TEMPERATURE STRESS; THERMOLUMINESCENCE; TOBACCO; TRANSGENIC PLANT;

ASCORBIC ACID; CHLOROPLASTS; COLD TEMPERATURE; ELECTRON TRANSPORT; GLUTATHIONE REDUCTASE; PHENOTYPE; PHOTOSYSTEM II PROTEIN COMPLEX; PLANTS, GENETICALLY MODIFIED; REACTIVE OXYGEN SPECIES; TOBACCO;

NICOTIANA OBTUSIFOLIA; NICOTIANA TABACUM;

EID: 84865682776     PISSN: 00052728     EISSN: 18792650     Source Type: Journal    
DOI: 10.1016/j.bbabio.2012.06.003     Document Type: Article

References (75)

1. P.D. Vivancos, Y. Dong, K. Ziegler, J. Markovic, F.V. Pallardó, T.K. Pellny, P.J. Verrier, and C.H. Foyer Recruitment of glutathione into the nucleus during cell proliferation adjusts whole-cell redox homeostasis in Arabidopsis thaliana and lowers the oxidative defense shield Plant J. 64 2010 825 838
2. G. Noctor, A. Mhamdi, S. Chaouch, Y. Han, J. Neukermans, B.M. Garcia, G. Queval, and C.H. Foyer Glutathione in plants: an integrated overview Plant Cell Environ. 35 2012 454 484
3. G. Noctor, L. Gomez, H. Vanacker, and C.H. Foyer Interactions between biosynthesis, compartmentation and transport in the control of glutathione homeostasis and signaling J. Exp. Bot. 53 2002 1283 1304
4. R.G. Alscher Biosynthesis and antioxidant function of glutathione in plants Physiol. Plant. 77 1989 457 464
5. G. Noctor, and C.H. Foyer Ascorbate and glutathione: keeping active oxygen under control Annu. Rev. Plant Physiol. Plant Mol. Biol. 49 1998 249 279
6. K. Asada The water-water cycle in chloroplasts: scavenging active oxygen species and dissipation of excess photons Annu. Rev. Plant Physiol. Plant Mol. Biol. 50 1999 601 639
7. M.J. May, T. Vernoux, C. Leaver, M.V. Montagu, and D. Inzé Glutathione homeostasis in plants: implications for environmental sensing and plant development J. Exp. Bot. 49 1998 649 667
8. G. Noctor, A.M. Arisi, L. Jouanin, K.J. Kunert, H. Rennenberg, and C.H. Foyer Glutathione: biosynthesis, metabolism and relationship to stress tolerance explored in transformed plants J. Exp. Bot. 49 1998 623 647
9. C.H. Foyer Oxygen metabolism and electron transport in photosynthesis J. Scandalios, Oxidative Stress and the Molecular Biology of Antioxidant Defenses 1997 Cold Spring Harbor Laboratory Press New York 587 621
10. R. Mittler Oxidative stress, antioxidants and stress tolerance Trends Plant Sci. 7 2002 405 410
11. G.P. Creissen, H. Reynolds, Y. Xue, and P.M. Mullineaux Simultaneous targeting of pea glutathione reductase and of a bacterial fusion protein to chloroplasts and mitochondria in transgenic tobacco Plant J. 8 1995 167 175
12. O. Chew, J. Whelan, and A.H. Millar Molecular definition of the ascorbate-glutathione cycle in Arabidopsis mitochondria reveals dual targeting of antioxidant defenses in plants J. Biol. Chem. 278 2003 46869 46877
13. E.A. Edwards, S. Rawsthorne, and P.M. Mullineaux Subcellular distribution of multiple forms of glutathione reductase in leaves of pea (Pisum sativum L.) Planta 180 1990 278 284
14. S. Ding, Q. Lu, Y. Zhang, Z. Yang, X. Wen, L. Zhang, and C. Lu Enhanced sensitivity to oxidative stress in transgenic tobacco plants with decreased glutathione reductase activity leads to a decrease in ascorbate pool and ascorbate redox state Plant Mol. Biol. 69 2009 577 592
15. L. Marty, W. Siala, M. Schwarzländer, M.D. Fricker, M. Wirtza, L.J. Sweetlove, Y. Meyer, A.J. Meyer, J.P. Reichheld, and R. Hell The NADPH-dependent thioredoxin system constitutes a functional backup for cytosolic glutathione reductase in Arabidopsis Proc. Natl. Acad. Sci. U. S. A. 106 2009 9109 9114
16. A. Jiménez, J.A. Hernandez, L.A. del Rio, and F. Sevilla Evidence for the presence of the ascorbate-glutathione cycle in mitochondria and peroxisomes of pea leaves Plant Physiol. 114 1997 275 284
17. A. Mhamdi, J. Hager, S. Chaouch, G. Queval, Y. Han, L. Taconnat, P. Saindrenan, H. Gouia, E. Issakidis-Bourguet, J.P. Renou, and G. Noctor Arabidopsis GLUTATHIONE REDUCTASE1 plays a crucial role in leaf responses to intracellular hydrogen peroxide and in ensuring appropriate gene expression through both salicylic acid and jasmonic acid signaling pathways Plant Physiol. 153 2010 1144 1160
18. C.H. Foyer, M. Lelandais, C. Galap, and K.J. Kunert Effects of elevated cytosolic glutathione reductase activity on the cellular glutathione pool and photosynthesis in leaves under normal and stress conditions Plant Physiol. 97 1991 863 872
19. M. Aono, A. Kubo, H. Saji, K.K. Tanaka, and N. Kondo Enhanced tolerance to photooxidative stress of transgenic Nicotiana tabacum with chloroplastic glutathione reductase activity Plant Cell Physiol. 34 1993 129 135
20. P. Broadbent, G.P. Creissen, B. Kular, A.R. Wellburn, and P.M. Mullineaux Oxidative stress responses in transgenic tobacco containing altered levels of glutathione reductase activity Plant J. 8 1995 247 255
21. C.H. Foyer, N. Souriau, S. Perret, M. Lelandais, K.J. Kunert, C. Pruvost, and L. Jouanin Overexpression of the glutathione reductase but not glutathione synthetase leads to increases in antioxidant capacity and resistance to photoinhibition in poplar trees Plant Physiol. 109 1995 1047 1057
22. P. Payton, R. Webb, D. Kornyeyev, R. Allen, and A.S. Holaday Protecting cotton photosynthesis during moderate chilling at high light intensity by increasing chloroplastic antioxidant enzyme activity J. Exp. Bot. 52 2001 2345 2354
23. D. Kornyeyev, B.A. Logan, P. Payton, R.D. Allen, and A.S. Holaday Elevated chloroplastic glutathione reducatase activities decrease chilling-induced photoinhibition by increasing rates of photochemistry, but not thermal energy dissipation, in transgenic cotton Funct. Plant Biol. 30 2003 101 110
24. M. Aono, H. Saji, K. Fujiyama, M. Sugita, N. Kondo, and K. Tanaka Decrease in activity of glutathione reductase enhanced paraquat sensitivity in transgenic Nicotiana tabacum Plant Physiol. 107 1995 645 648
25. D. Shu, L. Wang, M. Duan, Y. Deng, and Q. Meng Antisense-mediated depletion of tomato chloroplast glutathione reductase enhances susceptibility to chilling stress Plant Physiol. Biochem. 49 2011 1228 1237
26. D.J. Allen, and D.R. Ort Impacts of chilling temperatures on photosynthesis in warm-climate plants Trends Plant Sci. 6 2001 36 42
27. J.V. Anderson, B.I. Chevone, and J.L. Hess Seasonal variation in the antioxidant system of eastern white pine needles Plant Physiol. 98 1992 501 508
28. B.A. Logan, S.C. Grace, W.W. Adams III, and B. Demmig-Adams Seasonal differences in xanthophyll cycle characteristics and antioxidants in Mahonia repens growing in different light environments Oecologia 116 1998 9 17
29. M.A. Walker, and B.D. McKersie Role of the ascorbate-glutathione antioxidant system in chilling resistance of tomato J. Plant Physiol. 141 1993 234 239
30. D.M. Hodges, C.J. Andrews, D.A. Johnson, and R.I. Hamilton Antioxidant enzyme responses to chilling stress in differentially sensitive inbred maize lines J. Exp. Bot. 48 1997 1105 1113
31. Y.I. Kuk, J.S. Shin, N.R. Burgos, T.E. Hwang, O. Han, B.H. Cho, S. Jung, and J.O. Guh Antioxidative enzymes offer protection from chilling damage in rice plants Crop Sci. 43 2003 2109 2117
32. D. Kornyeyev, B.A. Logan, P. Payton, R.D. Allen, and A.S. Holaday Enhanced photochemical light utilization and decreased chilling-induced photoinhibition of photosystem II in cotton overexpressing genes encoding chloroplast-targeted antioxidant enzymes Physiol. Plant. 113 2001 323 331
33. Y. Zhang, S. Ding, Q. Lu, Z. Yang, X. Wen, L. Zhang, and C. Lu Characterization of photosystem II in transgenic tobacco plants with decreased iron superoxide dismutase Biochim. Biophys. Acta 1807 2011 391 403
34. J. Meurer, K. Meierhoff, and P. Westhoff Isolation of high chlorophyll-fluorescence mutants of Arabidopsis thaliana and their characterization by spectroscopy, immunoblotting and northern hybridization Planta 198 1996 385 396
35. L. Peng, J. Ma, W. Chi, J. Guo, S. Zhu, Q. Lu, C. Lu, and L. Zhang LOW PSII ACCUMULATION1 is involved in efficient assembly of photosystem II in Arabidopsis thaliana Plant Cell 18 2006 955 969
36. C.S. Bestwick, I.R. Brown, M.H. Bennett, and J.W. Mansfield Localization of hydrogen peroxide accumulation during the hypersensitive reaction of lettuce cells to Pseudomonas syringae pv phaseolicola Plant Cell 9 1997 209 221
37. M. Kawai-Yamada, Y. Ohori, and H. Uchimiya Dissection of Arabidopsis Bax inhibitor-1 suppressing Bax-, hydrogen peroxide-, and salicylic acid-induced cell death Plant Cell 16 2004 21 32
38. S. Veljovic-Jovanovic, G. Noctor, and C.H. Foyer Are leaf hydrogen peroxide concentrations commonly overestimated? The potential influence of artefactual interference by tissue phenolics and ascorbate Plant Physiol. Biochem. 40 2002 501 507
39. K. Yoshimura, K. Miyao, A. Gaber, T. Takeda, H. Kanaboshi, H. Miyasaka, and S. Shigeoka Enhancement of stress tolerance in transgenic tobacco plants overexpressing Chlamydomonas glutathione peroxidase in chloroplasts or cytosol Plant J. 37 2004 21 33
40. G.P. Robinson, and D.A. Walker Rapid separation of the chloroplast and cytoplasmic fractions from intact leaf protoplasts Arch. Biochem. Biophys. 196 1979 319 323
41. A. González, K.L. Steffen, and J.P. Lynch Light and excess manganese Plant Physiol. 118 1998 493 504
42. O.C. Knörzer, J. Durner, and P. Böger Alterations in the antioxidative system of suspension-cultured soybean cells (Glycine max) induced by oxidative stress Physiol. Plant. 97 1996 388 396
43. O. Arrigoni, S. Dipierro, and G. Borraccino Ascorbate free radical reductase: a key enzyme of the ascorbic acid system FEBS Lett. 125 1981 242 244
44. W.F. Beyer, and I. Fridovich Assaying for superoxide dismutase activity: some large consequences of minor changes in condition Anal. Biochem. 72 1987 248 254
45. Y.H. Zhou, J.Q. Yu, W.H. Mao, L.F. Huang, X.S. Song, and S. Nogués Genotypic variation of Rubisco expression, photosynthetic electron flow and antioxidant metabolism in the chloroplasts of chill-exposed cucumber plants Plant Cell Physiol. 47 2006 192 199
46. U.K. Laemmli Cleavage of structural proteins during the assembly of the head of bacteriophage T4 Nature 227 1970 680 685
47. D.I. Arnon Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris Plant Physiol. 24 1949 1 15
48. M.M. Bradford A rapid and sensitive method for the quantification of microgram quantities of protein using the principal of protein-dye binding Anal. Biochem. 72 1976 248 254
49. I. Vass, E. Turcsanyi, E. Touloupakis, D. Ghanotakis, and V. Petrouleas The mechanism of UV-A radiation-induced inhibition of photosystem II electron transport studied by EPR and chlorophyll fluorescence Biochemistry 41 2002 10200 10208
50. I. Vass, and Govindjee Thermoluminescence from the photosynthetic apparatus Photosynth. Res. 48 1996 117 126
51. Y. Inoue Photosynthetic thermoluminescence as a simple probe of photosystem II electron transport J. Amesz, J. Hoff, Biophysical Techniques in Photosynthesis Advances in Photosynthesis vol. 3 1996 Kluwer Academic Publishers Dordrecht 93 107
52. I. Vass, G. Horvath, T. Herczeg, and S. Demeter Photosynthetic energy conservation investigated by thermoluminescence. Activation energies and half-lives of thermoluminescence bands of chloroplasts determined by mathematical resolution of glow curves Biochim. Biophys. Acta 634 1981 140 152
53. A.W. Rutherford, A.R. Crofts, and Y. Inoue Thermoluminescence as a probe of photosystem II photochemistry: the origin of the flash-induced glow peaks Biochim. Biophys. Acta 682 1982 457 465
54. S. Demeter, and I. Vass Charge accumulation and recombination in photosystem II studied by thermoluminescence. I. Participation of the primary acceptor Q and secondary acceptor B in the generation of thermoluminescence of chloroplasts Biochim. Biophys. Acta 764 1984 24 32
55. J. Guo, Z. Zhang, Y. Bi, W. Yang, Y. Xu, and L. Zhang Decreased stability of photosystem I in dgd1 mutant of Arabidopsis thaliana FEBS Lett. 579 2005 3619 3624
56. Y. Nakano, and K. Asada Purification of ascorbate peroxidase in spinach chloroplasts; its inactivation in ascorbate-depleted medium and reactivation by monodehydroascorbate radical Plant Cell Physiol. 28 1987 131 140
57. G.X. Chen, and K. Asada Ascorbate peroxidase in tea leaves: occurrence of two isoenzymes and the differences in their enzymatic and molecular properties Plant Cell Physiol. 30 1989 987 998
58. C. Miyake, and K. Asada Thylakoid-bound ascorbate peroxidase in spinach chloroplasts and photoreduction of its primary oxidation product monodehydroascorbate radicals in thylakoids Plant Cell Physiol. 33 1992 541 553
59. L. Michelet, and A. Krieger-Liszkay Reactive oxygen intermediates produced by photosynthetic electron transport are enhanced in short-day grown plants Biochim. Biophys. Acta 1817 2012 1306 1313
60. A. Krieger-Liszkay, P.B. Kós, and É. Hideg Superoxide anion radicals generated by methylviologen in photosystem I damage photosystem II Physiol. Plant. 142 2011 17 25
61. Y. Nishiyama, S.I. Allakhverdiev, and N. Murata A new paradigm for the action of reactive oxygen species in the photoinhibition of photosystem II Biochim. Biophys. Acta 1757 2006 742 749
62. Y. Nishiyama, S.I. Allakhverdievb, and N. Murata Protein synthesis is the primary target of reactive oxygen species in the photoinhibition of photosystem II Physiol. Plant. 142 2011 35 46
63. Y. Nishiyama, H. Yamamoto, S.I. Allakhverdiev, H. Inaba, A. Yokota, and N. Murata Oxidative stress inhibits the repair of photodamage to the photosynthetic machinery EMBO J. 20 2001 5587 5594
64. K. Kojima, M. Oshita, Y. Nanjo, K. Kasai, Y. Tozawa, H. Hayashi, and Y. Nishiyama Oxidation of elongation factor G inhibits the synthesis of the D1 protein of photosystem II Mol. Microbiol. 65 2007 936 947
65. 2 across water channels J. Exp. Bot. 51 2000 2053 2066
66. G.P. Bienert, A.L. Moller, K.A. Kristiansen, A. Schulz, I.M. Moller, J.K. Schjoerring, and T.P. Jahn Specific aquaporins facilitate the diffusion of hydrogen peroxide across membranes J. Biol. Chem. 282 2007 1183 1192
67. 2 and its implication to signaling J. Exp. Bot. 61 2010 3577 3587
68. P. Pospíšil Production of reactive oxygen species by photosystem II Biochim. Biophys. Acta 1787 2009 1151 1160
69. P. Pospíšil Molecular mechanisms of production and scavenging of reactive oxygen species by photosystem II Biochim. Biophys. Acta 1817 2012 218 231
70. 2 evolution with lauroylcholine chloride Biochim. Biophys. Acta 1100 1992 303 311
71. M.R. Badger, S. Caemmerer, S. Ruuska, and H. Nakano Electron flow to oxygen in higher plants and algae: rates and control of direct photoreduction (Mehler reaction) and rubisco oxygenase Philos. Trans. R. Soc. Lond. B Biol. Sci. 355 2000 1433 1446
72. S.A. Khorobrykh, A.A. Khorobrykh, V.V. Klimov, and B.N. Ivanov Photoconsumption of oxygen in photosystem II preparations under impairment of water-oxidation complex Biochemistry (Moscow) 67 2002 683 688
73. A. Arato, N. Bondarava, and A. Krieger-Liszkay Production of reactive oxygen species in chloride- and calcium-depleted photosystem II and their involvement in photoinhibition Biochim. Biophys. Acta 1608 2004 171 180
74. L. Giacomelli, A. Masi, D.R. Ripoll, M.J. Lee, and K.J. van Wijk Arabidopsis thaliana deficient in two chloroplast ascorbate peroxidases shows accelerated light-induced necrosis when levels of cellular ascorbate are low Plant Mol. Biol. 65 2007 627 644
75. C. Miyake, and K. Asada Inactivation mechanism of ascorbate peroxidase at low concentrations of ascorbate; hydrogen peroxide decomposes compound I of ascorbate peroxidase Plant Cell Physiol. 37 1996 423 430