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Title: A thylakoid membrane-bound and redox-active rubredoxin (RBD1) functions in de novo assembly and repair of photosystem II

Abstract

Photosystem II (PSII) undergoes frequent photooxidative damage that, if not repaired, impairs photosynthetic activity and growth. How photosynthetic organisms protect vulnerable PSII intermediate complexes during de novo assembly and repair remains poorly understood. Here, we report the genetic and biochemical characterization of chloroplast-located rubredoxin 1 (RBD1), a PSII assembly factor containing a redox-active rubredoxin domain and a single C-terminal transmembrane α-helix (TMH) domain. RBD1 is an integral thylakoid membrane protein that is enriched in stroma lamellae fractions with the rubredoxin domain exposed on the stromal side. RBD1 also interacts with PSII intermediate complexes containing cytochrome b 559. Complementation of the Chlamydomonas reinhardtii(hereafter Chlamydomonas) RBD1-deficient 2pacmutant with constructs encoding RBD1 protein truncations and site-directed mutations demonstrated that the TMH domain is essential for de novo PSII assembly, whereas the rubredoxin domain is involved in PSII repair. The rubredoxin domain exhibits a redox midpoint potential of +114 mV and is proficient in 1-electron transfers to a surrogate cytochrome cin vitro. Reduction of oxidized RBD1 is NADPH dependent and can be mediated by ferredoxin-NADP +reductase (FNR) in vitro. We propose that RBD1 participates, together with the cytochrome b 559, in the protection of PSII intermediate complexes from photooxidative damage during de novo assemblymore » and repair. This role of RBD1 is consistent with its evolutionary conservation among photosynthetic organisms and the fact that it is essential in photosynthetic eukaryotes.« less

Authors:
 [1];  [2];  [3];  [4];  [5]; ORCiD logo [6]
  1. Univ. of California, Berkeley, CA (United States). Howard Hughes Medical Inst., and Dept. of Plant and Microbial Biology
  2. Univ. of California, Berkeley, CA (United States). Dept. of Chemistry
  3. Univ. of California, Berkeley, CA (United States). Dept. of Electron Microscope Laboratory
  4. Ruhr-University Bochum, Bochum (Germany). Molecular Biology of Plant Organelles
  5. Univ. of California, Berkeley, CA (United States). Dept. of Chemistry; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Materials Sciences Division
  6. Univ. of California, Berkeley, CA (United States). Howard Hughes Medical Inst., and Dept. of Plant and Microbial Biology; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Molecular Biophysics and Integrated Bioimaging Division
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1561943
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Volume: 116; Journal Issue: 33; Journal ID: ISSN 0027-8424
Publisher:
National Academy of Sciences, Washington, DC (United States)
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

García-Cerdán, José G., Furst, Ariel L., McDonald, Kent L., Schünemann, Danja, Francis, Matthew B., and Niyogi, Krishna K. A thylakoid membrane-bound and redox-active rubredoxin (RBD1) functions in de novo assembly and repair of photosystem II. United States: N. p., 2019. Web. doi:10.1073/pnas.1903314116.
García-Cerdán, José G., Furst, Ariel L., McDonald, Kent L., Schünemann, Danja, Francis, Matthew B., & Niyogi, Krishna K. A thylakoid membrane-bound and redox-active rubredoxin (RBD1) functions in de novo assembly and repair of photosystem II. United States. doi:10.1073/pnas.1903314116.
García-Cerdán, José G., Furst, Ariel L., McDonald, Kent L., Schünemann, Danja, Francis, Matthew B., and Niyogi, Krishna K. Mon . "A thylakoid membrane-bound and redox-active rubredoxin (RBD1) functions in de novo assembly and repair of photosystem II". United States. doi:10.1073/pnas.1903314116. https://www.osti.gov/servlets/purl/1561943.
@article{osti_1561943,
title = {A thylakoid membrane-bound and redox-active rubredoxin (RBD1) functions in de novo assembly and repair of photosystem II},
author = {García-Cerdán, José G. and Furst, Ariel L. and McDonald, Kent L. and Schünemann, Danja and Francis, Matthew B. and Niyogi, Krishna K.},
abstractNote = {Photosystem II (PSII) undergoes frequent photooxidative damage that, if not repaired, impairs photosynthetic activity and growth. How photosynthetic organisms protect vulnerable PSII intermediate complexes during de novo assembly and repair remains poorly understood. Here, we report the genetic and biochemical characterization of chloroplast-located rubredoxin 1 (RBD1), a PSII assembly factor containing a redox-active rubredoxin domain and a single C-terminal transmembrane α-helix (TMH) domain. RBD1 is an integral thylakoid membrane protein that is enriched in stroma lamellae fractions with the rubredoxin domain exposed on the stromal side. RBD1 also interacts with PSII intermediate complexes containing cytochromeb559. Complementation of theChlamydomonas reinhardtii(hereafterChlamydomonas) RBD1-deficient2pacmutant with constructs encoding RBD1 protein truncations and site-directed mutations demonstrated that the TMH domain is essential for de novo PSII assembly, whereas the rubredoxin domain is involved in PSII repair. The rubredoxin domain exhibits a redox midpoint potential of +114 mV and is proficient in 1-electron transfers to a surrogate cytochromecin vitro. Reduction of oxidized RBD1 is NADPH dependent and can be mediated by ferredoxin-NADP+reductase (FNR) in vitro. We propose that RBD1 participates, together with the cytochromeb559, in the protection of PSII intermediate complexes from photooxidative damage during de novo assembly and repair. This role of RBD1 is consistent with its evolutionary conservation among photosynthetic organisms and the fact that it is essential in photosynthetic eukaryotes.},
doi = {10.1073/pnas.1903314116},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 33,
volume = 116,
place = {United States},
year = {2019},
month = {7}
}

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Works referenced in this record:

Mechanism of photosystem II photoinactivation and D1 protein degradation at low light: The role of back electron flow
journal, February 1997

  • Keren, N.; Berg, A.; van Kan, P. J. M.
  • Proceedings of the National Academy of Sciences, Vol. 94, Issue 4
  • DOI: 10.1073/pnas.94.4.1579

Molecular mechanisms of photodamage in the Photosystem II complex
journal, January 2012


Photosystem II repair in plant chloroplasts — Regulation, assisting proteins and shared components with photosystem II biogenesis
journal, September 2015

  • Järvi, Sari; Suorsa, Marjaana; Aro, Eva-Mari
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1847, Issue 9
  • DOI: 10.1016/j.bbabio.2015.01.006

Rubredoxin: a new electron transfer protein from Clostridium pasteurianum.
journal, July 1965

  • Lovenberg, W.; Sobel, B. E.
  • Proceedings of the National Academy of Sciences, Vol. 54, Issue 1
  • DOI: 10.1073/pnas.54.1.193

Structure of spinach photosystem II–LHCII supercomplex at 3.2 Å resolution
journal, May 2016


Amino acid oxidation of the D1 and D2 proteins by oxygen radicals during photoinhibition of Photosystem II
journal, March 2017

  • Kale, Ravindra; Hebert, Annette E.; Frankel, Laurie K.
  • Proceedings of the National Academy of Sciences, Vol. 114, Issue 11
  • DOI: 10.1073/pnas.1618922114

Electrostatic destabilization of the cytochrome b6f complex in the thylakoid membrane.
journal, October 1991


Photosystem-II damage and repair cycle in chloroplasts: what modulates the rate of photodamage in vivo?
journal, April 1999


Assembly of oxygen-evolving Photosystem II efficiently occurs with the apo-Cyt b 559 but the holo-Cyt b 559 accelerates the recovery of a functional enzyme upon photoinhibition
journal, February 2015

  • Sugiura, Miwa; Nakamura, Makoto; Koyama, Kazumi
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1847, Issue 2
  • DOI: 10.1016/j.bbabio.2014.11.009

Compartmentalization of the protein repair machinery in photosynthetic membranes
journal, October 2014

  • Puthiyaveetil, S.; Tsabari, O.; Lowry, T.
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 44
  • DOI: 10.1073/pnas.1413739111

Removal of both Ycf48 and Psb27 in Synechocystis sp. PCC 6803 disrupts Photosystem II assembly and alters Q A oxidation in the mature complex
journal, August 2014


Investigating the Photoprotective Role of Cytochrome b-559 in Photosystem II in a Mutant with Altered Ligation of the Haem
journal, May 2014

  • Hamilton, Mary L.; Franco, Emanuel; Deák, Zsuzsanna
  • Plant and Cell Physiology, Vol. 55, Issue 7
  • DOI: 10.1093/pcp/pcu070

Photosystem II Assembly: From Cyanobacteria to Plants
journal, April 2013


Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å
journal, April 2011

  • Umena, Yasufumi; Kawakami, Keisuke; Shen, Jian-Ren
  • Nature, Vol. 473, Issue 7345
  • DOI: 10.1038/nature09913

Antisense Inhibition of the PsbX Protein Affects PSII Integrity in the Higher Plant Arabidopsis thaliana
journal, December 2008

  • García-Cerdán, José G.; Sveshnikov, Dmitry; Dewez, David
  • Plant and Cell Physiology, Vol. 50, Issue 2
  • DOI: 10.1093/pcp/pcn188

Characterization of the secondary electron-transfer pathway intermediates of photosystem II containing low-potential cytochrome b 559
journal, September 2008


Synthesis and assembly of thylakoid protein complexes: multiple assembly steps of photosystem II
journal, May 2005

  • Rokka, Anne; Suorsa, Marjaana; Saleem, Ammar
  • Biochemical Journal, Vol. 388, Issue 1
  • DOI: 10.1042/BJ20042098

yellow-in-the-dark Mutants of Chlamydomonas Lack the CHLL Subunit of Light-Independent Protochlorophyllide Reductase
journal, April 2000


Accumulation of the D2 Protein Is a Key Regulatory Step for Assembly of the Photosystem II Reaction Center Complex in Synechocystis PCC 6803
journal, September 2004

  • Komenda, Josef; Reisinger, Veronika; Müller, Bernd Christian
  • Journal of Biological Chemistry, Vol. 279, Issue 47
  • DOI: 10.1074/jbc.M405725200

Photoinhibition of Photosystem II. Inactivation, protein damage and turnover
journal, July 1993

  • Aro, Eva-Mari; Virgin, Ivar; Andersson, Bertil
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1143, Issue 2
  • DOI: 10.1016/0005-2728(93)90134-2

Organization and Topology of Photosystem I Subunits
journal, July 1992

  • Zilber, April L.; Malkin, Richard
  • Plant Physiology, Vol. 99, Issue 3
  • DOI: 10.1104/pp.99.3.901

Structure and assembly mechanism of plant C 2 S 2 M 2 -type PSII-LHCII supercomplex
journal, August 2017


MET1 Is a Thylakoid-Associated TPR Protein Involved in Photosystem II Supercomplex Formation and Repair in Arabidopsis
journal, January 2015

  • Bhuiyan, Nazmul H.; Friso, Giulia; Poliakov, Anton
  • The Plant Cell, Vol. 27, Issue 1
  • DOI: 10.1105/tpc.114.132787

Recent advances in understanding the assembly and repair of photosystem II
journal, March 2010

  • Nixon, Peter J.; Michoux, Franck; Yu, Jianfeng
  • Annals of Botany, Vol. 106, Issue 1
  • DOI: 10.1093/aob/mcq059

Intragenic Enhancers and Suppressors of Phytoene Desaturase Mutations in Chlamydomonas reinhardtii
journal, August 2012


Charge separation in Photosystem II: A comparative and evolutionary overview
journal, January 2012

  • Cardona, Tanai; Sedoud, Arezki; Cox, Nicholas
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1817, Issue 1
  • DOI: 10.1016/j.bbabio.2011.07.012

Chlorophyll fluorescence—a practical guide
journal, April 2000


A Conserved Rubredoxin Is Necessary for Photosystem II Accumulation in Diverse Oxygenic Photoautotrophs
journal, July 2013

  • Calderon, Robert H.; García-Cerdán, José G.; Malnoë, Alizée
  • Journal of Biological Chemistry, Vol. 288, Issue 37
  • DOI: 10.1074/jbc.M113.487629

Eukaryotically Encoded and Chloroplast-located Rubredoxin Is Associated with Photosystem II
journal, June 2000

  • Wastl, Jürgen; Duin, Evert C.; Iuzzolino, Lucia
  • Journal of Biological Chemistry, Vol. 275, Issue 39
  • DOI: 10.1074/jbc.M004629200

Differential Interaction of Maize Root Ferredoxin:NADP + Oxidoreductase with Photosynthetic and Non-Photosynthetic Ferredoxin Isoproteins
journal, July 2000

  • Onda, Yayoi; Matsumura, Tomohiro; Kimata-Ariga, Yoko
  • Plant Physiology, Vol. 123, Issue 3
  • DOI: 10.1104/pp.123.3.1037

An Electrochemical, Kinetic, and Spectroscopic Characterization of [2Fe–2S] Vegetative and Heterocyst Ferredoxins fromAnabaena7120 with Mutations in the Cluster Binding Loop
journal, July 1998

  • Weber-Main, Anne M.; Hurley, John K.; Cheng, Hong
  • Archives of Biochemistry and Biophysics, Vol. 355, Issue 2
  • DOI: 10.1006/abbi.1998.0743

Overexpression and purification of Treponema pallidum rubredoxin; kinetic evidence for a superoxide-mediated electron transfer with the superoxide reductase neelaredoxin
journal, August 2004

  • Auchère, Françoise; Sikkink, Robert; Cordas, Cristina
  • JBIC Journal of Biological Inorganic Chemistry, Vol. 9, Issue 7
  • DOI: 10.1007/s00775-004-0584-6

Mass spectrometry-based cross-linking study shows that the Psb28 protein binds to cytochrome b 559 in Photosystem II
journal, February 2017

  • Weisz, Daniel A.; Liu, Haijun; Zhang, Hao
  • Proceedings of the National Academy of Sciences, Vol. 114, Issue 9
  • DOI: 10.1073/pnas.1620360114

β-Carotene Redox Reactions in Photosystem II:  Electron Transfer Pathway
journal, May 2001

  • Faller, Peter; Pascal, Andy; Rutherford, A. William
  • Biochemistry, Vol. 40, Issue 21
  • DOI: 10.1021/bi0026021

Photosynthetic Water Oxidation in Cytochrome b 559 Mutants Containing a Disrupted Heme-binding Pocket
journal, June 2001

  • Morais, Francisco; Kühn, Kristina; Stewart, David H.
  • Journal of Biological Chemistry, Vol. 276, Issue 34
  • DOI: 10.1074/jbc.M103935200

Optimized native gel systems for separation of thylakoid protein complexes: novel super- and mega-complexes
journal, September 2011

  • Järvi, Sari; Suorsa, Marjaana; Paakkarinen, Virpi
  • Biochemical Journal, Vol. 439, Issue 2
  • DOI: 10.1042/BJ20102155

Location of PsbY in oxygen-evolving photosystem II revealed by mutagenesis and X-ray crystallography
journal, September 2007


A nuclear-encoded protein of prokaryotic origin is essential for the stability of photosystem II in Arabidopsis thaliana
journal, September 1998

  • Meurer, Jörg; Plücken, Henning; Kowallik, Klaus V.
  • The EMBO Journal, Vol. 17, Issue 18
  • DOI: 10.1093/emboj/17.18.5286

Photosystem II, a growing complex: Updates on newly discovered components and low molecular mass proteins
journal, January 2012

  • Shi, Lan-Xin; Hall, Michael; Funk, Christiane
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1817, Issue 1
  • DOI: 10.1016/j.bbabio.2011.08.008

Evidence that D1 Processing Is Required for Manganese Binding and Extrinsic Protein Assembly into Photosystem II
journal, August 2004

  • Roose, Johnna L.; Pakrasi, Himadri B.
  • Journal of Biological Chemistry, Vol. 279, Issue 44
  • DOI: 10.1074/jbc.M408458200

Mitotic Replication of Deoxyribonucleic acid in Chlamydomonas Reinhardi
journal, January 1960

  • Sueoka, N.
  • Proceedings of the National Academy of Sciences, Vol. 46, Issue 1
  • DOI: 10.1073/pnas.46.1.83

Site directed mutagenesis of the heme axial ligands of cytochrome b559 affects the stability of the photosystem II complex.
journal, July 1991


Cytochrome b559 and cyclic electron transfer within photosystem II
journal, January 2012

  • Shinopoulos, Katherine E.; Brudvig, Gary W.
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1817, Issue 1
  • DOI: 10.1016/j.bbabio.2011.08.002

Assembly of the Light-Harvesting Chlorophyll Antenna in the Green Alga Chlamydomonas reinhardtii Requires Expression of the TLA2 - CpFTSY Gene
journal, November 2011

  • Kirst, Henning; García-Cerdán, Jose Gines; Zurbriggen, Andreas
  • Plant Physiology, Vol. 158, Issue 2
  • DOI: 10.1104/pp.111.189910

Structure and Function of Photosystems i and ii
journal, June 2006


Oxidative stress inhibits the repair of photodamage to the photosynthetic machinery
journal, October 2001


Too much light? How β-carotene protects the photosystem II reaction centre
journal, January 2005

  • Telfer, Alison
  • Photochemical & Photobiological Sciences, Vol. 4, Issue 12
  • DOI: 10.1039/b507888c

TLP18.3, a novel thylakoid lumen protein regulating photosystem II repair cycle
journal, August 2007

  • Sirpiö, Sari; Allahverdiyeva, Yagut; Suorsa, Marjaana
  • Biochemical Journal, Vol. 406, Issue 3
  • DOI: 10.1042/BJ20070460

Apicomplexan Parasites Possess Distinct Nuclear-encoded, but Apicoplast-localized, Plant-type Ferredoxin-NADP + Reductase and Ferredoxin
journal, October 2000

  • Vollmer, Michael; Thomsen, Nadine; Wiek, Sabine
  • Journal of Biological Chemistry, Vol. 276, Issue 8
  • DOI: 10.1074/jbc.M009452200

The PsbW protein stabilizes the supramolecular organization of photosystem II in higher plants: PsbW needed for PSII supercomplexes
journal, December 2010


Reversible and irreversible intermediates during photoinhibition of photosystem II: stable reduced QA species promote chlorophyll triplet formation.
journal, February 1992

  • Vass, I.; Styring, S.; Hundal, T.
  • Proceedings of the National Academy of Sciences, Vol. 89, Issue 4
  • DOI: 10.1073/pnas.89.4.1408

Copper regulates cyclic-AMP-dependent lipolysis
journal, June 2016

  • Krishnamoorthy, Lakshmi; Cotruvo, Joseph A.; Chan, Jefferson
  • Nature Chemical Biology, Vol. 12, Issue 8
  • DOI: 10.1038/nchembio.2098

Redox properties of the photosystem II cytochromes b559 and c550 in the cyanobacterium Thermosynechococcus elongatus
journal, January 2003

  • Roncel, Mercedes; Boussac, Alain; Zurita, Jorge L.
  • JBIC Journal of Biological Inorganic Chemistry, Vol. 8, Issue 1
  • DOI: 10.1007/s00775-002-0406-7

Anaerobic Microbes: Oxygen Detoxification Without Superoxide Dismutase
journal, October 1999


Photosystem II: The Reaction Center of Oxygenic Photosynthesis
journal, June 2013


A chloroplast RNA binding protein from stromal thylakoid membranes specifically binds to the 5′ untranslated region of the psbA mRNA: Protein binding to the psbA 5′ UTR
journal, July 2002


Isolation of a photosystem II reaction center consisting of D-1 and D-2 polypeptides and cytochrome b-559
journal, January 1987

  • Nanba, O.; Satoh, K.
  • Proceedings of the National Academy of Sciences, Vol. 84, Issue 1
  • DOI: 10.1073/pnas.84.1.109

TEF30 Interacts with Photosystem II Monomers and Is Involved in the Repair of Photodamaged Photosystem II in Chlamydomonas reinhardtii
journal, December 2015

  • Muranaka, Ligia Segatto; Rütgers, Mark; Bujaldon, Sandrine
  • Plant Physiology, Vol. 170, Issue 2
  • DOI: 10.1104/pp.15.01458

The Chloroplast-encoded α Subunit of Cytochrome b- 559 Is Required for Assembly of the Photosystem Two Complex in both the Light and the Dark in Chlamydomonas reinhardtii
journal, November 1998

  • Morais, Francisco; Barber, James; Nixon, Peter J.
  • Journal of Biological Chemistry, Vol. 273, Issue 45
  • DOI: 10.1074/jbc.273.45.29315