Molecular bioenergetics and photosynthesis
CEA Saclay/Bât. 532
Tél: 01 69 08 29 40
alfred.rutherford@cea.fr
Photosystem II, one of the major chlorophyll-containing proteins of photosynthesis, is the enzyme that photolyses water. Our aims are to understand how it works at a molecular level not only in terms of its catalytic chemistry but also in terms of the multiple mechanisms that the enzyme has developed to protect itself against the reactive oxygen species that it generates.
Human resources
Alain BOUSSAC, Chercheur
Diana KIRILOVSKY, Chercheuse
A.William RUTHERFORD, Group Leader
Anja KRIEGER-LISZKAY, Researcher
Adjélée WILSON, Ingineer
Thanh Lan LAI, Research Technician
Véronique MARY, Technician
Tanai CARDONA LONDONO , Postdoctoral Fellow
Laure MICHELET, Postdoctoral Fellow
Thomas ROACH, Postdoctoral Fellow
Anne Lucie TEILLOUT, Postdoctoral Fellow
Michal GWIZDALA , PhD Student
Denis JALLET , PhD Student
Arezki SEDOUD, PhD Student
Research Programs
 |
Photosynthesis is the biological process used by plants, algae and certain bacteria to convert the light energy into chemical energy. This is by far the most important input of energy into the biosphere as well as being the main energy input for society being the original source of all food, biomass, fossil fuels etc. The electrons necessary for this process are extracted from water by Photosystem II resulting in the release of oxygen gas, while on the opposite side of the protein (and membrane), the electrons are used to reduce quinone. The reduced quinone feed into the next step of the electron transfer chain which leads eventually to fixation carbon dioxide as energy rich carbohydrates. The oxygen blows away rendering the atmosphere aerobic and, in the form of ozone, screening the surface of the planet from UV radiation. This enzyme is the centre of a good deal of interest for researchers who wish to produce artificial catalysts aimed at more efficient fuel production (by water electrolysis and photolysis) and more efficient production of electricity from fuel cells.
Despite the recently published crystallographic structural models, the enzyme mechanism remains poorly defined. Spectroscopic approaches are particularly important for understanding the reaction mechanism not only because they provide chemical details unobtainable by other methods but also because resolved crystal structures for each of the intermediate steps in the enzyme cycle remain a distant prospect. One approach that we have taken in this respect is to attempt to generate the reaction intermediates in the enzyme modified by metal substitution and/or by mutagenesis. A detailed understanding of the reaction mechanism is important for the design of biomimetic catalysts for alternative energy production and efficient energy use.
Light can be a major source of stress for photosynthetic species. PSII is the protein complex that is the most sensitive to photodamage. In strong light PSII itself can generate very reactive species derived from oxygen and thus the enzyme can be responsible for damaging itself. Singlet oxygen is formed by the reversal of the light-driven reactions (recombination of positive and negative charges) but that the the back reaction pathways, and whether they are harmful of not, is determined by the redox potential of the bound quinone cofactor, QA, the latter is modified depending on the functional state of the enzyme.
PSII has developed several different mechanisms to protect itself from oxidative and light stress. One of these mechanisms diminishes the energy arriving at the at the photosynthetic reaction centre by dissipating it as heat. We discovered that in cyanobacteria, a soluble protein that bears a single carotenoid molecule, acts as a photoreceptor and light energy dissipator. These new and unsuspected roles for carotenoid are being studied to understand their molecular mechanism
The approaches used in the lab include molecular biology, biochemistry and biophysics. We work on cyanobacteria algae and plants. The molecular enzymology of the water oxidising enzyme as well as the protective mechanisms represent a key part of the “biomimetic catalysts for alternative energy project” with our colleagues W. Leibl, A. Aukauloo and the University of Orsay.
Key words
Photosynthesis, electron transfer, water photolysis, photosynthetic reaction centre, Photosystem II, antenna, oxidative stress, photoinhibition, photoprotection, regulation of photosynthetic apparatus, spectroscopy, biophysics, molecular biology, biochemistry, oxygen production, manganese, molecular enzymology, chemistry of radical amino acids, water oxidation
Publications
Berera R, van Stokkum I H M, Gwizdala M, Wilson A, Kirilovsky D, van Grondelle R. (2012). The Photophysics of the Orange Carotenoid Protein, a Light-Powered Molecular Switch. J Phys Chem B. 116, 2568-2574.
Cardona T, Sedoud A, Cox N, Rutherford A W. (2012). Charge separation in Photosystem II: A comparative and evolutionary overview. Biochim Biophys Acta-Bioenerg. 1817, 26-43.
Michelet L, Krieger-Liszkay A. (2012). Reactive oxygen intermediates produced by photosynthetic electron transport are enhanced in short-day grown plants. Biochim Biophys Acta - Bioenerg. (Sous Presse).
Nordhues A, Schottler M A, Unger A K, Geimer S, Schonfelder S, Schmollinger S, Rutgers M, Finazzi G, Soppa B, Sommer F, Muhlhaus T, Roach T, Krieger-Liszkay A, Lokstein H, Crespo J L, Schroda M. (2012). Evidence for a Role of VIPP1 in the Structural Organization of the Photosynthetic Apparatus in Chlamydomonas. Plant Cell and Environment. 24, 637-59.
Sugiura M, Ogami S, Kusumi M, Un S, Rappaport F, Boussac A. (2012). Environment of TyrZ in Photosystem II from Thermosynechococcus elongatus in which PsbA2 is the D1 protein. J Biol Chem. 287, 13336-47.
Cox N, Rapatskiy L, Su JH, Pantazis DA, Sugiura M, Kulik L, Dorlet P, Rutherford AW, Neese F, Boussac A, Lubitz W, Messinger J. (2011). Effect of Ca2+/Sr2+ Substitution on the Electronic Structure of the Oxygen-Evolving Complex of Photosystem II: A Combined Multifrequency EPR, 55Mn-ENDOR, and DFT Study of the S2 State. J Am Chem Soc. 133, 3635–3648.
Guerrero F, Sedoud A, Kirilovsky D, Rutherford A W, Ortega j m, Roncel M. (2011). A High Redox Potential Form of Cytochrome c(550) in Photosystem II from Thermosynechococcus elongatus. J Biol Chem. 286, 5985-5994.
Gwizdala M, Wilson A, Kirilovsky D. (2011). In Vitro Reconstitution of the Cyanobacterial Photoprotective Mechanism Mediated by the Orange Carotenoid Protein in Synechocystis PCC 6803. Plant Cell. 23, 2631-2643.
Hannibal L, Somasundaram R, Tejero J, Wilson A, Stuehr D J. (2011). Influence of Heme-Thiolate in Shaping the Catalytic Properties of a Bacterial Nitric-oxide Synthase. J Biol Chem. 286, 39224-39235.
Hernandez-Prieto M A, Tibiletti T, Abasova L, Kirilovsky D, Vass I, Funk C. (2011). The small CAB-like proteins of the cyanobacterium Synechocystis sp PCC 6803: Their involvement in chlorophyll biogenesis for Photosystem II. Biochim Biophys Acta-Bioenerg. 1807, 1143-1151.
Herrero C, Quaranta A, Leibl W, Rutherford A W, Aukauloo A. (2011). Artificial photosynthetic systems. Using light and water to provide electrons and protons for the synthesis of a fuel. Energy Environ Sci. 4, 2353-2365.
Heyno E, Mary V, Schopfer P, Krieger-Liszkay A. (2011). Oxygen activation at the plasma membrane: relation between superoxide and hydroxyl radical production by isolated membranes. Planta. 234, 35-45.
Hideg E, Deak Z, Hakala-Yatkin M, Karonen M, Rutherford A W, Tyystjarvi E, Vass I, Krieger-Liszkay A. (2011). Pure forms of the singlet oxygen sensors TEMP and TEMPD do not inhibit Photosystem II. Biochim Biophys Acta. 1807, 1658-61.
Ido K, Gross C M, Guerrero F, Sedoud A, Lai T L, Ifuku K, Rutherford A W, Krieger-Liszkay A. (2011). High and low potential forms of the Q(A) quinone electron acceptor in Photosystem II of Thermosynechococcus elongatus and spinach. J Photochem Photobiol B-Biol. 104, 154-157.
Keren N, Krieger-Liszkay A. (2011). Photoinhibition: molecular mechanisms and physiological significance. Physiol Plant. 142, 1-5.
Krieger-Liszkay A, Kos P B, Hideg E. (2011). Superoxide anion radicals generated by methylviologen in photosystem I damage photosystem II. Physiol Plant. 142, 17-25.
Rappaport F, Ishida N, Sugiura M, Boussac A. (2011). Ca(2+) determines the entropy changes associated with the formation of transition states during water oxidation by Photosystem II. Energy Environ Sci. 4, 2520-2524.
Sedoud A, Cox N, Sugiura M, Lubitz W, Boussac A, Rutherford A W. (2011). Semiquinone-Iron Complex of Photosystem II: EPR Signals Assigned to the Low-Field Edge of the Ground State Doublet of Q(A)(center dot-)Fe(2+) and Q(B)(center dot-)Fe(2+). Biochemistry. 50, 6012-6021.
Sedoud A, Kastner L, Cox N, El-Alaoui S, Kirilovsky D, Rutherford A W. (2011). Effects of formate binding on the quinone-iron electron acceptor complex of photosystem II. Biochim Biophys Acta-Bioenerg. 1807, 216-226.
Su J H, Cox N, Ames W, Pantazis D A, Rapatskiy L, Lohmiller T, Kulik L V, Dorlet P, Rutherford A W, Neese F, Boussac A, Lubitz W, Messinger J. (2011). The electronic structures of the S-2 states of the oxygen-evolving complexes of photosystem II in plants and cyanobacteria in the presence and absence of methanol. Biochim Biophys Acta-Bioenerg. 107, 829-840.
Tian L J, van Stokkum I H M, Koehorst R B M, Jongerius A, Kirilovsky D, van Amerongen H. (2011). Site, Rate, and Mechanism of Photoprotective Quenching in Cyanobacteria. J Am Chem Soc. 133, 18304-18311.
Wilson A, Punginelli C, Couturier M, Perreau F, Kirilovsky D. (2011). Essential role of two tyrosines and two tryptophans on the photoprotection activity of the Orange Carotenoid Protein. Biochim Biophys Acta. 1807, 293-301.
Bondarava N, Gross C M, Mubarakshina M, Golecki J R, Johnson G N, Krieger-Liszkay A. (2010). Putative function of cytochrome b559 as a plastoquinol oxidase. PHYSIOL PLANTARUM. 138, 463-473.
Boulay C, Wilson A, D'Haene S, Kirilovsky D. (2010). Identification of a protein required for recovery of full antenna capacity in OCP-related photoprotective mechanism in cyanobacteria. Proc Natl Acad Sci U S A. 107, 11620-11625.
Boussac A, Sugiura M, Rappaport F. (2010). Probing the quinone binding site of Photosystem II from Thermosynechococcus elongatus containing either PsbA1 or PsbA3 as the D1 protein through the binding characteristics of herbicides. Biochim Biophys Acta - Bioenerg. (Sous Presse).
Herrero C, Hughes J L, Quaranta A, Cox N, Rutherford A W, Leibl W, Aukauloo A. (2010). Intramolecular light induced activation of a Salen-Mn-III complex by a ruthenium photosensitizer. Chem Commun. 46, 7605-7607.
Hughes J L, Cox N, Rutherford A W, Krausz E, Lai T L, Boussac A, Sugiura M. (2010). D1 protein variants in Photosystem II from Thermosynechococcus elongatus studied by low temperature optical spectroscopy. Biochim Biophys Acta - Bioenergetics. 1797, 11-19.Kirilovsky D. (2010). The photoactive orange carotenoid protein and photoprotection in cyanobacteria. Adv exp Med Biol. 675, 139-159.
Lanquar V, Ramos M S, Lelievre F, Barbier-Brygoo H, Krieger-Liszkay A, Kramer U, Thomine S. (2010). Export of Vacuolar Manganese by AtNRAMP3 and AtNRAMP4 Is Required for Optimal Photosynthesis and Growth under Manganese Deficiency. Plant Physiol. 152, 1986-1999.
Mubarakshina M M, Ivanov B N, Naydov I A, Hillier W, Badger M R, Krieger-Liszkay A. (2010). Production and diffusion of chloroplastic H2O2 and its implication to signalling. J Exp Bot. 61, 3577-3587.
Sugiura M, Harada S, Manabe T, Hayashi H, Kashino Y, Boussac A. (2010). Psb30 contributes to structurally stabilise the Photosystem II complex in the thermophilic cyanobacterium Thermosynechococcus elongatus. Biochim Biophys Acta-Bioenerg. 1797, 1546-1554.
Sugiura M, Iwai E, Hayashi H, Boussac A. (2010). Differences in the Interactions between the Subunits of Photosystem II Dependent on D1 Protein Variants in the Thermophilic Cyanobacterium Thermosynechococcus elongatus. J Biol Chem. 285, 30008-30018.
Sugiura M, Kato Y, Takahashi R, Suzuki H, Watanabe T, Noguchi T, Rappaport F, Boussac A. (2010). Energetics in Photosystem II from Thermosynechococcus elongatus with a D1 protein encoded by either the psbA(1) or psbA(3) gene. Biochim Biophys Acta-Bioenerg. 1797, 1491-1499.
Vittadello M, Gorbunov M Y, Mastrogiovanni D T, Wielunski L S, Garfunkel E L, Guerrero F, Kirilovsky D, Sugiura M, Rutherford A W, Safari A, Falkowski P G. (2010). Photoelectron Generation by Photosystem II Core Complexes Tethered to Gold Surfaces. ChemSusChem. 3, 471-475.
Wilson A, Kinney J N, Zwart P H, Punginelli C, D'Haene S, Perreau F, Klein M G, Kirilovsky D, Kerfeld C A. (2010). Structural Determinants Underlying Photoprotection in the Photoactive Orange Carotenoid Protein of Cyanobacteria. J Biol Chem. 285, 18364-18375.
Yu Q J, Schaub P, Ghisla S, Al-Babili S, Krieger-Liszkay A, Beyer P. (2010). The Lycopene Cyclase CrtY from Pantoea ananatis (Formerly Erwinia uredovora) Catalyzes an FAD(red)-dependent Non-redox Reaction. J Biol Chem. 285, 12109-12120.
Boussac A, Sugiura M, Rutherford AW, Dorlet P. (2009). Complete EPR Spectrum of the S3-State of the Oxygen-Evolving Photosystem II. J Am Chem Soc. 131, 5050-.
Cox N, Hughes JL, Steffen R, Smith PJ, Rutherford AW, Pace RJ, Krausz E. (2009). Identification of the Q(Y) Excitation of the Primary Electron Acceptor of Photosystem II: CD Determination of Its Coupling Environment. J Phys Chem B. 113, 12364-12374.
Muller K, Linkies A, Vreeburg R A M, Fry S C, Krieger-Liszkay A, Leubner-Metzger G. (2009). In Vivo Cell Wall Loosening by Hydroxyl Radicals during Cress Seed Germination and Elongation Growth. Plant Physiol. 150, 1855-1865.
Punginelli C, Wilson A, Routaboul JM, Kirilovsky, D.(2009). Influence of zeaxanthin and echinenone binding on the activity of the Orange Carotenoid Protein. Biochim Biophys Acta-Bioenerg. 1787, 280-288.
Takahashi R, Boussac A, Sugiura M, Noguchi T. (2009). Structural Coupling of a Tyrosine Side Chain with the Non-Heme Iron Center in Photosystem II As Revealed by Light-Induced Fourier Transform Infrared Difference Spectroscopy. Biochemistry. 48, 8994-9001.
Barber J, Rutherford AW. (2008). Revealing how nature uses sunlight to split water. Introduction. Philos Trans R Soc B. 363, 1125–1128.
Boulay C, Abasova L, Six C, Vass I, Kirilovsky D. (2008). Occurrence and function of the orange carotenoid protein in photoprotective mechanisms in various cyanobacteria. Biochim Biophys Acta Bioenergetics. 1777, 1344-1354.
Boussac A, Verbavatz JM, Sugiura M. (2008). Isotopic labelling of Photosystem II in Thermosynechococcus elongatus. Photosynth Res. 98, 285-92.
Boussac A, Sugiura M, Lai TL, Rutherford AW. (2008).Low-temperature photochemistry in photosystem II from Thermosynechococcus elongatus induced by visible and near-infrared light. Philos Trans R Soc Lond B Biol Sci. 363, 1203-10.
Christoforidis KC, Louloudi M, Rutherford AW, Deligiannakis Y. (2008). Semiquinone in molecularly imprinted hybrid amino acid-SiO2 biomimetic materials. An experimental and theoretical study. J Phys Chem B. 112, 12841-12852.
Herrero C, Lassalle-Kaiser B, Leibl W, Rutherford AW, Aukauloo A. (2008). Artificial systems related to light driven electron transfer processes in PSII. Coord Chem Rev. 252, 456-468.
Heyno E, Klose C, Krieger-Liszkay A. (2008). Origin of cadmium-induced reactive oxygen species production: mitochondrial electron transfer versus plasma membrane NADPH oxidase. New Phytol. 179, 687-99.
Hughes JL, Rutherford AW, Sugiura M, Krausz E. (2008). Quantum efficiency distributions of photo-induced side-pathway donor oxidation at cryogenic temperature in photosystem II. Photosynth Res. 98, 199-206.
Krieger-Liszkay A, Fufezan C, Trebst A. (2008). Singlet oxygen production in photosystem II and related protection mechanism Photosynth Res. 98, 551-64.
Ishida N, Sugiura M, Rappaport F, Lai TL, Rutherford AW, Boussac A. (2008). Biosynthetic exchange of bromide for chloride and strontium for calcium in the Photosystem II oxygen-evolving enzyme. J Biol Chem. 283, 13330-40.
Lassalle-Kaiser B, Guillot R, Sainton J, Charlot MF, Aukauloo A. (2008). Proton-mediated redox control in a nickel(II)-bisimidazolate complex: spectroscopic characterisation and density functional analysis. Chemistry. 14, 4307-17.
Murray JW, Maghlaoui K, Kargul J, Ishida N, Lai TL, Rutherford AW, Sugiura M, Boussac A, Barber J. (2008). X-ray crystallography identifies two chloride binding sites in the oxygen evolving centre of Photosystem II. Energy & Environ Sci. 1, 161 - 166.
Pantani O, Naskar S, Guillot R, Millet P, Anxolabehere-Mallart E, Aukauloo A. (2008). Cobalt Clathrochelate Complexes as Hydrogen-Producing Catalysts Angew Chem-Int Edit. 47, 9948-9950
Pushkar Y, Yano J, Sauer K, Boussac A, Yachandra VK. (2008). Structural Changes in the Mn4Ca Cluster and the Mechanism of Photosynthetic Water Splitting. Proc Natl Acad Sci U S A. 105, 1879-1884.
Shao N, Beck CF, Lemaire SD, Krieger-Liszkay A. (2008). Photosynthetic electron flow affects H(2)O (2) signaling by inactivation of catalase in Chlamydomonas reinhardtii. Planta. 228, 1055-66.
Schopfer P, Heyno E, Drepper F, Krieger-Liszkay A. (2008). Naphthoquinone-dependent generation of superoxide radicals by quinone reductase isolated from the plasma membrane of soybean. Plant Physiol. 147, 864-78.
Sugiura M, Boussac A, Noguchi T, Rappaport F. (2008). Influence of Histidine-198 of the D1 subunit on the properties of the primary electron donor, P(680), of photosystem II in Thermosynechococcus elongatus. Biochim Biophys Acta Bioenergetics. 1777, 331-42.
Bondarava N, Un S, Krieger-Liszkay A. (2007). Manganese binding to the 23 kDa etrinsic protein of Photosystem II. Biochim Biophys Acta Bioenergetics. 1767, 583-8.
Ducruet JM, Peeva V, Havaux M. (2007). Chlorophyll thermofluorescence and thermoluminescence as complementary tools for the study of temperature stress in plants Photosynthes Res. 93, 159-71.
Fischer BB, Krieger-Liszkay A, Hideg E, Snyrychová I, Wiesendanger M, Eggen RI. (2007).Role of singlet oxygen in chloroplast to nucleus retrograde signaling in Chlamydomonas reinhardtii. FEBS Lett. 581, 5555-60.
Fufezan C, Gross CM, Sjo Din M, Rutherford AW, Krieger-Liszkay A, Kirilovsky D. (2007). Influence of the redox potential of the primary quinone electron acceptor on photoinhibition in photosystem II. J Biol Chem. 282, 12492-12502.
Junge W, Rutherford AW. (2007).Obituary: Horst Tobias Witt (1922-2007). Nature. 448: 425.
Kargul J, Maghlaoui K, Murray JW, Deak Z, Boussac A, Rutherford AW, Vass I, Barber J. (2007). Purification, crystallization and X-ray diffraction analyses of the T. elongatus PSII core dimer with strontium replacing calcium in the oxygen-evolving complex. Biochim Biophys Acta Bioenergetics. 1767, 404-413.
Kirilovsky D (2007) Photoprotection in cyanobacteria : The Orange Carotenoid Protein (OCP)-related-No-Photochemical-Quenching mechanism. Photosynth. Res. 93, 7-16.
Picciocchi A, Saguez C, Boussac A, Cassier-Chauvat C, Chauvat F. (2007).CGFS-Type Monothiol Glutaredoxins from the Cyanobacterium Synechocystis PCC6803 and Other Evolutionary Distant Model Organisms Possess a Glutathione-Ligated [2Fe-2S] Cluster. Biochemistry. 46:15018-26.
Roncel M, Yruela I, Kirilovsky D, Guerrero F, Alfonso M, Picores R, Ortega J.M. (2007) Changes in photosynthetic electrón transfer and state-transitions in an herbicide-resistant D1 mutant from soybean cell cultures. Biochim. Biophys. Acta 1767, 694-702.
Shao N, Krieger-Liszkay A, Schroda M, Beck CF. (2007).A reporter system for the individual detection of hydrogen peroxide and singlet oxygen: its use for the assay of reactive oxygen species produced in vivo. Plant J. 50: 475-87.
Un S, Boussac A, Sugiura M. (2007). Characterization of the Tyrosine-Z Radical and Its Environment in the Spin-Coupled S(2)Tyr(Z)(*) State of Photosystem II from Thermosynechococcus elongatus. Biochemistry. 46, 3138-3150.
Wilson A, Boulay C, Wilde A, Kerfeld CA, Kirilovsky D. (2007). Light-Induced Energy Dissipation in Iron-Starved Cyanobacteria: Roles of OCP and IsiA Proteins. Plant Cell. 19, 656-672.
Balland V, Bouzhir-Sima L, Anxolabehere-Mallart E, Boussac A, Vos MH, Liebl U, Mattioli TA. (2006). Functional Implications of the Propionate 7-Arginine 220 Interaction in the FixLH Oxygen Sensor from Bradyrhizobium japonicum. Biochemistry. 45, 2072-2084.
Hillier W, McConnell I, Badger MR, Boussac A, Klimov VV, Dismukes GC, Wydrzynski T. (2006). Quantitative Assessment of Intrinsic Carbonic Anhydrase Activity and the Capacity for Bicarbonate Oxidation in Photosystem II. Biochemistry. 45, 2094-2102.
Krieger-Liszkay A, Trebst A. (2006). Tocopherol is the scavenger of singlet oxygen produced by the triplet states of chlorophyll in the PSII reaction centre. J Exp Bot. 57, 1677-1684.
Marboutin L, Boussac A, Berthomieu C. (2006). Redox infrared markers of the heme and axial ligands in microperoxidase: bases for the analysis of c-type cytochromes. J Biol Inorg Chem. 11, 811-823.
Suzuki H, Taguchi Y, Sugiura M, Boussac A, Noguchi T. (2006). Structural Perturbation of the Carboxylate Ligands to the Manganese Cluster upon Ca(2+)/Sr(2+) Exchange in the S-State Cycle of Photosynthetic Oxygen Evolution As Studied by Flash-Induced FTIR Difference Spectroscopy. Biochemistry. 45, 13454-13464.
Wilson A, Ajlani G, Verbavatz JM, Vass I, Kerfeld CA, Kirilovsky D. (2006). A Soluble Carotenoid Protein Involved in Phycobilisome-Related Energy Dissipation in Cyanobacteria Plant Cell. 18, 992-1007.
Boussac A, Sugiura M, Kirilovsky D, Rutherford AW. (2005). Near-Infrared-Induced Transitions in the Manganese Cluster of Photosystem II: Action Spectra for the S2 and S3 Redox States. Plant Cell Physiol. 46, 837-842.
Charlot MF, Boussac A, Blondin G. (2005). Towards a spin coupling model for the Mn(4) cluster in Photosystem II. Biochim Biophys Acta Bioenergetics. 1708, 120-132.
Ducruet JM, Roman M, Havaux M, Janda T, Gallais A. (2005). Cyclic electron flow around PSI monitored by afterglow luminescence in leaves of maize inbred lines (Zea mays L.): correlation with chilling tolerance. Planta. 221, 567-579.
Ducruet JM, Roman M, Ortega JM, Janda T. (2005). Role of the oxidized secondary acceptor Q(B) of Photosystem II in the delayed 'afterglow' chlorophyll luminescence. Photosynthes Res. 84, 161-166.
Fufezan C, Drepper F, Juhnke HD, Lancaster CRD, Un S, Rutherford AW, Krieger-Liszkay A. (2005). Herbicide-induced changes in charge recombination and redox potential of Q(A) in the T4 mutant of Blastochloris viridis. Biochemistry. 44, 5931-5939.
Fufezan C, Zhang C, Krieger-Liszkay A, Rutherford AW. (2005). Secondary quinone in photosystem II of Thermosynechococcus elongatus: semiquinone-iron EPR signals and temperature dependence of electron transfer Biochemistry. 44, 12780-12789.
Havaux M, Rumeau D, Ducruet JM. (2005). Probing the FQR and NDH activities involved in cyclic electron transport around Photosystem I by the ‘afterglow’ luminescence Biochim Biophys Acta Bioenergetics. 1709, 203-213.
Boussac A, Rappaport F, Carrier P, Verbavatz JM, Gobin R, Kirilovsky D, Rutherford AW, Sugiura M. (2004). Biosynthetic Ca2+/Sr2+ exchange in the photosystem II oxygen evolving enzyme of Thermosynechococcus elongatus. J Biol Chem. 279, 22809-22819.
Kirilovsky D, Roncel M, Boussac A, Wilson A, Zurita JL, Ducruet JM, Bottin H, Sugiura M, Ortega JM, Rutherford AW. (2004). Cytochrome c550 in the cyanobacterium thermosynechococcus elongatus: Study of redox mutants. J Biol Chem. 279, 52869-52880.
Pospisil P, Arato A, Krieger-Liszkay A, Rutherford AW. (2004). Hydroxyl Radical Generation by Photosystem II. Biochemistry. 43, 6783-6792.
Rutherford AW, Boussac A. (2004). Water photolysis in biology. Science. 303, 1782-1784.
Rutherford AW, Boussac A, Faller P. (2004). The stable tyrosyl radical in Photosystem II: why D? Biochim Biophys Acta Bioenergetics. 1655, 222-230.
Sétif P, Meimberg K, Mühlenhoff U, Boussac A. (2004). Photoaccumulation of two ascorbyl free radicals per photosystem I at 200 K Biochim Biophys Acta Bioenergetics. 1656, 203-213.
Sugiura M, Rappaport F, Brettel K, Noguchi T, Rutherford AW, Boussac A. (2004). Site-Directed Mutagenesis of Thermosynechococcus elongatus Photosystem II: The O(2)-Evolving Enzyme Lacking the Redox-Active Tyrosine D. Biochemistry. 43, 13549-13563.
Zhang C, Boussac A, Rutherford AW. (2004). Low-Temperature Electron Transfer in Photosystem II: A Tyrosyl Radical and Semiquinone Charge Pair. Biochemistry. 43, 13787-13795.
Bondarava N, De Pascalis L, Al-Babili S, Goussias C, Golecki JR, Beyer P, Bock R, Krieger-Liszkay A. (2003). Evidence that cytochrome b559 mediates the oxidation of reduced plastoquinone in the dark. J Biol Chem. 278, 13554-13560.
Ducruet JM. (2003). Chlorophyll thermoluminescence of leaf discs: simple instruments and progress in signal interpretation open the way to new ecophysiological indicators. J Exp Bot. 54, 2419-2430.
Faller P, Goussias C, Rutherford AW, Un S. (2003). Resolving intermediates in biological proton-coupled electron transfer: a tyrosyl radical prior to proton movement. Proc Natl Acad Sci U S A. 100, 8732-8735.
Kerfeld CA, Yoshida S, Tran KT, Yeates TO, Cascio D, Bottin H, Berthomieu C, Sugiura M, Boussac A. (2003). The 1.6 A resolution structure of Fe-superoxide dismutase from the thermophilic cyanobacterium Thermosynechococcus elongatus. J Biol Inorg Chem. 8, 707-714.
Kerfeld CA, Sawaya MR, Bottin H, Tran KT, Sugiura M, Cascio D, Desbois A, Yeates TO, Kirilovsky D, Boussac A. (2003). Structural and EPR characterization of the soluble form of cytochrome c-550 and of the psbV2 gene product from the cyanobacterium Thermosynechococcus elongatus. Plant Cell Physiol. 44, 697-706.
Le Moigne C, Picaud T, Boussac A, Loock B, Momenteau M, Desbois A. (2003). Absorption and Resonance Raman Investigations of Ligand Rotation and Nonplanar Heme Distortion in Bis-Base Low-Spin Iron(II)-Tetrakis(o-pivalamidophenyl)porphyrin Complexes. Inorg Chem. 42, 6081-6088.
Roncel M, Boussac A, Zurita JL, Bottin H, Sugiura M, Kirilovsky D, Ortega JM. (2003). Redox properties of the photosystem II cytochromes b559 and c550 in the cyanobacterium Thermosynechococcus elongatus. J Biol Inorg Chem. 8, 206-216.
Rutherford AW, Faller P. (2003). Photosystem II: evolutionary perspectives Philos Trans R Soc Lond B. 358, 245-253.
Schmidt K, Fufezan C, Krieger-Liszkay A, Satoh H, Paulsen H. (2003). Recombinant water-soluble chlorophyll protein from Brassica oleracea Var. botrys binds various chlorophyll derivatives. Biochemistry. 42, 7427-7433.
Amblard-Gross G, Ferard JF, Carrot F, Bonnin-Mosbah M, Maul S, Ducruet JM, Coddeville P, Beguinel P, Ayrault S. (2002). Biological fluxes conversion and SXRF experiment with a new active biomonitoring tool for atmospheric metals and trace element deposition. Environ Pollut. 120, 47-58.
Deligiannakis Y, Ivancich A, Rutherford AW. (2002). 2D-hyperfine sublevel correlation spectroscopy of tyrosyl radicals. Spectrochim Acta Part A. 58, 1191-1200.
Faller P, Rutherford AW, Debus RJ. (2002). Tyrosine D oxidation at cryogenic temperature in photosystem II. Biochemistry. 41, 12914-12920.
Fufezan C, Rutherford AW, Krieger-Liszkay A. (2002). Singlet oxygen production in herbicide-treated photosystem II. FEBS Lett. 532, 407-410.
Fuhs M, Schnegg A, Prisner T, Kohne I, Hanley J, Rutherford AW, Mobius K. (2002). Orientation selection in photosynthetic PS I multilayers: structural investigation of the charge separated state P (+.)(700) A(1)(-.) by high-field/high-frequency time-resolved EPR at 3.4 T/95 GHz Biochim Biophys Acta Bioenergetics. 1556, 81-88.
Gournis D, Deligiannakis Y, Karakassides MA., Boussac A, Ioannidis N, Petridis D. (2002) Stability study of tyrosinate radical in a restricted phyllomorphous medium. Langmuir 18, 10024-10029.
Goussias C, Boussac A, Rutherford AW. (2002). Photosystem II and photosynthetic oxidation of water: an overview. Philos Trans R Soc Lond B. 357, 1369-1381.
Leu E, Krieger-Liszkay A, Goussias C, Gross EM. (2002). Polyphenolic allelochemicals from the aquatic angiosperm Myriophyllum spicatum inhibit photosystem II. Plant Physiol. 130, 2011-2018.
Schansker G, Goussias C, Petrouleas V, Rutherford AW. (2002). Reduction of the Mn cluster of the water oxidizing enzyme by nitric oxide: formation of an S-2 state. Biochemistry. 41, 3057-3064.