Changes in antenna sizes of photosystems during state transitions in granal and stroma-exposed thylakoid membrane of intact chloroplasts in arabidopsis mesophyll protoplasts

Plant and Cell Physiology

Volumn 56, Issue 4, 2015, Pages 759-768

  Kim, Eunchul ^a   Ahn, Tae Kyu ^a   Kumazaki, Shigeichi ^b  

^a Sungkyunkwan University   (South Korea)

^b KYOTO UNIVERSITY   (Japan)

Author keywords

Chloroplast; Fluorescence spectromicroscopy; Light harvesting complex; Photosystem; State transition; Thylakoid membrane

Indexed keywords

LIGHT HARVESTING SYSTEM; PHOTOSYSTEM I; PHOTOSYSTEM II;

ARABIDOPSIS; LIGHT HARVESTING SYSTEM; MESOPHYLL CELL; METABOLISM; PHOTOSYSTEM I; PHOTOSYSTEM II; PROTOPLAST; SPECTROFLUOROMETRY; THYLAKOID;

ARABIDOPSIS; LIGHT-HARVESTING PROTEIN COMPLEXES; MESOPHYLL CELLS; PHOTOSYSTEM I PROTEIN COMPLEX; PHOTOSYSTEM II PROTEIN COMPLEX; PROTOPLASTS; SPECTROMETRY, FLUORESCENCE; THYLAKOIDS;

EID: 84942118366     PISSN: 00320781     EISSN: 14719053     Source Type: Journal    
DOI: 10.1093/pcp/pcv004     Document Type: Article

References (75)

1. Agati, G., Fusi, F., Mazzinghi, P. and Dipaolo, M.L. (1993) A simple approach to the evaluation of the reabsorption of chlorophyll fluorescence spectra in intact leaves. J. Photochem. Photobiol. B 17: 163-171.
2. Albertsson, P.A° . (2001) A quantitative model of the domain structure of the photosynthetic membrane. Trends Plant Sci. 6: 349-354.
3. Allen, J.F. (1992) Protein phosphorylation in regulation of photosynthesis. Biochim. Biophys. Acta 1098: 275-335.
4. Amunts, A., Toporik, H., Borovikova, A. and Nelson, N. (2010) Structure determination and improved model of plant photosystem I. J. Biol. Chem. 285: 3478-3486.
5. Andersson, B.A., kerlund, H.-E., Jergil, B. and Larsson, C. (1982) Differential phosphorylation of the light-harvesting chlorophyll-protein complex in appressed and non-appressed regions of the thylakoid membrane. FEBS Lett. 149: 181-185.
6. Andersson, B. and Anderson, J.M. (1980) Lateral heterogeneity in the distribution of chlorophyll-protein complexes of the thylakoid membranes of spinach chloroplasts. Biochim. Biophys. Acta 593: 427-440.
7. Aro, E.M. and Ohad, I. (2003) Redox regulation of thylakoid protein phosphorylation. Antioxid. Redox Signal. 5: 55-67.
8. Barera, S., Pagliano, C., Pape, T., Saracco, G. and Barber, J. (2012) Characterization of PSII-LHCII supercomplexes isolated from pea thylakoid membrane by one-step treatment with alpha-and beta-dodecyl-D-maltoside. Philos. Trans. R. Soc. B: Biol. Sci. 367: 3389-3399.
9. Bartošková, H., Nauš, J. and Výkruta, M. (1999) The arrangement of chloroplasts in cells influences the reabsorption of chlorophyll fluorescence emission. The effect of desiccation on the chlorophyll fluorescence spectra of Rhizomnium punctatum leaves. Photosynth. Res. 62: 251-260.
10. Bellafiore, S., Barneche, F., Peltier, G. and Rochaix, J.D. (2005) State transitions and light adaptation require chloroplast thylakoid protein kinase STN7. Nature 433: 892-895.
11. Bennett, J. (1983) Regulation of photosynthesis by reversible phosphorylation of the light-harvesting chlorophyll a/b protein. Biochem. J. 212: 1-13.
12. Bennett, J. (1991) Protein phosphorylation in green plant chloroplasts. Annu. Rev. Plant Physiol. Plant Mol. Biol. 42: 281-311.
13. Bennett, J., Steinback, K.E. and Arntzen, C.J. (1980) Chloroplast phosphoproteins: Regulation of excitation energy transfer by phosphorylation of thylakoid membrane polypeptides. Proc. Natl Acad. Sci. USA 77: 5253-5257.
14. Black, M.T., Lee, P. and Horton, P. (1986) Changes in topography and function of thylakoid membranes following membrane protein phosphorylation. Planta 168: 330-336.
15. Blankenship, R.E. (2002) Molecular Mechanisms of Photosynthesis Blackwell Science Ltd, Oxford; Malden, MA.
16. Bonaventura, C. and Myers, J. (1969) Fluorescence and oxygen evolution from Chlorella pyrenoidosa. Biochim. Biophys. Acta 189: 366-383.
17. Caffarri, S., Broess, K., Croce, R. and van Amerongen, H. (2011) Excitation energy transfer and trapping in higher plant photosystem II complexes with different antenna sizes. Biophys. J. 100: 2094-2103.
18. Chow, W.S., Telfer, A., Chapman, D.J. and Barber, J. (1981) State 1-state 2 transitions in leaves and its association with ATP induced chlorophyll fluorescence quenching. Biochim. Biophys. Acta 638: 60-68.
19. Chuartzman, S.G., Nevo, R., Shimoni, E., Charuvi, D., Kiss, V., Ohad, I. et al. (2008) Thylakoid membrane remodeling during state transitions in Arabidopsis. Plant Cell 20: 1029-1039.
20. Cordón, G.B. and Lagorio, M.G. (2006) Re-absorption of chlorophyll fluorescence in leaves revisited. A comparison of correction models. Photochem. Photobiol. Sci. 5: 735-740.
21. Danielsson, R., Albertsson, P.A° ., Mamedov, F. and Styring, S. (2004) Quantification of photosystem I and II in different parts of the thylakoid membrane from spinach. Biochim. Biophys. Acta 1608: 53-61.
22. Dekker, J.P. and Boekema, E.J. (2005) Supramolecular organization of thylakoid membrane proteins in green plants. Biochim. Biophys. Acta 1706: 12-39.
23. Dietzel, L., Bräutigam, K., Steiner, S., Schüffler, K., Lepetit, B., Grimm, B. et al. (2011) Photosystem II supercomplex remodeling serves as an entry mechanism for state transitions in Arabidopsis. Plant Cell 23: 2964-2977.
24. Drop, B., Yadav, K.N.S., Boekema, E.J. and Croce, R. (2014) Consequences of state transitions on the structural and functional organization of Photosystem I in the green alga Chlamydomonas reinhardtii. Plant J. 78: 181-191.
25. Galka, P., Santabarbara, S., Thi, T.H.K., Degand, H., Morsomme, P., Jennings, R.C. et al. (2012) Functional analyses of the plant photosystem I-light-harvesting complex II supercomplex reveal that light-harvesting complex II loosely bound to photosystem II is a very efficient antenna for photosystem I in state II. Plant Cell 24: 2963-2978 .
26. Gitelson, A.A., Buschmann, C. and Lichtenthaler, H.K. (1998) Leaf chlorophyll fluorescence corrected for re-absorption by means of absorption and reflectance measurements. J. Plant Physiol. 152: 283-296.
27. Govindjee. (2007) Chlorophyll a fluorescence: A bit of basics and history. In Chlorophyll a Fluorescence: A Signature of Photosynthesis. Edited by Papageorgiou, G.C. and Govindjee. pp. 1-42. Springer, Dordrecht.
28. Govindjee. and Yang, L. (1966) Structure of the red fluorescence band of chloroplasts. J. Gen. Physiol. 22: 131-160.
29. Grieco, M., Tikkanen, M., Paakkarinen, V., Kangasjärvi, S. and Aro, E.M. (2012) Steady-state phosphorylation of light-harvesting complex II proteins preserves photosystem I under fluctuating white light. Plant Physiol. 160: 1896-1910.
30. Hasegawa, M., Shiina, T., Terazima, M. and Kumazaki, S. (2010) Selective excitation of photosystems in chloroplasts inside plant leaves observed by near-infrared laser-based fluorescence spectral microscopy. Plant Cell Physiol. 51: 225-238.
31. Hasegawa, M., Yoshida, T., Yabuta, M., Terazima, M. and Kumazaki, S. (2011) Anti-Stokes fluorescence spectra of chloroplasts in Parachlorella kessleri and maize at room temperature as characterized by near-infrared continuous-wave laser fluorescence microscopy and absorption microscopy. J. Phys. Chem. B 115: 4184-4194.
32. Herbstová, M., Tietz, S., Kinzel, C., Turkina, M.V. and Kirchhoff, H. (2012) Architectural switch in plant photosynthetic membranes induced by light stress. Proc. Natl Acad. Sci. USA 109: 20130-20135.
33. Hou, C.X., Pursiheimo, S., Rintamäki, E. and Aro, E.M. (2002) Environmental and metabolic control of LHCII protein phosphorylation: Revealing the mechanisms for dual regulation of the LHCII kinase. Plant Cell Environ. 25: 1515-1525.
34. Hou, C.X., Rintamäki, E. and Aro, E.M. (2003) Ascorbate-mediated LHCII protein phosphorylation-LHCII kinase regulation in light and in darkness. Biochemistry 42: 5828-5836.
35. Iwai, M., Yokono, M., Inada, N. and Minagawa, J. (2010) Live-cell imaging of photosystem II antenna dissociation during state transitions. Proc. Natl Acad. Sci. USA 107: 2337-2342.
36. Iwai, M., Pack, C.G., Takenaka, Y., Sako, Y. and Nakano, A. (2013) Photosystem II antenna phosphorylation-dependent protein diffusion determined by fluorescence correlation spectroscopy. Sci. Rep. 3: 2833.
37. Järvi, S., Suorsa, M., Paakkarinen, V. and Aro, E.M. (2011) Optimized native gel systems for separation of thylakoid protein complexes: novel superand mega-complexes. Biochem. J. 439: 207-214.
38. Kouřil, R., Wientjes, E., Bultema, J.B., Croce, R. and Boekema, E.J. (2013) High-light vs. low-light: Effect of light acclimation on photosystem II composition and organization in Arabidopsis thaliana. Biochim. Biophys. Acta 1827: 411-419.
39. Kouřil, R., Zygadlo, A., Arteni, A.A., de Wit, C.D., Dekker, J.P., Jensen, P.E. et al. (2005) Structural characterization of a complex of photosystem I and light-harvesting complex II of Arabidopsis thaliana. Biochemistry 44: 10935-10940.
40. Kumazaki, S., Akari, M. and Hasegawa, M. (2013) Transformation of thylakoid membranes during differentiation from vegetative cell into heterocyst visualized by microscopic spectral imaging. Plant Physiol. 161: 1321-1333.
41. Kumazaki, S., Hasegawa, M., Ghoneim, M., Shimizu, Y., Okamoto, K., Nishiyama, M. et al. (2007) A line-scanning semi-confocal multiphoton fluorescence microscope with a simultaneous broadband spectral acquisition and its application to the study of the thylakoid membrane of a cyanobacterium Anabaena PCC7120. J. Microsc. 228: 240-254.
42. Kyle, D.J., Kuang, T.-Y., Watson, J.L. and Arntzen, C.J. (1984a) Movement of a sub-population of the light harvesting complex (LHCII) from grana to stroma lamellae as a consequence of its phosphorylation. Biochim. Biophys. Acta 765: 89-96.
43. Kyle, D.J., Ohad, I. and Arntzen, C.J. (1984b) Membrane-protein damage and repair-selective loss of a quinone-protein function in chloroplast membranes. Proc. Natl Acad. Sci. USA 81: 4070-4074.
44. Kyle, D.J., Staehelin, L.A. and Arntzen, C.J. (1983) Lateral mobility of the light harvesting chlorophyll protein in chloroplast membranes controls excitation energy distribution in higher plants. Biochim. Biophys. Acta 222: 527-541.
45. Lagorio, M.G., Dicelio, L.E., Litter, M.I. and Román, E.S. (1998) Modeling of fluorescence quantum yields of supported dyes-aluminium carboxyphthalocyanine on cellulose. J. Chem. Soc. Faraday Trans. 94: 419-425.
46. Lambrev, P.H., Varkonyi, Z., Krumova, S., Kovács, L., Miloslavina, Y., Holzwarth, A.R. et al. (2007) Importance of trimer-trimer interactions for the native state of the plant light-harvesting complex II. Biochim. Biophys. Acta 1767: 847-853.
47. Larsson, U.K., Jergil, B. and Andersson, B. (1983) Changes in the lateral distribution of the light-harvesting chlorophyll-a/b-protein complex induced by its phosphorylation. Eur. J. Biochern. 136: 25-29.
48. Larsson, U.K., Sundby, C. and Andersson, B. (1987) Characterization of two different subpopulations of spinach light-harvesting chlorophyll a/b-protein complex (LHC II): polypeptide composition, phosphorylation pattern and association with Photosystem II. Biochim. Biophys. Acta 894: 59-68.
49. Li, X.P., Gilmore, A.M., Caffarri, S., Bassi, R., Golan, T., Kramer, D. et al. (2004) Regulation of photosynthetic light harvesting involves intrathylakoid lumen pH sensing by the PsbS protein. J. Biol. Chem. 279: 22866-22874.
50. Li, X.P., Müller-Moulé, P., Gilmore, A.M. and Niyogi, K.K. (2002) PsbS-dependent enhancement of feedback de-excitation protects photosystem II from photoinhibition. Proc. Natl Acad. Sci. USA 99: 15222-15227.
51. Lichtenthaler, H.K. and Pfister, K. (1978) Praktikum der Photosynthesis. Quelle und Meyer, Heidelberg.
52. Liu, Z.F., Yan, H.C., Wang, K.B., Kuang, T.Y., Zhang, J.P., Gui, L.L. et al. (2004) Crystal structure of spinach major light-harvesting complex at 2.72 angstrom resolution. Nature 428: 287-292.
53. Minagawa, J. (2011) State transitions-the molecular remodeling of photosynthetic supercomplexes that controls energy flow in the chloroplast. Biochim. Biophys. Acta 1807: 897-905.
54. Murata, N. (1969) Control of excitation transfer in photosynthesis. I. Lightinduced change of chlorophyll a fluorescence in Porphyridium cruentum. Biochim. Biophys. Acta 172: 242-251.
55. Mustárdy, L. and Garab, G. (2003) Granum revisited. A three-dimensional model-where things fall into place. Trends Plant Sci. 8: 117-122.
56. Owens, T.G., Webb, S.P., Mets, L., Alberte, R.S. and Fleming, G.R. (1987) Antenna size dependence of fluorescence decay in the core antenna of photosystem I. Proc. Natl. Acad. Sci. USA 84: 1532-1536.
57. Papageorgiou, G.C. and Govindjee. (2011) Photosystem II fluorescence: slow changes-scaling from the past. J. Photochem. Photobiol. B 104: 258-270.
58. Pedrós, R., Moya, I., Goulas, Y. and Jacquemoud, S. (2008) Chlorophyll fluorescence emission spectrum inside a leaf. Photochem. Photobiol. Sci. 7: 498-502.
59. Ramos, M.E. and Lagorio, M.G. (2004) True fluorescence spectra of leaves. Photochem. Photobiol. Sci. 3: 1063-1066.
60. Ramos, M.E. and Lagorio, M.G. (2006) A model considering light reabsorption processes to correct in vivo chlorophyll fluorescence spectra in apples. Photochem. Photobiol. Sci. 5: 508-512.
61. Rochaix, J.D. (2011) Reprint of: Regulation of photosynthetic electron transport. Biochim. Biophys. Acta 1807: 878-886.
62. Ruban, A.V. and Johnson, M.P. (2009) Dynamics of higher plant photosystem cross-section associated with state transitions. Photosynth. Res. 99: 173-183.
63. Ruban, A.V., Rees, D., Pascal, A.A. and Horton, P. (1992) Mechanism of Delta-pH-dependent dissipation of absorbed excitation-energy by photosynthetic membranes. 2. The relationship between LHCII aggregation in vitro and Qe in isolated thylakoids. Biochim. Biophys. Acta 1102: 39-44.
64. Samson, G. and Bruce, D. (1995) Complementary changes in absorption cross-sections of photosystems-I and photosystems-II due to phosphorylation and Mg2+-depletion in spinach thylakoids. Biochim. Biophys. Acta 1232: 21-26.
65. Staehelin, L.A. and Arntzen, C.J. (1983) Regulation of chloroplast membrane function: protein phosphorylation changes the spatial organization of membrane components. J. Cell Biol. 97: 1327-1337.
66. Takahashi, H., Iwai, M., Takahashi, Y. and Minagawa, J. (2006) Identification of the mobile light-harvesting complex II polypeptides for state transitions in Chlamydomonas reinhardtii. Proc. Natl Acad. Sci. USA 103: 477-482.
67. Tikkanen, M., Grieco, M., Kangasjärvi, S. and Aro, E.M. (2010) Thylakoid protein phosphorylation in higher plant chloroplasts optimizes electron transfer under fluctuating light. Plant Physiol. 152: 723-735.
68. Tikkanen, M., Nurmi, M., Suorsa, M., Danielsson, R., Mamedov, F., Styring, S. et al. (2008) Phosphorylation-dependent regulation of excitation energy distribution between the two photosystems in higher plants. Biochim. Biophys. Acta 1777: 425-432.
69. Tikkanen, M., Pippo, M., Suorsa, M., Sirpio, S., Mulo, P., Vainonen, J. et al. (2006) State transitions revisited-a buffering system for dynamic low light acclimation of Arabidopsis. Plant. Mol. Biol. 62: 779-793.
70. Tokutsu, R., Iwai, M. and Minagawa, J. (2009) CP29, a monomeric lightharvesting complex II protein, is essential for state transitions in Chlamydomonas reinhardtii. J. Biol. Chem. 284: 7777-7782.
71. Ü nlü, C., Drop, B., Croce, R. and van Amerongen, H. (2014) State transitions in Chlamydomonas reinhardtii strongly modulate the functional size of photosystem II but not of photosystem I. Proc. Natl Acad. Sci. USA 111: 3460-3465.
72. van Oort, B., Alberts, M., de Bianchi, S., Dall'Osto, L., Bassi, R., Trinkunas, G. et al. (2010) Effect of antenna-depletion in photosystern II on excitation energy transfer in Arabidopsis thaliana. Biophys. J. 98: 922-931.
73. Wientjes, E., Drop, B., Kouril, R., Boekema, E.J. and Croce, R. (2013a) During state 1 to state 2 transition in Arabidopsis thaliana, the photosystem II supercomplex gets phosphorylated but does not disassemble. J. Biol. Chem. 288: 32821-32826.
74. Wientjes, E., van Amerongen, H. and Croce, R. (2013b) LHCII is an antenna of both photosystems after long-term acclimation. Biochim. Biophys. Acta 1827: 420-426.
75. Yoo, S.D., Cho, Y.H. and Sheen, J. (2007) Arabidopsis mesophyll protoplasts: A versatile cell system for transient gene expression analysis. Nat. Protoc. 2: 1565-1572.