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

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...

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Autores principales: Claesson, Elin, Wahlgren, Weixiao Yuan, Takala, Heikki, Pandey, Suraj, Castillon, Leticia, Kuznetsova, Valentyna, Henry, Léocadie, Panman, Matthijs, Carrillo, Melissa, Kübel, Joachim, Nanekar, Rahul, Isaksson, Linnéa, Nimmrich, Amke, Cellini, Andrea, Morozov, Dmitry, Maj, Michał, Kurttila, Moona, Bosman, Robert, Nango, Eriko, Tanaka, Rie, Tanaka, Tomoyuki, Fangjia, Luo, Iwata, So, Owada, Shigeki, Moffat, Keith, Groenhof, Gerrit, Stojković, Emina A, Ihalainen, Janne A, Schmidt, Marius, Westenhoff, Sebastian
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7164956/
https://www.ncbi.nlm.nih.gov/pubmed/32228856
http://dx.doi.org/10.7554/eLife.53514
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author Claesson, Elin
Wahlgren, Weixiao Yuan
Takala, Heikki
Pandey, Suraj
Castillon, Leticia
Kuznetsova, Valentyna
Henry, Léocadie
Panman, Matthijs
Carrillo, Melissa
Kübel, Joachim
Nanekar, Rahul
Isaksson, Linnéa
Nimmrich, Amke
Cellini, Andrea
Morozov, Dmitry
Maj, Michał
Kurttila, Moona
Bosman, Robert
Nango, Eriko
Tanaka, Rie
Tanaka, Tomoyuki
Fangjia, Luo
Iwata, So
Owada, Shigeki
Moffat, Keith
Groenhof, Gerrit
Stojković, Emina A
Ihalainen, Janne A
Schmidt, Marius
Westenhoff, Sebastian
author_facet Claesson, Elin
Wahlgren, Weixiao Yuan
Takala, Heikki
Pandey, Suraj
Castillon, Leticia
Kuznetsova, Valentyna
Henry, Léocadie
Panman, Matthijs
Carrillo, Melissa
Kübel, Joachim
Nanekar, Rahul
Isaksson, Linnéa
Nimmrich, Amke
Cellini, Andrea
Morozov, Dmitry
Maj, Michał
Kurttila, Moona
Bosman, Robert
Nango, Eriko
Tanaka, Rie
Tanaka, Tomoyuki
Fangjia, Luo
Iwata, So
Owada, Shigeki
Moffat, Keith
Groenhof, Gerrit
Stojković, Emina A
Ihalainen, Janne A
Schmidt, Marius
Westenhoff, Sebastian
author_sort Claesson, Elin
collection PubMed
description 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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spelling pubmed-71649562020-04-20 The primary structural photoresponse of phytochrome proteins captured by a femtosecond X-ray laser Claesson, Elin Wahlgren, Weixiao Yuan Takala, Heikki Pandey, Suraj Castillon, Leticia Kuznetsova, Valentyna Henry, Léocadie Panman, Matthijs Carrillo, Melissa Kübel, Joachim Nanekar, Rahul Isaksson, Linnéa Nimmrich, Amke Cellini, Andrea Morozov, Dmitry Maj, Michał Kurttila, Moona Bosman, Robert Nango, Eriko Tanaka, Rie Tanaka, Tomoyuki Fangjia, Luo Iwata, So Owada, Shigeki Moffat, Keith Groenhof, Gerrit Stojković, Emina A Ihalainen, Janne A Schmidt, Marius Westenhoff, Sebastian eLife Structural Biology and Molecular Biophysics 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. eLife Sciences Publications, Ltd 2020-03-31 /pmc/articles/PMC7164956/ /pubmed/32228856 http://dx.doi.org/10.7554/eLife.53514 Text en © 2020, Claesson et al http://creativecommons.org/licenses/by/4.0/ http://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Structural Biology and Molecular Biophysics
Claesson, Elin
Wahlgren, Weixiao Yuan
Takala, Heikki
Pandey, Suraj
Castillon, Leticia
Kuznetsova, Valentyna
Henry, Léocadie
Panman, Matthijs
Carrillo, Melissa
Kübel, Joachim
Nanekar, Rahul
Isaksson, Linnéa
Nimmrich, Amke
Cellini, Andrea
Morozov, Dmitry
Maj, Michał
Kurttila, Moona
Bosman, Robert
Nango, Eriko
Tanaka, Rie
Tanaka, Tomoyuki
Fangjia, Luo
Iwata, So
Owada, Shigeki
Moffat, Keith
Groenhof, Gerrit
Stojković, Emina A
Ihalainen, Janne A
Schmidt, Marius
Westenhoff, Sebastian
The primary structural photoresponse of phytochrome proteins captured by a femtosecond X-ray laser
title The primary structural photoresponse of phytochrome proteins captured by a femtosecond X-ray laser
title_full The primary structural photoresponse of phytochrome proteins captured by a femtosecond X-ray laser
title_fullStr The primary structural photoresponse of phytochrome proteins captured by a femtosecond X-ray laser
title_full_unstemmed The primary structural photoresponse of phytochrome proteins captured by a femtosecond X-ray laser
title_short The primary structural photoresponse of phytochrome proteins captured by a femtosecond X-ray laser
title_sort primary structural photoresponse of phytochrome proteins captured by a femtosecond x-ray laser
topic Structural Biology and Molecular Biophysics
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7164956/
https://www.ncbi.nlm.nih.gov/pubmed/32228856
http://dx.doi.org/10.7554/eLife.53514
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