A unique supramolecular organization of photosystem I in the moss Physcomitrella patens

Iwai, Masakazu; Grob, Patricia; Iavarone, Anthony T.; Nogales, Eva; Niyogi, Krishna K.

doi:10.1038/s41477-018-0271-1

A unique supramolecular organization of photosystem I in the moss Physcomitrella patens

Journal Article · Mon Oct 29 00:00:00 EDT 2018 · Nature Plants

DOI:https://doi.org/10.1038/s41477-018-0271-1· OSTI ID:1532292

^[1]; Grob, Patricia ^[1]; Iavarone, Anthony T. ^[2]; Nogales, Eva ^[1]; ^[1]

Univ. of California, Berkeley, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Univ. of California, Berkeley, CA (United States)

The photosynthesis machinery in chloroplast thylakoid membranes is comprised of multiple protein complexes and supercomplexes. Here, we show a novel supramolecular organization of photosystem I (PSI) in the moss Physcomitrella patens by single-particle cryo-electron microscopy. The moss-specific light-harvesting complex (LHC) protein Lhcb9 is involved in this PSI supercomplex, which has been shown to have a molecular density similar to that of the green alga Chlamydomonas reinhardtii. Our results show that the structural organization is unexpectedly different—two rows of the LHCI belt exist as in C. reinhardtii, but the outer one is shifted toward the PsaK side. Furthermore, one trimeric LHC protein and one monomeric LHC protein position alongside PsaL/K, filling the gap between these subunits and the outer LHCI belt. We provide evidence showing that Lhcb9 is a key factor, acting as a linkage between the PSI core and the outer LHCI belt to form the unique supramolecular organization of the PSI supercomplex in P. patens.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1532292

Journal Information:: Nature Plants, Journal Name: Nature Plants Journal Issue: 11 Vol. 4; ISSN 2055-0278

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

References (36)

UCSF Chimera?A visualization system for exploratory research and analysis Pettersen, Eric F.; Goddard, Thomas D.; Huang, Conrad C. Journal of Computational Chemistry, Vol. 25, Issue 13 https://doi.org/10.1002/jcc.20084	journal	January 2004
Structural and functional diversification of the light-harvesting complexes in photosynthetic eukaryotes Neilson, Jonathan A. D.; Durnford, Dion G. Photosynthesis Research, Vol. 106, Issue 1-2 https://doi.org/10.1007/s11120-010-9576-2	journal	July 2010
Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy Porra, R. J.; Thompson, W. A.; Kriedemann, P. E. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 975, Issue 3 https://doi.org/10.1016/S0005-2728(89)80347-0	journal	August 1989
Supramolecular organization of photosystem I and light-harvesting complex I in Chlamydomonas reinhardtii Germano, Marta; Yakushevska, Alevtyna E.; Keegstra, Wilko FEBS Letters, Vol. 525, Issue 1-3 https://doi.org/10.1016/S0014-5793(02)03100-9	journal	July 2002
Accurate determination of local defocus and specimen tilt in electron microscopy Mindell, Joseph A.; Grigorieff, Nikolaus Journal of Structural Biology, Vol. 142, Issue 3 https://doi.org/10.1016/S1047-8477(03)00069-8	journal	June 2003
A guide to the Lhc genes and their relatives in Arabidopsis Jansson, S. Trends in Plant Science, Vol. 4, Issue 6 https://doi.org/10.1016/S1360-1385(99)01419-3	journal	June 1999
Supramolecular organization of thylakoid membrane proteins in green plants Dekker, Jan P.; Boekema, Egbert J. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1706, Issue 1-2 https://doi.org/10.1016/j.bbabio.2004.09.009	journal	January 2005
Structure, function and regulation of plant photosystem I Jensen, Poul Erik; Bassi, Roberto; Boekema, Egbert J. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1767, Issue 5 https://doi.org/10.1016/j.bbabio.2007.03.004	journal	May 2007
Evolution and function of light harvesting proteins Büchel, Claudia Journal of Plant Physiology, Vol. 172 https://doi.org/10.1016/j.jplph.2014.04.018	journal	January 2015
RELION: Implementation of a Bayesian approach to cryo-EM structure determination Scheres, Sjors H. W. Journal of Structural Biology, Vol. 180, Issue 3, p. 519-530 https://doi.org/10.1016/j.jsb.2012.09.006	journal	December 2012
Light-harvesting antenna complexes in the moss Physcomitrella patens: implications for the evolutionary transition from green algae to land plants Iwai, Masakazu; Yokono, Makio Current Opinion in Plant Biology, Vol. 37 https://doi.org/10.1016/j.pbi.2017.04.002	journal	June 2017
Multi-Level Light Capture Control in Plants and Green Algae Wobbe, Lutz; Bassi, Roberto; Kruse, Olaf Trends in Plant Science, Vol. 21, Issue 1 https://doi.org/10.1016/j.tplants.2015.10.004	journal	January 2016
Structural Characterization of a Complex of Photosystem I and Light-Harvesting Complex II of Arabidopsis thaliana ^† Kouřil, Roman; Zygadlo, Agnieszka; Arteni, Ana A. Biochemistry, Vol. 44, Issue 33 https://doi.org/10.1021/bi051097a	journal	August 2005
Addressing preferred specimen orientation in single-particle cryo-EM through tilting Tan, Yong Zi; Baldwin, Philip R.; Davis, Joseph H. Nature Methods, Vol. 14, Issue 8 https://doi.org/10.1038/nmeth.4347	journal	July 2017
Light-harvesting complex Lhcb9 confers a green alga-type photosystem I supercomplex to the moss Physcomitrella patens Iwai, Masakazu; Yokono, Makio; Kono, Masaru Nature Plants, Vol. 1, Issue 2 https://doi.org/10.1038/nplants.2014.8	journal	January 2015
Structure of the plant photosystem I supercomplex at 2.6 Å resolution Mazor, Yuval; Borovikova, Anna; Caspy, Ido Nature Plants, Vol. 3, Issue 3 https://doi.org/10.1038/nplants.2017.14	journal	March 2017
A LHCB9-dependent photosystem I megacomplex induced under low light in Physcomitrella patens Pinnola, Alberta; Alboresi, Alessandro; Nosek, Lukáš Nature Plants, Vol. 4, Issue 11 https://doi.org/10.1038/s41477-018-0270-2	journal	October 2018
Development of a pVEC peptide-based ribonucleoprotein (RNP) delivery system for genome editing using CRISPR/Cas9 in Chlamydomonas reinhardtii Kang, Seongsu; Jeon, Seungjib; Kim, Seungcheol Scientific Reports, Vol. 10, Issue 1 https://doi.org/10.1038/s41598-020-78968-x	journal	December 2020
Cytochrome f and plastocyanin: their sequence in the photosynthetic electron transport chain of Chlamydomonas reinhardi. Gorman, D. S.; Levine, R. P. Proceedings of the National Academy of Sciences, Vol. 54, Issue 6 https://doi.org/10.1073/pnas.54.6.1665	journal	December 1965
A Red-shifted Antenna Protein Associated with Photosystem II in Physcomitrella patens Alboresi, Alessandro; Gerotto, Caterina; Cazzaniga, Stefano Journal of Biological Chemistry, Vol. 286, Issue 33 https://doi.org/10.1074/jbc.M111.226126	journal	June 2011
Photosystem I of Chlamydomonas reinhardtii Contains Nine Light-harvesting Complexes (Lhca) Located on One Side of the Core Drop, Bartlomiej; Webber-Birungi, Mariam; Fusetti, Fabrizia Journal of Biological Chemistry, Vol. 286, Issue 52 https://doi.org/10.1074/jbc.M111.301101	journal	November 2011
Three-dimensional Reconstruction of a Light-harvesting Complex I- Photosystem I (LHCI-PSI) Supercomplex from the Green Alga Chlamydomonas reinhardtii : INSIGHTS INTO LIGHT HARVESTING FOR PSI Kargul, Joanna; Nield, Jon; Barber, James Journal of Biological Chemistry, Vol. 278, Issue 18 https://doi.org/10.1074/jbc.M300262200	journal	February 2003
A Novel Type of Chloroplast Stromal Hexokinase Is the Major Glucose-phosphorylating Enzyme in the Moss Physcomitrella patens Olsson, Tina; Thelander, Mattias; Ronne, Hans Journal of Biological Chemistry, Vol. 278, Issue 45 https://doi.org/10.1074/jbc.M306265200	journal	August 2003
The Role of Lhca Complexes in the Supramolecular Organization of Higher Plant Photosystem I Wientjes, Emilie; Oostergetel, Gert T.; Jansson, Stefan Journal of Biological Chemistry, Vol. 284, Issue 12 https://doi.org/10.1074/jbc.M808395200	journal	January 2009
Tagged Mutagenesis and Gene-trap in the Moss, Physcomitrella patens by Shuttle Mutagenesis Nishiyama, T. DNA Research, Vol. 7, Issue 1 https://doi.org/10.1093/dnares/7.1.9	journal	January 2000
Effect of the energy supply on filamentous growth and development in Physcomitrella patens Thelander, M. Journal of Experimental Botany, Vol. 56, Issue 412 https://doi.org/10.1093/jxb/eri040	journal	January 2005
Involvement of PpDof1 transcriptional repressor in the nutrient condition-dependent growth control of protonemal filaments in Physcomitrella patens Sugiyama, Takumi; Ishida, Tetsuya; Tabei, Nobumitsu Journal of Experimental Botany, Vol. 63, Issue 8 https://doi.org/10.1093/jxb/ers042	journal	February 2012
Composition and structure of photosystem I in the moss Physcomitrella patens Busch, Andreas; Petersen, Jørgen; Webber-Birungi, Mariam T. Journal of Experimental Botany, Vol. 64, Issue 10 https://doi.org/10.1093/jxb/ert126	journal	May 2013
Molecular Remodeling of Photosystem II during State Transitions in Chlamydomonas reinhardtii Iwai, Masakazu; Takahashi, Yuichiro; Minagawa, Jun The Plant Cell, Vol. 20, Issue 8 https://doi.org/10.1105/tpc.108.059352	journal	August 2008
Programmed Changes in Form during Moss Development. Schumaker, K. S.; Dietrich, M. A. The Plant Cell https://doi.org/10.1105/tpc.9.7.1099	journal	July 1997
Consequences of state transitions on the structural and functional organization of Photosystem I in the green alga Chlamydomonas reinhardtii Drop, Bartlomiej; Yadav K. N., Sathish; Boekema, Egbert J. The Plant Journal, Vol. 78, Issue 2 https://doi.org/10.1111/tpj.12459	journal	March 2014
The Physcomitrella Genome Reveals Evolutionary Insights into the Conquest of Land by Plants Rensing, S. A.; Lang, D.; Zimmer, A. D. Science, Vol. 319, Issue 5859 https://doi.org/10.1126/science.1150646	journal	December 2007
Structural basis for energy transfer pathways in the plant PSI-LHCI supercomplex Qin, X.; Suga, M.; Kuang, T. Science, Vol. 348, Issue 6238 https://doi.org/10.1126/science.aab0214	journal	May 2015
Structure and Energy Transfer in Photosystems of Oxygenic Photosynthesis Nelson, Nathan; Junge, Wolfgang Annual Review of Biochemistry, Vol. 84, Issue 1 https://doi.org/10.1146/annurev-biochem-092914-041942	journal	June 2015
Structure and Function of Photosystems i and ii Nelson, Nathan; Yocum, Charles F. Annual Review of Plant Biology, Vol. 57, Issue 1 https://doi.org/10.1146/annurev.arplant.57.032905.105350	journal	June 2006
In Silico and Biochemical Analysis of Physcomitrella patens Photosynthetic Antenna: Identification of Subunits which Evolved upon Land Adaptation Alboresi, Alessandro; Caffarri, Stefano; Nogue, Fabien PLoS ONE, Vol. 3, Issue 4 https://doi.org/10.1371/journal.pone.0002033	journal	April 2008

Cited By (5)

Formation of a PSI–PSII megacomplex containing LHCSR and PsbS in the moss Physcomitrella patens Furukawa, Ryo; Aso, Michiki; Fujita, Tomomichi Journal of Plant Research, Vol. 132, Issue 6 https://doi.org/10.1007/s10265-019-01138-2	journal	September 2019
Natively oxidized amino acid residues in the spinach PS I-LHC I supercomplex Kale, Ravindra; Sallans, Larry; Frankel, Laurie K. Photosynthesis Research, Vol. 143, Issue 3 https://doi.org/10.1007/s11120-019-00698-7	journal	January 2020
A LHCB9-dependent photosystem I megacomplex induced under low light in Physcomitrella patens Pinnola, Alberta; Alboresi, Alessandro; Nosek, Lukáš Nature Plants, Vol. 4, Issue 11 https://doi.org/10.1038/s41477-018-0270-2	journal	October 2018
The rise and fall of Light-Harvesting Complex Stress-Related proteins as photoprotection agents during evolution Pinnola, Alberta Journal of Experimental Botany, Vol. 70, Issue 20 https://doi.org/10.1093/jxb/erz317	journal	August 2019
Isolation and characterization of a large photosystem I–light‐harvesting complex II supercomplex with an additional Lhca1–a4 dimer in Arabidopsis Crepin, Aurélie; Kučerová, Zuzana; Kosta, Artemis The Plant Journal, Vol. 102, Issue 2 https://doi.org/10.1111/tpj.14634	journal	January 2020