The primary structural photoresponse of phytochrome proteins captured by a femtosecond X-ray laser
- University of Gothenburg, Sweden
- University of Jyvaskyla, Finland
- University of Wisconsin-Milwaukee, United States
- Northeastern Illinois University, United States
- Kyoto University, Japan
- University of Chicago, United States
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 signalling 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.
Data availability
Crystallography data have been submitted to protein data bank (PDB)dark:ID: D_1292104678 and PDB ID: 6T3L1ps:ID: D_1292104679 and PDB ID: 6T3URaw diffraction images are in the process of being uploaded to CXIDB
Article and author information
Author details
Sebastian Westenhoff
Funding
European Research Council (279944)
- Sebastian Westenhoff
Academy of Finland (285461)
- Sebastian Westenhoff
Academy of Finland (296135)
- Sebastian Westenhoff
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Werner Kühlbrandt, Max Planck Institute of Biophysics, Germany
Version history
- Received: November 11, 2019
- Accepted: March 13, 2020
- Accepted Manuscript published: March 31, 2020 (version 1)
- Version of Record published: April 17, 2020 (version 2)
Copyright
© 2020, Claesson et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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The primary structural photoresponse of phytochrome proteins captured by a femtosecond X-ray laser
eLife 9:e53514.
https://doi.org/10.7554/eLife.53514
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