Use of protein cross-linking and radiolytic footprinting to elucidate PsbP and PsbQ interactions within higher plant Photosystem II

Mummadisetti, Manjula P.; Frankel, Laurie K.; Bellamy, Henry D.; Sallans, Larry; Goettert, Jost S.; Brylinski, Michal; Limbach, Patrick A.; Bricker, Terry M.

doi:10.1073/pnas.1415165111

Title: Use of protein cross-linking and radiolytic footprinting to elucidate PsbP and PsbQ interactions within higher plant Photosystem II

Journal Article · Mon Oct 27 00:00:00 EDT 2014 · Proceedings of the National Academy of Sciences of the United States of America

DOI:https://doi.org/10.1073/pnas.1415165111· OSTI ID:1356192

Mummadisetti, Manjula P. ^[1]; Frankel, Laurie K. ^[1]; Bellamy, Henry D. ^[2]; Sallans, Larry ^[3]; Goettert, Jost S. ^[2]; Brylinski, Michal ^[4]; Limbach, Patrick A. ^[3]; Bricker, Terry M. ^[1]

Louisiana State Univ., Baton Rouge, LA (United States). Dept. of Biological Sciences
Louisiana State Univ., Baton Rouge, LA (United States). J. Bennett Johnston Sr. Center for Advanced Microstructures and Devices
Univ. of Cincinnati, OH (United States). Dept. of Chemistry
Louisiana State Univ., Baton Rouge, LA (United States). Dept. of Biological Sciences and Center for Computation and Technology

We used protein cross-linking and radiolytic footprinting coupled with high-resolution mass spectrometry to examine the structure of PsbP and PsbQ when they are bound to Photosystem II, in this paper. In its bound state, the N-terminal 15-amino-acid residue domain of PsbP, which is unresolved in current crystal structures, interacts with domains in the C terminus of the protein. These interactions may serve to stabilize the structure of the N terminus and may facilitate PsbP binding and function. These interactions place strong structural constraints on the organization of PsbP when associated with the Photosystem II complex. Additionally, amino acid residues in the structurally unresolved loop 3A domain of PsbP (⁹⁰K–¹⁰⁷V), ⁹³Y and ⁹⁶K, are in close proximity (≤11.4 Å) to the N-terminal 1E residue of PsbQ. Our findings are the first, to our knowledge, to identify a putative region of interaction between these two components. Cross-linked domains within PsbQ were also identified, indicating that two PsbQ molecules can interact in higher plants in a manner similar to that observed by Liu et al. [(2014) Proc Natl Acad Sci 111(12):4638–4643] in cyanobacterial Photosystem II. Furthermore, this interaction is consistent with either intra-Photosystem II dimer or inter-Photosystem II dimer models in higher plants. Finally, OH• produced by synchrotron radiolysis of water was used to oxidatively modify surface residues on PsbP and PsbQ. Finally, domains on the surface of both protein subunits were resistant to modification, indicating that they were shielded from water and appear to define buried regions that are in contact with other Photosystem II components.

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Research Organization:: Louisiana State Univ., Baton Rouge, LA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES); National Institutes of Health (NIH)

Grant/Contract Number:: FG02-98ER20310; RR019900; GM58843

OSTI ID:: 1356192

Journal Information:: Proceedings of the National Academy of Sciences of the United States of America, Vol. 111, Issue 45; ISSN 0027-8424

Publisher:: National Academy of Sciences, Washington, DC (United States)Copyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 30 works

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References (52)

The extrinsic proteins of Photosystem II Roose, Johnna L.; Wegener, Kimberly M.; Pakrasi, Himadri B. Photosynthesis Research, Vol. 92, Issue 3 https://doi.org/10.1007/s11120-006-9117-1	journal	January 2007
The extrinsic proteins of Photosystem II Bricker, Terry M.; Roose, Johnna L.; Fagerlund, Robert D. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1817, Issue 1 https://doi.org/10.1016/j.bbabio.2011.07.006	journal	January 2012
The structure and function of the 33 kDa extrinsic protein of Photosystem II: A critical assessment Bricker, Terry M.; Frankel, Laurie K. Photosynthesis Research, Vol. 56, Issue 2, p. 157-173 https://doi.org/10.1023/A:1006068615220	journal	January 1998
The Manganese-stabilizing Protein Is Required for Photosystem II Assembly/Stability and Photoautotrophy in Higher Plants Yi, Xiaoping; McChargue, Myriam; Laborde, Susan Journal of Biological Chemistry, Vol. 280, Issue 16 https://doi.org/10.1074/jbc.M501550200	journal	February 2005
The PsbP Protein Is Required for Photosystem II Complex Assembly/Stability and Photoautotrophy in Arabidopsis thaliana Yi, Xiaoping; Hargett, Stefan R.; Liu, Haijun Journal of Biological Chemistry, Vol. 282, Issue 34 https://doi.org/10.1074/jbc.M705011200	journal	June 2007
The PsbP protein, but not the PsbQ protein, is required for normal thylakoid architecture in Arabidopsis thaliana Yi, Xiaoping; Hargett, Stefan R.; Frankel, Laurie K. FEBS Letters, Vol. 583, Issue 12 https://doi.org/10.1016/j.febslet.2009.05.048	journal	June 2009
Knockdown of the PsbP protein does not prevent assembly of the dimeric PSII core complex but impairs accumulation of photosystem II supercomplexes in tobacco Ido, Kunio; Ifuku, Kentaro; Yamamoto, Yumiko Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1787, Issue 7 https://doi.org/10.1016/j.bbabio.2009.03.004	journal	July 2009
Auxiliary functions of the PsbO, PsbP and PsbQ proteins of higher plant Photosystem II: A critical analysis Bricker, Terry M.; Frankel, Laurie K. Journal of Photochemistry and Photobiology B: Biology, Vol. 104, Issue 1-2 https://doi.org/10.1016/j.jphotobiol.2011.01.025	journal	July 2011
Arabidopsis plants lacking PsbQ and PsbR subunits of the oxygen-evolving complex show altered PSII super-complex organization and short-term adaptive mechanisms Allahverdiyeva, Yagut; Suorsa, Marjaana; Rossi, Fabio The Plant Journal, Vol. 75, Issue 4 https://doi.org/10.1111/tpj.12230	journal	June 2013
The PsbQ Protein Is Required in Arabidopsis for Photosystem II Assembly/Stability and Photoautotrophy under Low Light Conditions Yi, Xiaoping; Hargett, Stefan R.; Frankel, Laurie K. Journal of Biological Chemistry, Vol. 281, Issue 36 https://doi.org/10.1074/jbc.M603582200	journal	July 2006
Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å Umena, Yasufumi; Kawakami, Keisuke; Shen, Jian-Ren Nature, Vol. 473, Issue 7345 https://doi.org/10.1038/nature09913	journal	April 2011
Raman Spectroscopy Adds Complementary Detail to the High-Resolution X-Ray Crystal Structure of Photosynthetic PsbP from Spinacia oleracea Kopecky, Vladimir; Kohoutova, Jaroslava; Lapkouski, Mikalai PLoS ONE, Vol. 7, Issue 10 https://doi.org/10.1371/journal.pone.0046694	journal	October 2012
The 1.49Å Resolution Crystal Structure of PsbQ from Photosystem II of Spinacia oleracea Reveals a PPII Structure in the N-terminal Region Balsera, Mónica; Arellano, Juan B.; Revuelta, José L. Journal of Molecular Biology, Vol. 350, Issue 5 https://doi.org/10.1016/j.jmb.2005.05.044	journal	July 2005
Structure and dynamics of the N-terminal loop of PsbQ from photosystem II of Spinacia oleracea Ristvejová, Jaroslava; Kopecký, Vladimír; Sovová, Žofie Biochemical and Biophysical Research Communications, Vol. 345, Issue 1 https://doi.org/10.1016/j.bbrc.2006.04.087	journal	June 2006
The PsbP and PsbQ family proteins in the photosynthetic machinery of chloroplasts Ifuku, Kentaro Plant Physiology and Biochemistry, Vol. 81 https://doi.org/10.1016/j.plaphy.2014.01.001	journal	August 2014
MS-based cross-linking analysis reveals the location of the PsbQ protein in cyanobacterial photosystem II Liu, H.; Zhang, H.; Weisz, D. A. Proceedings of the National Academy of Sciences, Vol. 111, Issue 12 https://doi.org/10.1073/pnas.1323063111	journal	February 2014
Partial degradation of the 18-kDa protein of the photosynthetic oxygen-evolving complex: A study of a binding site Kuwabara, Tomohiko; Murata, Teruyo; Miyao, Mitsue Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 850, Issue 1 https://doi.org/10.1016/0005-2728(86)90019-8	journal	June 1986
Partial degradation of the extrinsic 23-kDa protein of the Photosystem II complex of spinach Miyao, Mitsue; Fujimura, Yoko; Murata, Norio Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 936, Issue 3 https://doi.org/10.1016/0005-2728(88)90024-2	journal	December 1988
Association of Extrinsic Proteases with Spinach Photosystem II Membranes Kuwabara, Tomohiko; Shinohara, Kenji Current Research in Photosynthesis https://doi.org/10.1007/978-94-009-0511-5_599	book	January 1990
Chemical cross-linking and mass spectrometry to map three-dimensional protein structures and protein–protein interactions Sinz, Andrea Mass Spectrometry Reviews, Vol. 25, Issue 4 https://doi.org/10.1002/mas.20082	journal	January 2006
Importance of the N-terminal sequence of the extrinsic 23 kDa polypeptide in Photosystem II in ion retention in oxygen evolution Ifuku, Kentaro; Sato, Fumihiko Biochimica et Biophysica Acta (BBA) - Protein Structure and Molecular Enzymology, Vol. 1546, Issue 1 https://doi.org/10.1016/S0167-4838(01)00139-X	journal	March 2001
Water-soluble 17 and 23 kDa polypeptides restore oxygen evolution activity by creating a high-affinity binding site for Ca ²⁺ on the oxidizing side of Photosystem II Ghanotakis, Demetrios F.; Topper, James N.; Babcock, Gerald T. FEBS Letters, Vol. 170, Issue 1 https://doi.org/10.1016/0014-5793(84)81393-9	journal	May 1984
Calcium ions can be substituted for the 24-kDa polypeptide in photosynthetic oxygen evolution Miyao, Mitsue; Murata, Norio FEBS Letters, Vol. 168, Issue 1 https://doi.org/10.1016/0014-5793(84)80218-5	journal	March 1984
On the role of water-soluble polypeptides (17, 23 kDa), calcium and chloride in photosynthetic oxygen evolution Ghanotakis, Demetrios F.; Babcock, Gerald T.; Yocum, Charles F. FEBS Letters, Vol. 192, Issue 1 https://doi.org/10.1016/0014-5793(85)80030-2	journal	November 1985
Cross-linking Evidence for Multiple Interactions of the PsbP and PsbQ Proteins in a Higher Plant Photosystem II Supercomplex Ido, Kunio; Nield, Jon; Fukao, Yoichiro Journal of Biological Chemistry, Vol. 289, Issue 29 https://doi.org/10.1074/jbc.M114.574822	journal	June 2014
GeneSilico protein structure prediction meta-server Kurowski, M. A. Nucleic Acids Research, Vol. 31, Issue 13 https://doi.org/10.1093/nar/gkg557	journal	July 2003
Comparative Protein Structure Modeling Using MODELLER Eswar, Narayanan; Webb, Ben; Marti-Renom, Marc A. Current Protocols in Protein Science, Vol. 50, Issue 1 https://doi.org/10.1002/0471140864.ps0209s50	journal	November 2007
The Conserved His-144 in the PsbP Protein Is Important for the Interaction between the PsbP N-terminus and the Cyt b ₅₅₉ Subunit of Photosystem II Ido, Kunio; Kakiuchi, Shusuke; Uno, Chihiro Journal of Biological Chemistry, Vol. 287, Issue 31 https://doi.org/10.1074/jbc.M112.385286	journal	June 2012
The mode of binding of three extrinsic proteins of 33 kDa, 23 kDa and 18 kDa in the photosystem II complex of spinach Miyao, Mitsue; Murata, Norio Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 977, Issue 3 https://doi.org/10.1016/S0005-2728(89)80086-6	journal	December 1989
A Truncated Mutant of the Extrinsic 23-kDa Protein that Absolutely Requires the Extrinsic 17-kDa Protein for Ca2+ Retention in Photosystem II Ifuku, Kentaro; Sato, Fumihiko Plant and Cell Physiology, Vol. 43, Issue 10 https://doi.org/10.1093/pcp/pcf136	journal	October 2002
The PsbQ protein stabilizes the functional binding of the PsbP protein to photosystem II in higher plants Kakiuchi, Shusuke; Uno, Chihiro; Ido, Kunio Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1817, Issue 8 https://doi.org/10.1016/j.bbabio.2012.01.009	journal	August 2012
Development and testing of an automated approach to protein docking Tovchigrechko, Andrei; Vakser, Ilya A. Proteins: Structure, Function, and Bioinformatics, Vol. 60, Issue 2 https://doi.org/10.1002/prot.20573	journal	June 2005
Radiolytic Protein Footprinting with mass Spectrometry to Probe the Structure of Macromolecular Complexes Takamoto, Keiji; Chance, Mark R. Annual Review of Biophysics and Biomolecular Structure, Vol. 35, Issue 1 https://doi.org/10.1146/annurev.biophys.35.040405.102050	journal	June 2006
Visualizing Water Molecules in Transmembrane Proteins Using Radiolytic Labeling Methods Orban, Tivadar; Gupta, Sayan; Palczewski, Krzysztof Biochemistry, Vol. 49, Issue 5 https://doi.org/10.1021/bi901889t	journal	February 2010
Identification of the basic amino acid residues on the PsbP protein involved in the electrostatic interaction with photosystem II Nishimura, Taishi; Uno, Chihiro; Ido, Kunio Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1837, Issue 9 https://doi.org/10.1016/j.bbabio.2013.12.012	journal	September 2014
Identification of domains on the extrinsic 23 kDa protein possibly involved in electrostatic interaction with the extrinsic 33 kDa protein in spinach photosystem II: Interaction between the 23 and 33 kDa proteins Tohri, Akihiko; Dohmae, Naoshi; Suzuki, Takehiro European Journal of Biochemistry, Vol. 271, Issue 5 https://doi.org/10.1111/j.1432-1033.2004.03998.x	journal	February 2004
Association of the 17-kDa Extrinsic Protein with Photosystem II in Higher Plants ^† Meades,, Glen D.; McLachlan, Anne; Sallans, Larry Biochemistry, Vol. 44, Issue 46 https://doi.org/10.1021/bi051704u	journal	November 2005
A highly resolved, oxygen-evolving photosystem II preparation from spinach thylakoid membranes: EPR and electron-transport properties Berthold, Deborah A.; Babcock, Gerald T.; Yocum, Charles F. FEBS Letters, Vol. 134, Issue 2 https://doi.org/10.1016/0014-5793(81)80608-4	journal	November 1981
COPPER ENZYMES IN ISOLATED CHLOROPLASTS. POLYPHENOLOXIDASE IN BETA VULGARIS Arnon, Daniel I. Plant Physiology, Vol. 24, Issue 1 https://doi.org/10.1104/pp.24.1.1	journal	January 1949
Unexpected products from the reaction of the synthetic cross-linker 3,3′-dithiobis(sulfosuccinimidyl propionate), DTSSP with peptides Swaim, Catherine L.; Smith, Jean B.; Smith, David L. Journal of the American Society for Mass Spectrometry, Vol. 15, Issue 5 https://doi.org/10.1016/j.jasms.2004.01.011	journal	May 2004
Chances and pitfalls of chemical cross-linking with amine-reactive N-hydroxysuccinimide esters Kalkhof, Stefan; Sinz, Andrea Analytical and Bioanalytical Chemistry, Vol. 392, Issue 1-2 https://doi.org/10.1007/s00216-008-2231-5	journal	July 2008
Chemical cross-linking with NHS esters: a systematic study on amino acid reactivities Mädler, Stefanie; Bich, Claudia; Touboul, David Journal of Mass Spectrometry, Vol. 44, Issue 5 https://doi.org/10.1002/jms.1544	journal	May 2009
Measurement of protein using bicinchoninic acid Smith, P. K.; Krohn, R. I.; Hermanson, G. T. Analytical Biochemistry, Vol. 150, Issue 1 https://doi.org/10.1016/0003-2697(85)90442-7	journal	October 1985
Radiolytic Mapping of Solvent-Contact Surfaces in Photosystem II of Higher Plants: EXPERIMENTAL IDENTIFICATION OF PUTATIVE WATER CHANNELS WITHIN THE PHOTOSYSTEM Frankel, Laurie K.; Sallans, Larry; Bellamy, Henry Journal of Biological Chemistry, Vol. 288, Issue 32 https://doi.org/10.1074/jbc.M113.487033	journal	June 2013
Lithium dodecyl sulfate/polyacrylamide gel electrophoresis of thylakoid membranes at 4 C: Characterizations of two additional chlorophyll a-protein complexes Delepelaire, P.; Chua, N. -H. Proceedings of the National Academy of Sciences, Vol. 76, Issue 1 https://doi.org/10.1073/pnas.76.1.111	journal	January 1979
Prevention of artifactual protein oxidation generated during sodium dodecyl sulfate-gel electrophoresis Sun, Gang; Anderson, Vernon E. ELECTROPHORESIS, Vol. 25, Issue 78 https://doi.org/10.1002/elps.200305800	journal	April 2004
Identification of Oxidized Amino Acid Residues in the Vicinity of the Mn ₄ CaO ₅ Cluster of Photosystem II: Implications for the Identification of Oxygen Channels within the Photosystem Frankel, Laurie K.; Sallans, Larry; Limbach, Patrick A. Biochemistry, Vol. 51, Issue 32 https://doi.org/10.1021/bi300650n	journal	July 2012
A mass accuracy sensitive probability based scoring algorithm for database searching of tandem mass spectrometry data Xu, Hua; Freitas, Michael A. BMC Bioinformatics, Vol. 8, Issue 1 https://doi.org/10.1186/1471-2105-8-133	journal	April 2007
MassMatrix: A database search program for rapid characterization of proteins and peptides from tandem mass spectrometry data Xu, Hua; Freitas, Michael A. PROTEOMICS, Vol. 9, Issue 6 https://doi.org/10.1002/pmic.200700322	journal	March 2009
PROCHECK: a program to check the stereochemical quality of protein structures Laskowski, R. A.; MacArthur, M. W.; Moss, D. S. Journal of Applied Crystallography, Vol. 26, Issue 2 https://doi.org/10.1107/S0021889892009944	journal	April 1993
Recognition of errors in three-dimensional structures of proteins Sippl, Manfred J. Proteins: Structure, Function, and Genetics, Vol. 17, Issue 4 https://doi.org/10.1002/prot.340170404	journal	December 1993
ProSA-web: interactive web service for the recognition of errors in three-dimensional structures of proteins Wiederstein, M.; Sippl, M. J. Nucleic Acids Research, Vol. 35, Issue Web Server https://doi.org/10.1093/nar/gkm290	journal	May 2007

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photosynthesis
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mass spectrometry

Title: Use of protein cross-linking and radiolytic footprinting to elucidate PsbP and PsbQ interactions within higher plant Photosystem II

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