Browse
Submit Data
Databases
API
Help

Dataset Information

47 Views

0 Connections

0 Citations

0 Reanalyses

0 Downloads

Omics score: 0

Dynamics and mechanism of dimer dissociation of photoreceptor UVR8.

ABSTRACT: Photoreceptors are a class of light-sensing proteins with critical biological functions. UVR8 is the only identified UV photoreceptor in plants and its dimer dissociation upon UV sensing activates UV-protective processes. However, the dissociation mechanism is still poorly understood. Here, by integrating extensive mutations, ultrafast spectroscopy, and computational calculations, we find that the funneled excitation energy in the interfacial tryptophan (Trp) pyramid center drives a directional Trp-Trp charge separation in 80 ps and produces a critical transient Trp anion, enabling its ultrafast charge neutralization with a nearby positive arginine residue in 17 ps to destroy a key salt bridge. A domino effect is then triggered to unzip the strong interfacial interactions, which is facilitated through flooding the interface by channel and interfacial water molecules. These detailed dynamics reveal a unique molecular mechanism of UV-induced dimer monomerization.

SUBMITTER: Li X

PROVIDER: S-EPMC8748919 | biostudies-literature | 2022 Jan

REPOSITORIES: biostudies-literature

ACCESS DATA

Json Xml

Publications

Dynamics and mechanism of dimer dissociation of photoreceptor UVR8.

Li Xiankun X Liu Zheyun Z Ren Haisheng H Kundu Mainak M Zhong Frank W FW Wang Lijuan L Gao Jiali J Zhong Dongping D

Nature communications 20220110 1

Photoreceptors are a class of light-sensing proteins with critical biological functions. UVR8 is the only identified UV photoreceptor in plants and its dimer dissociation upon UV sensing activates UV-protective processes. However, the dissociation mechanism is still poorly understood. Here, by integrating extensive mutations, ultrafast spectroscopy, and computational calculations, we find that the funneled excitation energy in the interfacial tryptophan (Trp) pyramid center drives a directional ...[more]

PMID: 35013256

Similar Datasets

On the mechanism of photoinduced dimer dissociation in the plant UVR8 photoreceptor.

Project description:UV-B absorption by the photoreceptor UV resistance locus 8 (UVR8) consisting of two identical protein units triggers a signal chain used by plants in connection with protection and repair of UV-B induced damage. X-ray structural analysis of the purified protein [Christie JM, et al. (2012) Science 335(6075):1492-1496] [Wu D, et al. (2012) Nature 484(7393): 214-220] has revealed that the dimer is held together by arginine-aspartate salt bridges. In this paper we address the initial processes in the signal chain. On the basis of high-level quantum-chemical calculations, we propose a mechanism for the photodissociation of UVR8 that consists of three steps: (i) In each monomer, multiple tryptophans form an extended light-harvesting system in which the La excited state of Trp233 experiences strong electrostatic stabilization by the protein environment. The strong stabilization singles out this tryptophan to be an efficient exciton acceptor that accumulates the excitation energy from the entire protein subunit. (ii) A fast decay of the locally excited state by charge separation generates the radical ion pair Trp285(+)-Trp233(-) with a dipole moment of ?18 D. (iii) Key to the proposed mechanism is that this large dipole moment drives the breaking of the salt bridges between the two monomer subunits. The suggested mechanism for the UV-B-driven dissociation of the dimer that rests on the prominent players Trp233 and Trp285 explains the experimental results obtained from mutagenesis of UVR8.

| S-EPMC3986182 | biostudies-literature

Dynamics and mechanism of light harvesting in UV photoreceptor UVR8.

Project description:Photosynthetic pigments form light-harvesting networks to enable nearly perfect quantum efficiency in photosynthesis via excitation energy transfer. However, similar light-harvesting mechanisms have not been reported in light sensing processes in other classes of photoreceptors during light-mediated signaling. Here, based on our earlier report, we mapped out a striking energy-transfer network composed of 26 structural tryptophan residues in the plant UV-B photoreceptor UVR8. The spectra of the tryptophan chromophores are tuned by the protein environments, funneling all excitation energy to a cluster of four tryptophan residues, a pyramid center, where the excitation-induced monomerization is initiated for cell signaling. With extensive site-directed mutagenesis, various time-resolved fluorescence techniques, and combined QM/MM simulations, we determined the energy-transfer rates for all donor-acceptor pairs, revealing the time scales from tens of picoseconds to nanoseconds. The overall light harvesting quantum efficiency by the pyramid center is significantly increased to 73%, compared to a direct excitation probability of 35%. UVR8 is the only photoreceptor discovered so far using a natural amino-acid tryptophan without utilizing extrinsic chromophores to form a network to carry out both light harvesting and light perception for biological functions.

| S-EPMC8163212 | biostudies-literature

Gallium Trichloride Fluid: Dimer Dissociation Mechanism, Local Structure, and Atomic Dynamics.

Project description:Molten gallium trichloride emerges as a promising solvent for oxidative metal recycling. The use of supercritical fluid enhances the performance and kinetics of metal dissolution due to significantly lower viscosity in the reaction media. Additionally, the dual molecular nature of gallium trichloride, existing as edge-sharing ES-Ga2Cl6 dimers at low temperatures and high pressure, or flat trigonal GaCl3 monomers in the vicinity of the critical point and low pressures, creates the possibility to tailor the chemical geometry to a particular metallic species. Nevertheless, the mechanism of dimer dissociation, local structure, and atomic dynamics in supercritical gallium trichloride fluids are not known. Using first-principles molecular dynamics, validated by comparison with our high-energy X-ray diffraction results, we illustrate the elementary steps in dimer dissociation. These include the formation of intermediate corner-sharing CS-Ga2Cl6 dimers, the partial disproportionation of GaCl3 monomers at high temperatures and low pressures, changes in the local environment of molecular entities, and unusual atomic dynamics in supercritical fluids.

| S-EPMC10976267 | biostudies-literature

A FRET method for investigating dimer/monomer status and conformation of the UVR8 photoreceptor.

Project description:The photoreceptor UVR8 has a pivotal role in mediating plant responses to UV-B wavelengths. Dimeric UVR8 dissociates into monomers following UV-B photoreception, and there is evidence that this process is accompanied by conformational changes that may facilitate interaction of UVR8 with other proteins to initiate signaling. Hence monitoring UVR8 dimer/monomer status and conformation is key to understanding UVR8 action. Here we have used Fluorescence Resonance Energy Transfer (FRET) to study these processes in both wild-type and mutant UVR8 proteins in vivo. UVR8 was fused to GFP and mCherry at the C- and N-termini, respectively and both the FRET efficiency and loss of GFP fluorescence after photobleaching were measured. In addition, measurements were made for UVR8 fused to either GFP or mCherry to eliminate intra-molecular FRET signals. The results indicate that dissociation of UVR8 dimer to monomer principally accounts for the loss of FRET signal for wild-type UVR8 and there is little evidence of a contribution from conformational change in vivo. Examination of plants expressing UVR8W285F and UVR8D96N,D107N are consistent with these mutant proteins being constitutively dimeric and monomeric, respectively. The methods employed here will be valuable for monitoring UVR8 dimer/monomer status in vivo in relation to signaling, and will facilitate characterization of dimer/monomer status and conformation of further UVR8 mutants.

| S-EPMC6374739 | biostudies-literature

Regulation of UVR8 photoreceptor dimer/monomer photo-equilibrium in Arabidopsis plants grown under photoperiodic conditions.

Project description:The UV RESISTANCE LOCUS 8 (UVR8) photoreceptor specifically mediates photomorphogenic responses to UV-B. Photoreception induces dissociation of dimeric UVR8 into monomers to initiate responses. However, the regulation of dimer/monomer status in plants growing under photoperiodic conditions has not been examined. Here we show that UVR8 establishes a dimer/monomer photo-equilibrium in plants growing in diurnal photoperiods in both controlled environments and natural daylight. The photo-equilibrium is determined by the relative rates of photoreception and dark-reversion to the dimer. Experiments with mutants in REPRESSOR OF UV-B PHOTOMORPHOGENESIS 1 (RUP1) and RUP2 show that these proteins are crucial in regulating the photo-equilibrium because they promote reversion to the dimer. In plants growing in daylight, the UVR8 photo-equilibrium is most strongly correlated with low ambient fluence rates of UV-B (up to 1.5 μmol m(-2) s(-1) ), rather than higher fluence rates or the amount of photosynthetically active radiation. In addition, the rate of reversion of monomer to dimer is reduced at lower temperatures, promoting an increase in the relative level of monomer at approximately 8-10 °C. Thus, UVR8 does not behave like a simple UV-B switch under photoperiodic growth conditions but establishes a dimer/monomer photo-equilibrium that is regulated by UV-B and also influenced by temperature.

| S-EPMC5103188 | biostudies-literature

Plant UVR8 photoreceptor senses UV-B by tryptophan-mediated disruption of cross-dimer salt bridges.

Project description:The recently identified plant photoreceptor UVR8 (UV RESISTANCE LOCUS 8) triggers regulatory changes in gene expression in response to ultraviolet-B (UV-B) light through an unknown mechanism. Here, crystallographic and solution structures of the UVR8 homodimer, together with mutagenesis and far-UV circular dichroism spectroscopy, reveal its mechanisms for UV-B perception and signal transduction. ?-propeller subunits form a remarkable, tryptophan-dominated, dimer interface stitched together by a complex salt-bridge network. Salt-bridging arginines flank the excitonically coupled cross-dimer tryptophan "pyramid" responsible for UV-B sensing. Photoreception reversibly disrupts salt bridges, triggering dimer dissociation and signal initiation. Mutation of a single tryptophan to phenylalanine retunes the photoreceptor to detect UV-C wavelengths. Our analyses establish how UVR8 functions as a photoreceptor without a prosthetic chromophore to promote plant development and survival in sunlight.

| S-EPMC3505452 | biostudies-literature

Mechanisms of UV-B light-induced photoreceptor UVR8 nuclear localization dynamics.

Project description:Light regulates the subcellular localization of plant photoreceptors, a key step in light signaling. Ultraviolet-B radiation (UV-B) induces the plant photoreceptor UV RESISTANCE LOCUS 8 (UVR8) nuclear accumulation, where it regulates photomorphogenesis. However, the molecular mechanism for the UV-B-regulated UVR8 nuclear localization dynamics is unknown. With fluorescence recovery after photobleaching (FRAP), cell fractionation followed by immunoblotting and co-immunoprecipitation (Co-IP) assays we tested the function of UVR8-interacting proteins including CONSTITUTIVELY PHOTOMORPHOGENIC 1 (COP1), REPRESSOR OF UV-B PHOTOMORPHOGENESIS 1 (RUP1) and RUP2 in the regulation of UVR8 nuclear dynamics in Arabidopsis thaliana. We showed that UV-B-induced rapid UVR8 nuclear translocation is independent of COP1, which previously was shown to be required for UV-B-induced UVR8 nuclear accumulation. Instead, we provide evidence that the UV-B-induced UVR8 homodimer-to-monomer photo-switch and the concurrent size reduction of UVR8 enables its monomer nuclear translocation, most likely via free diffusion. Nuclear COP1 interacts with UV-B-activated UVR8 monomer, thereby promoting UVR8 nuclear retention. Conversely, RUP1and RUP2, whose expressions are induced by UV-B, inhibit UVR8 nuclear retention via attenuating the UVR8-COP1 interaction, allowing UVR8 to exit the nucleus. Collectively, our data suggest that UV-B-induced monomerization of UVR8 promotes its nuclear translocation via free diffusion. In the nucleus, COP1 binding promotes UVR8 monomer nuclear retention, which is counterbalanced by the major negative regulators RUP1 and RUP2.

| S-EPMC9825989 | biostudies-literature

Dimer/monomer status and in vivo function of salt-bridge mutants of the plant UV-B photoreceptor UVR8.

Project description:UV RESISTANCE LOCUS8 (UVR8) is a photoreceptor for ultraviolet-B (UV-B) light that initiates photomorphogenic responses in plants. UV-B photoreception causes rapid dissociation of dimeric UVR8 into monomers that interact with CONSTITUTIVELY PHOTOMORPHOGENIC1 (COP1) to initiate signal transduction. Experiments with purified UVR8 show that the dimer is maintained by salt-bridge interactions between specific charged amino acids across the dimer interface. However, little is known about the importance of these charged amino acids in determining dimer/monomer status and UVR8 function in plants. Here we evaluate the use of different methods to examine dimer/monomer status of UVR8 and show that mutations of several salt-bridge amino acids affect dimer/monomer status, interaction with COP1 and photoreceptor function of UVR8 in vivo. In particular, the salt-bridges formed between arginine 286 and aspartates 96 and 107 are key to dimer formation. Mutation of arginine 286 to alanine impairs dimer formation, interaction with COP1 and function in vivo, whereas mutation to lysine gives a weakened dimer that is functional in vivo, indicating the importance of the positive charge of the arginine/lysine residue for dimer formation. Notably, a UVR8 mutant in which aspartates 96 and 107 are conservatively mutated to asparagine is strongly impaired in dimer formation but mediates UV-B responses in vivo with a similar dose-response relationship to wild-type. The UV-B responsiveness of this mutant does not correlate with dimer formation and monomerisation, indicating that monomeric UVR8 has the potential for UV-B photoreception, initiating signal transduction and responses in plants.

| S-EPMC5091643 | biostudies-literature

Constitutively active UVR8 photoreceptor variant in Arabidopsis.

Project description:Arabidopsis thaliana UV RESISTANCE LOCUS 8 (UVR8) is a UV-B photoreceptor that initiates photomorphogenic responses underlying acclimation and UV-B tolerance in plants. UVR8 is a homodimer in its ground state, and UV-B exposure results in its instantaneous monomerization followed by interaction with CONSTITUTIVELY PHOTOMORPHOGENIC 1 (COP1), a major factor in UV-B signaling. UV-B photoreception by UVR8 is based on intrinsic tryptophan aromatic amino acid residues, with tryptophan-285 as the main chromophore. We generated transgenic plants expressing UVR8 with a single amino acid change of tryptophan-285 to alanine. UVR8(W285A) appears monomeric and shows UV-B-independent interaction with COP1. Phenotypically, the plants expressing UVR8(W285A) exhibit constitutive photomorphogenesis associated with constitutive activation of target genes, elevated levels of anthocyanins, and enhanced, acclimation-independent UV-B tolerance. Moreover, we have identified COP1, REPRESSOR OF UV-B PHOTOMORPHOGENESIS 1 and 2 (RUP1 and RUP2), and the SUPPRESSOR OF PHYA-105 (SPA) family as proteins copurifying with UVR8(W285A). Whereas COP1, RUP1, and RUP2 are known to directly interact with UVR8, we show that SPA1 interacts with UVR8 indirectly through COP1. We conclude that UVR8(W285A) is a constitutively active UVR8 photoreceptor variant in Arabidopsis, as is consistent with the crucial importance of monomer formation and COP1 binding for UVR8 activity.

| S-EPMC3864333 | biostudies-literature

How Does Photoreceptor UVR8 Perceive a UV-B Signal?

Project description:UVR8 is the only known plant photoreceptor that mediates light responses to UV-B (280-315 nm) of the solar spectrum. UVR8 perceives a UV-B signal via light-induced dimer dissociation, which triggers a wide range of cellular responses involved in photomorphogenesis and photoprotection. Two recent crystal structures of Arabidopsis thaliana UVR8 (AtUVR8) have revealed unusual clustering of UV-B-absorbing Trp pigments at the dimer interface and provided a structural framework for further mechanistic investigation. This review summarizes recent advances in spectroscopic, computational and crystallographic studies on UVR8 that are directed toward full understanding of UV-B perception at the molecular level.

| S-EPMC4560659 | biostudies-literature

OmicsDI is part of the ELIXIR infrastructure

OmicsDI is an Elixir interoperability service. Learn more ›

Tweets

OmicsDI Databases

PRIDE
PeptideAtlas
MassIVE
JPOST Repository
Physiome Model Repository

EGA
EVA
ENA
LINCS
PAXDB
Cell Collective

MetaboLights
Metabolomics Workbench
MetabolomeExpress
GNPS
BioModels
FAIRDOMHub

ArrayExpress
dbGaP
ExpressionAtlas
GEO
NODE

Information

Databases
Help
API
Contact us
Code on GitHub
Terms of use
Submit Data