Rubredoxin 1 promotes the proper folding of D1 and is not required for heme b559 assembly in Chlamydomonas photosystem II

Calderon, Robert H.; de Vitry, Catherine; Wollman, Francis-André; Niyogi, Krishna K.

doi:10.1016/j.jbc.2023.102968

Rubredoxin 1 promotes the proper folding of D1 and is not required for heme b₅₅₉ assembly in Chlamydomonas photosystem II

Journal Article · Thu Feb 02 00:00:00 EST 2023 · Journal of Biological Chemistry

DOI:https://doi.org/10.1016/j.jbc.2023.102968· OSTI ID:2470927

^[1]; ^[2]; Wollman, Francis-André ^[2]; ^[3]

University of California, Berkeley, CA (United States); Umeå University (Sweden)
Centre National de la Recherche Scientifique and Sorbonne Université, Paris (France)
University of California, Berkeley, CA (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Photosystem II (PSII), the water:plastoquinone oxidoreductase of oxygenic photosynthesis, contains a heme b₅₅₉ iron whose axial ligands are provided by histidine residues from the α (PsbE) and β (PsbF) subunits. PSII assembly depends on accessory proteins that facilitate the step-wise association of its protein and pigment components into a functional complex, a process that is challenging to study due to the low accumulation of assembly intermediates. Here, we examined the putative role of the iron[1Fe-0S]-containing protein rubredoxin 1 (RBD1) as an assembly factor for cytochrome b₅₅₉, using the RBD1-lacking 2pac mutant from Chlamydomonas reinhardtii, in which the accumulation of PSII was rescued by the inactivation of the thylakoid membrane FtsH protease. To this end, we constructed the double mutant 2pac ftsh1-1, which harbored PSII dimers that sustained its photoautotrophic growth. We purified PSII from the 2pac ftsh1-1 background and found that α and β cytochrome b₅₅₉ subunits are still present and coordinate heme b₅₅₉ as in the WT. Interestingly, immunoblot analysis of dark- and low light–grown 2pac ftsh1-1 showed the accumulation of a 23-kDa fragment of the D1 protein, a marker typically associated with structural changes resulting from photodamage of PSII. Its cleavage occurs in the vicinity of a nonheme iron which binds to PSII on its electron acceptor side. Altogether, our findings demonstrate that RBD1 is not required for heme b₅₅₉ assembly and point to a role for RBD1 in promoting the proper folding of D1, possibly via delivery or reduction of the nonheme iron during PSII assembly.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: Agence Nationale de la Recherche; French State; National Institutes of Health (NIH); USDOE

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 2470927

Journal Information:: Journal of Biological Chemistry, Journal Name: Journal of Biological Chemistry Journal Issue: 3 Vol. 299; ISSN 0021-9258

Publisher:: American Society for Biochemistry and Molecular BiologyCopyright Statement

Country of Publication:: United States

Language:: English

References (60)

Partial characterization of the biosynthesis and integration of the Photosystem II reaction centers in the thylakoid membrane of Chlamydomonas reinhardtii Delepelaire, Philippe The EMBO Journal, Vol. 3, Issue 4 https://doi.org/10.1002/j.1460-2075.1984.tb01872.x	journal	April 1984
Identification of a primary in vivo degradation product of the rapidly-turning-over 32 kd protein of photosystem II. Greenberg, B. M.; Gaba, V.; Mattoo, A. K. The EMBO Journal, Vol. 6, Issue 10 https://doi.org/10.1002/j.1460-2075.1987.tb02588.x	journal	October 1987
The assembly of cytochrome b6/f complexes: an approach using genetic transformation of the green alga Chlamydomonas reinhardtii. Kuras, R.; Wollman, F. A. The EMBO Journal, Vol. 13, Issue 5 https://doi.org/10.1002/j.1460-2075.1994.tb06350.x	journal	March 1994
Characterization of photosystem II mutants of Chlamydomonas reinhardii lacking the psbA gene Bennoun, Pierre; Spierer-Herz, Muriel; Erickson, Jeanne Plant Molecular Biology, Vol. 6, Issue 3 https://doi.org/10.1007/BF00021484	journal	January 1986
A new setup for in vivo fluorescence imaging of photosynthetic activity Johnson, Xenie; Vandystadt, Guillaume; Bujaldon, Sandrine Photosynthesis Research, Vol. 102, Issue 1 https://doi.org/10.1007/s11120-009-9487-2	journal	August 2009
Two sites of primary degradation of the D1-protein induced by acceptor or donor side photo-inhibition in photosystem II core complexes De Las Rivas, Javier; Andersson, Bertil; Barber, James FEBS Letters, Vol. 301, Issue 3 https://doi.org/10.1016/0014-5793(92)80250-K	journal	April 1992
Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy Porra, R. J.; Thompson, W. A.; Kriedemann, P. E. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 975, Issue 3 https://doi.org/10.1016/S0005-2728(89)80347-0	journal	August 1989
Chlamydomonas genetics, a tool for the study of bioenergetic pathways Hippler, Michael; Redding, Kevin; Rochaix, Jean-David Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1367, Issue 1-3 https://doi.org/10.1016/S0005-2728(98)00136-4	journal	October 1998
Photosystem II particles from Chlamydomonas reinhardtii. Purification, molecular weight, small subunit composition, and protein phosphorylation. de Vitry, C.; Diner, B. A.; Popo, J. L. Journal of Biological Chemistry, Vol. 266, Issue 25 https://doi.org/10.1016/S0021-9258(18)55345-X	journal	September 1991
Extinction coefficients of cytochromes b559 and c550 of Thermosynechococcus elongatus and Cyt b559/PS II stoichiometry of higher plants Kaminskaya, Olga; Kern, Jan; Shuvalov, Vladimir A. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1708, Issue 3 https://doi.org/10.1016/j.bbabio.2005.05.002	journal	July 2005
On the advantages of using green light to study fluorescence yield changes in leaves Rappaport, Fabrice; Béal, Daniel; Joliot, Anne Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1767, Issue 1 https://doi.org/10.1016/j.bbabio.2006.10.002	journal	January 2007
Role of FtsH2 in the repair of Photosystem II in mutants of the cyanobacterium Synechocystis PCC 6803 with impaired assembly or stability of the CaMn4 cluster Komenda, Josef; Knoppová, Jana; Krynická, Vendula Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1797, Issue 5 https://doi.org/10.1016/j.bbabio.2010.02.006	journal	May 2010
Photodamaged D1 protein is degraded in Arabidopsis mutants lacking the Deg2 protease Huesgen, Pitter F.; Schuhmann, Holger; Adamska, Iwona FEBS Letters, Vol. 580, Issue 30 https://doi.org/10.1016/j.febslet.2006.11.058	journal	December 2006
Assembling and maintaining the Photosystem II complex in chloroplasts and cyanobacteria Komenda, Josef; Sobotka, Roman; Nixon, Peter J. Current Opinion in Plant Biology, Vol. 15, Issue 3 https://doi.org/10.1016/j.pbi.2012.01.017	journal	June 2012
ATR-FTIR Spectroelectrochemical Study on the Mechanism of the pH Dependence of the Redox Potential of the Non-Heme Iron in Photosystem II Kato, Yuki; Watanabe, Hiroki; Noguchi, Takumi Biochemistry, Vol. 60, Issue 27 https://doi.org/10.1021/acs.biochem.1c00341	journal	June 2021
Specific Degradation of the D1 Protein of Photosystem II by Treatment with Hydrogen Peroxide in Darkness: Implications for the Mechanism of Degradation of the D1 Protein under Illumination Miyao, Mitsue; Ikeuchi, Masahiko; Yamamoto, Naoki Biochemistry, Vol. 34, Issue 31 https://doi.org/10.1021/bi00031a025	journal	August 1995
Acceptor side mechanism of photoinduced proteolysis of the D1 protein in photosystem II reaction centers De Las Rivas, Javier; Shipton, Catherine A.; Ponticos, Markella Biochemistry, Vol. 32, Issue 27 https://doi.org/10.1021/bi00078a019	journal	July 1993
Single Molecule Force Spectroscopy Reveals That Iron Is Released from the Active Site of Rubredoxin by a Stochastic Mechanism Zheng, Peng; Takayama, Shin-ichi J.; Mauk, A. Grant Journal of the American Chemical Society, Vol. 135, Issue 21 https://doi.org/10.1021/ja402150q	journal	May 2013
Cleavage of Structural Proteins during the Assembly of the Head of Bacteriophage T4 Laemmli, U. K. Nature, Vol. 227, Issue 5259, p. 680-685 https://doi.org/10.1038/227680a0	journal	August 1970
Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å Umena, Yasufumi; Kawakami, Keisuke; Shen, Jian-Ren Nature, Vol. 473, Issue 7345 https://doi.org/10.1038/nature09913	journal	April 2011
Photosynthetic growth despite a broken Q-cycle Malnoë, Alizée; Wollman, Francis-André; de Vitry, Catherine Nature Communications, Vol. 2, Issue 1 https://doi.org/10.1038/ncomms1299	journal	May 2011
A highly active histidine-tagged Chlamydomonas reinhardtii Photosystem II preparation for structural and biophysical analysis Cullen, Matthew; Ray, Nicola; Husain, Sally Photochemical & Photobiological Sciences, Vol. 6, Issue 11 https://doi.org/10.1039/b708611n	journal	November 2007
Biogenic membranes of the chloroplast in Chlamydomonas reinhardtii Schottkowski, M.; Peters, M.; Zhan, Y. Proceedings of the National Academy of Sciences, Vol. 109, Issue 47 https://doi.org/10.1073/pnas.1209860109	journal	November 2012
A thylakoid membrane-bound and redox-active rubredoxin (RBD1) functions in de novo assembly and repair of photosystem II García-Cerdán, José G.; Furst, Ariel L.; McDonald, Kent L. Proceedings of the National Academy of Sciences, Vol. 116, Issue 33 https://doi.org/10.1073/pnas.1903314116	journal	July 2019
Tocopherol controls D1 amino acid oxidation by oxygen radicals in Photosystem II Kumar, Aditya; Prasad, Ankush; Sedlářová, Michaela Proceedings of the National Academy of Sciences, Vol. 118, Issue 4 https://doi.org/10.1073/pnas.2019246118	journal	January 2021
Mitotic Replication of Deoxyribonucleic acid in Chlamydomonas Reinhardi Sueoka, N. Proceedings of the National Academy of Sciences, Vol. 46, Issue 1 https://doi.org/10.1073/pnas.46.1.83	journal	January 1960
Rubredoxin: a new electron transfer protein from Clostridium pasteurianum. Lovenberg, W.; Sobel, B. E. Proceedings of the National Academy of Sciences, Vol. 54, Issue 1 https://doi.org/10.1073/pnas.54.1.193	journal	July 1965
Cytochrome f and plastocyanin: their sequence in the photosynthetic electron transport chain of Chlamydomonas reinhardi. Gorman, D. S.; Levine, R. P. Proceedings of the National Academy of Sciences, Vol. 54, Issue 6 https://doi.org/10.1073/pnas.54.6.1665	journal	December 1965
Chlorophyll regulates accumulation of the plastid-encoded chlorophyll apoproteins CP43 and D1 by increasing apoprotein stability. Mullet, J. E.; Klein, P. G.; Klein, R. R. Proceedings of the National Academy of Sciences, Vol. 87, Issue 11 https://doi.org/10.1073/pnas.87.11.4038	journal	June 1990
Mechanism of photosystem II photoinactivation and D1 protein degradation at low light: The role of back electron flow Keren, N.; Berg, A.; van Kan, P. J. M. Proceedings of the National Academy of Sciences, Vol. 94, Issue 4 https://doi.org/10.1073/pnas.94.4.1579	journal	February 1997
GTP bound to chloroplast thylakoid membranes is required for light-induced, multienzyme degradation of the photosystem II D1 protein Spetea, Cornelia; Hundal, Torill; Lohmann, Felix Proceedings of the National Academy of Sciences, Vol. 96, Issue 11 https://doi.org/10.1073/pnas.96.11.6547	journal	May 1999
Occupation of the QB-binding Pocket by a Photosystem II Inhibitor Triggers Dark Cleavage of the D1 Protein Subjected to Brief Preillumination Nakajima, Yoshihiro; Yoshida, Shigeo; Inoue, Yorinao Journal of Biological Chemistry, Vol. 271, Issue 29 https://doi.org/10.1074/jbc.271.29.17383	journal	July 1996
Identification, Characterization, and Molecular Cloning of a Homologue of the Bacterial FtsH Protease in Chloroplasts of Higher Plants Lindahl, Marika; Tabak, Sarit; Cseke, Leland Journal of Biological Chemistry, Vol. 271, Issue 46 https://doi.org/10.1074/jbc.271.46.29329	journal	November 1996
Eukaryotically Encoded and Chloroplast-located Rubredoxin Is Associated with Photosystem II Wastl, Jürgen; Duin, Evert C.; Iuzzolino, Lucia Journal of Biological Chemistry, Vol. 275, Issue 39 https://doi.org/10.1074/jbc.M004629200	journal	June 2000
Investigating the Early Stages of Photosystem II Assembly in Synechocystis sp. PCC 6803 : ISOLATION OF CP47 AND CP43 COMPLEXES Boehm, Marko; Romero, Elisabet; Reisinger, Veronika Journal of Biological Chemistry, Vol. 286, Issue 17 https://doi.org/10.1074/jbc.M110.207944	journal	February 2011
A Conserved Rubredoxin Is Necessary for Photosystem II Accumulation in Diverse Oxygenic Photoautotrophs Calderon, Robert H.; García-Cerdán, José G.; Malnoë, Alizée Journal of Biological Chemistry, Vol. 288, Issue 37 https://doi.org/10.1074/jbc.M113.487629	journal	July 2013
An Iron Reservoir to the Catalytic Metal: THE RUBREDOXIN IRON IN AN EXTRADIOL DIOXYGENASE Liu, Fange; Geng, Jiafeng; Gumpper, Ryan H. Journal of Biological Chemistry, Vol. 290, Issue 25 https://doi.org/10.1074/jbc.M115.650259	journal	April 2015
Assembly of Photosystem I: I. INACTIVATION OF THE Shen, Gaozhong; Zhao, Jindong; Reimer, Susan K. Journal of Biological Chemistry, Vol. 277, Issue 23 https://doi.org/10.1074/jbc.M201103200	journal	March 2002
Accumulation of the D2 Protein Is a Key Regulatory Step for Assembly of the Photosystem II Reaction Center Complex in Synechocystis PCC 6803 Komenda, Josef; Reisinger, Veronika; Müller, Bernd Christian Journal of Biological Chemistry, Vol. 279, Issue 47 https://doi.org/10.1074/jbc.M405725200	journal	September 2004
The FtsH Protease slr0228 Is Important for Quality Control of Photosystem II in the Thylakoid Membrane of Synechocystis sp. PCC 6803 Komenda, Josef; Barker, Myles; Kuviková, Stanislava Journal of Biological Chemistry, Vol. 281, Issue 2 https://doi.org/10.1074/jbc.M503852200	journal	November 2005
Posttranslational events leading to the assembly of photosystem II protein complex: a study using photosynthesis mutants from Chlamydomonas reinhardtii de Vitry, C. The Journal of Cell Biology, Vol. 109, Issue 3 https://doi.org/10.1083/jcb.109.3.991	journal	September 1989
Membrane protein damage and repair: removal and replacement of inactivated 32-kilodalton polypeptides in chloroplast membranes Ohad, I. The Journal of Cell Biology, Vol. 99, Issue 2 https://doi.org/10.1083/jcb.99.2.481	journal	August 1984
Recent advances in understanding the assembly and repair of photosystem II Nixon, Peter J.; Michoux, Franck; Yu, Jianfeng Annals of Botany, Vol. 106, Issue 1 https://doi.org/10.1093/aob/mcq059	journal	March 2010
A chloroplast DegP2 protease performs the primary cleavage of the photodamaged D1 protein in plant photosystem II Haubetauhl, K. The EMBO Journal, Vol. 20, Issue 4 https://doi.org/10.1093/emboj/20.4.713	journal	February 2001
Complexome profiling on the Chlamydomonas lpa2 mutant reveals insights into PSII biogenesis and new PSII associated proteins Spaniol, Benjamin; Lang, Julia; Venn, Benedikt Journal of Experimental Botany, Vol. 73, Issue 1 https://doi.org/10.1093/jxb/erab390	journal	August 2021
Assembly of D1/D2 complexes of photosystem II: Binding of pigments and a network of auxiliary proteins Knoppová, Jana; Sobotka, Roman; Yu, Jianfeng Plant Physiology https://doi.org/10.1093/plphys/kiac045	journal	February 2022
The Stromal Chloroplast Deg7 Protease Participates in the Repair of Photosystem II after Photoinhibition in Arabidopsis Sun, Xuwu; Fu, Tingjiao; Chen, Ning Plant Physiology, Vol. 152, Issue 3 https://doi.org/10.1104/pp.109.150722	journal	January 2010
Cooperative D1 Degradation in the Photosystem II Repair Mediated by Chloroplastic Proteases in Arabidopsis Kato, Yusuke; Sun, Xuwu; Zhang, Lixin Plant Physiology, Vol. 159, Issue 4 https://doi.org/10.1104/pp.112.199042	journal	June 2012
The Chlamydomonas deg1c Mutant Accumulates Proteins Involved in High Light Acclimation Theis, Jasmine; Lang, Julia; Spaniol, Benjamin Plant Physiology, Vol. 181, Issue 4 https://doi.org/10.1104/pp.19.01052	journal	October 2019
The Thylakoid Lumen Protease Deg1 Is Involved in the Repair of Photosystem II from Photoinhibition in Arabidopsis Kapri-Pardes, Einat; Naveh, Leah; Adam, Zach The Plant Cell, Vol. 19, Issue 3 https://doi.org/10.1105/tpc.106.046573	journal	March 2007
The Arabidopsis Thylakoid Protein PAM68 Is Required for Efficient D1 Biogenesis and Photosystem II Assembly Armbruster, Ute; Zühlke, Jessica; Rengstl, Birgit The Plant Cell, Vol. 22, Issue 10 https://doi.org/10.1105/tpc.110.077453	journal	October 2010
Thylakoid FtsH Protease Contributes to Photosystem II and Cytochrome b ₆ f Remodeling in Chlamydomonas reinhardtii under Stress Conditions Malnoë, Alizée; Wang, Fei; Girard-Bascou, Jacqueline The Plant Cell, Vol. 26, Issue 1 https://doi.org/10.1105/tpc.113.120113	journal	January 2014
Conditional Depletion of the Chlamydomonas Chloroplast ClpP Protease Activates Nuclear Genes Involved in Autophagy and Plastid Protein Quality Control Ramundo, Silvia; Casero, David; Mühlhaus, Timo The Plant Cell, Vol. 26, Issue 5 https://doi.org/10.1105/tpc.114.124842	journal	May 2014
Systems-Wide Analysis of Acclimation Responses to Long-Term Heat Stress and Recovery in the Photosynthetic Model OrganismChlamydomonas reinhardtii Hemme, Dorothea; Veyel, Daniel; Mühlhaus, Timo The Plant Cell, Vol. 26, Issue 11 https://doi.org/10.1105/tpc.114.130997	journal	November 2014
The Thylakoid FtsH Protease Plays a Role in the Light-Induced Turnover of the Photosystem II D1 Protein Lindahl, Marika; Spetea, Cornelia; Hundal, Torill The Plant Cell, Vol. 12, Issue 3 https://doi.org/10.1105/tpc.12.3.419	journal	March 2000
A Photosynthesis-Specific Rubredoxin-Like Protein Is Required for Efficient Association of the D1 and D2 Proteins during the Initial Steps of Photosystem II Assembly Kiss, Éva; Knoppová, Jana; Aznar, Guillem Pascual The Plant Cell, Vol. 31, Issue 9 https://doi.org/10.1105/tpc.19.00155	journal	July 2019
Photosystem II Assembly: From Cyanobacteria to Plants Nickelsen, Jörg; Rengstl, Birgit Annual Review of Plant Biology, Vol. 64, Issue 1 https://doi.org/10.1146/annurev-arplant-050312-120124	journal	April 2013
The family of Deg/HtrA proteases in plants Schuhmann, Holger; Huesgen, Pitter F.; Adamska, Iwona BMC Plant Biology, Vol. 12, Issue 1 https://doi.org/10.1186/1471-2229-12-52	journal	April 2012
FtsH Protease in the Thylakoid Membrane: Physiological Functions and the Regulation of Protease Activity Kato, Yusuke; Sakamoto, Wataru Frontiers in Plant Science, Vol. 9 https://doi.org/10.3389/fpls.2018.00855	journal	June 2018
Rubredoxin 1 Is Required for Formation of the Functional Photosystem II Core Complex in Arabidopsis thaliana Che, Liping; Meng, Han; Ruan, Junxiang Frontiers in Plant Science, Vol. 13 https://doi.org/10.3389/fpls.2022.824358	journal	February 2022

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37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY
59 BASIC BIOLOGICAL SCIENCES
FtsH
biochemistry & molecular biology
cytochrome
heme
iron
metalloprotein
photosynthesis
photosystem
photosystem II
protease
rubredoxin

Rubredoxin 1 promotes the proper folding of D1 and is not required for heme b559 assembly in Chlamydomonas photosystem II

Citation Formats

References (60)

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Rubredoxin 1 promotes the proper folding of D1 and is not required for heme b₅₅₉ assembly in Chlamydomonas photosystem II