Biological Sciences Division
Published March 31, 2020 | Version v1
Journal article Open

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

Creators

  • 1. University of Gothenburg
  • 2. University of Jyvaskyla
  • 3. University of Wisconsin-Milwaukee
  • 4. Northeastern Illinois University
  • 5. Kyoto University
  • 6. University of Chicago

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.

Notes

Due to the large number of authors, only the first 20 and the University of Chicago authors are included on the above author list. Please download the article for the complete list of authors.

Data availability

Crystallography data have been submitted to protein data bank (PDB) dark:ID: D_1292104678 and PDB ID: 6T3L 1ps:ID: D_1292104679 and PDB ID: 6T3U. Raw diffraction images are deposited under ID 121 at CXIDB.

The following data sets were generated:

Claesson E Wahlgren WY Takala H Pandey S Castillon L Kuznetsova V Henry L Panman M Carrillo M Kübel J Nanekar R Isaksson L Nimmrich A Cellini A Morozov D Maj M Kurttila M Bosman R Nango E Tanaka R Tanaka T Fangjia L Iwata S Owada S Moffat K Groenhof G Stojković E AIhalainen JA Schmidt M Westenhoff S (2020) CXIDB The primary structural photoresponse of phytochrome proteins captured by a femtosecond X-ray laser. https://doi.org/10.11577/1607859

Claesson E Takala H Wahlgren W Pandey S Schmidt M Westenhoff S (2020) RCSB Protein Data Bank ID 6T3L. PAS-GAF fragment from Deinococcus radiodurans phytochrome in dark state. http://www.rcsb.org/structure/6T3L

Claesson E Takala H Wahlgren W Pandey S Schmidt M Westenhoff S (2020) RCSB Protein Data Bank ID 6T3U. PAS-GAF fragment from Deinococcus radiodurans phytochrome 1ps after photoexcitation. http://www.rcsb.org/structure/6T3U

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Additional details

Identifiers

DOI
10.7554/eLife.53514
Other
oai:uchicago.tind.io:10181

Funding

European Research Council
279944
Academy of Finland
285461
Academy of Finland
296135
Jane and Aatos Erkko Foundation
National Science Foundation
NSF-MCB-RUI 141336
National Science Foundation
NSF-MCB-EAGER 183951
Horizon 2020
H2020-INFRAEDI-02-2018-82383
Horizon 2020
H2020-EINFRA-2015-1-67572
National Science Foundation
NSF-1231306

UChicago Information

Division(s)
Biological Sciences Division
Department(s)
Biochemistry and Molecular Biology