Structure of plant photosystem I-light harvesting complex I supercomplex at 2.4 Å resolution.

crystal structure, Lhca, LHCI, light-harvesting pea photosynthesis photosystem I

Journal

Journal of integrative plant biology
ISSN: 1744-7909
Titre abrégé: J Integr Plant Biol
Pays: China (Republic : 1949- )
ID NLM: 101250502

Informations de publication

Date de publication:
Jul 2021
Historique:
received: 10 12 2020
accepted: 14 03 2021
pubmed: 1 4 2021
medline: 28 12 2021
entrez: 31 3 2021
Statut: ppublish

Résumé

Photosystem I (PSI) is one of the two photosystems in photosynthesis, and performs a series of electron transfer reactions leading to the reduction of ferredoxin. In higher plants, PSI is surrounded by four light-harvesting complex I (LHCI) subunits, which harvest and transfer energy efficiently to the PSI core. The crystal structure of PSI-LHCI supercomplex has been analyzed up to 2.6 Å resolution, providing much information on the arrangement of proteins and cofactors in this complicated supercomplex. Here we have optimized crystallization conditions, and analyzed the crystal structure of PSI-LHCI at 2.4 Å resolution. Our structure showed some shift of the LHCI, especially the Lhca4 subunit, away from the PSI core, suggesting the indirect connection and inefficiency of energy transfer from this Lhca subunit to the PSI core. We identified five new lipids in the structure, most of them are located in the gap region between the Lhca subunits and the PSI core. These lipid molecules may play important roles in binding of the Lhca subunits to the core, as well as in the assembly of the supercomplex. The present results thus provide novel information for the elucidation of the mechanisms for the light-energy harvesting, transfer and assembly of this supercomplex.

Identifiants

pubmed: 33788400
doi: 10.1111/jipb.13095
doi:

Substances chimiques

Photosystem I Protein Complex 0
Chlorophyll 1406-65-1

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

1367-1381

Subventions

Organisme : National Key Research and Development Program of China
Organisme : Chinese Academy of Sciences Key Research Program of Frontier Sciences
Organisme : Strategic Priority Research Program of CAS
Organisme : National Basic Research Program of China
Organisme : National Natural Science Foundation of China
Organisme : Youth Innovation Promotion Association of CAS
Organisme : Taishan Scholars Project, and the Natural Science Foundation of Shandong Province China

Informations de copyright

© 2021 Institute of Botany, Chinese Academy of Sciences.

Références

Adams, P.D., Afonine, P.V., Bunkóczi, G., Chen, V.B., Davis, I.W., Echols, N., Headd, J.J., Hung, L.W., Kapral, G.J., Grosse-Kunstleve, R.W., McCoy, A.J., Moriarty, N.W., Oeffner, R., Read, R.J., Richardson, D.C., Richardson, J.S., Terwilliger, T.C., and Zwart, P.H. (2010). PHENIX: A comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66: 213-221.
Alcorn, T., and Juers, D.H. (2010). Progress in rational methods of cryoprotection in macromolecular crystallography. Acta Crystallogr. D Biol. Crystallogr. 66: 366-373.
Amunts, A., Drory, O., and Nelson, N. (2007). The structure of a plant photosystem I supercomplex at 3.4 Å resolution. Nature 447: 58-63.
Antoshvili, M., Caspy, I., Hippler, M., and Nelson, N. (2018). Structure and function of photosystem I in Cyanidioschyzon merolae. Photosynth. Res. 139: 499-508.
Bailey, S., Walters, R.G., and Horton, J.P. (2001). Acclimation of Arabidopsis thaliana to the light environment: The existence of separate low light and high light responses. Planta 213: 794-801.
Ben-Shem, A., Frolow, F., and Nelson, N. (2003). Crystal structure of plant photosystem I. Nature 426: 630-635.
Chen, M., Perez-Boerema, A., Zhang, L., Li, Y., Yang, M., Li, S., and Amunts, A. (2020). Distinct structural modulation of photosystem I and lipid environment stabilizes its tetrameric assembly. Nat. Plants 6: 314-320.
Croce, R. (2020). Beyond ‘seeing is believing’: The antenna size of the photosystems in vivo. New Phytol. 228: 1214-1218.
Dall'Osto, L., Bressan, M., and Bassi, R. (2015). Biogenesis of light harvesting proteins. Biochim. Biophys. Acta 1847: 861-871.
Emsley, P., and Cowtan, K. (2004). Coot: Model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60: 2126-2132.
Hasan, S.S., Yamashita, E., Ryan, C.M., Whitelegge, J.P., and Cramer, W.A. (2011). Conservation of lipid functions in cytochrome bc complexes. J. Mol. Biol. 414: 145-162.
Kato, K., Nagao, R., Jiang, T.Y., Ueno, Y., Yokono, M., Chan, S.K., Watanabe, M., Ikeuchi, M., Shen, J.-R., Akimoto, S., Miyazaki, N., and Akita, F. (2019). Structure of a cyanobacterial photosystem I tetramer revealed by cryo-electron microscopy. Nat. Commun. 10: 4929.
Jansson, S. (1999). A guide to the Lhc genes and their relatives in Arabidopsis. Trends Plant Sci. 4: 236-240.
Jordan, P., Fromme, P., Witt, H.T., Klukas, O., Saenger, W., and Krauss, N. (2001). Three-dimensional structure of cyanobacterial photosystem I at 2.5 Å resolution. Nature 411: 909-917.
Juers, D.H., and Matthews, B.W. (2004). Cryo-cooling in macromolecular crystallography: Advantages, disadvantages and optimization. Q. Rev. Biophys. 37: 105-119.
Kansy, M., Wilhelm, C., and Goss, R. (2014). Influence of thylakoid membrane lipids on the structure and function of the plant photosystem II core complex. Planta 240: 781-796.
Kawamoto, M., Kawano, Y., and Kamiya, N. (2001). The bio-crystallography beamline (BL41XU) at SPring-8. Nucl. Instrum. Methods A467-468: 1375-1379.
Kriminski, S., Caylor, C.L., Nonato, M.C., Finkelstein, K.D., and Thorne, R.E. (2002). Flash-cooling and annealing of protein crystals. Acta Crystallogr. D Biol. Crystallogr. 58: 459-471.
Liu, H., and Blankenship, R.E. (2019). On the interface of light-harvesting antenna complexes and reaction centers in oxygenic photosynthesis. Biochim. Biophys. Acta Bioenerg. 1860: 148079.
Malavath, T., Caspy, I., Netzer-El, S.Y., Klaiman, D., and Nelson, N. (2018). Structure and function of wild-type and subunit-depleted photosystem I in Synechocystis. Biochim. Biophys. Acta Bioenerg. 1859: 645-654.
Mazor, Y., Anna, B., and Nathan, N. (2015). The structure of plant photosystem I super-complex at 2.8 Å resolution. eLife 4: e07433.
Mazor, Y., Borovikova, A., Caspy, I., and Nelson, N. (2017). Structure of the plant photosystem I supercomplex at 2.6 Å resolution. Nat. Plants 3: 17014.
Mizusawa, N., and Wada, H. (2012). The role of lipids in photosystem II. Biochim. Biophys. Acta 1817: 194-208.
Nagao, R., Kato, K., Ifuku, K., Suzuki, T., Kumazawa, M., Uchiyama, I., Kashino, Y., Dohmae, N., Akimoto, S., Shen, J.-R., Miyazaki, N., and Akita, F. (2020). Structural basis for assembly and function of a diatom photosystem I-light-harvesting supercomplex. Nat. Commun. 11: 2481.
Nakajima, Y., Umena, Y., Nagao, R., Endo, K., Kobayashi, K., Akita, F., Suga, M., Wada, H., Noguchi, T., and Shen, J.-R. (2018). Thylakoid membrane lipid sulfoquinovosyl-diacylglycerol (SQDG) is required for full functioning of photosystem II in Thermosynechococcus elongatus. J. Biol. Chem. 293: 14786-14797.
Nellaepalli, S., Zsiros, O., Tóth, T., Yadavalli, V., Garab, G., Subramanyam, R., and Kovács, L. (2014). Heat- and light-induced detachment of the light harvesting complex from isolated photosystem I supercomplexes. J. Photochem. Photobiol. B 137: 13-20.
Nelson, N., and Junge, W. (2015). Structure and energy transfer in photosystems of oxygenic photosynthesis. Annu. Rev. Biochem. 84: 659-683.
Otwinowski, Z., and Minor, W. (1997). Processing of x-ray diffraction data collected in oscillation mode. Methods Enzymol. 276: 307-326.
Ozawa, S., Onishi, T., and Takahashi, Y. (2010). Identification and characterization of an assembly intermediate subcomplex of photosystem I in the green alga Chlamydomonas reinhardtii. J. Biol. Chem. 285: 20072-20079.
Pan, X., Cao, P., Su, X., Liu, Z., and Li, M. (2020). Structural analysis and comparison of light-harvesting complexes I and II. Biochim. Biophys. Acta Bioenerg. 1861: 148038.
Pan, X., Ma, J., Su, X., Cao, P., Chang, W., Liu, Z., Zhang, X., and Li, M. (2018). Structure of the maize photosystem I supercomplex with light-harvesting complexes I and II. Science 360: 1109-1113.
Pi, X., Tian, L., Dai, H., Qin, X., Cheng, L., Kuang, T., Sui, S.F., and Shen, J.-R. (2018). Unique organization of photosystem I-light-harvesting supercomplex revealed by cryo-EM from a red alga. Proc. Natl. Acad. Sci. USA 115: 4423-4428.
Qin, X., Pi, X., Wang, W., Han, G., Zhu, L., Liu, M., Cheng, L., Shen, J.-R., Kuang, T., and Sui, S.F. (2019). Structure of a green algal photosystem I in complex with a large number of light-harvesting complex I subunits. Nat. Plants 5: 263-272.
Qin, X., Suga, M., Kuang, T., and Shen, J.-R. (2015). Structural basis for energy transfer pathways in the plant PSI-LHCI supercomplex. Science 348: 989-995.
Rupp, B. (2010). Biomolecular crystallography. Garland Science. New York: Taylor & Francis Group, LLC.
Shen, C., Julius, E.F., Tyree, T.J., Moreau, D.W., Atakisi, H., and Thorne, R.E. (2016). Thermal contraction of aqueous glycerol and ethylene glycol solutions for optimized protein-crystal cryoprotection. Acta Crystallogr. D Struct. Biol. 72: 742-752.
Su, X., Ma, J., Pan, X., Zhao, X., Chang, W., Liu, Z., Zhang, X., and Li, M. (2019). Antenna arrangement and energy transfer pathways of a green algal photosystem-I-LHCI supercomplex. Nat. Plants 5: 273-281.
Suga, M., Ozawa, S.I., Yoshida-Motomura, K., Akita, F., Miyazaki, N., and Takahashi, Y. (2019). Structure of the green algal photosystem supercomplex with a decameric light-harvesting complex I. Nat. Plants 5: 626-636.
Suga, M., Qin, X., Kuang, T., and Shen, J.-R. (2016). Structure and energy transfer pathways of the plant photosystem I-LHCI supercomplex. Curr. Opin. Struct. Biol. 39: 46-53.
Suga, M., and Shen, J.-R. (2020). Structural variations of photosystem I-antenna supercomplex in response to adaptations to different light environments. Curr. Opin. Struct. Biol. 63: 10-17.
Wang, Q.S., Zhang, K.H., Cui, Y., Wang, Z.J., Pan, Q.Y., Liu, K., Sun, B., Zhou, H., Li, M.J., Xu, Q., Xu, C.Y., Yu, F., and He, J.H. (2018). Upgrade of macromolecular crystallography beamline BL17U1 at SSRF. Nucl. Sci. Tech. 29: 68.
Wientjes, E., and Croce, R. (2011). The light-harvesting complexes of higher-plant Photosystem I: Lhca1/4 and Lhca2/3 form two red-emitting heterodimers. Biochem. J. 433: 477-485.
Wientjes, E., Oostergetel, G.T., Jansson, S., Boekema, E.J., and Croce, R. (2009). The role of lhca complexes in the supramolecular organization of higher plant photosystem I. J. Biol. Chem. 284: 7803-7810.
Wittenberg, G., Järvi, S., Hojka, M., Tóth, S.Z., Meyer, E.H., Aro, E.M., Schöttler, M.A., and Bock, R. (2017). Identification and characterization of a stable intermediate in photosystem I assembly in tobacco. Plant J. 90: 478-490.
Xu, C., Pi, X., Huang, Y., Han, G., Chen, X., Qin, X., Huang, G., Zhao, S., Yang, Y., Kuang, T., Wang, W., Sui, S.F., and Shen, J.-R. (2020). Structural basis for energy transfer in a huge diatom PSI-FCPI supercomplex. Nat. Commun. 11: 5081.
Yan, Q., Zhao, L., Wang, W., Pi, X., Han, G., Wang, J., Cheng, L., He, Y.-K., Kuang, T., Qin, X., Sui, S.F., and Shen, J.-R. (2021). Antenna arrangement and energy transfer pathways of PSI-LHCI from the moss Physcomitrella patens. Cell Discov. 7: 10.
Zhang, C.Y., Wu, Z.Q., Yin, D.C., Zhou, B.R., Guo, Y.Z., Lu, H.M., Zhou, R.B., and Shang, P. (2013). A strategy for selecting the pH of protein solutions to enhance crystallization. Acta Crystallogr. Sect. F. Struct. Biol. Cryst. Commun. 69: 821-826.
Zheng, L., Li, Y., Li, X., Zhong, Q., Li, N., Zhang, K., Zhang, Y., Chu, H., Ma, C., Li, G., Zhao, J., and Gao, N. (2019). Structural and functional insights into the tetrameric photosystem I from heterocyst-forming cyanobacteria. Nat. Plants 5: 1087-1097.

Auteurs

Jie Wang (J)

Photosynthesis Research Center, Key Laboratory of Photobiology, Institute of Botany, Chinese Academy of Sciences, Beijing, 100093, China.
University of Chinese Academy of Sciences, Beijing, 100049, China.

Long-Jiang Yu (LJ)

Photosynthesis Research Center, Key Laboratory of Photobiology, Institute of Botany, Chinese Academy of Sciences, Beijing, 100093, China.

Wenda Wang (W)

Photosynthesis Research Center, Key Laboratory of Photobiology, Institute of Botany, Chinese Academy of Sciences, Beijing, 100093, China.

Qiujing Yan (Q)

Photosynthesis Research Center, Key Laboratory of Photobiology, Institute of Botany, Chinese Academy of Sciences, Beijing, 100093, China.
University of Chinese Academy of Sciences, Beijing, 100049, China.

Tingyun Kuang (T)

Photosynthesis Research Center, Key Laboratory of Photobiology, Institute of Botany, Chinese Academy of Sciences, Beijing, 100093, China.

Xiaochun Qin (X)

School of Biological Science and Technology, University of Jinan, Jinan, 250022, China.

Jian-Ren Shen (JR)

Photosynthesis Research Center, Key Laboratory of Photobiology, Institute of Botany, Chinese Academy of Sciences, Beijing, 100093, China.
Research Institute for Interdisciplinary Science, and Graduate School of Natural Science and Technology, Okayama University, Okayama, 700-8530, Japan.

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