Photosystem II antenna phosphorylation-dependent protein diffusion determined by fluorescence correlation spectroscopy

Scientific Reports

Volumn 3, Issue , 2013, Pages

  Iwai, Masakazu ^a   Pack, Chan Gi ^b   Takenaka, Yoshiko ^c   Sako, Yasushi ^c,e   Nakano, Akihiko ^d  

^a Institute of Physical and Chemical Research   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^c RIKEN   (Japan)

^d UNIVERSITY OF TOKYO   (Japan)

^e NATIONAL INSTITUTE OF ADVANCED INDUSTRIAL SCIENCE AND TECHNOLOGY AIST   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ALGAL PROTEIN; LIGHT HARVESTING SYSTEM; PHOTOSYSTEM II;

CHLAMYDOMONAS REINHARDTII; DIFFUSION; FLUORESCENCE; LIGHT; LIGHT HARVESTING SYSTEM; METABOLISM; PHOSPHORYLATION; PHOTOSYNTHESIS; PHOTOSYSTEM II; PROCEDURES; SPECTROFLUOROMETRY; THYLAKOID;

ALGAL PROTEINS; CHLAMYDOMONAS REINHARDTII; DIFFUSION; FLUORESCENCE; LIGHT; LIGHT-HARVESTING PROTEIN COMPLEXES; PHOSPHORYLATION; PHOTOSYNTHESIS; PHOTOSYSTEM II PROTEIN COMPLEX; SPECTROMETRY, FLUORESCENCE; THYLAKOIDS;

EID: 84885163553     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep02833     Document Type: Article

References (58)

1. Niyogi, K. K. & Truong, T. B. Evolution of flexible non-Photochemical quenching mechanisms that regulate light harvesting in oxygenic photosynthesis. Curr. Opin. Plant Biol. 16, 1-8 (2013).
2. Zito, F. et al. The Qo site of cytochrome b6f complexes controls the activation of the LHCII kinase. EMBO J. 18, 2961-2969 (1999).
3. Allen, J. F., Bennet, J., Steinback, K. E. & Arntzen, C. J. Chloroplast protein phosphorylation couples plastoquinone redox state to distribution of excitation energy between photosystems. Nature 291, 21-25 (1981).
4. Depege, N., Bellafiore, S.& Rochaix, J. D. Role of chloroplast protein kinase Stt7 in LHCII phosphorylation and state transition in Chlamydomonas. Science 299, 1572-1575 (2003).
5. Wollman, F. A. State transitions reveal the dynamics and flexibility of the photosynthetic apparatus. EMBO J. 20, 3623-3630 (2001).
6. Minagawa, J. State transitions-The molecular remodeling of photosynthetic supercomplexes that controls energy flow in the chloroplast. Biochim. Biophys. Acta 1807, 897-905 (2011).
7. Allen, J. F. State transitions-A question of balance. Science 299, 1530-1532 (2003).
8. Iwai, M., Takahashi, Y. & Minagawa, J. Molecular remodeling of photosystem II during state transitions in Chlamydomonas reinhardtii. Plant Cell 20, 2177-2189 (2008).
9. Takahashi, H., Iwai, M., Takahashi, Y. &Minagawa, J. Identification of the mobile light-Harvesting complex II polypeptides for state transitions in Chlamydomonas reinhardtii. Proc. Natl. Acad. Sci. USA 103, 477-482 (2006).
10. Kour?il, R. et al. Structural characterization of a complex of photosystem I and light-Harvesting complex II of Arabidopsis thaliana. Biochemistry 44, 10935-10940 (2005).
11. Kargul, J. et al. Light-Harvesting complex II protein CP29 binds to photosystem I of Chlamydomonas reinhardtii under State 2 conditions. FEBS J. 272, 4797-4806 (2005).
12. Andersson, B., Akerlund, H. E., Jergil, B. & Larsson, C. Differential phosphorylation of the light-Harvesting chlorophyll protein complex in appressed and non-Appressed regions of the thylakoid membrane. FEBS Lett. 149, 181-185 (1982).
13. Kyle, D. J., Staehelin, L. A. & Arntzen, C. J. Lateral mobility of the light-Harvesting complex in chloroplast membranes controls excitation energy distribution in higher plants. Arch. Biochem. Biophys. 222, 527-541 (1983).
14. Bassi, R., Giacometti, G. M. & Simpson, D. J. Changes in the organization of stromamembranes induced by in vivo state 1 state 2 transition. Biochim. Biophys. Acta 935, 152-165 (1988).
15. Delosme, R., Olive, J. &Wollman, F. A. Changes in light energy distribution upon state transitions: An in vivo photoacoustic study of the wild type and photosynthesis mutants from Chlamydomonas reinhardtii. Biochim. Biophys. Acta 1273, 150-158 (1996).
16. Rochaix, J. D. Role of thylakoid protein kinases in photosynthetic acclimation. FEBS Lett. 581, 2768-2775 (2007).
17. Rigler, R., Mets, U., Widengren, J. & Kask, P. Fluorescence correlation spectroscopy with high count rate and low-Background-Analysis of translational diffusion. Eur. Biophys. J. 22, 169-175 (1993).
18. Haustein, E. & Schwille, P. Single-Molecule spectroscopic methods. Curr. Opin. Struct. Biol. 14, 531-540 (2004).
19. Politz, J. C., Browne, E. S., Wolf, D. E. & Pederson, T. Intranuclear diffusion and hybridization state of oligonucleotides measured by fluorescence correlation spectroscopy in living cells. Proc. Natl. Acad. Sci. USA 95, 6043-6048 (1998).
20. Wachsmuth, M. et al. Analyzing intracellular binding and diffusion with continuous fluorescence photobleaching. Biophys. J. 84, 3353-3363 (2003).
21. Milan-Lobo, L. et al. Subtype-Specific differences in corticotropin-Releasing factor receptor complexes detected by fluorescence spectroscopy. Mol. Pharmacol. 76, 1196-1210 (2009).
22. Bark, N., Foldes-Papp, Z. & Rigler, R. The incipient stage in thrombin-Induced fibrin polymerization detected by FCS at the single molecule level. Biochem. Biophys. Res. Commun. 260, 35-41 (1999).
23. Mozziconacci, J., Sandblad, L., Wachsmuth, M., Brunner, D. & Karsenti, E. Tubulin dimers oligomerize before their incorporation into microtubules. PLoS One 3, e3821 (2008).
24. Madge, D., Elson, E. & Webb, W. W. Thermodynamic fluctuations in a reacting systemMeasurement by fluorescence correlation spectroscopy. Phys. Rev. Lett. 29, 705-708 (1972).
25. Bulte, L., Gans, P., Rebeille, F. &Wollman, F. A. ATP control on state transitions in vivo in Chlamydomonas reinhardtii. Biochim. Biophys. Acta 1020, 72-80 (1990).
26. Daum, B. & Kuhlbrandt,W. Electron tomography of plant thylakoid membranes. J. Exp. Bot. 62, 2393-2402 (2011).
27. Bacia, K., Majoul, I. V. & Schwille, P. Probing the endocytic pathway in live cells using dual-Color fluorescence cross-Correlation analysis. Biophys. J. 83, 1184-1193 (2002).
28. Weidemann, T. et al. Counting nucleosomes in living cells with a combination of fluorescence correlation spectroscopy and confocal imaging. J. Mol. Biol. 334, 229-240 (2003).
29. Kirchhoff, H., Haferkamp, S., Allen, J. F., Epstein, D. B. & Mullineaux, C. W. Protein diffusion and macromolecular crowding in thylakoid membranes. Plant Physiol. 146, 1571-1578 (2008).
30. Tokutsu, R., Iwai, M. & Minagawa, J. CP29, a monomeric light-Harvesting complex II protein, is essential for state transitions in Chlamydomonas reinhardtii. J. Biol. Chem. 284, 7777-7782 (2009).
31. Turkina, M. V. et al. Environmentally modulated phosphoproteome of photosynthetic membranes in the green alga Chlamydomonas reinhardtii. Mol. Cell Proteomics 5, 1412-1425 (2006).
32. Finazzi, G., Barbagallo, R. P., Bergo, E., Barbato, R. & Forti, G. Photoinhibition of Chlamydomonas reinhardtii in State 1 and State 2: Damages to the photosynthetic apparatus under linear and cyclic electron flow. J. Biol. Chem. 276, 22251-22257 (2001).
33. Croce, R., Breton, J. & Bassi, R. Conformational changes induced by phosphorylation in the CP29 subunit of photosystem II. Biochemistry 35, 11142-11148 (1996).
34. Nilsson, A. et al. Phosphorylation controls the three-Dimensional structure of plant light harvesting complex II. J. Biol. Chem. 272, 18350-18357 (1997).
35. Zer, H. et al. Regulation of thylakoid protein phosphorylation at the substrate level: Reversible light-Induced conformational changes expose the phosphorylation site of the light-Harvesting complex II. Proc. Natl. Acad. Sci. USA 96, 8277-8282 (1999).
36. Peter, G. F. & Thornber, J. P. Biochemical composition and organization of higher plant photosystem II light-Harvesting pigment-Proteins. J. Biol. Chem. 266, 16745-16754 (1991).
37. Akerlund, H. E. & Andersson, B. Quantitative separation of spinach thylakoids into photosystem-II-Enriched inside-Out vesicles and photosystem-I-Enriched right-Side-Out vesicles. Biochim. Biophys. Acta 725, 34-40 (1983).
38. Wendler, J. & Holzwarth, A. R. State transitions in the green alga Scenedesmus Obliquus probed by time-Resolved chlorophyll fluorescence spectroscopy and global data analysis. Biophys. J. 52, 717-728 (1987).
39. Consoli, E., Croce, R., Dunlap, D. D. & Finzi, L. Diffusion of light-Harvesting complex II in the thylakoid membranes. EMBO Rep. 6, 782-786 (2005).
40. Jansson, S. The light-Harvesting chlorophyll a/b-Binding proteins. Biochim. Biophys. Acta 1184, 1-19 (1994).
41. Adkins, E. M. et al. Membrane mobility and microdomain association of the dopamine transporter studied with fluorescence correlation spectroscopy and fluorescence recovery after photobleaching. Biochemistry 46, 10484-10497 (2007).
42. Feder, T. J., Brust-Mascher, I., Slattery, J. P., Baird, B. &Webb, W. W. Constrained diffusion or immobile fraction on cell surfaces: A new interpretation. Biophys. J. 70, 2767-2773 (1996).
43. Verkman, A. S. Solute and macromolecule diffusion in cellular aqueous compartments. Trends Biochem. Sci. 27, 27-33 (2002).
44. Ellis, R. J. Macromolecular crowding: Obvious but underappreciated. Trends Biochem. Sci. 26, 597-604 (2001).
45. Marenduzzo, D., Finan, K. & Cook, P. R. The depletion attraction: An underappreciated force driving cellular organization. J. Cell Biol. 175, 681-686 (2006).
46. Kirchhoff, H. Molecular crowding and order in photosynthetic membranes. Trends Plant Sci. 13, 201-207 (2008).
47. Eberhard, S., Finazzi, G.&Wollman, F.A. The dynamics of photosynthesis. Annu. Rev. Genetics 42, 463-515 (2008).
48. Iwai, M. et al. Isolation of the elusive supercomplex that drives cyclic electron flow in photosynthesis. Nature 464, 1210-1213 (2010).
49. Johnson, M. P. et al. Photoprotective energy dissipation involves the reorganization of photosystem II light-Harvesting complexes in the grana membranes of spinach chloroplasts. Plant Cell 23, 1468-1479 (2011).
50. Aro, E. M. et al. Dynamics of photosystem II: A proteomic approach to thylakoid protein complexes. J. Exp. Bot. 56, 347-356 (2005).
51. Gorman, D. S. & Levine, R. P. Cytochrome f and plastocyanin: Their sequence in the photosynthetic electron transport chain of Chlamydomonas reinhardtii. Proc. Natl. Acad. Sci. USA 54, 1665-1669 (1965).
52. Porra, R. J., Thompson, W. A. & Kriedemann, P. E. Determination of accurate extinction coefficients and simultaneous-Equations for assaying chlorophyll-A and chlorophyll-B extracted with 4 different solvents-Verification of the concentration of chlorophyll standards by atomic-Absorption spectroscopy. Biochim. Biophys. Acta 975, 384-394 (1989).
53. Iwai, M., Yokono,M., Inada, N. &Minagawa, J. Live-Cell imaging of photosystem II antenna dissociation during state transitions. Proc. Natl. Acad. Sci. USA 107, 2337-2342 (2010).
54. Stauber, E. J. et al. Proteomics of Chlamydomonas reinhardtii light-Harvesting proteins. Eukaryot. Cell 2, 978-994 (2003).
55. Scheuring, S. et al.Watching the photosynthetic apparatus in native membranes. Proc. Natl. Acad. Sci. USA 101, 11293-11297 (2004).
56. Pack, C., Saito, K., Tamura, M. & Kinjo, M. Microenvironment and effect of energy depletion in the nucleus analyzed by mobility of multiple oligomeric EGFPs. Biophys. J. 91, 3921-3936 (2006).
57. Ohsugi, Y., Saito, K., Tamura, M. & Kinjo, M. Lateral mobility of membranebinding proteins in living cells measured by total internal reflection fluorescence correlation spectroscopy. Biophys. J. 91, 3456-3464 (2006).
58. Zhao, M. et al. Afterpulsing and its correction in fluorescence correlation spectroscopy experiments. Appl. Optics 42, 4031-4036 (2003).