Feeling the Strain: Quantifying Ligand Deformation in Photosynthesis

Lin, Chientzu; Mazor, Yuval; Reppert, Mike

doi:10.1021/acs.jpcb.3c06488

Title: Feeling the Strain: Quantifying Ligand Deformation in Photosynthesis

Journal Article · 05 March 2024 · Journal of Physical Chemistry. B

DOI: https://doi.org/10.1021/acs.jpcb.3c06488 · OSTI ID:2396739

^[1]; Mazor, Yuval ^[2];

^[3]

Purdue University, West Lafayette, IN (United States); Purdue University
Arizona State University, Tempe, AZ (United States)
Purdue University, West Lafayette, IN (United States)

Structural distortion of protein-bound ligands can play a critical role in enzyme function by tuning the electronic and chemical properties of the ligand molecule. However, quantifying these effects is difficult due to the limited resolution of protein structures and the difficulty of generating accurate structural restrains for non-protein ligands. Here, we seek to quantify these effects through a statistical analysis of ligand distortion in Chlorophyll (Chl) proteins (CP), where ring deformation is thought to play a role in energy and electron transfer. To assess the accuracy of ring-deformation estimates from available structural data, we take advantage of the C₂ symmetry of Photosystem II (PSII), comparing ring-deformation estimates for equivalent sites both within and between 113 distinct X-ray and Cryogenic electron microscopy (CryoEM) PSII structures. Significantly, we find that several deformation modes exhibit considerable variability in predictions, even for equivalent monomers, down to 2 Å resolution, to an extent that probably prevents their utilization in optical calculations. We further find that refinement restrains play a critical role in determining deformation values to resolution as low as 2 Å. However, for those modes that are well-resolved in the structural data, ring deformation in PSII is strongly conserved across all species tested, from cyanobacteria to algae. Furthermore, these results highlight both the opportunities and limitations inherent in the structure-based analysis of the bioenergetic and optical properties of CPs and other protein-ligand complexes.

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Research Organization:: Purdue University, West Lafayette, IN (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division (CSGB)

Grant/Contract Number:: SC0022884; SC0022956

OSTI ID:: 2396739

Journal Information:: Journal of Physical Chemistry. B, Journal Name: Journal of Physical Chemistry. B Journal Issue: 10 Vol. 128; ISSN 1520-6106

Publisher:: American Chemical SocietyCopyright Statement

Country of Publication:: United States

Language:: English

References (80)

The Key–Lock Theory and the Induced Fit Theory Koshland, Daniel E. Angewandte Chemie International Edition in English, Vol. 33, Issue 2324 https://doi.org/10.1002/anie.199423751	journal	January 1995
Fine Tuning of Chlorophyll Spectra by Protein-Induced Ring Deformation Bednarczyk, Dominika; Dym, Orly; Prabahar, Vadivel Angewandte Chemie International Edition, Vol. 55, Issue 24 https://doi.org/10.1002/anie.201512001	journal	April 2016
Accurate assessment of the strain energy in a protein-bound drug using QM/MM X-ray refinement and converged quantum chemistry Fu, Zheng; Li, Xue; Merz, Kenneth M. Journal of Computational Chemistry, Vol. 32, Issue 12 https://doi.org/10.1002/jcc.21838	journal	May 2011
Out‐of‐plane deformations of the heme group in different ferrocytochrome c proteins probed by resonance Raman spectroscopy Hagarman, Andrew; Wallace, Carmichael J.; Laberge, Monique M. Journal of Raman Spectroscopy, Vol. 39, Issue 12 https://doi.org/10.1002/jrs.2050	journal	July 2008
Homology-based hydrogen bond information improves crystallographic structures in the PDB: Homology-Based H-Bond Restraints Improve PDB Entries van Beusekom, Bart; Touw, Wouter G.; Tatineni, Mahidhar Protein Science, Vol. 27, Issue 3 https://doi.org/10.1002/pro.3353	journal	December 2017
Structural basis of light‐harvesting in the photosystem II core complex Müh, Frank; Zouni, Athina Protein Science, Vol. 29, Issue 5 https://doi.org/10.1002/pro.3841	journal	February 2020
An exciting but challenging road ahead for computational enzyme design: Computational Enzyme Design Baker, David Protein Science, Vol. 19, Issue 10 https://doi.org/10.1002/pro.481	journal	September 2010
Frequently asked questions about chlorophyll fluorescence, the sequel Kalaji, Hazem M.; Schansker, Gert; Brestic, Marian Photosynthesis Research, Vol. 132, Issue 1 https://doi.org/10.1007/s11120-016-0318-y	journal	November 2016
Structure and X-ray amino acid sequence of a bacteriochlorophyll a protein from Prosthecochloris aestuarii refined at 1.9 Å resolution Tronrud, D. E.; Schmid, M. F.; Matthews, B. W. Journal of Molecular Biology, Vol. 188, Issue 3 https://doi.org/10.1016/0022-2836(86)90167-1	journal	April 1986
Relevance of the diastereotopic ligation of magnesium atoms of chlorophylls in Photosystem I Balaban, Teodor Silviu; Fromme, Petra; Holzwarth, Alfred R. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1556, Issue 2-3 https://doi.org/10.1016/S0005-2728(02)00363-8	journal	December 2002
The Endogenous Calcium Ions of Horseradish Peroxidase C Are Required to Maintain the Functional Nonplanarity of the Heme Laberge, Monique; Huang, Qing; Schweitzer-Stenner, Reinhard Biophysical Journal, Vol. 84, Issue 4 https://doi.org/10.1016/S0006-3495(03)75059-0	journal	April 2003
Conservation of the Conformation of the Porphyrin Macrocycle in Hemoproteins Jentzen, Walter; Ma, Jian-Guo; Shelnutt, John A. Biophysical Journal, Vol. 74, Issue 2 https://doi.org/10.1016/S0006-3495(98)74000-7	journal	February 1998
Interaction of the PsbH subunit with a chlorophyll bound to histidine 114 of CP47 is responsible for the red 77K fluorescence of Photosystem II D'Haene, Sandrine E.; Sobotka, Roman; Bučinská, Lenka Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1847, Issue 10 https://doi.org/10.1016/j.bbabio.2015.07.003	journal	October 2015
Contribution of bacteriochlorophyll conformation to the distribution of site-energies in the FMO protein MacGowan, Stuart A.; Senge, Mathias O. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1857, Issue 4 https://doi.org/10.1016/j.bbabio.2016.02.001	journal	April 2016
The lowest-energy chlorophyll of photosystem II is adjacent to the peripheral antenna: Emitting states of CP47 assigned via circularly polarized luminescence Hall, Jeremy; Renger, Thomas; Müh, Frank Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1857, Issue 9 https://doi.org/10.1016/j.bbabio.2016.06.007	journal	September 2016
Interplay between conformational selection and induced fit in multidomain protein–ligand binding probed by paramagnetic relaxation enhancement Clore, G. Marius Biophysical Chemistry, Vol. 186 https://doi.org/10.1016/j.bpc.2013.08.006	journal	February 2014
A variety of electrostatic interactions and adducts can activate NAD(P) cofactors for hydride transfer Meijers, Rob; Cedergren-Zeppezauer, Eila Chemico-Biological Interactions, Vol. 178, Issue 1-3 https://doi.org/10.1016/j.cbi.2008.10.043	journal	March 2009
Current trends in computer aided drug design and a highlight of drugs discovered via computational techniques: A review Sabe, Victor T.; Ntombela, Thandokuhle; Jhamba, Lindiwe A. European Journal of Medicinal Chemistry, Vol. 224 https://doi.org/10.1016/j.ejmech.2021.113705	journal	November 2021
Marvels of enzyme catalysis at true atomic resolution: distortions, bond elongations, hidden flips, protonation states and atom identities Neumann, Piotr; Tittmann, Kai Current Opinion in Structural Biology, Vol. 29 https://doi.org/10.1016/j.sbi.2014.11.001	journal	December 2014
Induced fit, conformational selection and independent dynamic segments: an extended view of binding events Csermely, Peter; Palotai, Robin; Nussinov, Ruth Trends in Biochemical Sciences, Vol. 35, Issue 10 https://doi.org/10.1016/j.tibs.2010.04.009	journal	October 2010
Global Analysis of Heme Proteins Elucidates the Correlation between Heme Distortion and the Heme-Binding Pocket Kondo, Hiroko X.; Fujii, Masanori; Tanioka, Takuma Journal of Chemical Information and Modeling, Vol. 62, Issue 4 https://doi.org/10.1021/acs.jcim.1c01315	journal	February 2022
Flexible Fitting of Small Molecules into Electron Microscopy Maps Using Molecular Dynamics Simulations with Neural Network Potentials Vant, John W.; Lahey, Shae-Lynn J.; Jana, Kalyanashis Journal of Chemical Information and Modeling, Vol. 60, Issue 5 https://doi.org/10.1021/acs.jcim.9b01167	journal	March 2020
Measurement of Heme Ruffling Changes in MhuD Using UV–vis Spectroscopy Graves, Amanda B.; Graves, Max T.; Liptak, Matthew D. The Journal of Physical Chemistry B, Vol. 120, Issue 16 https://doi.org/10.1021/acs.jpcb.6b01497	journal	April 2016
Toward an Understanding of the Excitonic Structure of the CP47 Antenna Protein Complex of Photosystem II Revealed via Circularly Polarized Luminescence Jassas, Mahboobe; Reinot, Tonu; Kell, Adam The Journal of Physical Chemistry B, Vol. 121, Issue 17 https://doi.org/10.1021/acs.jpcb.7b00362	journal	April 2017
Mutation of Chlorophyll Ligands in the Chlorophyll-Binding CP47 Protein As Studied in a Synechocystis sp. PCC 6803 Photosystem I-less Background Shen, Gaozhong; Vermaas, Wim F. J. Biochemistry, Vol. 33, Issue 23 https://doi.org/10.1021/bi00189a044	journal	June 1994
Identifying the Lowest Electronic States of the Chlorophylls in the CP47 Core Antenna Protein of Photosystem II de Weerd, Frank L.; Palacios, Miguel A.; Andrizhiyevskaya, Elena G. Biochemistry, Vol. 41, Issue 51 https://doi.org/10.1021/bi0261948	journal	November 2002
The Q _y Absorption Spectrum of the Light-Harvesting Complex II As Determined by Structure-Based Analysis of Chlorophyll Macrocycle Deformations Zucchelli, Giuseppe; Santabarbara, Stefano; Jennings, Robert C. Biochemistry, Vol. 51, Issue 13 https://doi.org/10.1021/bi201677q	journal	March 2012
Deformation of Chlorin Rings in the Photosystem II Crystal Structure Saito, Keisuke; Umena, Yasufumi; Kawakami, Keisuke Biochemistry, Vol. 51, Issue 21 https://doi.org/10.1021/bi300428s	journal	May 2012
The Structural Origin of Nonplanar Heme Distortions in Tetraheme Ferricytochromes c ₃ ^† Ma, Jian-Guo; Zhang, Jun; Franco, Ricardo Biochemistry, Vol. 37, Issue 36 https://doi.org/10.1021/bi981189i	journal	September 1998
Computational Quantification of the Physicochemical Effects of Heme Distortion: Redox Control in the Reaction Center Cytochrome Subunit of Blastochloris viridis MacGowan, Stuart A.; Senge, Mathias O. Inorganic Chemistry, Vol. 52, Issue 3 https://doi.org/10.1021/ic301530t	journal	January 2013
Consequences of Oxidation in Nonplanar Porphyrins: Molecular Structure and Diamagnetism of the .pi. Cation Radical of Copper(II) Octaethyltetraphenylporphyrin Renner, Mark W.; Barkigia, Kathleen M.; Zhang, Yun Journal of the American Chemical Society, Vol. 116, Issue 19 https://doi.org/10.1021/ja00098a019	journal	September 1994
Structural and theoretical models of photosynthetic chromophores. Implications for redox, light-absorption properties and vectorial electron flow Barkigia, K. M.; Chantranupong, L.; Smith, K. M. Journal of the American Chemical Society, Vol. 110, Issue 22 https://doi.org/10.1021/ja00230a063	journal	October 1988
Heme Distortions in Sperm-Whale Carbonmonoxy Myoglobin: Correlations between Rotational Strengths and Heme Distortions in MD-Generated Structures Kiefl, Christoph; Sreerama, Narasimha; Haddad, Raid Journal of the American Chemical Society, Vol. 124, Issue 13 https://doi.org/10.1021/ja011961w	journal	March 2002
Origin of the Red Shifts in the Optical Absorption Bands of Nonplanar Tetraalkylporphyrins Haddad, Raid E.; Gazeau, Stéphanie; Pécaut, Jacques Journal of the American Chemical Society, Vol. 125, Issue 5 https://doi.org/10.1021/ja0280933	journal	February 2003
Light Harvesting in Photosystem II Core Complexes Is Limited by the Transfer to the Trap: Can the Core Complex Turn into a Photoprotective Mode? Raszewski, Grzegorz; Renger, Thomas Journal of the American Chemical Society, Vol. 130, Issue 13 https://doi.org/10.1021/ja7099826	journal	April 2008
Coherence Spectroscopy Investigations of the Low-Frequency Vibrations of Heme: Effects of Protein-Specific Perturbations Gruia, Flaviu; Kubo, Minoru; Ye, Xiong Journal of the American Chemical Society, Vol. 130, Issue 15 https://doi.org/10.1021/ja7104027	journal	March 2008
Nonplanar Heme Deformations and Excited State Displacements in Nickel Porphyrins Detected by Raman Spectroscopy at Soret Excitation Huang, Qing; Medforth, Craig J.; Schweitzer-Stenner, Reinhard The Journal of Physical Chemistry A, Vol. 109, Issue 46 https://doi.org/10.1021/jp052986a	journal	October 2005
Static Normal Coordinate Deformations of the Heme Group in Mutants of Ferrocytochrome c from Saccharomyces cerevisiae Probed by Resonance Raman Spectroscopy Schweitzer-Stenner, Reinhard; Huang, Qing; Hagarman, Andrew The Journal of Physical Chemistry B, Vol. 111, Issue 23 https://doi.org/10.1021/jp070445a	journal	May 2007
Role of Heme Distortion on Oxygen Affinity in Heme Proteins: The Protoglobin Case Bikiel, Damián E.; Forti, Flavio; Boechi, Leonardo The Journal of Physical Chemistry B, Vol. 114, Issue 25 https://doi.org/10.1021/jp102135p	journal	June 2010
Lowest Electronic States of the CP47 Antenna Protein Complex of Photosystem II: Simulation of Optical Spectra and Revised Structural Assignments ^† Reppert, Mike; Acharya, Khem; Neupane, Bhanu The Journal of Physical Chemistry B, Vol. 114, Issue 36 https://doi.org/10.1021/jp103995h	journal	September 2010
Structural Characterization of Synthetic and Protein-Bound Porphyrins in Terms of the Lowest-Frequency Normal Coordinates of the Macrocycle Jentzen, Walter; Song, Xing-Zhi; Shelnutt, John A. The Journal of Physical Chemistry B, Vol. 101, Issue 9 https://doi.org/10.1021/jp963142h	journal	February 1997
Modeling the Bacterial Photosynthetic Reaction Center. 2. A Combined Quantum Mechanical/Molecular Mechanical Study of the Structure of the Cofactors in the Reaction Centers of Purple Bacteria Hutter, Michael C.; Hughes, Jason M.; Reimers, Jeffrey R. The Journal of Physical Chemistry B, Vol. 103, Issue 23 https://doi.org/10.1021/jp9833808	journal	May 1999
Raman Optical Activity Probing Structural Deformations of the 4-Hydroxycinnamyl Chromophore in Photoactive Yellow Protein Shingae, Takahito; Kubota, Kensuke; Kumauchi, Masato The Journal of Physical Chemistry Letters, Vol. 4, Issue 8 https://doi.org/10.1021/jz400454j	journal	April 2013
Active Site Structure of Photoactive Yellow Protein with a Locked Chromophore Analogue Revealed by Near-Infrared Raman Optical Activity Kubota, Kensuke; Shingae, Takahito; Foster, Nicole D. The Journal of Physical Chemistry Letters, Vol. 4, Issue 18 https://doi.org/10.1021/jz4016266	journal	August 2013
Crystal structure of spinach major light-harvesting complex at 2.72 Å resolution Liu, Zhenfeng; Yan, Hanchi; Wang, Kebin Nature, Vol. 428, Issue 6980 https://doi.org/10.1038/nature02373	journal	March 2004
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
The coming of age of de novo protein design Huang, Po-Ssu; Boyken, Scott E.; Baker, David Nature, Vol. 537, Issue 7620 https://doi.org/10.1038/nature19946	journal	September 2016
Finding better protein engineering strategies Kazlauskas, Romas J.; Bornscheuer, Uwe T. Nature Chemical Biology, Vol. 5, Issue 8 https://doi.org/10.1038/nchembio0809-526	journal	August 2009
Subunit and chlorophyll organization of the plant photosystem II supercomplex van Bezouwen, Laura S.; Caffarri, Stefano; Kale, Ravindra S. Nature Plants, Vol. 3, Issue 7 https://doi.org/10.1038/nplants.2017.80	journal	June 2017
Rethinking drug design in the artificial intelligence era Schneider, Petra; Walters, W. Patrick; Plowright, Alleyn T. Nature Reviews Drug Discovery, Vol. 19, Issue 5 https://doi.org/10.1038/s41573-019-0050-3	journal	December 2019
Structures of the intermediates of Kok’s photosynthetic water oxidation clock Kern, Jan; Chatterjee, Ruchira; Young, Iris D. Nature, Vol. 563, Issue 7731 https://doi.org/10.1038/s41586-018-0681-2	journal	November 2018
Ultrafast structural changes within a photosynthetic reaction centre Dods, Robert; Båth, Petra; Morozov, Dmitry Nature, Vol. 589, Issue 7841, p. 310-314 https://doi.org/10.1038/s41586-020-3000-7	journal	December 2020
Structural evidence for intermediates during O2 formation in photosystem II Bhowmick, Asmit; Hussein, Rana; Bogacz, Isabel Nature, Vol. 617, Issue 7961 https://doi.org/10.1038/s41586-023-06038-z	journal	May 2023
High-resolution model of Arabidopsis Photosystem II reveals the structural consequences of digitonin-extraction Graça, André T.; Hall, Michael; Persson, Karina Scientific Reports, Vol. 11, Issue 1 https://doi.org/10.1038/s41598-021-94914-x	journal	July 2021
Engineering new catalytic activities in enzymes Chen, Kai; Arnold, Frances H. Nature Catalysis, Vol. 3, Issue 3 https://doi.org/10.1038/s41929-019-0385-5	journal	January 2020
Conformational control of cofactors in nature – the influence of protein-induced macrocycle distortion on the biological function of tetrapyrroles Senge, Mathias O.; MacGowan, Stuart A.; O'Brien, Jessica M. Chemical Communications, Vol. 51, Issue 96 https://doi.org/10.1039/C5CC06254C	journal	January 2015
Combined strategies in structure-based virtual screening Wang, Zhe; Sun, Huiyong; Shen, Chao Physical Chemistry Chemical Physics, Vol. 22, Issue 6 https://doi.org/10.1039/C9CP06303J	journal	January 2020
Spectral tuning of chlorophylls in proteins – electrostatics vs. ring deformation Lahav, Yigal; Noy, Dror; Schapiro, Igor Physical Chemistry Chemical Physics, Vol. 23, Issue 11 https://doi.org/10.1039/D0CP06582J	journal	January 2021
Nonplanar porphyrins and their significance in proteins A. Shelnutt, John; Song, Xing-Zhi; Ma, Jian-Guo Chemical Society Reviews, Vol. 27, Issue 1 https://doi.org/10.1039/a827031z	journal	January 1998
Conformational control of cofactors in nature—functional tetrapyrrole conformations in the photosynthetic reaction centers of purple bacteria MacGowan, Stuart A.; Senge, Mathias O. Chemical Communications, Vol. 47, Issue 42 https://doi.org/10.1039/c1cc14686f	journal	January 2011
Investigations of heme distortion, low-frequency vibrational excitations, and electron transfer in cytochrome c Sun, Y.; Benabbas, A.; Zeng, W. Proceedings of the National Academy of Sciences, Vol. 111, Issue 18 https://doi.org/10.1073/pnas.1322274111	journal	April 2014
High-resolution cryo-electron microscopy structure of photosystem II from the mesophilic cyanobacterium, Synechocystis sp. PCC 6803 Gisriel, Christopher J.; Wang, Jimin; Liu, Jinchan Proceedings of the National Academy of Sciences, Vol. 119, Issue 1 https://doi.org/10.1073/pnas.2116765118	journal	December 2021
Heme Distortion Modulated by Ligand-Protein Interactions in Inducible Nitric-oxide Synthase Li, David; Stuehr, Dennis J.; Yeh, Syun-Ru Journal of Biological Chemistry, Vol. 279, Issue 25 https://doi.org/10.1074/jbc.M400968200	journal	June 2004
PyDISH: database and analysis tools for heme porphyrin distortion in heme proteins Kondo, Hiroko X.; Kanematsu, Yusuke; Masumoto, Gen Database, Vol. 2023 https://doi.org/10.1093/database/baaa066	journal	October 2020
Folding funnels and binding mechanisms Ma, Buyong; Kumar, Sandeep; Tsai, Chung-Jung Protein Engineering, Design and Selection, Vol. 12, Issue 9 https://doi.org/10.1093/protein/12.9.713	journal	September 1999
Accurate bond and angle parameters for X-ray protein structure refinement Engh, R. A.; Huber, R. Acta Crystallographica Section A Foundations of Crystallography, Vol. 47, Issue 4 https://doi.org/10.1107/S0108767391001071	journal	July 1991
REFMAC 5 dictionary: organization of prior chemical knowledge and guidelines for its use Vagin, Alexei A.; Steiner, Roberto A.; Lebedev, Andrey A. Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12 https://doi.org/10.1107/S0907444904023510	journal	November 2004
Re-refinement from deposited X-ray data can deliver improved models for most PDB entries Joosten, Robbie P.; Womack, Thomas; Vriend, Gert Acta Crystallographica Section D Biological Crystallography, Vol. 65, Issue 2 https://doi.org/10.1107/S0907444908037591	journal	January 2009
electronic Ligand Builder and Optimization Workbench ( eLBOW ): a tool for ligand coordinate and restraint generation Moriarty, Nigel W.; Grosse-Kunstleve, Ralf W.; Adams, Paul D. Acta Crystallographica Section D Biological Crystallography, Vol. 65, Issue 10 https://doi.org/10.1107/S0907444909029436	journal	September 2009
REFMAC 5 for the refinement of macromolecular crystal structures Murshudov, Garib N.; Skubák, Pavol; Lebedev, Andrey A. Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4 https://doi.org/10.1107/S0907444911001314	journal	March 2011
Towards automated crystallographic structure refinement with phenix.refine Afonine, Pavel V.; Grosse-Kunstleve, Ralf W.; Echols, Nathaniel Acta Crystallographica Section D Biological Crystallography, Vol. 68, Issue 4 https://doi.org/10.1107/S0907444912001308	journal	March 2012
The PDB_REDO server for macromolecular structure model optimization Joosten, Robbie P.; Long, Fei; Murshudov, Garib N. IUCrJ, Vol. 1, Issue 4 https://doi.org/10.1107/S2052252514009324	journal	May 2014
The Cambridge Structural Database Groom, Colin R.; Bruno, Ian J.; Lightfoot, Matthew P. Acta Crystallographica Section B Structural Science, Crystal Engineering and Materials, Vol. 72, Issue 2, p. 171-179 https://doi.org/10.1107/S2052520616003954	journal	April 2016
In situ ligand restraints from quantum-mechanical methods Liebschner, Dorothee; Moriarty, Nigel W.; Poon, Billy K. Acta Crystallographica Section D Structural Biology, Vol. 79, Issue 2 https://doi.org/10.1107/S2059798323000025	journal	January 2023
AceDRG : a stereochemical description generator for ligands Long, Fei; Nicholls, Robert A.; Emsley, Paul Acta Crystallographica Section D Structural Biology, Vol. 73, Issue 2 https://doi.org/10.1107/s2059798317000067	journal	February 2017
CERES: a cryo-EM re-refinement system for continuous improvement of deposited models Liebschner, Dorothee; Afonine, Pavel V.; Moriarty, Nigel W. Acta Crystallographica Section D Structural Biology, Vol. 77, Issue 1 https://doi.org/10.1107/s2059798320015879	journal	January 2021
Chlorophyll Ring Deformation Modulates Qy Electronic Energy in Chlorophyll-Protein Complexes and Generates Spectral Forms Zucchelli, Giuseppe; Brogioli, Doriano; Casazza, Anna Paola Biophysical Journal, Vol. 93, Issue 6 https://doi.org/10.1529/biophysj.107.104554	journal	September 2007
Chlorophylls, Symmetry, Chirality, and Photosynthesis Senge, Mathias; Ryan, Aoife; Letchford, Kristie Symmetry, Vol. 6, Issue 3 https://doi.org/10.3390/sym6030781	journal	September 2014
On the Conflicting Estimations of Pigment Site Energies in Photosynthetic Complexes: A Case Study of the CP47 Complex Reinot, Tonu; Chen, Jinhai; Kell, Adam Analytical Chemistry Insights, Vol. 11 https://doi.org/10.4137/aci.s32151	journal	January 2016
Absence of electron-transfer-associated changes in the time-dependent X-ray free-electron laser structures of the photosynthetic reaction center Nishikawa, Gai; Sugo, Yu; Saito, Keisuke eLife, Vol. 12 https://doi.org/10.7554/elife.88955.4	journal	October 2023

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Title: Feeling the Strain: Quantifying Ligand Deformation in Photosynthesis

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