Photosynthetic electron flow affects H2O2 signaling by inactivation of catalase in Chlamydomonas reinhardtii

Planta

Volumn 228, Issue 6, 2008, Pages 1055-1066

  Shao, Ning ^a,b   Beck, Christoph F ^a   Lemaire, Stéphane D ^c   Krieger Liszkay, Anja ^d  

^a UNIVERSITY OF FREIBURG   (Germany)

^b MAX PLANCK INSTITUTE OF MOLECULAR PLANT PHYSIOLOGY   (Germany)

^c INSTITUTE OF PLANT SCIENCES PARIS SACLAY IPS2   (France)

^d SERVICE DE CHIMIE BIOORGANIQUE ET DE MARQUAGE   (France)

Author keywords

Catalase; Chlamydomonas; Hydrogen peroxide; Signaling; Thioredoxin

Indexed keywords

CHLAMYDOMONAS; CHLAMYDOMONAS REINHARDTII;

EID: 55849108834     PISSN: 00320935     EISSN: 14322048     Source Type: Journal    
DOI: 10.1007/s00425-008-0807-0     Document Type: Article

References (56)

1. K Apel H Hirt 2004 Reactive oxygen species: metabolism, oxidative stress, and signal transduction Annu Rev Plant Biol 55 373 399
2. K Asada 1999 The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons Annu Rev Plant Physiol Plant Mol Biol 50 601 639
3. Y Balmer WH Vensel CK Tanaka WJ Hurkman E Gelhaye N Rouhier JP Jacquot W Manieri P Schürmann M Droux BB Buchanan 2004 Thioredoxin links redox to the regulation of fundamental processes of plant mitochondria Proc Natl Acad Sci USA 101 2642 2647
4. GP Bienert AL Møller KA Kristiansen A Schulz IM Møller JK Schjoerring TP Jahn 2007 Specific aquaporins facilitate the diffusion of hydrogen peroxide across membranes J Biol Chem 282 1183 1192
5. S Davletova L Rizhsky H Liang Z Shengqiang DJ Oliver J Coutu V Shulaev K Schlauch R Mittler 2005 Cytosolic ascorbate peroxidase 1 is a central component of the reactive oxygen gene network of Arabidopsis Plant Cell 17 268 281
6. KJ Dietz S Jacob ML Oelze M Laxa V Tognetti SM de Miranda M Baier I Finkemeier 2006 The function of peroxiredoxins in plant organelle redox metabolism J Exp Bot 57 1697 1709
7. M Drabokova W Admiraal B Marsalek 2007 Combined exposure to hydrogen peroxide and light-selective effects on cyanobacteria, green algae, and diatoms Environ Sci Technol 41 309 314
8. MC de Pinto A Paradiso P Leonetti L De Gara 2006 Hydrogen peroxide, nitric oxide and cytosolic ascorbate peroxidase at the crossroad between defence and cell death Plant J 48 784 795
9. N Engel M Schmidt C Lutz J Feierabend 2006 Molecular identification, heterologous expression and properties of light-insensitive plant catalases Plant Cell Environ 29 593 607
10. Feierabend J (2005) Catalases in plants: molecular and functional properties and role in stress defence. In: Smirnoff N (ed) Antioxidants and reactive oxygen species in plants. Blackwell, Oxford, pp 101-140
11. J Feierabend S Engel 1986 Photoinactivation of catalase in vitro and in leaves Arch Biochem Biophys 251 567 576
12. CH Foyer G Noctor 2005 Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses Plant Cell 17 1866 1875
13. M Fuhrmann A Hausherr L Ferbitz T Schodl M Heitzer P Hegemann 2004 Monitoring dynamic expression of nuclear genes in Chlamydomonas reinhardtii by using a synthetic luciferase reporter gene Plant Mol Biol 55 869 881
14. I Gadjev S Vanderauwera TS Gechev C Laloi IN Minkov V Shulaev K Apel D Inze R Mittler F van Breusegem 2006 Transcriptomic footprints disclose specificity of reactive oxygen species signaling in Arabidopsis Plant Physiol 141 436 445
15. T Gechev I Gadjev F van Breusegem D Inze S Dukiandjiev V Toneva I Minkov 2002 Hydrogen peroxide protects tobacco from oxidative stress by inducing a set of antioxidant enzymes Cell Mol Life Sci 59 708 714
16. E Gelhaye N Navrot IK Macdonald N Rouhier EL Raven JP Jacquot 2006 Ascorbate peroxidase-thioredoxin interaction Photosynth Res 89 193 200
17. N Grotjohann A Janning R Eising 1997 In vitro photoinactivation of catalase isoforms from cotyledons of sunflower (Helianthus annuus L.) Arch Biochem Biophys 346 208 218
18. R Gupta S Luan 2003 Redox control of protein tyrosine phosphatases and mitogen-activated protein kinases in plants Plant Physiol 132 1149 1152
19. Harris E (1989) The Chlamydomonas sourcebook: a comprehensive guide to biology and laboratory use. Academic Press, San Diego
20. JL Heazlewood J Tonti-Filippini RE Verboom AH Millar 2005 Combining experimental and predicted datasets for determination of the subcellular location of proteins in Arabidopsis Plant Physiol 139 598 609
21. AN Hiner JN Rodriguez-Lopez MB Arnao E Lloyd Raven F Garcia-Canovas M Acosta 2000 Kinetic study of the inactivation of ascorbate peroxidase by hydrogen peroxide Biochem J 348 321 328
22. C Jakopitsch A Wanasinghe W Jantschko PG Furtmuller C Obinger 2005 Kinetics of interconversion of ferrous enzymes, compound II and compound III, of wild-type synechocystis catalase-peroxidase and Y249F: proposal for the catalytic mechanism J Biol Chem 280 9037 9042
23. JH Joo S Wang JG Chen AM Jones NV Fedoroff 2005 Different signaling and cell death roles of heterotrimeric G protein alpha and beta subunits in the Arabidopsis oxidative stress response to ozone Plant Cell 17 957 970
24. 2 fixation of isolated intact chloroplasts Biochim Biophys Acta 440 476 482
25. J Kato T Yamahara K Tanaka S Takio T Satoh 1997 Characterization of catalase from green alga Chlamydomonas reinhardtii J Plant Physiol 151 262 268
26. KL Kindle 1990 High-frequency nuclear transformation of Chlamydomonas reinhardtii Proc Natl Acad Sci USA 87 1228 1232
27. Y Kovtun WL Chiu G Tena J Sheen 2000 Functional analysis of oxidative stress-activated mitogen-activated protein kinase cascade in plants Proc Natl Acad Sci USA 97 2940 2945
28. R Kuras FA Wollman 1994 The assembly of cytochrome b6/f complexes: an approach using genetic transformation of the green alga Chlamydomonas reinhardtii EMBO J 13 1019 1027
29. C Laloi K Apel A Danon 2004 Reactive oxygen signalling: the latest news Curr Opin Plant Biol 7 323 328
30. SD Lemaire V Collin E Keryer E Issakidis-Bourguet D Lavergne M Miginiac-Maslow 2003 Chlamydomonas reinhardtii: a model organism for the study of the thioredoxin family Plant Physiol Biochem 41 513 521
31. SD Lemaire B Guillon P Le Maréchal E Keryer M Miginiac-Maslow P Decottignies 2004 New thioredoxin targets in the unicellular photosynthetic eukaryote Chlamydomonas reinhardtii Proc Natl Acad Sci USA 101 7475 7480
32. SD Lemaire A Quesada F Merchan JM Corral MI Igeno E Keryer E Issakidis-Bourguet M Hirasawa DB Knaff M Miginiac-Maslow 2005 NADP-malate dehydrogenase from unicellular green alga Chlamydomonas reinhardtii. A first step toward redox regulation? Plant Physiol 137 514 521
33. SD Lemaire L Michelet M Zaffagnini V Massot E Issakidis-Bourguet 2007 Thioredoxins in chloroplasts Curr Genet 51 343 355
34. K Maeda C Finnie B Svensson 2004 Cy5 maleimide labelling for sensitive detection of free thiols in native protein extracts: identification of seed proteins targeted by barley thioredoxin h isoforms Biochem J 378 497 507
35. C Marchand P Le Maréchal Y Meyer M Miginiac-Maslow E Issakidis-Bourguet P Decottignies 2004 New targets of Arabidopsis thioredoxins revealed by proteomic analysis Proteomics 4 2696 2706
36. L Michelet M Zaffagnini V Massot E Keryer H Vanacker M Miginiac-Maslow E Issakidis-Bourguet SD Lemaire 2006 Thioredoxins, glutaredoxins, and glutathionylation: new crosstalks to explore Photosynth Res 89 225 245
37. I Minko SP Holloway S Nikaido M Carter OW Odom CH Johnson DL Herrin 1999 Renilla luciferase as a vital reporter for chloroplast gene expression in Chlamydomonas Mol Gen Genet 262 421 425
38. C Miyake K Asada 1996 Inactivation mechanism of ascorbate peroxidase at low concentrations of ascorbate; hydrogen peroxide decomposes compound I of ascorbate peroxidase Plant Cell Physiol 37 423 430
39. C Miyake Y Shinzaki M Nishioka S Horiguchi K Tomizawa 2006 Photoinactivation of ascorbate peroxidase in isolated tobacco chloroplasts: Galdieria partita APX maintains the electron flux through the water-water cycle in transplastomic tobacco plants Plant Cell Physiol 47 200 210
40. II Panchuk U Zentgraf RA Volkov 2005 Expression of the Apx gene family during leaf senescence of Arabidopsis thaliana Planta 222 926 932
41. T Pfannschmidt K Liere 2005 Redox regulation and modification of proteins controlling chloroplast gene expression Antioxid Redox Signal 7 607 618
42. MC Rentel D Lecourieux F Ouaked SL Usher L Petersen H Okamoto H Knight SC Peck CS Grierson H Hirt MR Knight 2004 OXI1 kinase is necessary for oxidative burst-mediated signalling in Arabidopsis Nature 427 858 861
43. R Scheibe 2004 Malate valves to balance cellular energy supply Physiol Plant 120 21 26
44. N Shao A Krieger-Liszkay M Schroda CF Beck 2007 A reporter system for the individual detection of hydrogen peroxide and singlet oxygen: its use for the assay of reactive oxygen species produced in vivo Plant J 50 475 487
45. S Shigeoka T Ishikawa M Tamoi Y Miyagawa T Takeda Y Yabuta K Yoshimura 2002 Regulation and function of ascorbate peroxidase isoenzymes J Exp Bot 53 1305 1319
46. T Shikanai T Takeda H Yamauchi S Sano KI Tomizawa A Yokota S Shigeoka 1998 Inhibition of ascorbate peroxidase under oxidative stress in tobacco having bacterial catalase in chloroplasts FEBS Lett 428 47 51
47. RJ Spreitzer M Goldschmidt-Clermont M Rahire JD Rochaix 1985 Nonsense mutations in the Chlamydomonas chloroplast gene that codes for the large subunit of ribulosebisphosphate carboxylase/oxygenase Proc Natl Acad Sci USA 82 5460 5464
48. FK Teixeira L Menezes-Benavente VC Galvao R Margis M Margis-Pinheiro 2006 Rice ascorbate peroxidase gene family encodes functionally diverse isoforms localized in different subcellular compartments Planta 224 300 314
49. S Vandenabeele S Vanderauwera M Vuylsteke S Rombauts C Langebartels HK Seidlitz M Zabeau M Van Montagu D Inze F van Breusegem 2004 Catalase deficiency drastically affects gene expression induced by high light in Arabidopsis thaliana Plant J 39 45 58
50. C Vieira Dos Santos P Rey 2006 Plant thioredoxins are key actors in the oxidative stress response Trends Plant Sci 11 329 334
51. ED von Gromoff U Treier CF Beck 1989 Three light-inducible heat shock genes of Chlamydomonas reinhardtii Mol Cell Biol 9 3911 3918
52. J von Kampen U Nieländer M Wettern 1993 Stress-dependent transcription of a gene encoding a Gβ-like polypeptide from Chlamydomonas reinhardtii J Plant Physiol 143 756 758
53. S Waffenschmidt JP Woessner K Beer UW Goodenough 1993 Isodityrosine cross-linking mediates insolubilization of cell walls in Chlamydomonas Plant Cell 5 809 820
54. JH Wong N Cai Y Balmer CK Tanaka WH Vensel WJ Hurkman BB Buchanan 2004 Thioredoxin targets of developing wheat seeds identified by complementary proteomic approaches Phytochemistry 65 1629 1640
55. Y Yabuta T Maruta K Yoshimura T Ishikawa S Shigeoka 2004 Two distinct redox signaling pathways for cytosolic APX induction under photooxidative stress Plant Cell Physiol 45 1586 1594
56. D Yamazaki K Motohashi T Kasama Y Hara T Hisabori 2004 Target proteins of the cytosolic thioredoxins in Arabidopsis thaliana Plant Cell Physiol 45 18 27