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Internal conversion of the anionic GFP chromophore: in and out of the I-twisted S(1)/S(0) conical intersection seam

The functional diversity of the green fluorescent protein (GFP) family is intimately connected to the interplay between competing photo-induced transformations of the chromophore motif, anionic p-hydroxybenzylidene-2,3-dimethylimidazolinone (HBDI(−)). Its ability to undergo Z/E-isomerization is of p...

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Autores principales: List, Nanna H., Jones, Chey M., Martínez, Todd J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Royal Society of Chemistry 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8729814/
https://www.ncbi.nlm.nih.gov/pubmed/35126970
http://dx.doi.org/10.1039/d1sc05849e
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author List, Nanna H.
Jones, Chey M.
Martínez, Todd J.
author_facet List, Nanna H.
Jones, Chey M.
Martínez, Todd J.
author_sort List, Nanna H.
collection PubMed
description The functional diversity of the green fluorescent protein (GFP) family is intimately connected to the interplay between competing photo-induced transformations of the chromophore motif, anionic p-hydroxybenzylidene-2,3-dimethylimidazolinone (HBDI(−)). Its ability to undergo Z/E-isomerization is of particular importance for super-resolution microscopy and emerging opportunities in optogenetics. Yet, key dynamical features of the underlying internal conversion process in the native HBDI(−) chromophore remain largely elusive. We investigate the intrinsic excited-state behavior of isolated HBDI(−) to resolve competing decay pathways and map out the factors governing efficiency and the stereochemical outcome of photoisomerization. Based on non-adiabatic dynamics simulations, we demonstrate that non-selective progress along the two bridge-torsional (i.e., phenolate, P, or imidazolinone, I) pathways accounts for the three decay constants reported experimentally, leading to competing ultrafast relaxation primarily along the I-twisted pathway and S(1) trapping along the P-torsion. The majority of the population (∼70%) is transferred to S(0) in the vicinity of two approximately enantiomeric minima on the I-twisted intersection seam (MECI-Is). Despite their sloped, reactant-biased topographies (suggesting low photoproduct yields), we find that decay through these intersections leads to products with a surprisingly high quantum yield of ∼30%. This demonstrates that E-isomer generation results at least in part from direct isomerization on the excited state. A photoisomerization committor analysis reveals a difference in intrinsic photoreactivity of the two MECI-Is and that the observed photoisomerization is the combined result of two effects: early, non-statistical dynamics around the less reactive intersection followed by later, near-statistical behavior around the more reactive MECI-I. Our work offers new insight into internal conversion of HBDI(−) that both establishes the intrinsic properties of the chromophore and enlightens principles for the design of chromophore derivatives and protein variants with improved photoswitching properties.
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spelling pubmed-87298142022-02-04 Internal conversion of the anionic GFP chromophore: in and out of the I-twisted S(1)/S(0) conical intersection seam List, Nanna H. Jones, Chey M. Martínez, Todd J. Chem Sci Chemistry The functional diversity of the green fluorescent protein (GFP) family is intimately connected to the interplay between competing photo-induced transformations of the chromophore motif, anionic p-hydroxybenzylidene-2,3-dimethylimidazolinone (HBDI(−)). Its ability to undergo Z/E-isomerization is of particular importance for super-resolution microscopy and emerging opportunities in optogenetics. Yet, key dynamical features of the underlying internal conversion process in the native HBDI(−) chromophore remain largely elusive. We investigate the intrinsic excited-state behavior of isolated HBDI(−) to resolve competing decay pathways and map out the factors governing efficiency and the stereochemical outcome of photoisomerization. Based on non-adiabatic dynamics simulations, we demonstrate that non-selective progress along the two bridge-torsional (i.e., phenolate, P, or imidazolinone, I) pathways accounts for the three decay constants reported experimentally, leading to competing ultrafast relaxation primarily along the I-twisted pathway and S(1) trapping along the P-torsion. The majority of the population (∼70%) is transferred to S(0) in the vicinity of two approximately enantiomeric minima on the I-twisted intersection seam (MECI-Is). Despite their sloped, reactant-biased topographies (suggesting low photoproduct yields), we find that decay through these intersections leads to products with a surprisingly high quantum yield of ∼30%. This demonstrates that E-isomer generation results at least in part from direct isomerization on the excited state. A photoisomerization committor analysis reveals a difference in intrinsic photoreactivity of the two MECI-Is and that the observed photoisomerization is the combined result of two effects: early, non-statistical dynamics around the less reactive intersection followed by later, near-statistical behavior around the more reactive MECI-I. Our work offers new insight into internal conversion of HBDI(−) that both establishes the intrinsic properties of the chromophore and enlightens principles for the design of chromophore derivatives and protein variants with improved photoswitching properties. The Royal Society of Chemistry 2021-12-08 /pmc/articles/PMC8729814/ /pubmed/35126970 http://dx.doi.org/10.1039/d1sc05849e Text en This journal is © The Royal Society of Chemistry https://creativecommons.org/licenses/by-nc/3.0/
spellingShingle Chemistry
List, Nanna H.
Jones, Chey M.
Martínez, Todd J.
Internal conversion of the anionic GFP chromophore: in and out of the I-twisted S(1)/S(0) conical intersection seam
title Internal conversion of the anionic GFP chromophore: in and out of the I-twisted S(1)/S(0) conical intersection seam
title_full Internal conversion of the anionic GFP chromophore: in and out of the I-twisted S(1)/S(0) conical intersection seam
title_fullStr Internal conversion of the anionic GFP chromophore: in and out of the I-twisted S(1)/S(0) conical intersection seam
title_full_unstemmed Internal conversion of the anionic GFP chromophore: in and out of the I-twisted S(1)/S(0) conical intersection seam
title_short Internal conversion of the anionic GFP chromophore: in and out of the I-twisted S(1)/S(0) conical intersection seam
title_sort internal conversion of the anionic gfp chromophore: in and out of the i-twisted s(1)/s(0) conical intersection seam
topic Chemistry
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8729814/
https://www.ncbi.nlm.nih.gov/pubmed/35126970
http://dx.doi.org/10.1039/d1sc05849e
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