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Chemical Protein Crosslinking-Coupled Mass Spectrometry Reveals Interaction of LHCI with LHCII and LHCSR3 in Chlamydomonas reinhardtii
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Abstract
The photosystem I (PSI) of the green alga Chlamydomonas reinhardtii associates with 10 light-harvesting proteins (LHCIs) to form the PSI-LHCI complex. In the context of state transitions, two LHCII trimers bind to the PSAL, PSAH and PSAO side of PSI to produce the PSI-LHCI-LHCII complex. In this work, we took advantage of chemical crosslinking of proteins in conjunction with mass spectrometry to identify protein–protein interactions between the light-harvesting proteins of PSI and PSII. We detected crosslinks suggesting the binding of LHCBM proteins to the LHCA1-PSAG side of PSI as well as protein–protein interactions of LHCSR3 with LHCA5 and LHCA3. Our data indicate that the binding of LHCII to PSI is more versatile than anticipated and imply that LHCSR3 might be involved in the regulation of excitation energy transfer to the PSI core via LHCA5/LHCA3.
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Highly accurate protein structure prediction with AlphaFold
Jumper, J., Evans, R., Pritzel, A., Green, T., Figurnov, M., Ronneberger, O., Tunyasuvunakool, K., Bates, R., Žídek, A., Potapenko, A., et al. (2021) · Nature · doi:10.1038/s41586-021-03819-2 · Cited by 43,764
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Research works printed but not linked: 74
- Whatley, 1963, Separation of Light and Dark Reactions in Electron Transfer during Photosynthesis, Proc. Natl. Acad. Sci. USA, 49, 266, 10.1073/pnas.49.2.266 · DOI
- Mitchell, 1961, Coupling of phosphorylation to electron and hydrogen transfer by a chemi-osmotic type of mechanism, Nature, 191, 144, 10.1038/191144a0 · DOI · Paper page
- Frolow, 2003, Crystal structure of plant photosystem I, Nature, 426, 630, 10.1038/nature02200 · DOI
- Amunts, 2007, The structure of a plant photosystem I supercomplex at 3.4 A resolution, Nature, 447, 58, 10.1038/nature05687 · DOI
- Jordan, 2001, Three-dimensional structure of cyanobacterial photosystem I at 2.5 A resolution, Nature, 411, 909, 10.1038/35082000 · DOI
- Nelson, 2004, The complex architecture of oxygenic photosynthesis, Nat. Rev. Mol. Cell Biol., 5, 971, 10.1038/nrm1525 · DOI
- Mazor, 2017, Structure of the plant photosystem I supercomplex at 2.6 A resolution, Nat. Plants, 3, 17014, 10.1038/nplants.2017.14 · DOI
- Mazor, 2015, The structure of plant photosystem I super-complex at 2.8 A resolution, eLife, 4, e07433, 10.7554/eLife.07433 · DOI
- Qin, 2015, Photosynthesis. Structural basis for energy transfer pathways in the plant PSI-LHCI supercomplex, Science, 348, 989, 10.1126/science.aab0214 · DOI
- Suga, 2019, Structure of the green algal photosystem I supercomplex with a decameric light-harvesting complex I, Nat. Plants, 5, 626, 10.1038/s41477-019-0438-4 · DOI
- Tokutsu, 2019, Ten antenna proteins are associated with the core in the supramolecular organization of the photosystem I supercomplex in Chlamydomonas reinhardtii, J. Biol. Chem., 294, 4304, 10.1074/jbc.RA118.006536 · DOI
- Ozawa, 2018, Configuration of Ten Light-Harvesting Chlorophyll a/b Complex I Subunits in Chlamydomonas reinhardtii Photosystem I, Plant Physiol., 178, 583, 10.1104/pp.18.00749 · DOI
- Su, 2019, Antenna arrangement and energy transfer pathways of a green algal photosystem-I-LHCI supercomplex, Nat. Plants, 5, 273, 10.1038/s41477-019-0380-5 · DOI
- Qin, 2019, Structure of a green algal photosystem I in complex with a large number of light-harvesting complex I subunits, Nat. Plants, 5, 263, 10.1038/s41477-019-0379-y · DOI
- Crepin, 2020, Isolation and characterization of a large photosystem I-light-harvesting complex II supercomplex with an additional Lhca1-a4 dimer in Arabidopsis, Plant J., 102, 398, 10.1111/tpj.14634 · DOI
- Rochaix, 2014, Regulation and dynamics of the light-harvesting system, Annu. Rev. Plant Biol., 65, 287, 10.1146/annurev-arplant-050213-040226 · DOI
- Murata, 1969, Control of excitation transfer in photosynthesis. I. Light-induced change of chlorophyll a fluorescence in Porphyridium cruentum, Biochim. Biophys. Acta, 172, 242, 10.1016/0005-2728(69)90067-X · DOI
- Bonaventura, 1969, Fluorescence and oxygen evolution from Chlorella pyrenoidosa, Biochim. Biophys. Acta, 189, 366, 10.1016/0005-2728(69)90168-6 · DOI
- Lemeille, 2010, State transitions at the crossroad of thylakoid signalling pathways, Photosynth. Res., 106, 33, 10.1007/s11120-010-9538-8 · DOI
- Rochaix, 2012, Protein kinases and phosphatases involved in the acclimation of the photosynthetic apparatus to a changing light environment, Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci., 367, 3466, 10.1098/rstb.2012.0064 · DOI
- Cariti, 2020, Regulation of light harvesting in Chlamydomonas reinhardtii two protein phosphatases are involved in state transitions, Plant Physiol., 183, 1749, 10.1104/pp.20.00384 · DOI
- Depege, 2003, Role of chloroplast protein kinase Stt7 in LHCII phosphorylation and state transition in Chlamydomonas, Science, 299, 1572, 10.1126/science.1081397 · DOI
- Bellafiore, 2005, State transitions and light adaptation require chloroplast thylakoid protein kinase STN7, Nature, 433, 892, 10.1038/nature03286 · DOI
- Pan, 2018, Structure of the maize photosystem I supercomplex with light-harvesting complexes I and II, Science, 360, 1109, 10.1126/science.aat1156 · DOI
- Pan, 2021, Structural basis of LhcbM5-mediated state transitions in green algae, Nat. Plants, 7, 1119, 10.1038/s41477-021-00960-8 · DOI
- Huang, 2021, Structure of photosystem I-LHCI-LHCII from the green alga Chlamydomonas reinhardtii in State 2, Nat. Commun., 12, 1100, 10.1038/s41467-021-21362-6 · DOI
- Bergner, 2015, STATE TRANSITION7-Dependent Phosphorylation Is Modulated by Changing Environmental Conditions, and Its Absence Triggers Remodeling of Photosynthetic Protein Complexes, Plant Physiol., 168, 615, 10.1104/pp.15.00072 · DOI
- Naschberger, 2022, Algal photosystem I dimer and high-resolution model of PSI-plastocyanin complex, Nat. Plants, 8, 1191, 10.1038/s41477-022-01253-4 · DOI
- Caspy, I., Schwartz, T., Bayro-Kaiser, V., Fadeeva, M., Kessel, A., Ben-Tal, N., and Nelson, N. (2021). Dimeric and high-resolution structures of Chlamydomonas Photosystem I from a temperature-sensitive Photosystem II mutant. Commun. Biol., 4. · DOI
- Iwai, 2010, Isolation of the elusive supercomplex that drives cyclic electron flow in photosynthesis, Nature, 464, 1210, 10.1038/nature08885 · DOI
- Terashima, 2012, Calcium-dependent regulation of cyclic photosynthetic electron transfer by a CAS, ANR1, and PGRL1 complex, Proc. Natl. Acad. Sci. USA, 109, 17717, 10.1073/pnas.1207118109 · DOI
- Steinbeck, 2018, Structure of a PSI-LHCI-cyt b(6)f supercomplex in Chlamydomonas reinhardtii promoting cyclic electron flow under anaerobic conditions, Proc. Natl. Acad. Sci. USA, 115, 10517, 10.1073/pnas.1809973115 · DOI
- Li, 2000, A pigment-binding protein essential for regulation of photosynthetic light harvesting, Nature, 403, 391, 10.1038/35000131 · DOI
- Peers, 2009, An ancient light-harvesting protein is critical for the regulation of algal photosynthesis, Nature, 462, 518, 10.1038/nature08587 · DOI
- Allorent, 2013, A dual strategy to cope with high light in Chlamydomonas reinhardtii, Plant Cell, 25, 545, 10.1105/tpc.112.108274 · DOI
- Yamano, 2008, Expression analysis of genes associated with the induction of the carbon-concentrating mechanism in Chlamydomonas reinhardtii, Plant Physiol., 147, 340, 10.1104/pp.107.114652 · DOI
- Maruyama, 2014, Transcriptional regulation of the stress-responsive light harvesting complex genes in Chlamydomonas reinhardtii, Plant Cell Physiol., 55, 1304, 10.1093/pcp/pcu068 · DOI
- Liguori, 2013, Regulation of light harvesting in the green alga Chlamydomonas reinhardtii: The C-terminus of LHCSR is the knob of a dimmer switch, J. Am. Chem. Soc., 135, 18339, 10.1021/ja4107463 · DOI
- Bonente, G., Ballottari, M., Truong, T.B., Morosinotto, T., Ahn, T.K., Fleming, G.R., Niyogi, K.K., and Bassi, R. (2011). Analysis of LhcSR3, a protein essential for feedback de-excitation in the green alga Chlamydomonas reinhardtii. PLoS Biol., 9. · DOI
- Ballottari, 2016, Identification of pH-sensing Sites in the Light Harvesting Complex Stress-related 3 Protein Essential for Triggering Non-photochemical Quenching in Chlamydomonas reinhardtii, J. Biol. Chem., 291, 7334, 10.1074/jbc.M115.704601 · DOI
- Tokutsu, 2013, Energy-dissipative supercomplex of photosystem II associated with LHCSR3 in Chlamydomonas reinhardtii, Proc. Natl. Acad. Sci. USA, 110, 10016, 10.1073/pnas.1222606110 · DOI
- Xue, 2015, PHOTOSYSTEM II SUBUNIT R is required for efficient binding of LIGHT-HARVESTING COMPLEX STRESS-RELATED PROTEIN3 to photosystem II-light-harvesting supercomplexes in Chlamydomonas reinhardtii, Plant Physiol., 167, 1566, 10.1104/pp.15.00094 · DOI
- Lemeille, 2010, Stt7-dependent phosphorylation during state transitions in the green alga Chlamydomonas reinhardtii, Mol. Cell. Proteom., 9, 1281, 10.1074/mcp.M000020-MCP201 · DOI
- Bullock, 2016, The importance of non-accessible crosslinks and solvent accessible surface distance in modeling proteins with restraints from crosslinking mass spectrometry, Mol. Cell. Proteom., 15, 2491, 10.1074/mcp.M116.058560 · DOI
- Cohen, 2023, A deep learning model for predicting optimal distance range in crosslinking mass spectrometry data, Proteomics, 23, 2200341, 10.1002/pmic.202200341 · DOI
- Graham, M., Combe, C., Kolbowski, L., and Rappsilber, J. (2019). xiView: A common platform for the downstream analysis of Crosslinking Mass Spectrometry data. bioRxiv. · DOI
- Emanuelsson, 2000, Predicting subcellular localization of proteins based on their N-terminal amino acid sequence, J. Mol. Biol., 300, 1005, 10.1006/jmbi.2000.3903 · DOI
- Emanuelsson, 2007, Locating proteins in the cell using TargetP, SignalP and related tools, Nat. Protoc., 2, 953, 10.1038/nprot.2007.131 · DOI
- Camargo, 2021, The Role of Acidic Residues in the C Terminal Tail of the LHCSR3 Protein of Chlamydomonas reinhardtii in Non-Photochemical Quenching, J. Phys. Chem. Lett., 12, 6895, 10.1021/acs.jpclett.1c01382 · DOI
- Naumann, 2005, N-terminal processing of Lhca3 Is a key step in remodeling of the photosystem I-light-harvesting complex under iron deficiency in Chlamydomonas reinhardtii, J. Biol. Chem., 280, 20431, 10.1074/jbc.M414486200 · DOI
- Schiphorst, 2022, The role of light-harvesting complex I in excitation energy transfer from LHCII to photosystem I in Arabidopsis, Plant Physiol., 188, 2241, 10.1093/plphys/kiab579 · DOI
- Bressan, 2018, Loss of LHCI system affects LHCII re-distribution between thylakoid domains upon state transitions, Photosynth. Res., 135, 251, 10.1007/s11120-017-0444-1 · DOI
- Benson, 2015, An intact light harvesting complex I antenna system is required for complete state transitions in, Nat. Plants, 1, 15176, 10.1038/nplants.2015.176 · DOI
- Bos, 2019, Digitonin-sensitive LHCII enlarges the antenna of Photosystem I in stroma lamellae of after far-red and blue-light treatment, BBA Bioenerg., 1860, 651, 10.1016/j.bbabio.2019.07.001 · DOI
- Yadav, 2017, Supercomplexes of plant photosystem I with cytochrome b6f, light-harvesting complex II and NDH, Biochim. Biophys. Acta, 1858, 12, 10.1016/j.bbabio.2016.10.006 · DOI
- Pinnola, 2015, Light-Harvesting Complex Stress-Related Proteins Catalyze Excess Energy Dissipation in Both Photosystems of Physcomitrella patens, Plant Cell, 27, 3213, 10.1105/tpc.15.00443 · DOI
- Girolomoni, 2019, LHCSR3 is a nonphotochemical quencher of both photosystems in Chlamydomonas reinhardtii, Proc. Natl. Acad. Sci. USA, 116, 4212, 10.1073/pnas.1809812116 · DOI
- Yamano, 2013, Rapid transformation of Chlamydomonas reinhardtii without cell-wall removal, J. Biosci. Bioeng., 115, 691, 10.1016/j.jbiosc.2012.12.020 · DOI
- Chua, 1975, A chlorophyll-protein complex lacking in photosystem I mutants of Chlamydomonas reinhardtii, J. Cell. Biol., 67, 361, 10.1083/jcb.67.2.361 · DOI
- Tokutsu, 2012, Revisiting the supramolecular organization of photosystem II in Chlamydomonas reinhardtii, J. Biol. Chem., 287, 31574, 10.1074/jbc.M111.331991 · DOI
- Laemmli, 1970, Cleavage of structural proteins during the assembly of the head of bacteriophage T4, Nature, 227, 680, 10.1038/227680a0 · DOI · Paper page
- Naumann, 2007, Comparative quantitative proteomics to investigate the remodeling of bioenergetic pathways under iron deficiency in Chlamydomonas reinhardtii, Proteomics, 7, 3964, 10.1002/pmic.200700407 · DOI
- Hippler, 2001, Towards functional proteomics of membrane protein complexes: Analysis of thylakoid membranes from Chlamydomonas reinhardtii, Plant J., 28, 595, 10.1046/j.1365-313X.2001.01175.x · DOI
- Shevchenko, 2006, In-gel digestion for mass spectrometric characterization of proteins and proteomes, Nat. Protoc., 1, 2856, 10.1038/nprot.2006.468 · DOI
- Rappsilber, 2007, Protocol for micro-purification, enrichment, pre-fractionation and storage of peptides for proteomics using StageTips, Nat. Protoc., 2, 1896, 10.1038/nprot.2007.261 · DOI · Paper page
- Mendes, M.L., Fischer, L., Chen, Z.A., Barbon, M., O’Reilly, F.J., Giese, S.H., Bohlke-Schneider, M., Belsom, A., Dau, T., and Combe, C.W. (2019). An integrated workflow for crosslinking mass spectrometry. Mol. Syst. Biol., 15. · DOI
- Busch, 2022, Accurate and automated high-coverage identification of chemically cross-linked peptides with MaxLynx, Anal. Chem., 94, 1608, 10.1021/acs.analchem.1c03688 · DOI
- Pettelkau, 2014, Automated assignment of MS/MS cleavable cross-links in protein 3D-structure analysis, J. Am. Soc. Mass Spectrom., 26, 83
- Sarpe, 2016, High sensitivity crosslink detection coupled with integrative structure modeling in the mass spec studio, Mol. Cell. Proteom., 15, 3071, 10.1074/mcp.O116.058685 · DOI
- Chambers, 2012, A cross-platform toolkit for mass spectrometry and proteomics, Nat. Biotechnol., 30, 918, 10.1038/nbt.2377 · DOI
- Elias, 2010, Target-decoy search strategy for mass spectrometry-based proteomics, Methods Mol Biol., 604, 55, 10.1007/978-1-60761-444-9_5 · DOI · Paper page
- Pettersen, 2021, UCSF ChimeraX: Structure visualization for researchers, educators, and developers, Protein Sci., 30, 70, 10.1002/pro.3943 · DOI
- Meng, 2023, UCSF ChimeraX: Tools for structure building and analysis, Protein Sci., 32, e4792, 10.1002/pro.4792 · DOI
- Csordas, 2019, The PRIDE database and related tools and resources in 2019: Improving support for quantification data, Nucleic Acids Res., 47, D442, 10.1093/nar/gky1106 · DOI
Metadata
- Authors
- Mosebach, L., Ozawa, S.-I., Younas, M., Xue, H., Scholz, M., Takahashi, Y., & Hippler, M.
- Affiliations
- University of Münster (DE)
- Okayama University (JP)
- Corresponding author
- Hippler, Michael
- ORCID
- Venue
- Plants
- Publisher
- MDPI AG
- Published
- 2024-06-13
- Volume
- 13
- Issue
- 12
- Pages
- 1632
- ISSN
- 2223-7747 (ISSN-L)
- PMC
- PMC11207971
- OpenAlex
- W4399623903
- Cited by
- 4
- References
- 1
- Citations by year
- 2026: 2 · 2025: 1 · 2024: 1
- FWCI
- 0.54
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Plants (publishedVersion, cc-by)
- Preprints.org (acceptedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- DFG (Deutsche Forschungsgemeinschaft) (HI 739/13-1-3, G-1483-207/2018, 24K09488, 21H02510, 21K06217, 23H04959)
- German-Israeli Foundation for Scientific Research and Development (HI 739/13-1-3, G-1483-207/2018, 24K09488, 21H02510, 21K06217, 23H04959)
- JSPS KAKENHI (HI 739/13-1-3, G-1483-207/2018, 24K09488, 21H02510, 21K06217, 23H04959)
- RECTOR program (Okayama University, Japan) (HI 739/13-1-3, G-1483-207/2018, 24K09488, 21H02510, 21K06217, 23H04959)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Photosynthetic Processes and Mechanisms
- Physical Sciences › Physics and Astronomy › Atomic and Molecular Physics, and Optics › Spectroscopy and Quantum Chemical Studies
- Physical Sciences › Chemistry › Spectroscopy › Advanced Proteomics Techniques and Applications
- Keywords
- light-harvesting complex II, LHCSR3, protein-protein interaction, Chlamydomonas reinhardtii, photosystem I, photosystem II, state transitions, excitation energy transfer, light-harvesting proteins, chemical crosslinking
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