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The primary structural photoresponse of phytochrome proteins captured by a femtosecond X-ray laser

Journal article
Authors Elin Claesson
Weixiao Yuan Wahlgren
H. Takala
S. Pandey
Leticia Castillon
V. Kuznetsova
Léocadie Henry
Matthijs R Panman
M. Carrillo
Joachim Kübel
R. Nanekar
Linnéa Isaksson
Amke Nimmrich
Andrea Cellini
D. Morozov
Michal Maj
M. Kurttila
Robert Bosman
E. Nango
R. Tanaka
T. Tanaka
L. Fangjia
S. Iwata
S. Owada
K. Moffat
G. Groenhof
E. A. Stojkovic
J. A. Ihalainen
M. Schmidt
Sebastian Westenhoff
Published in eLife
Volume 9
ISSN 2050-084X
Publication year 2020
Published at Department of Chemistry and Molecular Biology
Language en
Links dx.doi.org/10.7554/eLife.53514
Keywords crystal-structure, proton-transfer, excited-state, d-ring, crystallography, diffraction, dynamics, isomerization, reveals, Life Sciences & Biomedicine - Other Topics
Subject categories Chemical Sciences

Abstract

Phytochrome proteins control the growth, reproduction, and photosynthesis of plants, fungi, and bacteria. Light is detected by a bilin cofactor, but it remains elusive how this leads to activation of the protein through structural changes. We present serial femtosecond X-ray crystallographic data of the chromophore-binding domains of a bacterial phytochrome at delay times of 1 ps and 10 ps after photoexcitation. The data reveal a twist of the D-ring, which leads to partial detachment of the chromophore from the protein. Unexpectedly, the conserved so-called pyrrole water is photodissociated from the chromophore, concomitant with movement of the A-ring and a key signaling aspartate. The changes are wired together by ultrafast backbone and water movements around the chromophore, channeling them into signal transduction towards the output domains. We suggest that the observed collective changes are important for the phytochrome photoresponse, explaining the earliest steps of how plants, fungi and bacteria sense red light.

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