eLife (Mar 2020)
The primary structural photoresponse of phytochrome proteins captured by a femtosecond X-ray laser
- Elin Claesson,
- Weixiao Yuan Wahlgren,
- Heikki Takala,
- Suraj Pandey,
- Leticia Castillon,
- Valentyna Kuznetsova,
- Léocadie Henry,
- Matthijs Panman,
- Melissa Carrillo,
- Joachim Kübel,
- Rahul Nanekar,
- Linnéa Isaksson,
- Amke Nimmrich,
- Andrea Cellini,
- Dmitry Morozov,
- Michał Maj,
- Moona Kurttila,
- Robert Bosman,
- Eriko Nango,
- Rie Tanaka,
- Tomoyuki Tanaka,
- Luo Fangjia,
- So Iwata,
- Shigeki Owada,
- Keith Moffat,
- Gerrit Groenhof,
- Emina A Stojković,
- Janne A Ihalainen,
- Marius Schmidt,
- Sebastian Westenhoff
Affiliations
- Elin Claesson
- Department of Chemistry and Molecular Biology, University of Gothenburg, Gothenburg, Sweden
- Weixiao Yuan Wahlgren
- ORCiD
- Department of Chemistry and Molecular Biology, University of Gothenburg, Gothenburg, Sweden
- Heikki Takala
- ORCiD
- Department of Biological and Environmental Science, Nanoscience Center, University of Jyvaskyla, Jyvaskyla, Finland; Department of Anatomy, Faculty of Medicine, University of Helsinki, Helsinki, Finland
- Suraj Pandey
- Physics Department, University of Wisconsin-Milwaukee, Milwaukee, United States
- Leticia Castillon
- Department of Chemistry and Molecular Biology, University of Gothenburg, Gothenburg, Sweden
- Valentyna Kuznetsova
- Department of Biological and Environmental Science, Nanoscience Center, University of Jyvaskyla, Jyvaskyla, Finland
- Léocadie Henry
- Department of Chemistry and Molecular Biology, University of Gothenburg, Gothenburg, Sweden
- Matthijs Panman
- ORCiD
- Department of Chemistry and Molecular Biology, University of Gothenburg, Gothenburg, Sweden
- Melissa Carrillo
- Department of Biology, Northeastern Illinois University, Chicago, United States
- Joachim Kübel
- Department of Chemistry and Molecular Biology, University of Gothenburg, Gothenburg, Sweden
- Rahul Nanekar
- Department of Biological and Environmental Science, Nanoscience Center, University of Jyvaskyla, Jyvaskyla, Finland
- Linnéa Isaksson
- Department of Chemistry and Molecular Biology, University of Gothenburg, Gothenburg, Sweden
- Amke Nimmrich
- Department of Chemistry and Molecular Biology, University of Gothenburg, Gothenburg, Sweden
- Andrea Cellini
- Department of Chemistry and Molecular Biology, University of Gothenburg, Gothenburg, Sweden
- Dmitry Morozov
- Department of Chemistry, Nanoscience Center, University of Jyvaskyla, Jyvaskyla, Finland
- Michał Maj
- Department of Chemistry and Molecular Biology, University of Gothenburg, Gothenburg, Sweden
- Moona Kurttila
- Department of Biological and Environmental Science, Nanoscience Center, University of Jyvaskyla, Jyvaskyla, Finland
- Robert Bosman
- Department of Chemistry and Molecular Biology, University of Gothenburg, Gothenburg, Sweden
- Eriko Nango
- Department of Cell Biology, Graduate School of Medicine, Kyoto University, Kyoto, Japan; RIKEN SPring-8 Center, Hyogo, Japan
- Rie Tanaka
- Department of Cell Biology, Graduate School of Medicine, Kyoto University, Kyoto, Japan; RIKEN SPring-8 Center, Hyogo, Japan
- Tomoyuki Tanaka
- Department of Cell Biology, Graduate School of Medicine, Kyoto University, Kyoto, Japan; RIKEN SPring-8 Center, Hyogo, Japan
- Luo Fangjia
- Department of Cell Biology, Graduate School of Medicine, Kyoto University, Kyoto, Japan; RIKEN SPring-8 Center, Hyogo, Japan
- So Iwata
- Department of Cell Biology, Graduate School of Medicine, Kyoto University, Kyoto, Japan; RIKEN SPring-8 Center, Hyogo, Japan
- Shigeki Owada
- RIKEN SPring-8 Center, Hyogo, Japan; Japan Synchrotron Radiation Research Institute, Hyogo, Japan
- Keith Moffat
- Department of Biochemistry and Molecular Biology and Institute for Biophysical Dynamics, University of Chicago, Chicago, United States
- Gerrit Groenhof
- Department of Chemistry, Nanoscience Center, University of Jyvaskyla, Jyvaskyla, Finland
- Emina A Stojković
- Department of Biology, Northeastern Illinois University, Chicago, United States
- Janne A Ihalainen
- ORCiD
- Department of Biological and Environmental Science, Nanoscience Center, University of Jyvaskyla, Jyvaskyla, Finland
- Marius Schmidt
- Physics Department, University of Wisconsin-Milwaukee, Milwaukee, United States
- Sebastian Westenhoff
- ORCiD
- Department of Chemistry and Molecular Biology, University of Gothenburg, Gothenburg, Sweden
- DOI
- https://doi.org/10.7554/eLife.53514
- Journal volume & issue
-
Vol. 9
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.
Keywords
