Impairment of the photorespiratory pathway accelerates photoinhibition of photosystem II by suppression of repair but not acceleration of damage processes in Arabidopsis

Plant Physiology

Volumn 144, Issue 1, 2007, Pages 487-494

  Takahashi, Shunichi ^a   Bauwe, Hermann ^b   Badger, Murray ^a  

^a AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

^b UNIVERSITY OF ROSTOCK   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

MUTAGENS; OXYGENATION; PHOTOSYNTHESIS; PLANTS (BOTANY);

ARABIDOPSIS; MUTANTS; PHOTORESPIRATORY PATHWAY; PHOTOSYSTEM II;

ENZYME INHIBITION;

CATALYSTS; ENZYMES; INHIBITION; PHOTOSYNTHESIS; PLANTS;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 34250667413     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.107.097253     Document Type: Article

References (56)

1. Allahverdiyeva Y, Mamedov F, Mäenpää P, Vass I, Aro EM (2005) Modulation of photosynthetic electron transport in the absence of terminal electron acceptors: characterization of the rbcL deletion mutant of tobacco. Biochim Biophys Acta 1709: 69-83
2. Allakhverdiev SI, Murata N (2004) Environmental stress inhibits the synthesis de novo of proteins involved in the photodamage-repair cycle of photosystem II in Synechocystis sp PCC 6803. Biochim Biophys Acta 1657: 23-32
3. Allakhverdiev SI, Nishiyama Y, Takahashi S, Miyairi S, Suzuki I, Murata N (2005) Systematic analysis of the relation of electron transport and ATP synthesis to the photodamage and repair of photosystem II in Synechocystis. Plant Physiol 137: 263-273
4. Aro EM, McCaffery S, Anderson JM (1993a) Photoinhibition and D1 protein degradation in peas acclimated to different growth irradiances. Plant Physiol 103: 835-843
5. Aro EM, Suorsa M, Rokka A, Allahverdiyeva Y, Paakkarinen V, Saleem A, Battchikova N, Rintamäki E (2005) Dynamics of photosystem II: a proteomic approach to thylakoid protein complexes. J Exp Bot 56: 347-356
6. Aro EM, Virgin I, Andersson B (1993b) Photoinhibition of photosystem II: inactivation, protein damage and turnover. Biochim Biophys Acta 1143: 113-134
7. Asada K (2006) Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol 141: 391-396
8. 2 in intact spinach chloroplasts: evidence for scavenging of hydrogen peroxide by peroxidase. Plant Cell Physiol 25: 1169-1179
9. Boldt R, Edner C, Kolukisaoglu Ü, Hagemann M, Weckwerth W, Wienkoop S, Morgenthal K, Bauwe H (2005) D-GLYCERATE 3-KINASE, the last unknown enzyme in the photorespiratory cycle in Arabidopsis, belongs to a novel kinase family. Plant Cell 17: 2413-2420
10. 2 specificity of ribulose-1,5-bisphosphate carboxylase oxygenase and the rate of respiration in the light: estimates from gas-exchange measurements on spinach. Planta 165: 397-406
11. Campbell WJ, Ogren WL (1990) Glyoxylate inhibition of ribulosebisphosphate carboxylase/oxygenase activation in intact, lysed, and reconstituted chloroplasts. Photosynth Res 23: 257-268
12. Chow WS, Lee HY, Park YI, Park YM, Hong YN, Anderson JM (2002) The role of inactive photosystem-II-mediated quenching in a last-ditch community defence against high light stress in vivo. Philos Trans R Soc Lond B Biol Sci 357: 1441-1449
13. Critchley C (1981) Studies on the mechanism of photoinhibition in higher plants. Plant Physiol 67: 1161-1165
14. Czechowski T, Stitt M, Altmann T, Udvardi MK, Scheible WR (2005) Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiol 139: 5-17
15. Danon A (2002) Redox reactions of regulatory proteins: do kinetics promote specificity? Trends Biochem Sci 27: 197-203
16. Givan CV, Joy KW, Kleczkowski LA (1988) A decade of photorespiratory nitrogen cycling. Trends Biochem Sci 13: 433-437
17. Hakala M, Rantamäki S, Puputti EM, Tyystjärvi T, Tyystjärvi E (2006) Photoinhibition of manganese enzymes: insights into the mechanism of photosystem II photoinhibition. J Exp Bot 57: 1809-1816
18. Hakala M, Tuominen I, Keränen M, Tyystjärvi T, Tyystjärvi E (2005) Evidence for the role of the oxygen-evolving manganese complex in photoinhibition of photosystem II. Biochim Biophys Acta 1706: 68-80
19. Häusler RE, Bailey KJ, Lea PJ, Leegood RC (1996) Control of photosynthesis in barley mutants with reduced activities of glutamine synthetase and glutamate synthase. III. Aspects of glyoxylate metabolism and effects of glyoxylate on the activation state of ribulose-1,5-bisphosphate carboxylase-oxygenase. Planta 200: 388-396
20. Jones LW, Kok B (1966a) Photoinhibition of chloroplast reactions. I. Kinetics and action spectra. Plant Physiol 41: 1037-1043
21. Jones LW, Kok B (1966b) Photoinhibition of chloroplast reactions. II. Multiple effects. Plant Physiol 41: 1044-1049
22. Keys AJ, Bird IF, Cornelius MJ, Lea PJ, Wallsgrove RM, Miflin BJ (1978) Photorespiratory nitrogen cycle. Nature 275: 741-743
23. Kok B (1956) On the inhibition of photosynthesis by intense light. Biochim Biophys Acta 21: 234-244
24. Kozaki A, Takeba G (1996) Photorespiration protects C3 plants from photooxidation. Nature 384: 557-560
25. Leegood RC, Lea PJ, Adcock MD, Häusler RE (1995) The regulation and control of photorespiration. J Exp Bot 46: 1397-1414
26. Linka M, Weber APM (2005) Shuffling ammonia between mitochondria and plastids during photorespiration. Trends Plant Sci 10: 461-465
27. Long SP, Humphries S, Falkowski PG (1994) Photoinhibition of photosynthesis in nature. Annu Rev Plant Physiol Plant Mol Biol 45: 633-662
28. Mattoo AK, Edelman M (1987) Intramembrane translocation and posttranslational palmitoylation of the chloroplast 32-KDa herbicide-binding protein. Proc Natl Acad Sci USA 84: 1497-1501
29. Mattoo AK, Giardi MT, Raskind A, Edelman M (1999) Dynamic metabolism of photosystem II reaction center proteins and pigments. Physiol Plant 107: 454-461
30. Mattoo AK, Hoffman-Falk H,Marder JB, Edelman M (1984) Regulation of protein metabolism: coupling of photosynthetic electron transport to in vivo degradation of the rapidly metabolized 32-kilodalton protein of the chloroplast membranes. Proc Natl Acad Sci USA 81: 1380-1384
31. Mattoo AK, Marder JB, Edelman M (1989) Dynamics of the photosystem II reaction center. Cell 56: 241-246
32. Moreno JI, Martin R, Castresana C (2005) Arabidopsis SHMT1, a serine hydroxymethyltransferase that functions in the photorespiratory pathway influences resistance to biotic and abiotic stress. Plant J 41: 451-463
33. Nishiyama Y, Allakhverdiev SI, Murata N (2005) Inhibition of the repair of photosystem II by oxidative stress in cyanobacteria. Photosynth Res 84: 1-7
34. Nishiyama Y, Allakhverdiev SI, Murata N (2006) A new paradigm for the action of reactive oxygen species in the photoinhibition of photosystem II. Biochim Biophys Acta 1757: 742-749
35. Nishiyama Y, Allakhverdiev SI, Yamamoto H, Hayashi H, Murata N (2004) Singlet oxygen inhibits the repair of photosystem II by suppressing the translation elongation of the D1 protein in Synechocystis sp. PCC 6803. Biochemistry 43: 11321-11330
36. Nishiyama Y, Yamamoto H, Allakhverdiev SI, Inaba M, Yokota A, Murata N (2001) Oxidative stress inhibits the repair of photodamage to the photosynthetic machinery. EMBO J 20: 5587-5594
37. Ogren WL (1984) Photorespiration: pathways, regulation, and modification. Annu Rev Plant Physiol 35: 415-442
38. Ogren WL, Bowes G (1971) Ribulose diphosphate carboxylase regulates soybean photorespiration. Nat New Biol 230: 159-160
39. Ohad I, Kyle DJ, Arntzen CJ (1984) Membrane protein damage and repair: removal and replacement of inactivated 32-kilodalton polypeptides in chloroplast membranes. J Cell Biol 99: 481-485
40. Ohnishi N, Allakhverdiev SI, Takahashi S, Higashi S, Watanabe M, Nishiyama Y,Murata N (2005) Two-step mechanism of photodamage to photosystem II: step one occurs at the oxygen-evolving complex and step two occurs at the photochemical reaction center. Biochemistry 44: 8494-8499
41. Osmond B, Badger M, Maxwell K, Björkman O, Leegood R (1997) Too many photos: photorespiration, photoinhibition and photooxidation. Trends Plant Sci 2: 119-121
42. Osmond CB (1981) Photorespiration and photoinhibition: some implications for the energetics of photosynthesis. Biochim Biophys Acta 639: 77-98
43. Osmond CB, Grace SC (1995) Perspectives on photoinhibition and photorespiration in the field: quintessential inefficiencies of the light and dark reactions of photosynthesis? J Exp Bot 46: 1351-1362
44. Porra RJ, Thompson WA, Kriedemann PE (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophyll a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochim Biophys Acta 975: 384-394
45. Renné P, Dreßen U, Hebbeker U, Hille D, Flügge UI, Westhoff P, Weber APM (2003) The Arabidopsis mutant dct is deficient in the plastidic glutamate/malate translocator DiT2. Plant J 35: 316-331
46. Sarvikas P, Hakala M, Pätsikkä E, Tyystjärvi T, Tyystjärvi E (2006) Action spectrum of photoinhibition in leaves of wild type and npq1-2 and npq4-1 mutants of Arabidopsis thaliana. Plant Cell Physiol 47: 391-400
47. Somerville CR (1986) Analysis of photosynthesis with mutants of higher plants and algae. Annu Rev Plant Physiol Plant Mol Biol 37: 467-507
48. Somerville CR, Ogren WL (1980) Inhibition of photosynthesis in Arabidopsis mutants lacking leaf glutamate synthase activity. Nature 286: 257-259
49. Somerville CR, Ogren WL (1981) Photorespiration-deficient mutants of Arabidopsis thaliana lacking mitochondrial serine transhydroxymethylase activity. Plant Physiol 67: 666-671
50. Somerville SC, Ogren WL (1983) An Arabidopsis thaliana mutant defective in chloroplast dicarboxylate transport. Proc Natl Acad Sci USA 80: 1290-1294
51. Somerville SC, Somerville CR (1985) A mutant of Arabidopsis deficient in chloroplast dicarboxylate transport is missing an envelope protein. Plant Sci Lett 37: 217-220
52. Takahashi S, Murata N (2005) Interruption of the Calvin cycle inhibits the repair of photosystem II from photodamage. Biochim Biophys Acta 1708: 352-361
53. 2 fixation in the Calvin cycle, is critical for the synthesis of the D1 protein of photosystem II. Biochim Biophys Acta 1757: 198-205
54. Tyystjärvi E, Aro EM (1996) The rate constant of photoinhibition, measured in lincomycin-treated leaves, is directly proportional to light intensity. Proc Natl Acad Sci USA 93: 2213-2218
55. Voll LM, Jamai A, Renné P, Voll H, McClung CR, Weber APM (2006) The photorespiratory Arabidopsis shm1 mutant is deficient in SHM1. Plant Physiol 140: 59-66
56. Wingler A, Lea PJ, Quick WP, Leegood RC (2000) Photorespiration: metabolic pathways and their role in stress protection. Philos Trans R Soc Lond B Biol Sci 355: 1517-1529