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Title: An evolutionarily conserved iron-sulfur cluster underlies redox sensory function of the Chloroplast Sensor Kinase

Abstract

Photosynthetic efficiency depends on equal light energy conversion by two spectrally distinct, serially-connected photosystems. The redox state of the plastoquinone pool, located between the two photosystems, is a key regulatory signal that initiates acclimatory changes in the relative abundance of photosystems. The Chloroplast Sensor Kinase (CSK) links the plastoquinone redox signal with photosystem gene expression but the mechanism by which it monitors the plastoquinone redox state is unclear. Here we show that the purified Arabidopsis and Phaeodactylum CSK and the cyanobacterial CSK homologue, Histidine kinase 2 (Hik2), are iron-sulfur proteins. The Fe-S cluster of CSK is further revealed to be a high potential redox-responsive [3Fe-4S] center. CSK responds to redox agents with reduced plastoquinone suppressing its autokinase activity. Redox changes within the CSK iron-sulfur cluster translate into conformational changes in the protein fold. These results provide key insights into redox signal perception and propagation by the CSK-based chloroplast two-component system.

Authors:
ORCiD logo [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1];  [1]; ORCiD logo [1]
  1. Purdue Univ., West Lafayette, IN (United States)
Publication Date:
Research Org.:
Argonne National Lab. (ANL), Argonne, IL (United States). Advanced Photon Source (APS); Purdue Univ., West Lafayette, IN (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES); Showalter Trust; National Science Foundation (NSF); Canadian Light Source
OSTI Identifier:
1624537
Grant/Contract Number:  
AC02-06CH11357; SC0018238; CHE-1900476
Resource Type:
Accepted Manuscript
Journal Name:
Communications Biology
Additional Journal Information:
Journal Volume: 3; Journal Issue: 1; Journal ID: ISSN 2399-3642
Publisher:
Springer Nature
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; life sciences & biomedicine - other topics; science & technology - other topics; C3 photosynthesis; light responses

Citation Formats

Ibrahim, Iskander M., Wu, Huan, Ezhov, Roman, Kayanja, Gilbert E., Zakharov, Stanislav D., Du, Yanyan, Tao, Weiguo Andy, Pushkar, Yulia, Cramer, William A., and Puthiyaveetil, Sujith. An evolutionarily conserved iron-sulfur cluster underlies redox sensory function of the Chloroplast Sensor Kinase. United States: N. p., 2020. Web. https://doi.org/10.1038/s42003-019-0728-4.
Ibrahim, Iskander M., Wu, Huan, Ezhov, Roman, Kayanja, Gilbert E., Zakharov, Stanislav D., Du, Yanyan, Tao, Weiguo Andy, Pushkar, Yulia, Cramer, William A., & Puthiyaveetil, Sujith. An evolutionarily conserved iron-sulfur cluster underlies redox sensory function of the Chloroplast Sensor Kinase. United States. https://doi.org/10.1038/s42003-019-0728-4
Ibrahim, Iskander M., Wu, Huan, Ezhov, Roman, Kayanja, Gilbert E., Zakharov, Stanislav D., Du, Yanyan, Tao, Weiguo Andy, Pushkar, Yulia, Cramer, William A., and Puthiyaveetil, Sujith. Wed . "An evolutionarily conserved iron-sulfur cluster underlies redox sensory function of the Chloroplast Sensor Kinase". United States. https://doi.org/10.1038/s42003-019-0728-4. https://www.osti.gov/servlets/purl/1624537.
@article{osti_1624537,
title = {An evolutionarily conserved iron-sulfur cluster underlies redox sensory function of the Chloroplast Sensor Kinase},
author = {Ibrahim, Iskander M. and Wu, Huan and Ezhov, Roman and Kayanja, Gilbert E. and Zakharov, Stanislav D. and Du, Yanyan and Tao, Weiguo Andy and Pushkar, Yulia and Cramer, William A. and Puthiyaveetil, Sujith},
abstractNote = {Photosynthetic efficiency depends on equal light energy conversion by two spectrally distinct, serially-connected photosystems. The redox state of the plastoquinone pool, located between the two photosystems, is a key regulatory signal that initiates acclimatory changes in the relative abundance of photosystems. The Chloroplast Sensor Kinase (CSK) links the plastoquinone redox signal with photosystem gene expression but the mechanism by which it monitors the plastoquinone redox state is unclear. Here we show that the purified Arabidopsis and Phaeodactylum CSK and the cyanobacterial CSK homologue, Histidine kinase 2 (Hik2), are iron-sulfur proteins. The Fe-S cluster of CSK is further revealed to be a high potential redox-responsive [3Fe-4S] center. CSK responds to redox agents with reduced plastoquinone suppressing its autokinase activity. Redox changes within the CSK iron-sulfur cluster translate into conformational changes in the protein fold. These results provide key insights into redox signal perception and propagation by the CSK-based chloroplast two-component system.},
doi = {10.1038/s42003-019-0728-4},
journal = {Communications Biology},
number = 1,
volume = 3,
place = {United States},
year = {2020},
month = {1}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Figures / Tables:

Fig. 1 Fig. 1: UV-Vis absorbance spectra of cyanobacterial and chloroplast CSK proteins. Coloration of the purified and reconstituted proteins. a On the far-left side is Syn-CSK purified from bacteria, followed by buffer control and the reconstituted CSK proteins. UV-Vis absorbance spectra of b Synechocystis sp. PCC 6803 CSK, c Phaeodactylum tricornutummore » CSK, and d Arabidopsis thaliana CSK. The absorbance spectra of each CSK protein as purified from bacteria before reconstitution (blue) and after reconstitution (red) are shown.« less

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