Dynamic crystallography reveals early signalling events in ultraviolet photoreceptor UVR8
Abstract
Arabidopsis thaliana UVR8 (AtUVR8) is a long-sought-after photoreceptor that undergoes dimer dissociation in response to UV-B light. Crystallographic and mutational studies have identified two crucial tryptophan residues for UV-B responses in AtUVR8. However, the mechanism of UV-B perception and structural events leading up to dimer dissociation remain elusive at the molecular level. We applied dynamic crystallography to capture light-induced structural events in photoactive AtUVR8 crystals. Here we report two intermediate structures at 1.67Å resolution. At the epicenter of UV-B signaling, concerted motions associated with Trp285/Trp233 lead to ejection of a water molecule, which weakens an intricate network of hydrogen bonds and salt bridges at the dimer interface. Partial opening of the β-propeller structure due to thermal relaxation of conformational strains originating in the epicenter further disrupts the dimer interface and leads to dimer dissociation. Ultimately, these dynamic crystallographic observations provide structural insights into the photo-perception and signaling mechanism of UVR8.
- Authors:
-
- Huazhong Agricultural Univ., Hubei (People's Republic of China)
- Renz Research Inc., Westmont, IL (United States)
- City Univ. of Hong Kong, Kowloon (Hong Kong)
- The Univ. of Chicago, Chicago, IL (United States)
- Publication Date:
- Research Org.:
- UChicago, LLC., Argonne, IL (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Basic Energy Sciences (BES)
- OSTI Identifier:
- 1347118
- Grant/Contract Number:
- AC02-06CH11357; GM036452; EY024363; 31270893; 31110103912
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Nature Plants (Online)
- Additional Journal Information:
- Journal Name: Nature Plants (Online); Journal Volume: 1; Journal Issue: 1; Journal ID: ISSN 2055-0278
- Publisher:
- Nature Publishing Group
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; 54 ENVIRONMENTAL SCIENCES; photoreceptor; light signaling; dynamic crystallography; UVR8; photo-perception mechanism
Citation Formats
Zeng, Xiaoli, Ren, Zhong, Wu, Qi, Fan, Jun, Peng, Pan -Pan, Tang, Kun, Zhang, Ruiqin, Zhao, Kai -Hong, and Yang, Xiaojing. Dynamic crystallography reveals early signalling events in ultraviolet photoreceptor UVR8. United States: N. p., 2015.
Web. doi:10.1038/nplants.2014.6.
Zeng, Xiaoli, Ren, Zhong, Wu, Qi, Fan, Jun, Peng, Pan -Pan, Tang, Kun, Zhang, Ruiqin, Zhao, Kai -Hong, & Yang, Xiaojing. Dynamic crystallography reveals early signalling events in ultraviolet photoreceptor UVR8. United States. https://doi.org/10.1038/nplants.2014.6
Zeng, Xiaoli, Ren, Zhong, Wu, Qi, Fan, Jun, Peng, Pan -Pan, Tang, Kun, Zhang, Ruiqin, Zhao, Kai -Hong, and Yang, Xiaojing. Thu .
"Dynamic crystallography reveals early signalling events in ultraviolet photoreceptor UVR8". United States. https://doi.org/10.1038/nplants.2014.6. https://www.osti.gov/servlets/purl/1347118.
@article{osti_1347118,
title = {Dynamic crystallography reveals early signalling events in ultraviolet photoreceptor UVR8},
author = {Zeng, Xiaoli and Ren, Zhong and Wu, Qi and Fan, Jun and Peng, Pan -Pan and Tang, Kun and Zhang, Ruiqin and Zhao, Kai -Hong and Yang, Xiaojing},
abstractNote = {Arabidopsis thaliana UVR8 (AtUVR8) is a long-sought-after photoreceptor that undergoes dimer dissociation in response to UV-B light. Crystallographic and mutational studies have identified two crucial tryptophan residues for UV-B responses in AtUVR8. However, the mechanism of UV-B perception and structural events leading up to dimer dissociation remain elusive at the molecular level. We applied dynamic crystallography to capture light-induced structural events in photoactive AtUVR8 crystals. Here we report two intermediate structures at 1.67Å resolution. At the epicenter of UV-B signaling, concerted motions associated with Trp285/Trp233 lead to ejection of a water molecule, which weakens an intricate network of hydrogen bonds and salt bridges at the dimer interface. Partial opening of the β-propeller structure due to thermal relaxation of conformational strains originating in the epicenter further disrupts the dimer interface and leads to dimer dissociation. Ultimately, these dynamic crystallographic observations provide structural insights into the photo-perception and signaling mechanism of UVR8.},
doi = {10.1038/nplants.2014.6},
journal = {Nature Plants (Online)},
number = 1,
volume = 1,
place = {United States},
year = {Thu Jan 08 00:00:00 EST 2015},
month = {Thu Jan 08 00:00:00 EST 2015}
}
Free Publicly Available Full Text
Publisher's Version of Record
Other availability
Search WorldCat to find libraries that may hold this journal
Cited by: 42 works
Citation information provided by
Web of Science
Web of Science
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.
Works referenced in this record:
Light-Induced Structural Changes in a Photosynthetic Reaction Center Caught by Laue Diffraction
journal, April 2010
- Wohri, A. B.; Katona, G.; Johansson, L. C.
- Science, Vol. 328, Issue 5978
In Vivo Function of Tryptophans in the Arabidopsis UV-B Photoreceptor UVR8
journal, September 2012
- O’Hara, Andrew; Jenkins, Gareth I.
- The Plant Cell, Vol. 24, Issue 9
Structural basis of ultraviolet-B perception by UVR8
journal, February 2012
- Di Wu, ; Hu, Qi; Yan, Zhen
- Nature, Vol. 484, Issue 7393
Ultraviolet stress delays chromosome replication in light/dark synchronized cells of the marine cyanobacterium Prochlorococcus marinus PCC9511
journal, January 2010
- Kolowrat, Christian; Partensky, Frédéric; Mella-Flores, Daniella
- BMC Microbiology, Vol. 10, Issue 1
Decomposition of Protein Tryptophan Fluorescence Spectra into Log-Normal Components. III. Correlation between Fluorescence and Microenvironment Parameters of Individual Tryptophan Residues
journal, September 2001
- Reshetnyak, Yana K.; Koshevnik, Yuly; Burstein, Edward A.
- Biophysical Journal, Vol. 81, Issue 3
C-terminal region of the UV-B photoreceptor UVR8 initiates signaling through interaction with the COP1 protein
journal, September 2012
- Cloix, C.; Kaiserli, E.; Heilmann, M.
- Proceedings of the National Academy of Sciences, Vol. 109, Issue 40
Photochemical Reaction Mechanism of UV-B-Induced Monomerization of UVR8 Dimers as the First Signaling Event in UV-B-Regulated Gene Expression in Plants
journal, January 2014
- Wu, Min; Strid, Åke; Eriksson, Leif A.
- The Journal of Physical Chemistry B, Vol. 118, Issue 4
Self-consistent-charge density-functional tight-binding method for simulations of complex materials properties
journal, September 1998
- Elstner, M.; Porezag, D.; Jungnickel, G.
- Physical Review B, Vol. 58, Issue 11, p. 7260-7268
Temperature-scan cryocrystallography reveals reaction intermediates in bacteriophytochrome
journal, October 2011
- Yang, Xiaojing; Ren, Zhong; Kuk, Jane
- Nature, Vol. 479, Issue 7373
Tight-binding approach to time-dependent density-functional response theory
journal, February 2001
- Niehaus, T. A.; Suhai, S.; Della Sala, F.
- Physical Review B, Vol. 63, Issue 8
Plants and near-ultraviolet radiation
journal, January 1978
- Klein, Richard M.
- The Botanical Review, Vol. 44, Issue 1
A UV-B-specific signaling component orchestrates plant UV protection
journal, December 2005
- Brown, B. A.; Cloix, C.; Jiang, G. H.
- Proceedings of the National Academy of Sciences, Vol. 102, Issue 50
Photoactivated UVR8-COP1 Module Determines Photomorphogenic UV-B Signaling Output in Arabidopsis
journal, March 2014
- Huang, Xi; Yang, Panyu; Ouyang, Xinhao
- PLoS Genetics, Vol. 10, Issue 3
Arabidopsis UVR8 Regulates Ultraviolet-B Signal Transduction and Tolerance and Contains Sequence Similarity to Human Regulator of Chromatin Condensation 1
journal, August 2002
- Kliebenstein, Daniel J.; Lim, Jackie E.; Landry, Laurie G.
- Plant Physiology, Vol. 130, Issue 1
Crystal structure of spinach major light-harvesting complex at 2.72 Å resolution
journal, March 2004
- Liu, Zhenfeng; Yan, Hanchi; Wang, Kebin
- Nature, Vol. 428, Issue 6980
UV-B photoreceptor-mediated signalling in plants
journal, April 2012
- Heijde, Marc; Ulm, Roman
- Trends in Plant Science, Vol. 17, Issue 4
On the mechanism of photoinduced dimer dissociation in the plant UVR8 photoreceptor
journal, March 2014
- Voityuk, A. A.; Marcus, R. A.; Michel-Beyerle, M. -E.
- Proceedings of the National Academy of Sciences, Vol. 111, Issue 14
Constitutively active UVR8 photoreceptor variant in Arabidopsis
journal, November 2013
- Heijde, M.; Binkert, M.; Yin, R.
- Proceedings of the National Academy of Sciences, Vol. 110, Issue 50
The UV-B Photoreceptor UVR8: From Structure to Physiology
journal, January 2014
- Jenkins, Gareth I.
- The Plant Cell, Vol. 26, Issue 1
Ultraviolet light-emitting diodes operating in the 340nm wavelength range and application to time-resolved fluorescence spectroscopy
journal, August 2004
- Peng, H.; Makarona, E.; He, Y.
- Applied Physics Letters, Vol. 85, Issue 8
Photoinduced transformation of UVR8 monitored by vibrational and fluorescence spectroscopy
journal, January 2015
- Heilmann, Monika; Christie, John M.; Kennis, John T. M.
- Photochemical & Photobiological Sciences, Vol. 14, Issue 2
Quenching Dynamics of Ultraviolet-Light Perception by UVR8 Photoreceptor
journal, December 2013
- Liu, Zheyun; Li, Xiankun; Zhong, Frank W.
- The Journal of Physical Chemistry Letters, Vol. 5, Issue 1
Plant UVR8 Photoreceptor Senses UV-B by Tryptophan-Mediated Disruption of Cross-Dimer Salt Bridges
journal, February 2012
- Christie, J. M.; Arvai, A. S.; Baxter, K. J.
- Science, Vol. 335, Issue 6075
Interactions and Stabilities of the UV RESISTANCE LOCUS8 (UVR8) Protein Dimer and Its Key Mutants
journal, June 2013
- Wu, Min; Strid, Åke; Eriksson, Leif A.
- Journal of Chemical Information and Modeling, Vol. 53, Issue 7
Selective excitation of tryptophan fluorescence decay in proteins using a subnanosecond 295nm light-emitting diode and time-correlated single-photon counting
journal, June 2005
- McGuinness, Colin D.; Sagoo, Kulwinder; McLoskey, David
- Applied Physics Letters, Vol. 86, Issue 26
The Molecular Mechanism of the UVR8 UV-B Photoreceptor
journal, September 2012
- Hofmann, Nancy R.
- The Plant Cell, Vol. 24, Issue 9
Functional interaction of the circadian clock and UV RESISTANCE LOCUS 8-controlled UV-B signaling pathways in Arabidopsis thaliana: Interaction of UV-B and clock signaling
journal, April 2011
- Fehér, Balázs; Kozma-Bognár, László; Kevei, Éva
- The Plant Journal, Vol. 67, Issue 1
Construction of tight-binding-like potentials on the basis of density-functional theory: Application to carbon
journal, May 1995
- Porezag, D.; Frauenheim, Th.; Köhler, Th.
- Physical Review B, Vol. 51, Issue 19
A Molecular Movie at 1.8 Å Resolution Displays the Photocycle of Photoactive Yellow Protein, a Eubacterial Blue-Light Receptor, from Nanoseconds to Seconds †
journal, November 2001
- Ren, Zhong; Perman, Benjamin; Šrajer, Vukica
- Biochemistry, Vol. 40, Issue 46
The ancient regulatory-protein family of WD-repeat proteins
journal, September 1994
- Neer, Eva J.; Schmidt, Carl J.; Nambudripad, Raman
- Nature, Vol. 371, Issue 6495
Approximate time-dependent density functional theory
journal, November 2009
- Niehaus, T. A.
- Journal of Molecular Structure: THEOCHEM, Vol. 914, Issue 1-3
Perception of UV-B by the Arabidopsis UVR8 Protein
journal, March 2011
- Rizzini, L.; Favory, J. -J.; Cloix, C.
- Science, Vol. 332, Issue 6025
Modeling the Absorption Spectrum of Tryptophan in Proteins
journal, December 2005
- Rogers, David M.; Besley, Nicholas A.; O'Shea, Paul
- The Journal of Physical Chemistry B, Vol. 109, Issue 48
Interaction of COP1 and UVR8 regulates UV-B-induced photomorphogenesis and stress acclimation in Arabidopsis
journal, January 2009
- Favory, Jean-Jacques; Stec, Agnieszka; Gruber, Henriette
- The EMBO Journal, Vol. 28, Issue 5
Works referencing / citing this record:
Q&A: How do plants sense and respond to UV-B radiation?
journal, June 2015
- Ulm, Roman; Jenkins, Gareth I.
- BMC Biology, Vol. 13, Issue 1
Regulation of Arabidopsis gene expression by low fluence rate UV-B independently of UVR8 and stress signaling
journal, January 2019
- O'Hara, Andrew; Headland, Lauren R.; Díaz-Ramos, L. Aranzazú
- Photochemical & Photobiological Sciences, Vol. 18, Issue 7
UVR8-dependent reporters reveal spatial characteristics of signal spreading in plant tissues
journal, January 2019
- Vanhaelewyn, Lucas; Bernula, Péter; Van Der Straeten, Dominique
- Photochemical & Photobiological Sciences, Vol. 18, Issue 5
Structural basis of molecular logic OR in a dual-sensor histidine kinase
journal, September 2019
- Shin, Heewhan; Ren, Zhong; Zeng, Xiaoli
- Proceedings of the National Academy of Sciences, Vol. 116, Issue 40
A Comprehensive Phylogeny Reveals Functional Conservation of the UV-B Photoreceptor UVR8 from Green Algae to Higher Plants
journal, November 2016
- Fernández, María B.; Tossi, Vanesa; Lamattina, Lorenzo
- Frontiers in Plant Science, Vol. 7
Regulation of UVR8 photoreceptor dimer/monomer photo-equilibrium in Arabidopsis plants grown under photoperiodic conditions: UVR8 photo-equilibrium
journal, May 2016
- Findlay, Kirsten M. W.; Jenkins, Gareth I.
- Plant, Cell & Environment, Vol. 39, Issue 8
Difference in the action spectra for UVR8 monomerisation and HY5 transcript accumulation in Arabidopsis
journal, January 2018
- Díaz-Ramos, L. Aranzazú; O'Hara, Andrew; Kanagarajan, Selvaraju
- Photochemical & Photobiological Sciences, Vol. 17, Issue 8
A FRET method for investigating dimer/monomer status and conformation of the UVR8 photoreceptor
journal, January 2019
- Liao, Xinyang; Zhang, Ben; Blatt, Michael R.
- Photochemical & Photobiological Sciences, Vol. 18, Issue 2
The role of tryptophans in the UV-B absorption of a UVR8 photoreceptor – a computational study
journal, January 2015
- Wu, Qi; Huang, Bolong; Niehaus, T. A.
- Physical Chemistry Chemical Physics, Vol. 17, Issue 16
Signal transduction mediated by the plant UV‐B photoreceptor UVR8
journal, October 2018
- Liang, Tong; Yang, Yu; Liu, Hongtao
- New Phytologist, Vol. 221, Issue 3
Ultrafast Structural Changes Decomposed from Serial Crystallographic Data
journal, October 2019
- Ren, Zhong
- The Journal of Physical Chemistry Letters, Vol. 10, Issue 22
A Comprehensive Phylogeny Reveals Functional Conservation of the UV-B Photoreceptor UVR8 from Green Algae to Higher Plants
journal, November 2016
- Fernández, María B.; Tossi, Vanesa; Lamattina, Lorenzo
- Frontiers in Plant Science, Vol. 7
Photomorphogenic responses to ultraviolet-B light: Responses to UV-B
journal, March 2017
- Jenkins, Gareth I.
- Plant, Cell & Environment, Vol. 40, Issue 11
Native mass spectrometry reveals the conformational diversity of the UVR8 photoreceptor
journal, January 2019
- Camacho, Inês S.; Theisen, Alina; Johannissen, Linus O.
- Proceedings of the National Academy of Sciences, Vol. 116, Issue 4
Ultrafast Structural Changes Decomposed from Serial Crystallographic Data
posted_content, July 2019
- Ren, Zhong
Q&A: How do plants sense and respond to UV-B radiation?
journal, June 2015
- Ulm, Roman; Jenkins, Gareth I.
- BMC Biology, Vol. 13, Issue 1