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:
-
- 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. doi: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}
}
Figures / Tables:

Works referenced in this record:
ATHENA , ARTEMIS , HEPHAESTUS : data analysis for X-ray absorption spectroscopy using IFEFFIT
journal, June 2005
- Ravel, B.; Newville, M.
- Journal of Synchrotron Radiation, Vol. 12, Issue 4
Redox potentials of ubiquinone, menaquinone, phylloquinone, and plastoquinone in aqueous solution
journal, August 2017
- Kishi, Shinnosuke; Saito, Keisuke; Kato, Yuki
- Photosynthesis Research, Vol. 134, Issue 2
Functional, structural, and spectroscopic characterization of a glutathione-ligated [2Fe–2S] cluster in poplar glutaredoxin C1
journal, April 2007
- Rouhier, Nicolas; Unno, Hideaki; Bandyopadhyay, Sibali
- Proceedings of the National Academy of Sciences, Vol. 104, Issue 18
Reconstitution of the [4Fe-4S] cluster in FNR and demonstration of the aerobic-anaerobic transcription switch in vitro
journal, June 1996
- Green, Jeffrey; Bennett, Brian; Jordan, Peter
- Biochemical Journal, Vol. 316, Issue 3
PKS1, a Substrate Phosphorylated by Phytochrome That Modulates Light Signaling in Arabidopsis
journal, May 1999
- Fankhauser, C.
- Science, Vol. 284, Issue 5419
Iron-sulfur stoichiometry and structure of iron-sulfur clusters in three-iron proteins: Evidence for [3Fe-4S] clusters
journal, January 1983
- Beinert, H.; Emptage, M. H.; Dreyer, J. -L.
- Proceedings of the National Academy of Sciences, Vol. 80, Issue 2
Eukaryotic DNA polymerases require an iron-sulfur cluster for the formation of active complexes
journal, November 2011
- Netz, Daili J. A.; Stith, Carrie M.; Stümpfig, Martin
- Nature Chemical Biology, Vol. 8, Issue 1
Spectroscopic studies of ferricyanide oxidation of Azotobacter vinelandii ferredoxin I.
journal, April 1984
- Morgan, T. V.; Stephens, P. J.; Devlin, F.
- Proceedings of the National Academy of Sciences, Vol. 81, Issue 7
Evolutionary rewiring: a modified prokaryotic gene-regulatory pathway in chloroplasts
journal, July 2013
- Puthiyaveetil, Sujith; Ibrahim, Iskander M.; Allen, John F.
- Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 368, Issue 1622
Autophosphorylation Activity of the Arabidopsis Ethylene Receptor Multigene Family
journal, September 2004
- Moussatche, Patricia; Klee, Harry J.
- Journal of Biological Chemistry, Vol. 279, Issue 47
Spin Densities and Spin Coupling in Iron-Sulfur Clusters: A New Analysis of Hyperfine Coupling Constants
journal, August 1995
- Mouesca, J. -M.; Noodleman, L.; Case, D. A.
- Inorganic Chemistry, Vol. 34, Issue 17
Structure, Function, and Formation of Biological Iron-Sulfur Clusters
journal, June 2005
- Johnson, Deborah C.; Dean, Dennis R.; Smith, Archer D.
- Annual Review of Biochemistry, Vol. 74, Issue 1
Protein kinases and phosphatases involved in the acclimation of the photosynthetic apparatus to a changing light environment
journal, December 2012
- Rochaix, Jean-David; Lemeille, Sylvain; Shapiguzov, Alexey
- Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 367, Issue 1608
In-depth Analyses of Kinase-dependent Tyrosine Phosphoproteomes Based on Metal Ion-functionalized Soluble Nanopolymers
journal, June 2010
- Iliuk, Anton B.; Martin, Victoria A.; Alicie, Bethany M.
- Molecular & Cellular Proteomics, Vol. 9, Issue 10
Cleavage of Structural Proteins during the Assembly of the Head of Bacteriophage T4
journal, August 1970
- Laemmli, U. K.
- Nature, Vol. 227, Issue 5259, p. 680-685
Site-Specific Mutational Analysis of a Novel Cysteine Motif Proposed To Ligate the 4Fe-4S Cluster in the Iron-Sulfur Flavoprotein of the Thermophilic MethanoarchaeonMethanosarcina thermophila
journal, October 2000
- Leartsakulpanich, Ubolsree; Antonkine, Mikhail L.; Ferry, James G.
- Journal of Bacteriology, Vol. 182, Issue 19
Pyruvate dehydrogenase kinase from Arabidopsis thaliana: a protein histidine kinase that phosphorylates serine residues
journal, July 2000
- Thelen, Jay J.; Miernyk, Jan A.; Randall, Douglas D.
- Biochemical Journal, Vol. 349, Issue 1
Redox potential of plastoquinone A in spinach chloroplasts
journal, August 1976
- Okayama, Shigeki
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 440, Issue 2
A redox study of the electron transport pathway responsible for generation of the slow electrochromic phase in chloroplasts
journal, October 1984
- Girvin, M. E.; Cramer, W. A.
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 767, Issue 1
Long-Range Electron Tunneling
journal, February 2014
- Winkler, Jay R.; Gray, Harry B.
- Journal of the American Chemical Society, Vol. 136, Issue 8
Inhibition of methylene blue formation during determination of the acid-labile sulfide of iron-sulfur protein samples containing dithionite
journal, May 1977
- Chen, Jiann-Shin; Mortenson, Leonard E.
- Analytical Biochemistry, Vol. 79, Issue 1-2
The ancestral symbiont sensor kinase CSK links photosynthesis with gene expression in chloroplasts
journal, July 2008
- Puthiyaveetil, S.; Kavanagh, T. A.; Cain, P.
- Proceedings of the National Academy of Sciences, Vol. 105, Issue 29
X-ray structure of an asymmetrical trimeric ferredoxin–photosystem I complex
journal, April 2018
- Kubota-Kawai, Hisako; Mutoh, Risa; Shinmura, Kanako
- Nature Plants, Vol. 4, Issue 4
Uncoupler-dependent decrease in midpoint potential of the chloroplast cytochrome b6
journal, November 1973
- Böhme, H.; Cramer, W. A.
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 325, Issue 2
A Redox-Responsive Regulator of Photosynthesis Gene Expression in the Cyanobacterium Synechocystis sp. Strain PCC 6803
journal, August 2000
- Li, Hong; Sherman, Louis A.
- Journal of Bacteriology, Vol. 182, Issue 15
Quinone sensing by the circadian input kinase of the cyanobacterial circadian clock
journal, November 2006
- Ivleva, N. B.; Gao, T.; LiWang, A. C.
- Proceedings of the National Academy of Sciences, Vol. 103, Issue 46, p. 17468-17473
Oxygen control of nif gene expression in Klebsiella pneumoniae depends on NifL reduction at the cytoplasmic membrane by electrons derived from the reduced quinone pool
journal, April 2003
- Grabbe, Roman; Schmitz, Ruth A.
- European Journal of Biochemistry, Vol. 270, Issue 7
Location and mobility of ubiquinones of different chain lengths in artificial membrane vesicles
journal, May 1985
- Ulrich, E. L.; Girvin, M. E.; Cramer, W. A.
- Biochemistry, Vol. 24, Issue 10
Electrochemical Potential and pH Dependences of [3Fe-4S] ↔ [M3Fe-4S] Cluster Transformations (M = Fe, Zn, Co, and Cd) in Ferredoxin III from Desulfovibrio africanus and Detection of a Cluster with M = Pb
journal, October 1997
- Butt, Julea N.; Fawcett, Sarah E. J.; Breton, Jacques
- Journal of the American Chemical Society, Vol. 119, Issue 41
Redox Reactions of the Iron-Sulfur Cluster in a Ribosomal RNA Methyltransferase, RumA: OPTICAL AND EPR STUDIES
journal, June 2004
- Agarwalla, Sanjay; Stroud, Robert M.; Gaffney, Betty J.
- Journal of Biological Chemistry, Vol. 279, Issue 33
Transcriptional Control of Photosynthesis Genes: The Evolutionarily Conserved Regulatory Mechanism in Plastid Genome Function
journal, January 2010
- Puthiyaveetil, Sujith; Ibrahim, Iskander M.; Jeličić, Branka
- Genome Biology and Evolution, Vol. 2
Chloroplast two-component systems: evolution of the link between photosynthesis and gene expression
journal, February 2009
- Puthiyaveetil, Sujith; Allen, John F.
- Proceedings of the Royal Society B: Biological Sciences, Vol. 276, Issue 1665
IscR, an Fe-S cluster-containing transcription factor, represses expression of Escherichia coli genes encoding Fe-S cluster assembly proteins
journal, December 2001
- Schwartz, C. J.; Giel, J. L.; Patschkowski, T.
- Proceedings of the National Academy of Sciences, Vol. 98, Issue 26
Mossbauer studies of beef heart aconitase: evidence for facile interconversions of iron-sulfur clusters.
journal, February 1982
- Kent, T. A.; Dreyer, J. L.; Kennedy, M. C.
- Proceedings of the National Academy of Sciences, Vol. 79, Issue 4
Pyruvate dehydrogenase kinase from Arabidopsis thaliana: a protein histidine kinase that phosphorylates serine residues
journal, June 2000
- Thelen, Jay J.; Miernyk, Jan A.; Randall, Douglas D.
- Biochemical Journal, Vol. 349, Issue 1
Cyanobacterial Two-Component Proteins: Structure, Diversity, Distribution, and Evolution
journal, June 2006
- Ashby, M. K.; Houmard, J.
- Microbiology and Molecular Biology Reviews, Vol. 70, Issue 2
Theoretical approaches to x-ray absorption fine structure
journal, July 2000
- Rehr, J. J.; Albers, R. C.
- Reviews of Modern Physics, Vol. 72, Issue 3
An EPR Investigation of the Products of the Reaction of Cytosolic and Mitochondrial Aconitases with Nitric Oxide
journal, August 1997
- Kennedy, M. Claire; Antholine, William E.; Beinert, Helmut
- Journal of Biological Chemistry, Vol. 272, Issue 33
Novel Redox Chemistry of [3Fe−4S] Clusters: Electrochemical Characterization of the All-Fe(II) Form of the [3Fe−4S] Cluster Generated Reversibly in Various Proteins and Its Spectroscopic Investigation in Sulfolobus acidocaldarius Ferredoxin
journal, January 1996
- Duff, Jillian L. C.; Breton, Jacques L. J.; Butt, Julea N.
- Journal of the American Chemical Society, Vol. 118, Issue 36
Photosynthetic control of chloroplast gene expression
journal, February 1999
- Pfannschmidt, Thomas; Nilsson, Anders; Allen, John F.
- Nature, Vol. 397, Issue 6720
A Large-scale Protein–protein Interaction Analysis in Synechocystis sp. PCC6803
journal, January 2007
- Sato, Shusei; Shimoda, Yoshikazu; Muraki, Akiko
- DNA Research, Vol. 14, Issue 5
Core dimensions in the 3Fe cluster of Desulfovibrio gigas ferredoxin II by extended X-ray absorption fine structure spectroscopy.
journal, June 1982
- Antonio, M. R.; Averill, B. A.; Moura, I.
- Journal of Biological Chemistry, Vol. 257, Issue 12
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