Chromophore twisting in the excited state of a photoswitchable fluorescent protein captured by time-resolved serial femtosecond crystallography

Coquelle, Nicolas; Sliwa, Michel; Woodhouse, Joyce; Schirò, Giorgio; Adam, Virgile; Aquila, Andrew; Barends, Thomas R.  M.; Boutet, Sébastien; Byrdin, Martin; Carbajo, Sergio; De la Mora, Eugenio; Doak, R. Bruce; Feliks, Mikolaj; Fieschi, Franck; Foucar, Lutz; Guillon, Virginia; Hilpert, Mario; Hunter, Mark S.; Jakobs, Stefan; Koglin, Jason E.; Kovacsova, Gabriela; Lane, Thomas J.; Lévy, Bernard; Liang, Mengning; Nass, Karol; Ridard, Jacqueline; Robinson, Joseph S.; Roome, Christopher M.; Ruckebusch, Cyril; Seaberg, Matthew; Thepaut, Michel; Cammarata, Marco; Demachy, Isabelle; Field, Martin; Shoeman, Robert L.; Bourgeois, Dominique; Colletier, Jacques-Philippe; Schlichting, Ilme; Weik, Martin

doi:10.1038/nchem.2853

Title: Chromophore twisting in the excited state of a photoswitchable fluorescent protein captured by time-resolved serial femtosecond crystallography

Journal Article · 11 September 2017 · Nature Chemistry

DOI: https://doi.org/10.1038/nchem.2853 · OSTI ID:1426209

Coquelle, Nicolas ^[1];

^[2]; Woodhouse, Joyce ^[1]; Schirò, Giorgio ^[1];

^[1]; Aquila, Andrew ^[3]; Barends, Thomas R. M. ^[4]; Boutet, Sébastien ^[3]; Byrdin, Martin ^[1]; Carbajo, Sergio ^[3]; De la Mora, Eugenio ^[1]; Doak, R. Bruce ^[4]; Feliks, Mikolaj ^[1]; Fieschi, Franck ^[1]; Foucar, Lutz ^[4]; Guillon, Virginia ^[1]; Hilpert, Mario ^[4]; Hunter, Mark S. ^[3];

^[5]; Koglin, Jason E. ^[3] more »

Univ. of Grenoble (France). Inst. de Biologie Structurale
Univ. de Lille (France). Lab. de Spectrochimie Infrarouge et Raman
SLAC National Accelerator Lab., Menlo Park, CA (United States). Linac Coherent Light Source (LCLS)
Max-Planck-Inst. fur medizinische Forschung, Heidelberg (Germany)
Max-Planck-Inst. fur biophysikalische Chemie, Gottingen (Germany)
Univ. Paris-Sud, Orsay (France); Univ. Paris-Saclay, Orsay (France). Lab. de Chimie-Physique
Univ. of Rennes, Rennes (France). Dept. of Physics

Chromophores absorb light in photosensitive proteins and thereby initiate fundamental biological processes such as photosynthesis, vision and biofluorescence. An important goal in their understanding is the provision of detailed structural descriptions of the ultrafast photochemical events that they undergo, in particular of the excited states that connect chemistry to biological function. Here in this paper we report on the structures of two excited states in the reversibly photoswitchable fluorescent protein rsEGFP2. We populated the states through femtosecond illumination of rsEGFP2 in its non-fluorescent off state and observed their build-up (within less than one picosecond) and decay (on the several picosecond timescale). Using an X-ray free-electron laser, we performed picosecond time-resolved crystallography and show that the hydroxybenzylidene imidazolinone chromophore in one of the excited states assumes a near-canonical twisted configuration halfway between the trans and cis isomers. This is in line with excited-state quantum mechanics/molecular mechanics and classical molecular dynamics simulations. Our new understanding of the structure around the twisted chromophore enabled the design of a mutant that displays a twofold increase in its off-to-on photoswitching quantum yield.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES); European Union (EU)

Grant/Contract Number:: AC02-76SF00515

OSTI ID:: 1426209

Journal Information:: Nature Chemistry, Vol. 10, Issue 1; ISSN 1755-4330

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 127 works

Citation information provided by
Web of Science

References (36)

Chromophore Protonation State Controls Photoswitching of the Fluoroprotein asFP595 Schäfer, Lars V.; Groenhof, Gerrit; Boggio-Pasqua, Martial PLoS Computational Biology, Vol. 4, Issue 3 https://doi.org/10.1371/journal.pcbi.1000034	journal	March 2008
Photoisomerization by Hula-Twist: A Fundamental Supramolecular Photochemical Reaction Liu, Robert S. H. Accounts of Chemical Research, Vol. 34, Issue 7 https://doi.org/10.1021/ar000165c	journal	July 2001
Structural basis for reversible photoswitching in Dronpa Andresen, M.; Stiel, A. C.; Trowitzsch, S. Proceedings of the National Academy of Sciences, Vol. 104, Issue 32 https://doi.org/10.1073/pnas.0700629104	journal	July 2007
Photoswitchable fluorescent proteins enable monochromatic multilabel imaging and dual color fluorescence nanoscopy Andresen, Martin; Stiel, Andre C.; Fölling, Jonas Nature Biotechnology, Vol. 26, Issue 9 https://doi.org/10.1038/nbt.1493	journal	August 2008
Advances in fluorescence labeling strategies for dynamic cellular imaging Dean, Kevin M.; Palmer, Amy E. Nature Chemical Biology, Vol. 10, Issue 7 https://doi.org/10.1038/nchembio.1556	journal	June 2014
Brighter Red Fluorescent Proteins by Rational Design of Triple-Decker Motif Pandelieva, Antonia T.; Baran, Miranda J.; Calderini, Guido F. ACS Chemical Biology, Vol. 11, Issue 2 https://doi.org/10.1021/acschembio.5b00774	journal	January 2016
Crystallographic data processing for free-electron laser sources White, Thomas A.; Barty, Anton; Stellato, Francesco Acta Crystallographica Section D Biological Crystallography, Vol. 69, Issue 7 https://doi.org/10.1107/S0907444913013620	journal	June 2013
The Green Fluorescent Protein Tsien, Roger Y. Annual Review of Biochemistry, Vol. 67, Issue 1, p. 509-544 https://doi.org/10.1146/annurev.biochem.67.1.509	journal	June 1998
Structural characterization of IrisFP, an optical highlighter undergoing multiple photo-induced transformations Adam, V.; Lelimousin, M.; Boehme, S. Proceedings of the National Academy of Sciences, Vol. 105, Issue 47 https://doi.org/10.1073/pnas.0805949105	journal	November 2008
Structure-guided evolution of cyan fluorescent proteins towards a quantum yield of 93% Goedhart, Joachim; von Stetten, David; Noirclerc-Savoye, Marjolaine Nature Communications, Vol. 3, Issue 1 https://doi.org/10.1038/ncomms1738	journal	January 2012
Structure and rotation barriers for ground and excited states of the isolated chromophore of the green fluorescent protein Voityuk, Alexander A.; Michel-Beyerle, Maria-Elisabeth; Rösch, Notker Chemical Physics Letters, Vol. 296, Issue 3-4 https://doi.org/10.1016/S0009-2614(98)01035-5	journal	November 1998
Ground-state proton transfer in the photoswitching reactions of the fluorescent protein Dronpa Warren, Mark M.; Kaucikas, Marius; Fitzpatrick, Ann Nature Communications, Vol. 4, Issue 1 https://doi.org/10.1038/ncomms2460	journal	February 2013
Protonic Gating of Excited-State Twisting and Charge Localization in GFP Chromophores: A Mechanistic Hypothesis for Reversible Photoswitching Olsen, Seth; Lamothe, Kristina; Martínez, Todd J. Journal of the American Chemical Society, Vol. 132, Issue 4 https://doi.org/10.1021/ja907447k	journal	February 2010
CASS—CFEL-ASG software suite Foucar, Lutz; Barty, Anton; Coppola, Nicola Computer Physics Communications, Vol. 183, Issue 10 https://doi.org/10.1016/j.cpc.2012.04.023	journal	October 2012
Low-Temperature Chromophore Isomerization Reveals the Photoswitching Mechanism of the Fluorescent Protein Padron Regis Faro, Aline; Carpentier, Philippe; Jonasson, Gabriella Journal of the American Chemical Society, Vol. 133, Issue 41 https://doi.org/10.1021/ja207001y	journal	October 2011
rsEGFP2 enables fast RESOLFT nanoscopy of living cells Grotjohann, Tim; Testa, Ilaria; Reuss, Matthias eLife, Vol. 1 https://doi.org/10.7554/eLife.00248	journal	December 2012
Raster-scanning serial protein crystallography using micro- and nano-focused synchrotron beams Coquelle, Nicolas; Brewster, Aaron S.; Kapp, Ulrike Acta Crystallographica Section D Biological Crystallography, Vol. 71, Issue 5 https://doi.org/10.1107/S1399004715004514	journal	April 2015
Mapping GFP structure evolution during proton transfer with femtosecond Raman spectroscopy Fang, Chong; Frontiera, Renee R.; Tran, Rosalie Nature, Vol. 462, Issue 7270 https://doi.org/10.1038/nature08527	journal	November 2009
Femtosecond structural dynamics drives the trans/cis isomerization in photoactive yellow protein Pande, K.; Hutchison, C. D. M.; Groenhof, G. Science, Vol. 352, Issue 6286 https://doi.org/10.1126/science.aad5081	journal	May 2016
Phototransformable fluorescent proteins: Future challenges Adam, Virgile; Berardozzi, Romain; Byrdin, Martin Current Opinion in Chemical Biology, Vol. 20 https://doi.org/10.1016/j.cbpa.2014.05.016	journal	June 2014
Excited State Dynamics of the Green Fluorescent Protein on the Nanosecond Time Scale Jonasson, Gabriella; Teuler, Jean-Marie; Vallverdu, Germain Journal of Chemical Theory and Computation, Vol. 7, Issue 6 https://doi.org/10.1021/ct200150r	journal	May 2011
The Role of the Protein Matrix in Green Fluorescent Protein Fluorescence Maddalo, Scott L.; Zimmer, Marc Photochemistry and Photobiology, Vol. 82, Issue 2 https://doi.org/10.1562/2005-04-11-RA-485	journal	January 2006
Rational design of ultrastable and reversibly photoswitchable fluorescent proteins for super-resolution imaging of the bacterial periplasm El Khatib, Mariam; Martins, Alexandre; Bourgeois, Dominique Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep18459	journal	January 2016
Structure and mechanism of the reversible photoswitch of a fluorescent protein Andresen, M.; Wahl, M. C.; Stiel, A. C. Proceedings of the National Academy of Sciences, Vol. 102, Issue 37 https://doi.org/10.1073/pnas.0502772102	journal	August 2005
Real-Time Monitoring of Chromophore Isomerization and Deprotonation during the Photoactivation of the Fluorescent Protein Dronpa Yadav, Dheerendra; Lacombat, Fabien; Dozova, Nadia The Journal of Physical Chemistry B, Vol. 119, Issue 6 https://doi.org/10.1021/jp507094f	journal	August 2014
The Coherent X-ray Imaging instrument at the Linac Coherent Light Source Liang, Mengning; Williams, Garth J.; Messerschmidt, Marc Journal of Synchrotron Radiation, Vol. 22, Issue 3 https://doi.org/10.1107/S160057751500449X	journal	April 2015
Photocycle populations with femtosecond excitation of crystalline photoactive yellow protein Hutchison, Christopher D. M.; Kaucikas, Marius; Tenboer, Jason Chemical Physics Letters, Vol. 654 https://doi.org/10.1016/j.cplett.2016.04.087	journal	June 2016
Shedding light on the dark and weakly fluorescent states of green fluorescent proteins Weber, W.; Helms, V.; McCammon, J. A. Proceedings of the National Academy of Sciences, Vol. 96, Issue 11 https://doi.org/10.1073/pnas.96.11.6177	journal	May 1999
Excited state reactions in fluorescent proteins Meech, Stephen R. Chemical Society Reviews, Vol. 38, Issue 10 https://doi.org/10.1039/b820168b	journal	January 2009
CFEL–ASG Software Suite ( CASS ): usage for free-electron laser experiments with biological focus Foucar, Lutz Journal of Applied Crystallography, Vol. 49, Issue 4 https://doi.org/10.1107/S1600576716009201	journal	June 2016
Regulated Fast Nucleocytoplasmic Shuttling Observed by Reversible Protein Highlighting Ando, R. Science, Vol. 306, Issue 5700 https://doi.org/10.1126/science.1102506	journal	November 2004
Serial Femtosecond Crystallography and Ultrafast Absorption Spectroscopy of the Photoswitchable Fluorescent Protein IrisFP Colletier, Jacques-Philippe; Sliwa, Michel; Gallat, François-Xavier The Journal of Physical Chemistry Letters, Vol. 7, Issue 5 https://doi.org/10.1021/acs.jpclett.5b02789	journal	February 2016
Improved Estimation of Structure-Factor Difference Amplitudesfrom Poorly Accurate Data Ursby, T.; Bourgeois, D. Acta Crystallographica Section A Foundations of Crystallography, Vol. 53, Issue 5 https://doi.org/10.1107/S0108767397004522	journal	September 1997
Simple and efficient system for photoconverting light-sensitive proteins in serial crystallography experiments Schirò, Giorgio; Woodhouse, Joyce; Weik, Martin Journal of Applied Crystallography, Vol. 50, Issue 3 https://doi.org/10.1107/S1600576717006264	journal	June 2017
Difference refinement: obtaining differences between two related structures Terwilliger, T. C.; Berendzen, J. Acta Crystallographica Section D Biological Crystallography, Vol. 51, Issue 5 https://doi.org/10.1107/S0907444994013247	journal	September 1995
Direct observation of ultrafast collective motions in CO myoglobin upon ligand dissociation Barends, T. R. M.; Foucar, L.; Ardevol, A. Science, Vol. 350, Issue 6259 https://doi.org/10.1126/science.aac5492	journal	September 2015

Cited By (36)

Dual Illumination Enhances Transformation of an Engineered Green‐to‐Red Photoconvertible Fluorescent Protein Krueger, Taylor D.; Tang, Longteng; Zhu, Liangdong Angewandte Chemie, Vol. 132, Issue 4 https://doi.org/10.1002/ange.201911379	journal	November 2019
Dual Illumination Enhances Transformation of an Engineered Green‐to‐Red Photoconvertible Fluorescent Protein Krueger, Taylor D.; Tang, Longteng; Zhu, Liangdong Angewandte Chemie International Edition, Vol. 59, Issue 4 https://doi.org/10.1002/anie.201911379	journal	January 2020
NAMD goes quantum: an integrative suite for hybrid simulations Melo, Marcelo C. R.; Bernardi, Rafael C.; Rudack, Till Nature Methods, Vol. 15, Issue 5 https://doi.org/10.1038/nmeth.4638	journal	March 2018
Three-dimensional view of ultrafast dynamics in photoexcited bacteriorhodopsin Nass Kovacs, Gabriela; Colletier, Jacques-Philippe; Grünbein, Marie Luise Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-10758-0	journal	July 2019
Photoswitching mechanism of a fluorescent protein revealed by time-resolved crystallography and transient absorption spectroscopy Woodhouse, Joyce; Nass Kovacs, Gabriela; Coquelle, Nicolas Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-14537-0	journal	February 2020
Infrared spectroscopy reveals multi-step multi-timescale photoactivation in the photoconvertible protein archetype dronpa Laptenok, Sergey P.; Gil, Agnieszka A.; Hall, Christopher R. Nature Chemistry, Vol. 10, Issue 8 https://doi.org/10.1038/s41557-018-0073-0	journal	June 2018
Mechanistic investigation of mEos4b reveals a strategy to reduce track interruptions in sptPALM De Zitter, Elke; Thédié, Daniel; Mönkemöller, Viola Nature Methods, Vol. 16, Issue 8 https://doi.org/10.1038/s41592-019-0462-3	journal	July 2019
Viscosity-adjustable grease matrices for serial nanocrystallography Sugahara, Michihiro; Motomura, Koji; Suzuki, Mamoru Scientific Reports, Vol. 10, Issue 1 https://doi.org/10.1038/s41598-020-57675-7	journal	January 2020
Spiers Memorial Lecture : Introductory lecture: the impact of structure on photoinduced processes in nucleic acids and proteins Domratcheva, Tatiana; Schlichting, Ilme Faraday Discussions, Vol. 207 https://doi.org/10.1039/c8fd00058a	journal	January 2018
A new GFP fluorophore-based probe for lysosome labelling and tracing lysosomal viscosity in live cells Li, Xiaolin; Zhao, Rongrong; Wang, Yang Journal of Materials Chemistry B, Vol. 6, Issue 41 https://doi.org/10.1039/c8tb01885e	journal	January 2018
Comparative study of two near-infrared coumarin–BODIPY dyes for bioimaging and photothermal therapy of cancer Zhang, Yuandong; Song, Nan; Li, Yuanyuan Journal of Materials Chemistry B, Vol. 7, Issue 30 https://doi.org/10.1039/c9tb01165j	journal	January 2019
Data-driven challenges and opportunities in crystallography Glynn, Calina; Rodriguez, Jose A. Emerging Topics in Life Sciences, Vol. 3, Issue 4 https://doi.org/10.1042/etls20180177	journal	July 2019
Unveiling coupled electronic and vibrational motions of chromophores in condensed phases Fang, Chong; Tang, Longteng; Chen, Cheng The Journal of Chemical Physics, Vol. 151, Issue 20 https://doi.org/10.1063/1.5128388	journal	November 2019
An outlook on using serial femtosecond crystallography in drug discovery Mishin, Alexey; Gusach, Anastasiia; Luginina, Aleksandra Expert Opinion on Drug Discovery, Vol. 14, Issue 9 https://doi.org/10.1080/17460441.2019.1626822	journal	May 2019
A simple adaptation to a protein crystallography station to facilitate difference X-ray scattering studies Sharma, Amit; Berntsen, Peter; Harimoorthy, Rajiv Journal of Applied Crystallography, Vol. 52, Issue 2 https://doi.org/10.1107/s1600576719001900	journal	March 2019
Room-temperature photo-induced martensitic transformation in a protein crystal Dajnowicz, Steven; Langan, Patricia S.; Weiss, Kevin L. IUCrJ, Vol. 6, Issue 4 https://doi.org/10.1107/s2052252519005761	journal	May 2019
Specific radiation damage is a lesser concern at room temperature Gotthard, Guillaume; Aumonier, Sylvain; De Sanctis, Daniele IUCrJ, Vol. 6, Issue 4 https://doi.org/10.1107/s205225251900616x	journal	June 2019
Sample delivery for serial crystallography at free-electron lasers and synchrotrons Grünbein, Marie Luise; Nass Kovacs, Gabriela Acta Crystallographica Section D Structural Biology, Vol. 75, Issue 2 https://doi.org/10.1107/s205979831801567x	journal	January 2019
Well-based crystallization of lipidic cubic phase microcrystals for serial X-ray crystallography experiments Andersson, Rebecka; Safari, Cecilia; Båth, Petra Acta Crystallographica Section D Structural Biology, Vol. 75, Issue 10 https://doi.org/10.1107/s2059798319012695	journal	October 2019
A guide to sample delivery systems for serial crystallography Zhao, Feng‐Zhu; Zhang, Bin; Yan, Er‐Kai The FEBS Journal, Vol. 286, Issue 22 https://doi.org/10.1111/febs.15099	journal	August 2019
Analytical wave function of an atomic electron under the action of a powerful ultrashort electromagnetic field pulse Makarov, Dmitry N.; Eseev, Marat K.; Makarova, Ksenya A. Optics Letters, Vol. 44, Issue 12 https://doi.org/10.1364/ol.44.003042	journal	January 2019
Megahertz Data Collection from Protein Microcrystals at an X-Ray Free-Electron Laser Grünbein, Marie Luise; Bielecki, Johan; Gorel, Alexander Deutsches Elektronen-Synchrotron, DESY, Hamburg https://doi.org/10.3204/pubdb-2018-03217	text	January 2018
Retinal isomerization in bacteriorhodopsin captured by a femtosecond x-ray laser Nogly, Przemyslaw; Weinert, Tobias; James, Daniel Deutsches Elektronen-Synchrotron, DESY, Hamburg https://doi.org/10.3204/pubdb-2018-05837	text	January 2018
Recent Advances in Ultrafast Structural Techniques Sciaini, Germán Applied Sciences, Vol. 9, Issue 7 https://doi.org/10.3390/app9071427	journal	April 2019
Megahertz data collection from protein microcrystals at an X-ray free-electron laser Grünbein, Marie Luise; Bielecki, Johan; Gorel, Alexander Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-05953-4	journal	August 2018
Temperature-jump solution X-ray scattering reveals distinct motions in a dynamic enzyme Thompson, Michael C.; Barad, Benjamin A.; Wolff, Alexander M. Nature Chemistry, Vol. 11, Issue 11 https://doi.org/10.1038/s41557-019-0329-3	journal	September 2019
Mechanistic investigation of mEos4b reveals a strategy to reduce track interruptions in sptPALM De Zitter, Elke; Thédié, Daniel; Mönkemöller, Viola https://doi.org/10.1101/475939	posted_content	November 2018
Strategies for sample delivery for femtosecond crystallography Martiel, Isabelle; Müller-Werkmeister, Henrike M.; Cohen, Aina E. International Union of Crystallography (IUCr) https://doi.org/10.1107/s2059798318017953/ba5296sup1.pdf	text	January 2019
Retinal isomerization in bacteriorhodopsin captured by a femtosecond x-ray laser Nogly, Przemyslaw; Weinert, Tobias; James, Daniel Science https://doi.org/10.1126/science.aat0094	journal	June 2018
Initial observations of the femtosecond timing jitter at the European XFEL Kirkwood, Henry J.; Letrun, Romain; Tanikawa, Takanori Deutsches Elektronen-Synchrotron, DESY, Hamburg https://doi.org/10.3204/pubdb-2019-01958	text	January 2019
Three-dimensional view of ultrafast dynamics in photoexcited bacteriorhodopsin Kovacs, Gabriela Nass; Colletier, Jacques-Philippe; Grünbein, Marie arXiv https://doi.org/10.48550/arxiv.1905.09002	text	January 2019
Three-dimensional view of ultrafast dynamics in photoexcited bacteriorhodopsin in the multiphoton regime and biological relevance Miller, R. J. Dwayne; Paré-Labrosse, Olivier; Sarracini, Antoine Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-14971-0	journal	March 2020
Temperature-jump solution X-ray scattering reveals distinct motions in a dynamic enzyme Thompson, Michael C.; Barad, Benjamin A.; Wolff, Alexander M. Nature Chemistry, Vol. 11, Issue 11 https://doi.org/10.1038/s41557-019-0329-3	journal	September 2019
Megahertz Data Collection from Protein Microcrystals at an X-Ray Free-Electron Laser Grünbein, Marie Luise; Bielecki, Johan; Gorel, Alexander Deutsches Elektronen-Synchrotron, DESY, Hamburg https://doi.org/10.3204/pubdb-2018-03217	text	January 2018
Hydrogels With Tunable Mechanical Properties Based on Photocleavable Proteins Xiang, Dongfang; Wu, Xin; Cao, Wei Frontiers in Chemistry, Vol. 8 https://doi.org/10.3389/fchem.2020.00007	journal	January 2020
A tool for visualizing protein motions in time-resolved crystallography Cecilia, Wickstrand,; Gergely, Katona,; Takanori, Nakane, ETH Zurich https://doi.org/10.3929/ethz-b-000409850	text	January 2020

Similar Records

Internal conversion of the anionic GFP chromophore: in and out of the I-twisted S₁/S₀ conical intersection seam

Journal Article · 2021 · Chemical Science · OSTI ID:1834650

List, Nanna H.; Jones, Chey M.; Martínez, Todd J.

Rational Control of Off-State Heterogeneity in a Photoswitchable Fluorescent Protein Provides Switching Contrast Enhancement**

Journal Article · 2022 · ChemPhysChem · OSTI ID:1881341

Adam, Virgile; Hadjidemetriou, Kyprianos; Jensen, Nickels; +48 more

Resolving the ultrafast dynamics of the anionic green fluorescent protein chromophore in water

Journal Article · 2021 · Chemical Science · OSTI ID:1810989

Jones, Chey M.; List, Nanna H.; Martínez, Todd J.

Related Subjects

77 NANOSCIENCE AND NANOTECHNOLOGY
59 BASIC BIOLOGICAL SCIENCES
Nanocrystallography
Photobiology
Protein structure predictions

Title: Chromophore twisting in the excited state of a photoswitchable fluorescent protein captured by time-resolved serial femtosecond crystallography

Citation Formats

References (36)

Cited By (36)

Similar Records

Related Subjects