FtsH-mediated repair of the photosystem II complex in response to light stress

Journal of Experimental Botany

Volumn 56, Issue 411, 2005, Pages 357-363

  Nixon, Peter J ^a,c   Barker, Myles ^a   Boehm, Marko ^a   De Vries, Remco ^a   Komenda, Josef ^b,c  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b INSTITUTE OF MICROBIOLOGY   (Czech Republic)

^c UNIVERSITY OF SOUTH BOHEMIA   (Czech Republic)

Author keywords

Cyanobacteria; DegP HtrA proteases; FtsH proteases; Light stress; Photoinhibition

Indexed keywords

CATALYSIS; COMPLEXATION; ENZYMES; LIGHT ABSORPTION; MOLECULAR STRUCTURE; MUTAGENESIS; OXIDATION; OXYGEN; PHOTOSYNTHESIS; SYNTHESIS (CHEMICAL);

LIGHT STRESS; MOLECULAR OXYGEN; MUTANTS; PHOTOSYNTHETIC OXIDATION; PHOTOSYSTEM II (PSII);

PLANTS (BOTANY);

ADENOSINE TRIPHOSPHATE DEPENDENT PROTEINASE; ARABIDOPSIS PROTEIN; DEGP PROTEASE; HEAT SHOCK PROTEIN; MEMBRANE PROTEIN; PEPTIDE HYDROLASE; PERIPLASMIC PROTEIN; REACTIVE OXYGEN METABOLITE; SERINE PROTEINASE; VAR2 PROTEIN, ARABIDOPSIS; VEGETABLE PROTEIN;

ARABIDOPSIS; CONFERENCE PAPER; CYANOBACTERIUM; GENETICS; LIGHT; METABOLISM; PHOTOSYSTEM II; PHYSIOLOGY; RADIATION EXPOSURE; SIGNAL TRANSDUCTION; SYNECHOCYSTIS;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; ATP-DEPENDENT PROTEASES; CYANOBACTERIA; HEAT-SHOCK PROTEINS; LIGHT; MEMBRANE PROTEINS; PEPTIDE HYDROLASES; PERIPLASMIC PROTEINS; PHOTOSYSTEM II PROTEIN COMPLEX; PLANT PROTEINS; REACTIVE OXYGEN SPECIES; SERINE ENDOPEPTIDASES; SIGNAL TRANSDUCTION; SYNECHOCYSTIS;

ALGAE; ARABIDOPSIS; CYANOBACTERIA; SYNECHOCYSTIS; SYNECHOCYSTIS SP.; SYNECHOCYSTIS SP. PCC 6803;

EID: 13944266767     PISSN: 00220957     EISSN: None     Source Type: Journal    
DOI: 10.1093/jxb/eri021     Document Type: Conference Paper

References (57)

1. Adam Z, Clarke AK. 2002. Cutting edge of proteolysis. Trends in Plant Science 7, 451-456.
2. Adir N, Zer H, Shochat S, Ohad I. 2003. Photoinhibition - a historical perspective. Photosynthesis Research 76, 343-370.
3. Akiyama Y. 2002. Proton-motive force stimulates the proteolytic activity of FtsH, a membrane-bound ATP-dependent protease in Escherichia coli. Proceedings of the National Academy of Sciences, USA. 99, 8066-8071.
4. Akiyama Y, Ito K. 2001. Roles of homo-oligomerization and membrane association in ATPase and proteolytic activities of FtsH in vitro. Biochemistry 40, 7687-7693.
5. Akiyama Y, Ito K. 2003. Reconstitution of membrane proteolysis by FtsH. Journal of Biological Chemistry 278, 18146-18153.
6. Aro E-M, Virgin I, Andersson B. 1993. Photoinhibition of photosystem II. Inactivation, protein damage and turnover. Biochimica et Biophysica Acta 1143, 113-134.
7. Asada K. 1999. The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annual Review of Plant Physiology and Plant Molecular Biology 50, 601-639.
8. Bailey S, Thompson E, Nixon PJ, Horton P, Mullineaux CW, Robinson C, Mann NH. 2002. A critical role for the Var2 FtsH homologue of Arabidopsis thaliana in the PSII repair cycle in vivo. Journal of Biological Chemistry 277, 2006-2011.
9. Barber J, Andersson B. 1992. Too much of a good thing: light can be bad for photosynthesis. Trends in Biochemical Science 17, 61-66.
10. Bottomley W, Spencer D, Whitfeld PR. 1974. Protein synthesis in isolated spinach chloroplasts: comparison of light-driven and ATP-driven synthesis. Archives of Biochemistry and Biophysics 164, 106-117.
11. Chiba S, Akiyama Y, Mori H, Matsuo E, Ito K. 2000. Length recognition at the N-terminal tail for the initiation of FtsH-mediated proteolysis. EMBO Reports 1, 47-52.
12. Chiba S, Akiyama Y, Ito K. 2002. Membrane protein degradation by FtsH can be initiated from either end. Journal of Bacteriology 184, 4775-4782.
13. Clausen T, Southan C, Ehrmann M. 2002. The HtrA family of proteases: implications for protein composition and cell fate. Molecular Cell 10, 443-455.
14. Dalla Chiesa M, Friso G, Deak Z, Vass I, Barber J, Nixon PJ. 1997. Reduced turnover of the D1 polypeptide and photoactivation of electron transfer in novel herbicide resistant mutants of Synechocystis sp. PCC 6803. European Journal of Biochemistry 248, 731-740.
15. Diner BA, Rappaport F. 2002. Structure, dynamics, and energetics of the primary photochemistry of PSII of oxygenic photosynthesis. Annual Review of Plant Biology 53, 551-580.
16. Eaglesham ARJ, Ellis RJ. 1974. Protein synthesis in chloroplasts. II. Light-driven synthesis of membrane proteins by isolated pea chloroplasts. Biochimica et Biophysica Acta 335, 396-407.
17. Ferreira KN, Iverson TM, Maghlaoui K, Barber J, Iwata S. 2004. Architecture of the photosynthetic oxygen-evolving center. Science 303, 1782-1784.
18. Greenberg BM, Gaba V, Mattoo AK, Edelman M. 1987. Identification of a primary in vivo degradation product of the rapidly turning-over 32 kDa protein of PSII. EMBO Journal 6, 2865-2869.
19. Haußühl K, Andersson B, Adamska I. 2001. A chloroplast DegP2 protease performs the primary cleavage of the photodamaged D1 protein in plant PSII. EMBO Journal 20, 713-722.
20. Herman C, Prakash S, Lu CZ, Matouschek A, Gross CA. 2003. Lack of robust unfoldase activity confers a unique level of substrate specificity to the universal AAA protease FtsH. Molecular Cell 11, 659-669.
21. Kashino Y, Lauber WM, Carroll JA, Wang Q, Whitmarsh J, Satoh K, Pakrasi HB. 2002. Proteomic analysis of a highly active PSII preparation from the cyanobacterium Synechocystis sp. PCC 6803 reveals the presence of novel polypeptides. Biochemistry 41, 8004-8012.
22. Koivuniemi A, Aro E-M, Andersson B. 1995. Degradation of the D1 and D2 proteins of PSII in higher plants is regulated by reversible phosphorylation. Biochemistry 34, 16022-16029.
23. B site and dependent on protein synthesis. Biochemistry 34, 9625-9631.
24. Komenda J, Masojídek J. 1995. Functional and structural changes of the PSII complex induced by high irradiance in cyanobacterial cells. European Journal of Biochemistry 233, 677-682.
25. Kyle DJ, Ohad I, Arntzen CJ. 1984. Membrane protein damage and repair: selective loss of a quinone-protein function in chloroplast membranes. Proceedings of the National Academy of Sciences, USA 81, 4070-4074.
26. Langer T. 2000. AAA proteases: cellular machines for degrading membrane proteins. Trends in Biochemical Science 25, 247-251.
27. Lindahl M, Tabak S, Cseke L, Pichersky E, Andersson B, Adam Z. 1996. Identification, characterization and molecular cloning of a homologue of the bacterial FtsH protease in chloroplasts of higher plants. Journal of Biological Chemistry 271, 29329-29334.
28. Lindahl M, Spetea C, Hundal T, Oppenheim AB, Adam Z, Andersson B. 2000. The thylakoid FtsH protease plays a role in the light-induced turnover of the PSII D1 protein. The Plant Cell 12, 419-431.
29. Lupínková L, Komenda J. 2004. Oxidative modifications of the photosystem two D1 protein by reactive oxygen species: from isolated protein to cyanobacterial cells. Photochemistry and Photobiology 79, 152-162.
30. Mann N, Novac N, Mullineaux C, Newman J, Bailey S, Robinson C. 2000. Involvement of an FtsH homologue in the assembly of functional photosystem I in the cyanobacterium Synechocystis sp. PCC 6803. FEBS Letters 479, 72-77.
31. Mishra NP, Francke C, van Gorkom H J, Ghanotakis DF. 1994. Destructive role of singlet oxygen during aerobic illumination of the PSII core complex. Biochimica et Biophysica Acta 1186, 81-90.
32. Miyao M, Ikeuchi M, Yamamoto N, Ono T. 1995. Specific degradation of the D1 protein of PSII by treatment with hydrogen peroxide in darkness: implications for the mechanism of degradation of the D1 protein under illumination. Biochemistry 34, 10019-10026.
33. Mizusawa N, Tomo T, Satoh K, Miyao M. 2003. Degradation of the D1 protein of PSII under illumination in vivo: two different pathways involving cleavage and intermolecular cross-linking. Biochemistry 42, 10034-10044.
34. Nijtmans LG, de Jong L, Artal Sanz M, Coates PJ, Berden JA, Back JW, Muijsers AO, van der Spek H, Grivell LA. 2000. Prohibitins act as a membrane-bound chaperone for the stabilization of mitochondrial proteins. EMBO Journal 19, 2444-2451.
35. 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 Journal 20, 5587-5594.
36. B-binding pocket but does not prevent rapid turnover of D1. Journal of Biological Chemistry 270, 14919-14927.
37. Ogura T, Tomoyasu T, Yuki T, Morimura S, Begg KJ, Donachie WD, Mori H, Niki H, Hiraga S. 1991. Structure and function of the ftsH gene in Escherichia coli. Researches in Microbiology 142, 279-282.
38. Ohad I, Kyle DJ, Arntzen CJ. 1984. Membrane protein damage and repair: removal and replacement of inactivated 32-kilodalton polypeptides in chloroplast membranes. Journal of Cell Biology 270, 14919-14927.
39. Ohad I, Keren N, Zer H, Gong H, Mor TS, Gal A, Tal S, Domovich Y. 1994. Light-induced degradation of the PSII reaction centre D1 protein in vivo: an integrative approach. In: Baker NR, Bowyer JR, eds. Photoinhibition of photosynthesis. Oxford: Bios Scientific Publishers, 161-177.
40. Prasil O, Adir N, Ohad I. 1992. Dynamics of PSII: mechanism of photoinhibition and recovery processes. In: Barber J, ed. The photosystems: structure, function and molecular biology. Amsterdam: Elsevier Science Publishers, 295-248.
41. Saikawa N, Akiyama Y, Ito K. 2004. FtsH exists in an exceptionally large complex containing HflKC in the plasma membrane of Escherichia coli. Journal of Structural Biology 146, 123-129.
42. Sakamoto W, Tamura T, Hanba-Tomita Y, Murata M. 2002. The VAR1 locus of Arabidopsis encodes a chloroplastic FtsH and is responsible for leaf variegation in the mutant alleles. Genes Cells 7, 769-780.
43. Sakamoto W, Zaltsman A, Adam Z, Takahashi Y. 2003. Coordinated regulation and complex formation of YELLOW VARIEGATED1 and YELLOW VARIEGATED2, chloroplastic FtsH metalloproteases involved in the repair cycle of PSII in Arabidopsis thylakoid membranes. The Plant Cell 15, 2843-2855.
44. Sharma J, Panico M, Shipton CA, Nilsson F, Morris HR, Barber J. 1997. Primary structure characterization of the PSII D1 and D2 subunits. Journal of Biological Chemistry 272, 33158-33166.
45. Shetland Y, Shifrin A, Ziv T, Teff D, Koby S, Kobiler O, Oppenheim AB. 2000. Proteolysis of bacteriophage lambda CII by Escherichia coli FtsH (HflB). Journal of Bacteriology 182, 3111-3116.
46. Silva P, Nixon PJ. 2001. Identification of possible assembly and repair factors in photosystem II preparations of Synechocystis sp. PCC 6803: a new model for D1 turnover. 12th International Congress of Photosynthesis. Brisbane-Australia: CSIRO Publishing.
47. Silva P, Choi Y-J, Hassan HAG, Nixon PJ. 2002. Involvement of the HtrA family of proteases in the protection of the cyanobacterium Synechocystis PCC 6803 from light stress and in the repair of PSII. Philosophical Transactions of the Royal Society, London B 357, 1461-1468.
48. Silva P, Thompson E, Bailey S, Kruse O, Mullineaux CW, Robinson C, Mann NH, Nixon PJ. 2003. FtsH is involved in the early stages of repair of photosystem II in Synechocystis sp. PCC 6803. The Plant Cell 15, 2152-2164.
49. Smith D, Howe CJ. 1993. The distribution of photosystem I and PSII polypeptides between the cytoplasmic and thylakoid membranes of cyanobacteria. FEMS Microbiology Letters 110, 341-348.
50. Sokolenko A, Pojidaeva E, Zinchenko V, Panichkin V, Glaser VM, Herrmann RG, Shestakov SV. 2002. The gene complement for proteolysis in the cyanobacterium Synechocystis sp. PCC 6803 and Arabidopsis thaliana chloroplasts. Current Genetics 41, 291-310.
51. Spetea C, Hundal T, Lohmann F, Andersson B. 1999. GTP bound to chloroplast thylakoid membranes is required for light-induced, multienzyme degradation of the PSII D1 protein. Proceedings of the National Academy of Sciences, USA 96, 6547-6552.
52. Steglich G, Neupert W, Langer T. 1999. Prohibitins regulate membrane protein degradation by the m-AAA protease in mitochondria. Molecular and Cellular Biology 19, 3435-3442.
53. Tavernarakis N, Driscoll M, Kyrpides NC. 1999. The SPFH domain: implicated in regulating targeted protein turnover in stomatins and other membrane-associated proteins. Trends in Biochemical Science 24, 425-427.
54. Westphal S, Heins L, Soll J, Vothknecht UC. 2001. Vipp1 deletion mutant of Synechocystis: a connection between bacterial phage shock and thylakoid biogenesis? Proceedings of the National Academy of Sciences, USA 98, 4243-4248.
55. Yamamoto Y. 2001. Quality control of PSII. Plant Cell Physiology 42, 121-128.
56. Yu F, Park S, Rodermel SR. 2004. The Arabidopsis FtsH metalloprotease gene family: interchangeability of subunits in chloroplast oligomeric complexes. The Plant Journal 37, 864-876.
57. Zak E, Norling B, Maitra R, Huang F, Andersson B, Pakrasi HB. 2001. The initial steps of biogenesis of cyanobacterial photosystems occur in plasma membranes. Proceedings of the National Academy of Sciences, USA 98, 13443-13448.