Structure of spinach photosystem II-LHCII supercomplex at 3.2 Å resolution

Nature

Volumn 534, Issue 7605, 2016, Pages 69-74

  Wei, Xuepeng ^a,b   Su, Xiaodong ^a   Cao, Peng ^a   Liu, Xiuying ^a,b   Chang, Wenrui ^a   Li, Mei ^a   Zhang, Xinzheng ^a   Liu, Zhenfeng ^a  

^a INSTITUTE OF BIOPHYSICS   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CAROTENOID; CHLOROPHYLL; MONOMER; LIGHT HARVESTING SYSTEM; PHOTOSYSTEM II; PROTEIN SUBUNIT;

BIOLOGICAL ANALYSIS; CHLOROPHYLL; LEAFY VEGETABLE; OXYGEN; PHOTOSYNTHESIS; PHYSIOLOGY; PROTEIN;

ARTICLE; CRYOELECTRON MICROSCOPY; ENERGY TRANSFER; LIGHT HARVESTING COMPLEX II; LIGHT HARVESTING SYSTEM; PHOTOSYSTEM II; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN SUBUNIT; SPINACH; CHEMISTRY; ELECTRON TRANSPORT; ULTRASTRUCTURE;

SPINACIA OLERACEA;

CAROTENOIDS; CHLOROPHYLL; CRYOELECTRON MICROSCOPY; ELECTRON TRANSPORT; LIGHT-HARVESTING PROTEIN COMPLEXES; PHOTOSYSTEM II PROTEIN COMPLEX; PROTEIN SUBUNITS; SPINACIA OLERACEA;

EID: 84969857920     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature18020     Document Type: Article

References (66)

1. Nelson, N. & Junge, W. Structure and energy transfer in photosystems of oxygenic photosynthesis. Annu. Rev. Biochem. 84, 659-683 (2015).
2. Shen, J.-R. The structure of photosystem II and the mechanism of water oxidation in photosynthesis. Annu. Rev. Plant Biol. 66, 23-48 (2015).
3. Vinyard, D. J., Ananyev, G. M. & Dismukes, G. C. Photosystem II: The reaction center of oxygenic photosynthesis. Annu. Rev. Biochem. 82, 577-606 (2013).
4. Pan, X., Liu, Z., Li, M. & Chang, W. Architecture and function of plant light-harvesting complexes II. Curr. Opin. Struct. Biol. 23, 515-525 (2013).
5. Barros, T. & Kühlbrandt, W. Crystallisation, structure and function of plant light-harvesting Complex II. Biochim. Biophys. Acta 1787, 753-772 (2009).
6. Croce, R. & van Amerongen, H. Natural strategies for photosynthetic light harvesting. Nature Chem. Biol. 10, 492-501 (2014).
7. Umena, Y., Kawakami, K., Shen, J.-R. & Kamiya, N. Crystal structure of oxygen-evolving photosystem II at a resolution of 1. 9 Å. Nature 473, 55-60 (2011).
8. Suga, M. et al. Native structure of photosystem II at 1. 95 Å resolution viewed by femtosecond X-ray pulses. Nature 517, 99-103 (2015).
9. Rhee, K.-H., Morris, E. P., Barber, J. & Kuhlbrandt, W. Three-dimensional structure of the plant photosystem II reaction centre at 8 Å resolution. Nature 396, 283-286 (1998).
10. Hankamer, B., Morris, E. P. & Barber, J. Revealing the structure of the oxygen-evolving core dimer of photosystem II by cryoelectron crystallography. Nature Struct. Mol. Biol. 6, 560-564 (1999).
11. Hankamer, B., Morris, E., Nield, J., Gerle, C. & Barber, J. Three-dimensional structure of the photosystem II core dimer of higher plants determined by electron microscopy. J. Struct. Biol. 135, 262-269 (2001).
12. Liu, Z. et al. Crystal structure of spinach major light-harvesting complex at 2. 72 Å resolution. Nature 428, 287-292 (2004).
13. Standfuss, J., Terwisscha van Scheltinga, A. C., Lamborghini, M. & Kühlbrandt, W. Mechanisms of photoprotection and nonphotochemical quenching in pea light-harvesting complex at 2. 5 Å resolution. EMBO J. 24, 919-928 (2005).
14. Pan, X. et al. Structural insights into energy regulation of light-harvesting complex CP29 from spinach. Nature Struct. Mol. Biol. 18, 309-315 (2011).
15. Nield, J. & Barber, J. Refinement of the structural model for the Photosystem II supercomplex of higher plants. Biochim. Biophys. Acta 1757, 353-361 (2006).
16. Caffarri, S., Kouril, R., Kereiche, S., Boekema, E. J. & Croce, R. Functional architecture of higher plant photosystem II supercomplexes. EMBO J. 28, 3052-3063 (2009).
17. Drop, B. et al. Light-harvesting complex II (LHCII) and its supramolecular organization in Chlamydomonas reinhardtii. Biochim. Biophys. Acta 1837, 63-72 (2014).
18. Guskov, A. et al. Cyanobacterial photosystem II at 2. 9-Å resolution and the role of quinones, lipids, channels and chloride. Nature Struct. Mol. Biol. 16, 334-342 (2009).
19. Ferreira, K. N., Iverson, T. M., Maghlaoui, K., Barber, J. & Iwata, S. Architecture of the photosynthetic oxygen-evolving center. Science 303, 1831-1838 (2004).
20. Garcia-Cerdán, J. G. et al. The PsbW protein stabilizes the supramolecular organization of photosystem II in higher plants. Plant J. 65, 368-381 (2011).
21. Ago, H. et al. Novel features of eukaryotic photosystem II revealed by its crystal structure analysis from a red alga. J. Biol. Chem. 291, 5676-5687 (2016).
22. Shi, L. X. & Schroder, W. P. The low molecular mass subunits of the photosynthetic supracomplex, photosystem II. Biochim. Biophys. Acta 1608, 75-96 (2004).
23. Ballottari, M., Mozzo, M., Croce, R., Morosinotto, T. & Bassi, R. Occupancy and functional architecture of the pigment binding sites of photosystem II antenna complex Lhcb5. J. Biol. Chem. 284, 8103-8113 (2009).
24. Bricker, T. M., Roose, J. L., Fagerlund, R. D., Frankel, L. K. & Eaton-Rye, J. J. The extrinsic proteins of Photosystem II. Biochim. Biophys. Acta 1817, 121-142 (2012).
25. Ido, K. et al. Cross-linking evidence for multiple interactions of the PsbP and PsbQ proteins in a higher plant photosystem II supercomplex. J. Biol. Chem. 289, 20150-20157 (2014).
26. Mummadisetti, M. P. et al. Use of protein cross-linking and radiolytic footprinting to elucidate PsbP and PsbQ interactions within higher plant Photosystem II. Proc. Natl Acad. Sci. USA 111, 16178-16183 (2014).
27. Kapazoglou, A., Sagliocco, F. & Dure, L. PSII-T, a new nuclear encoded lumenal protein from photosystem II: Targeting and processing in isolated chloroplasts. J. Biol. Chem. 270, 12197-12202 (1995).
28. Shabestari, M. H., Wolfs, C. J. A. M. & Spruijt, R. B. van Amerongen, H. & Huber, M. Exploring the structure of the 100 amino-acid residue long N-terminus of the plant antenna protein CP29. Biophys. J. 106, 1349-1358 (2014).
29. Qin, X., Suga, M., Kuang, T. & Shen, J. R. Photosynthesis. Structural basis for energy transfer pathways in the plant PSI-LHCI supercomplex. Science 348, 989-995 (2015).
30. Mazor, Y., Borovikova, A. & Nelson, N. The structure of plant photosystem I super-complex at 2. 8 Å resolution. eLife 4, e07433 (2015).
31. Caffarri, S., Passarini, F., Bassi, R. & Croce, R. A specific binding site for neoxanthin in the monomeric antenna proteins CP26 and CP29 of Photosystem II. FEBS Lett. 581, 4704-4710 (2007).
32. Yakushevska, A. E. et al. The structure of photosystem II in Arabidopsis: localization of the CP26 and CP29 antenna complexes. Biochemistry 42, 608-613 (2003).
33. de Bianchi, S. et al. Arabidopsis mutants deleted in the light-harvesting protein Lhcb4 have a disrupted photosystem II macrostructure and are defective in photoprotection. Plant Cell 23, 2659-2679 (2011).
34. Ruf, S., Biehler, K. & Bock, R. A small chloroplast-encoded protein as a novel architectural component of the light-harvesting antenna. J. Cell Biol. 149, 369-378 (2000).
35. Baena-González, E., Gray, J. C., Tyystjärvi, E., Aro, E.-M. & Mäenpää, P. Abnormal regulation of photosynthetic electron transport in a chloroplast ycf9 inactivation mutant. J. Biol. Chem. 276, 20795-20802 (2001).
36. Swiatek, M. et al. The chloroplast gene ycf9 encodes a photosystem II (PSII) core subunit, PsbZ, that participates in PSII supramolecular architecture. Plant Cell 13, 1347-1368 (2001).
37. Remelli, R., Varotto, C., Sandona, D., Croce, R. & Bassi, R. Chlorophyll binding to monomeric light-harvesting complex. A mutation analysis of chromophorebinding residues. J. Biol. Chem. 274, 33510-33521 (1999).
38. Rogl, H. & Kühlbrandt, W. Mutant trimers of light-harvesting complex II exhibit altered pigment content and spectroscopic features. Biochemistry 38, 16214-16222 (1999).
39. Novoderezhkin, V. I., Palacios, M. A., van Amerongen, H. & van Grondelle, R. Excitation dynamics in the LHCII complex of higher plants: modeling based on the 2. 72 Å crystal structure. J. Phys. Chem. B 109, 10493-10504 (2005).
40. Novoderezhkin, V., Marin, A. & van Grondelle, R. Intra-and inter-monomeric transfers in the light harvesting LHCII complex: The Redfield-Förster picture. Phys. Chem. Chem. Phys. 13, 17093-17103 (2011).
41. Sun, R. et al. Direct energy transfer from the major antenna to the photosystem II core complexes in the absence of minor antennae in liposomes. Biochim. Biophys. Acta 1847, 248-261 (2015).
42. Dall'Osto, L., Ünlü, C., Cazzaniga, S. & van Amerongen, H. Disturbed excitation energy transfer in Arabidopsis thaliana mutants lacking minor antenna complexes of photosystem II. Biochim. Biophys. Acta 1837, 1981-1988 (2014).
43. Mozzo, M., Passarini, F., Bassi, R., van Amerongen, H. & Croce, R. Photoprotection in higher plants: The putative quenching site is conserved in all outer light-harvesting complexes of Photosystem II. Biochim. Biophys. Acta 1777, 1263-1267 (2008).
44. Ahn, T. K. et al. Architecture of a charge-transfer state regulating light harvesting in a plant antenna protein. Science 320, 794-797 (2008).
45. Pascal, A. A. et al. Molecular basis of photoprotection and control of photosynthetic light-harvesting. Nature 436, 134-137 (2005).
46. Caffarri, S., Broess, K., Croce, R. & van Amerongen, H. Excitation energy transfer and trapping in higher plant Photosystem II complexes with different antenna sizes. Biophys. J. 100, 2094-2103 (2011).
47. Bennett, D. I. G., Amarnath, K. & Fleming, G. R. A. Structure-based model of energy transfer reveals the principles of light harvesting in photosystem II supercomplexes. J. Am. Chem. Soc. 135, 9164-9173 (2013).
48. Schägger, H. Tricine-SDS-PAGE. Nature Protocols 1, 16-22 (2006).
49. Färber, A., Young, A. J., Ruban, A. V., Horton, P. & Jahns, P. Dynamics of xanthophyll-cycle activity in different antenna subcomplexes in the photosynthetic membranes of higher plants (the relationship between zeaxanthin conversion and nonphotochemical fluorescence quenching). Plant Physiol. 115, 1609-1618 (1997).
50. Li, X. et al. Electron counting and beam-induced motion correction enable near-atomic-resolution single-particle cryo-EM. Nature Methods 10, 584-590 (2013).
51. Mindell, J. A. & Grigorieff, N. Accurate determination of local defocus and specimen tilt in electron microscopy. J. Struct. Biol. 142, 334-347 (2003).
52. Tang, G. et al. EMAN2: An extensible image processing suite for electron microscopy. J. Struct. Biol. 157, 38-46 (2007).
53. Scheres, S. H. W. RELION: Implementation of a Bayesian approach to cryo-EM structure determination. J. Struct. Biol. 180, 519-530 (2012).
54. Pettersen, E. F. et al. UCSF Chimera-a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612 (2004).
55. Emsley, P., Lohkamp, B., Scott, W. G. & Cowtan, K. Features and development of Coot. Acta Crystallogr. D 66, 486-501 (2010).
56. Allahverdiyeva, Y. et al. Insights into the function of PsbR protein in Arabidopsis thaliana. Biochim. Biophys. Acta 1767, 677-685 (2007).
57. Koua, F. H. M., Umena, Y., Kawakami, K. & Shen, J.-R. Structure of Sr-substituted photosystem II at 2. 1 Å resolution and its implications in the mechanism of water oxidation. Proc. Natl Acad. Sci. USA 110, 3889-3894 (2013).
58. Li, X. P. et al. A pigment-binding protein essential for regulation of photosynthetic light harvesting. Nature 403, 391-395 (2000).
59. Fan, M. et al. Crystal structures of the PsbS protein essential for photoprotection in plants. Nature Struct. Mol. Biol. 22, 729-735 (2015).
60. Adams, P. D. et al. PHENIX: A comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D 66, 213-221 (2010).
61. Murshudov, G. N. et al. REFMAC5 for the refinement of macromolecular crystal structures. Acta Crystallogr. D 67, 355-367 (2011).
62. Winn, M. D. et al. Overview of the CCP4 suite and current developments. Acta Crystallogr. D 67, 235-242 (2011).
63. Green, B. R. & Durnford, D. G. The chlorophyll-carotenoid proteins of oxygenic photosynthesis. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47, 685-714 (1996).
64. Das, S. K. & Frank, H. A. Pigment compositions, spectral properties, and energy transfer efficiencies between the xanthophylls and chlorophylls in the major and minor pigment? protein complexes of photosystem II. Biochemistry 41, 13087-13095 (2002).
65. Pascal, A. et al. Spectroscopic characterization of the spinach Lhcb4 protein (CP29), a minor light-harvesting complex of photosystem II. Eur. J. Biochem. 262, 817-823 (1999).
66. van Amerongen, H. et al. Spectroscopic characterization of CP26, a chlorophyll ab binding protein of the higher plant Photosystem II complex. Biochim. Biophys. Acta 1188, 227-234 (1994).