Architectural switch in plant photosynthetic membranes induced by light stress

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 49, 2012, Pages 20130-20135

  Herbstová, Miroslava ^a,b,c   Tietz, Stefanie ^a   Kinzel, Christopher ^a   Turkina, Maria V ^d   Kirchhoff, Helmut ^a  

^a WASHINGTON STATE UNIVERSITY   (United States)

^b INSTITUTE OF PLANT MOLECULAR BIOLOGY   (Czech Republic)

^c UNIVERSITY OF SOUTH BOHEMIA   (Czech Republic)

^d LINKÖPING UNIVERSITY   (Sweden)

Author keywords

Confocal microscopy; Macromolecular crowding; Photosynthesis

Indexed keywords

STN7 PROTEIN; STN8 PROTEIN; THYLAKOID MEMBRANE PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; LAMELLAR BODY; LIGHT STRESS; NONHUMAN; PHOTOSYNTHESIS; PHOTOSYSTEM II; PLANT; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; PROTEIN TRANSPORT; PROTOPLAST; THYLAKOID; THYLAKOID MEMBRANE;

ARABIDOPSIS; FLUORESCENCE; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; IMAGE PROCESSING, COMPUTER-ASSISTED; IMMUNOBLOTTING; LIGHT; MICROSCOPY, CONFOCAL; PHOSPHORYLATION; PHOTOSYNTHESIS; PHOTOSYSTEM II PROTEIN COMPLEX; PROTEIN KINASES; PROTEIN TRANSPORT; SPECTROMETRY, FLUORESCENCE; THYLAKOIDS; TIME FACTORS;

EID: 84870627370     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1214265109     Document Type: Article

References (54)

1. 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(2):481-485.
2. Rokka A, Suorsa M, Saleem A, Battchikova N, Aro EM (2005) Synthesis and assembly of thylakoid protein complexes: Multiple assembly steps of photosystem II. Biochem J 388(Pt 1):159-168.
3. Caffarri S, Kouřil R, Kereïche S, Boekema EJ, Croce R (2009) Functional architecture of higher plant photosystem II supercomplexes. EMBO J 28(19):3052-3063.
4. Kouřil R, Dekker JP, Boekema EJ (2012) Supramolecular organization of photosystem II in green plants. Biochim Biophys Acta 1817(1):2-12.
5. Melis A (1999) Photosystem-II damage and repair cycle in chloroplasts: What modulates the rate of photodamage? Trends Plant Sci 4(4):130-135.
6. Kyle DJ, Ohad I, Arntzen CJ (1984) Membrane protein damage and repair: Selective loss of a quinone-protein function in chloroplast membranes. Proc Natl Acad Sci USA 81(13):4070-4074.
7. Mulo P, Sirpiö S, Suorsa M, Aro EM (2008) Auxiliary proteins involved in the assembly and sustenance of photosystem II. Photosynth Res 98(1-3):489-501. (Pubitemid 50206488)
8. Tikkanen M, Aro EM (2012) Thylakoid protein phosphorylation in dynamic regulation of photosystem II in higher plants. Biochim Biophys Acta 1817(1):232-238.
9. Pesaresi P, Pribil M, Wunder T, Leister D (2011) Dynamics of reversible protein phosphorylation in thylakoids of flowering plants: The roles of STN7, STN8 and TAP38. Biochim Biophys Acta 1807(8):887-896.
10. Kato Y, Sakamoto W (2009) Protein quality control in chloroplasts: A current model of D1 protein degradation in the photosystem II repair cycle. J Biochem 146(4):463-469.
11. Austin JR, 2nd, Staehelin LA (2011) Three-dimensional architecture of grana and stroma thylakoids of higher plants as determined by electron tomography. Plant Physiol 155(4):1601-1611.
12. Daum B, Kühlbrandt W (2011) Electron tomography of plant thylakoid membranes. J Exp Bot 62(7):2393-2402.
13. Nevo R, Chuartzman SG, Tsabari O, Reich Z (2009) Architecture of thylakoid membrane networks. Lipids in Photosynthesis: Essential and Regulatory Functions, eds Wada H, Murata N (Springer, Dordrecht, The Netherlands), pp 295-328.
14. Cox RP, Andersson B (1981) Lateral and transverse organization of cytochromes in the chloroplast thylakoid membrane. Biochem Biophys Res Commun 31:1336-1342.
15. Staehelin LA, van der Staay GWM (1996) Structure, composition, functional organization and dynamic properties of thylakoid membranes. Oxygenic Photosynthesis: The Light Reactions, eds Ort DA, Yocum CF (Kluwer, Dordrecht, The Netherlands), pp 11-30.
16. Albertsson P (2001) A quantitative model of the domain structure of the photosynthetic membrane. Trends Plant Sci 6(8):349-358.
17. Kirchhoff H (2008) Molecular crowding and order in photosynthetic membranes. Trends Plant Sci 13(5):201-207.
18. Kirchhoff H, Haferkamp S, Allen JF, Epstein D, Mullineaux CW (2008) Significance of macromolecular crowding for protein diffusion in thylakoid membranes of chloroplasts. Plant Physiol 146:1571-1578. (Pubitemid 352844058)
19. Goral TK, et al. (2010) Visualizing the mobility and distribution of chlorophyll proteins in higher plant thylakoid membranes: Effects of photoinhibition and protein phosphorylation. Plant J 62(6):948-959.
20. Kirchhoff H, Tremmel I, Haase W, Kubitscheck U (2004) Supramolecular photosystem II organization in grana thylakoid membranes: Evidence for a structured arrangement. Biochemistry 43(28):9204-9213. (Pubitemid 38924454)
21. Bonardi V, et al. (2005) Photosystem II core phosphorylation and photosynthetic acclimation require two different protein kinases. Nature 437(7062):1179-1182. (Pubitemid 41509357)
22. Vainonen JP, Hansson M, Vener AV (2005) STN8 protein kinase in Arabidopsis thaliana is specific in phosphorylation of photosystem II core proteins. J Biol Chem 280(39):33679-33686. (Pubitemid 41397170)
23. Fristedt R, Vener AV (2011) High light-induced disassembly of photosystem II supercomplexes in Arabidopsis requires STN7-dependent phosphorylation of CP29. PLoS ONE 6(9):e24565.
24. Tikkanen M, Nurmi M, Kangasjärvi S, Aro E-M (2008) Core protein phosphorylation facilitates the repair of photodamaged photosystem II at high light. Biochim Biophys Acta 1777(11):1432-1437.
25. Tremmel IG, Kirchhoff H, Weis E, Farquhar GD (2003) Dependence of plastoquinol diffusion on the shape, size, and density of integral thylakoid proteins. Biochim Biophys Acta 1607(2-3):97-109. (Pubitemid 37504988)
26. Kirchhoff H, et al. (2011) Dynamic control of protein diffusion within the granal thylakoid lumen. Proc Natl Acad Sci USA 108(50):20248-20253.
27. Chuartzman SG, et al. (2008) Thylakoid membrane remodeling during state transitions in Arabidopsis. Plant Cell 20(4):1029-1039. (Pubitemid 352843977)
28. Anderson JM (1988) Thylakoid membrane organization in sun/shade acclimation. Aust J Plant Physiol 15:11-26.
29. Khatoon M, et al. (2009) Quality control of photosystem II: Thylakoid unstacking is necessary to avoid further damage to the D1 protein and to facilitate D1 degradation under light stress in spinach thylakoids. J Biol Chem 284(37):25343-25352.
30. Fristedt R, et al. (2009) Phosphorylation of photosystem II controls functional macroscopic folding of photosynthetic membranes in Arabidopsis. Plant Cell 21(12):3950-3964.
31. 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(5):2213-2218. (Pubitemid 26079908)
32. Pokorska B, Zienkiewicz M, Powikrowska M, Drozak A, Romanowska E (2009) Differential turnover of the photosystem II reaction centre D1 protein in mesophyll and bundle sheath chloroplasts of maize. Biochim Biophys Acta 1787(10):1161-1169.
33. Fristedt R, Granath P, Vener AV (2010) A protein phosphorylation threshold for functional stacking of plant photosynthetic membranes. PLoS ONE 5(6):e10963.
34. Rochaix JD (2011) Regulation of photosynthetic electron transport. Biochim Biophys Acta 1807(3):375-383.
35. Kettunen R, Tyystjärvi E, Aro EM (1995) Do grana margins of thylakoid membranes form a functional domain during repair cycle of photosystem II?. Photosynthesis: From Light to Biosphere, ed Mathis P (Kluwer, Dordrecht, The Netherlands), Vol IV, pp 331-334.
36. Iwai M, Yokono M, Inada N, Minagawa J (2010) Live-cell imaging of photosystem II antenna dissociation during state transitions. Proc Natl Acad Sci USA 107(5):2337-2342.
37. Rintamäki E, Martinsuo P, Pursiheimo S, Aro EM (2000) Cooperative regulation of light-harvesting complex II phosphorylation via the plastoquinol and ferredoxin-thioredoxin system in chloroplasts. Proc Natl Acad Sci USA 97(21):11644-11649.
38. Rochaix JD (2007) Role of thylakoid protein kinases in photosynthetic acclimation. FEBS Lett 581(15):2768-2775.
39. Baena González E, Barbato R, Aro E-M (1999) Role of phosphorylation in the repair cycle and oligomeric structure of photosystem II. Planta 208:196-204.
40. Nixon PJ, Michoux F, Yu J, Boehm M, Komenda J (2010) Recent advances in understanding the assembly and repair of photosystem II. Ann Bot (Lond) 106(1):1-16.
41. Suno R, et al. (2006) Structure of the whole cytosolic region of ATP-dependent protease FtsH. Mol Cell 22(5):575-585. (Pubitemid 43817602)
42. Daum B, Nicastro D, Austin J II, McIntosh JR, Kühlbrandt W (2010) Arrangement of photosystem II and ATP synthase in chloroplast membranes of spinach and pea. Plant Cell 22(4):1299-1312.
43. Yoshioka M, et al. (2010) Quality control of photosystem II: FtsH hexamers are localized near photosystem II at grana for the swift repair of damage. J Biol Chem 285(53):41972-41981.
44. Yoshioka M, Yamamoto Y (2011) Quality control of photosystem II: Where and how does the degradation of the D1 protein by FtsH proteases start under light stress? Facts and hypotheses. J Photochem Photobiol B 104(1-2):229-235.
45. Consoli E, Croce R, Dunlap DD, Finzi L (2005) Diffusion of light-harvesting complex II in the thylakoid membranes. EMBO Rep 6(8):782-786. (Pubitemid 43108702)
46. Vladimirou E, et al. (2009) Diffusion of a membrane protein, Tat subunit Hcf106, is highly restricted within the chloroplast thylakoid network. FEBS Lett 583(22):3690-3696.
47. Murphy DJ (1986) The molecular organisation of the photosynthetic membranes of higher plants. Biochim Biophys Acta 864:33-94.
48. Sharpe RM, Mahajan A, Takacs EM, Stern DB, Cahoon AB (2011) Developmental and cell type characterization of bundle sheath and mesophyll chloroplast transcript abundance in maize. Curr Genet 57(2):89-102.
49. Staehelin LA (1976) Reversible particle movements associated with unstacking and restacking of chloroplast membranes in vitro. J Cell Biol 71(1):136-158.
50. Kirchhoff H, Borinski M, Lenhert S, Chi L, Büchel C (2004) Transversal and lateral exciton energy transfer in grana thylakoids of spinach. Biochemistry 43(45):14508-14516. (Pubitemid 39491985)
51. Porra RJ, Thompson WA, Kriedermann PE (1989) Determination of accurate extinction coefficient and simultaneous equations for essaying chlorophylls 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.
52. Kirchhoff H, Mukherjee U, Galla HJ (2002) The molecular architecture of the thylakoid membrane: The lipidic diffusion space for plastoquinone. Biochem 41:4872-4882. (Pubitemid 34298654)
53. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227(5259):680-685.
54. Towbin H, Staehelin T, Gordon J (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: Procedure and some applications. Proc Natl Acad Sci USA 76(9):4350-4354. (Pubitemid 9256559)