Effect of light acclimation on the organization of photosystem II super- and sub-complexes in arabidopsis thaliana

Frontiers in Plant Science

Volumn 7, Issue FEB2016, 2016, Pages

  Bielczynski, Ludwik W ^a   Schansker, Gert ^a   Croce, Roberta ^a  

^a VU UNIVERSITY AMSTERDAM   (Netherlands)

Author keywords

2D PAGE; Arabidopsis thaliana; BN PAGE; Light intensity acclimation; PSII

Indexed keywords

EID: 84960105357     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2016.00105     Document Type: Article

References (57)

1. Allen, J. F. (1992). Protein phosphorylation in regulation of photosynthesis. Biochim. Biophys. Acta 1098, 275-335. doi: 10.1016/S0005-2728(09)91014-3
2. Andaluz, S., López-Millán, A.-F., De las Rivas, J., Aro, E.-M., Abadía, J., and Abadía, A. (2006). Proteomic profiles of thylakoid membranes and changes in response to iron deficiency. Photosynth. Res. 89, 141-155. doi: 10.1007/s11120-006-9092-6
3. Andersson, I. (1996). Large structures at high resolution: the 1.6 Å crystal structure of spinach ribulose-1,5- bisphosphate carboxylase/oxygenase complexed with 2-carboxyarabinitol bisphosphate. J. Mol. Biol. 259, 160-174. doi: 10.1006/jmbi.1996.0310
4. Aro, E.-M., Suorsa, M., Rokka, A., Allahverdiyeva, Y., Paakkarinen, V., Saleem, A., et al. (2005). Dynamics of photosystem II: a proteomic approach to thylakoid protein complexes. J. Exp. Bot. 56, 347-356. doi: 10.1093/jxb/eri041
5. Asada, K. (2006). Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol. 141, 391-396. doi: 10.1104/pp.106.082040
6. Ballottari, M., Dall'Osto, L., Morosinotto, T., and Bassi, R. (2007). Contrasting behavior of higher plant photosystem I and II antenna systems during acclimation. J. Biol. Chem. 282, 8947-8958. doi: 10.1074/jbc.M606417200
7. Belgio, E., Kapitonova, E., Chmeliov, J., Duffy, C. D. P., Ungerer, P., Valkunas, L., et al. (2014). Economic photoprotection in photosystem II that retains a complete light-harvesting system with slow energy traps. Nat. Commun. 5, 1-8. doi: 10.1038/ncomms5433
8. Betterle, N., Ballottari, M., Zorzan, S., de Bianchi, S., Cazzaniga, S., Dall'Osto, L., et al. (2009). Light-induced dissociation of an antenna hetero-oligomer is needed for non-photochemical quenching induction. J. Biol. Chem. 284, 15255-15266. doi: 10.1074/jbc.M808625200
9. Caffarri, S., Kouřil, R., Kereïche, S., Boekema, E. J., and Croce, R. (2009). Functional architecture of higher plant photosystem II supercomplexes. EMBO J. 28, 3052-3063. doi: 10.1038/emboj.2009.232
10. Clarke, J. T., Warnock, R. C. M., and Donoghue, P. C. J. (2011). Establishing a time-scale for plant evolution. New Phytol. 192, 266-301. doi: 10.1111/j.1469-8137.2011.03794.x
11. Croce, R., Canino, G., Ros, F., and Bassi, R. (2002). Chromophore organization in the higher-plant photosystem II antenna protein CP26. Biochemistry 41, 7334-7343. doi: 10.1021/bi0257437
12. Danielsson, R., Suorsa, M., Paakkarinen, V., Albertsson, P.-A., Styring, S., Aro, E.-M., et al. (2006). Dimeric and monomeric organization of photosystem II. Distribution of five distinct complexes in the different domains of the thylakoid membrane. J. Biol. Chem. 281, 14241-14249. doi: 10.1074/jbc.M600634200
13. Dekker, J. P., and Boekema, E. J. (2005). Supramolecular organization of thylakoid membrane proteins in green plants. Biochim. Biophys. Acta 1706, 12-39. doi: 10.1016/j.bbabio.2004.09.009
14. Demmig-Adams, B., Adams, W. W., Heber, U., Neimanis, S., Winter, K., Krüger, A., et al. (1990). Inhibition of zeaxanthin formation and of rapid changes in radiationless energy dissipation by dithiothreitol in spinach leaves and chloroplasts. Plant Physiol.92, 293-301. doi: 10.1104/pp.92.2.293
15. Dietz, K.-J. (2015). Efficient high light acclimation involves rapid processes at multiple mechanistic levels. J. Exp. Bot. 66, 2401-2414. doi: 10.1093/jxb/eru505
16. Dinç, E., Ceppi, M. G., Tóth, S. Z., Bottka, S., and Schansker, G. (2012). The chl a fluorescence intensity is remarkably insensitive to changes in the chlorophyll content of the leaf as long as the chl a/b ratio remains unaffected. Biochim. Biophys. Acta1817, 770-779. doi: 10.1016/j.bbabio.2012.02.003
17. Evans, J. R., and Vogelmann, T. C. (2003). Profiles of C-14 fixation through spinach leaves in relation to light absorption and photosynthetic capacity. Plant Cell Environ.26, 547-560. doi: 10.1046/j.1365-3040.2003.00985.x
18. Fristedt, R., and Vener, A. V. (2011). High light induced disassembly of photosystem II supercomplexes in Arabidopsis requires STN7-dependent phosphorylation of CP29.PLoS ONE 6:e24565. doi: 10.1371/journal.pone.0024565
19. Garab, G., Cseh, Z., Kovács, L., Rajagopal, S., Várkonyi, Z., Wentworth, M., et al. (2002). Light-induced trimer to monomer transition in the main light-harvesting antenna complex of plants: thermo-optic mechanism. Biochemistry 41, 15121-15129. doi: 10.1021/bi026157g
20. Georgiou, C. D., Grintzalis, K., Zervoudakis, G., and Papapostolou, I. (2008). Mechanism of Coomassie brilliant blue G-250 binding to proteins: a hydrophobic assay for nanogram quantities of proteins. Anal. Bioanal. Chem. 391, 391-403. doi: 10.1007/s00216-008-1996-x
21. Gilmore, A. M., and Yamamoto, H. Y. (1991). Resolution of lutein and zeaxanthin using a non-endcapped, lightly carbon-loaded C18 high-performance liquid chromatographic column. J. Chromatogr. A 543, 137-145. doi: 10.1016/S0021-9673(01)95762-0
22. Hersch, M., Lorrain, S., de Wit, M., Trevisan, M., Ljung, K., Bergmann, S., et al. (2014). Light intensity modulates the regulatory network of the shade avoidance response in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 111, 6515-6520. doi: 10.1073/pnas.1320355111
23. Holzwarth, A. R., Miloslavina, Y., Nilkens, M., and Jahns, P. (2009). Identification of two quenching sites active in the regulation of photosynthetic light-harvesting studied by time-resolved fluorescence. Chem. Phys. Lett. 483, 262-267. doi: 10.1016/j.cplett.2009.10.085
24. Horton, P., Johnson, M. P., Perez-Bueno, M. L., Kiss, A. Z., and Ruban, A. V. (2008). Photosynthetic acclimation: does the dynamic structure and macro-organisation of photosystem II in higher plant grana membranes regulate light harvesting states?FEBS J. 275, 1069-1079. doi: 10.1111/j.1742-4658.2008.06263.x
25. Horton, P., and Ruban, A. (2005). Molecular design of the photosystem II light-harvesting antenna: photosynthesis and photoprotection. J. Exp. Bot. 56, 365-373. doi: 10.1093/jxb/eri023
26. Hundal, T., Virgin, I., Styring, S., and Andersson, B. (1990). Changes in the organization of photosystem II following light-induced D1-protein degradation.Biochim. Biophys. Acta 1017, 235-241. doi: 10.1016/0005-2728(90)90190-F
27. Ilioaia, C., Johnson, M. P., Horton, P., and Ruban, A. V. (2008). Induction of efficient energy dissipation in the isolated light-harvesting complex of photosystem II in the absence of protein aggregation. J. Biol. Chem. 283, 29505-29512. doi: 10.1074/jbc.M802438200
28. Jahns, P., and Holzwarth, A. R. (2012). The role of the xanthophyll cycle and of lutein in photoprotection of photosystem II. Biochim. Biophys. Acta 1817, 182-193. doi: 10.1016/j.bbabio.2011.04.012
29. Järvi, S., Suorsa, M., Paakkarinen, V., and Aro, E.-M. (2011). Optimized native gel systems for separation of thylakoid protein complexes: novel super- and mega-complexes. Biochem. J. 439, 207-214. doi: 10.1042/BJ20102155
30. Johnson, M. P., Goral, T. K., Duffy, C. D. P., Brain, A. P. R., Mullineaux, C. W., and Ruban, A. V. (2011). Photoprotective energy dissipation involves the reorganization of photosystem II light-harvesting complexes in the grana membranes of spinach chloroplasts. Plant Cell 23, 1468-1479. doi: 10.1105/tpc.110.081646
31. Keller, M. M., Jaillais, Y., Pedmale, U. V., Moreno, J. E., Chory, J., and Ballaré, C. L. (2011). Cryptochrome 1 and phytochrome B control shade-avoidance responses inArabidopsis via partially independent hormonal cascades. Plant J. 67, 195-207. doi: 10.1111/j.1365-313X.2011.04598.x
32. Kono, M., and Terashima, I. (2014). Long-term and short-term responses of the photosynthetic electron transport to fluctuating light. J. Photochem. Photobiol. B Biol. 137, 89-99. doi: 10.1016/j.jphotobiol.2014.02.016
33. 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. doi: 10.1016/j.bbabio.2012.12.003
34. Kovács, L., Damkjaer, J., Kereïche, S., Ilioaia, C., Ruban, A. V., and Boekema, E. J. (2006). Lack of the light-harvesting complex CP24 affects the structure and function of the grana membranes of higher plant chloroplasts. Plant Cell 18, 3106-3120. doi: 10.1105/tpc.106.045641
35. Li, X. P., Björkman, O., Shih, C., Grossman, A. R., Rosenquist, M., Jansson, S., et al. (2000). A pigment-binding protein essential for regulation of photosynthetic light harvesting. Nature 403, 391-395. doi: 10.1038/35000131
36. Natale, M., Maresca, B., Abrescia, P., and Bucci, E. (2011). Image analysis workflow for 2-D electrophoresis gels based on ImageJ. Proteomics Insights 4, 37-49. doi: 10.4137/PRI.S7971
37. Nishio, J., Sun, J., and Vogelmann, T. (1993). Carbon fixation gradients across spinach leaves do not follow internal light gradients. Plant Cell 5, 953-961. doi: 10.1105/tpc.5.8.953
38. Page, M., Sultana, N., Paszkiewicz, K., Florance, H., and Smirnoff, N. (2012). The influence of ascorbate on anthocyanin accumulation during high light acclimation inArabidopsis thaliana: further evidence for redox control of anthocyanin synthesis.Plant Cell Environ. 35, 388-404. doi: 10.1111/j.1365-3040.2011.02369.x
39. Park, Y., Chow, W. S., and Anderson, J. M. (1997). Antenna size dependency of photoinactivation of photosystem II in light-acclimated pea leaves. Plant Physiol. 115, 151-157. doi: 10.1104/pp.115.1.151
40. Pietrzykowska, M., Suorsa, M., Semchonok, D. A., Tikkanen, M., Boekema, E. J., Aro, E.-M., et al. (2014). The light-harvesting chlorophyll a/b binding proteins Lhcb1 and Lhcb2 play complementary roles during state transitions in Arabidopsis. Plant Cell 26, 3646-3660. doi: 10.1105/tpc.114.127373
41. Plöscher, M., Granvogl, B., Zoryan, M., Reisinger, V., and Eichacker, L. A. (2009). Mass spectrometric characterization of membrane integral low molecular weight proteins from photosystem II in barley etioplasts. Proteomics 9, 625-635. doi: 10.1002/pmic.200800337
42. Robinson, H., Sharp, R., and Yocum, C. (1980). Effect of manganese on the nuclear magnetic relaxivity of water protons in chloroplast suspensions. Biochem. Biophys. Res. Commun. 93, 755-761. doi: 10.1016/0006-291X(80)91141-9
43. Ruban, A. V., Johnson, M. P., and Duffy, C. D. P. (2012). The photoprotective molecular switch in the photosystem II antenna. Biochim. Biophys. Acta 1817, 167-181. doi: 10.1016/j.bbabio.2011.04.007
44. Schägger, H. (2006). Tricine-SDS-PAGE. Nat. Protoc. 1, 16-22. doi: 10.1038/nprot.2006.4
45. Shi, L.-X., Hall, M., Funk, C., and Schröder, W. P. (2012). Photosystem II, a growing complex: updates on newly discovered components and low molecular mass proteins.Biochim. Biophys. Acta 1817, 13-25. doi: 10.1016/j.bbabio.2011.08.008
46. Suorsa, M., Rantala, M., Mamedov, F., Lespinasse, M., Trotta, A., Grieco, M., et al. (2015). Light acclimation involves dynamic re-organization of the pigment-protein megacomplexes in non-appressed thylakoid domains. Plant J. 84, 360-373. doi: 10.1111/tpj.13004
47. Takabayashi, A., Kadoya, R., Kuwano, M., Kurihara, K., Ito, H., Tanaka, R., et al. (2013). Protein co-migration database (PCoM -DB) for Arabidopsis thylakoids and Synechocystis cells. Springerplus 2:148. doi: 10.1186/2193-1801-2-148
48. Terashima, I., Fujita, T., Inoue, T., Chow, W. S., and Oguchi, R. (2009). Green light drives leaf photosynthesis more efficiently than red light in strong white light: revisiting the enigmatic question of why leaves are green. Plant Cell Physiol. 50, 684-697. doi: 10.1093/pcp/pcp034
49. Tian, L., Dinç, E., and Croce, R. (2015). LHCII Populations in different quenching states are present in the thylakoid membranes in a ratio that depends on the light conditions. J. Phys. Chem. Lett. 6, 2339-2344. doi: 10.1021/acs.jpclett.5b00944
50. Tikkanen, M., and Aro, E.-M. (2012). Thylakoid protein phosphorylation in dynamic regulation of photosystem II in higher plants. Biochim. Biophys. Acta. 1817, 232-238. doi: 10.1016/j.bbabio.2011.05.005
51. Umena, Y., Kawakami, K., Shen, J.-R., and Kamiya, N. (2011). Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9?Å. Nature 473, 55-60. doi: 10.1038/nature09913
52. Vogelmann, T. C., and Han, T. (2000). Measurement of gradients of absorbed light in spinach leaves from chlorophyll fluorescence profiles. Plant Cell Environ. 23, 1303-1311. doi: 10.1046/j.1365-3040.2000.00649.x
53. Weston, E., Thorogood, K., Vinti, G., and López-Juez, E. (2000). Light quantity controls leaf-cell and chloroplast development in Arabidopsis thaliana wild type and blue-light-perception mutants. Planta 211, 807-815. doi: 10.1007/s004250000392
54. Wientjes, E., van Amerongen, H., and Croce, R. (2013a). LHCII is an antenna of both photosystems after long-term acclimation. Biochim. Biophys. Acta 1827, 420-426. doi: 10.1016/j.bbabio.2012.12.009
55. Wientjes, E., Van Amerongen, H., and Croce, R. (2013b). Quantum yield of charge separation in photosystem II: Functional effect of changes in the antenna size upon light acclimation. J. Phys. Chem. B 117, 11200-11208. doi: 10.1021/jp401663w
56. Wientjes, E., Drop, B., Kouril, R., Boekema, E. J., and Croce, R. (2013c). 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. doi: 10.1074/jbc.M113.511691
57. Xu, P., Tian, L., Kloz, M., and Croce, R. (2015). Molecular insights into zeaxanthin-dependent quenching in higher plants. Sci. Rep. 5:13679. doi: 10.1038/srep13679