PSII heterogeneity; chlorophyll fluorescence; PSIIα; PSIIβ; state transitions; Chlamydomonas reinhardtii
Abstract :
[en] PSII antenna size heterogeneity has been intensively studied in the past. Based on DCMU fluorescence rise kinetics, multiple types of photosystems with different properties were described. However, due to the complexity of fluorescence signal analysis, multiple questions remain unanswered. The number of different types of PSII is still debated as well as their degree of connectivity. In Chlamydomonas reinhardtii we found that PSIIα possesses a high degree of connectivity and an antenna 2-3 times larger than PSIIβ, as described previously. We also found some connectivity for PSIIβ in contrast with the majority of previous studies. This is in agreement with biochemical studies which describe PSII mega-, super- and core- complexes in Chlamydomonas. In these studies, the smallest unit of PSII in vivo would be a dimer of two core complexes hence allowing connectivity. We discuss the possible relationships between PSIIα and PSIIβ and the PSII mega-, super- and core- complexes. We also showed that strain and medium dependent variations in the half-time of the fluorescence rise can be explained by variations in the proportions of PSIIα and PSIIβ. When analyzing the state transition process in vivo, we found that this process induces an inter-conversion of PSIIα and PSIIβ. During a transition from state 2 to state 1, DCMU fluorescence rise kinetics are satisfactorily fitted by considering two PSII populations with constant kinetic parameters. We discuss our findings about PSII heterogeneity during state transitions in relation with recent results on the remodeling of the pigment-protein PSII architecture during this process.
C. Bonaventura, and J. Myers Fluorescence and oxygen evolution from chlorella pyrenoidosa BBA-Bioenergetics 189 1969 366 383
N. Murata Control of excitation transfer in photosynthesis i. light-induced change of chlorophyll a fluoresence in porphyridium cruentum BBA-Bioenergetics 172 1969 242 251
R. Delosme, J. Olive, and F.A. Wollman Changes in light energy distribution upon state transitions: an in vivo photoacoustic study of the wild type and photosynthesis mutants from Chlamydomonas reinhardtii BBA-Bioenergetics 1273 1996 150 158 (Pubitemid 26072614)
A.V. Vener, P.J. Van Kan, P.R. Rich, I. Ohad, and B. Andersson Plastoquinol at the quinol oxidation site of reduced cytochrome bf mediates signal transduction between light and protein phosphorylation: thylakoid protein kinase deactivation by a single-turnover flash PNAS 94 1997 1585 1590
F. Zito, G. Finazzi, R. Delosme, W. Nitschke, D. Picot, and F.-A. Wollman The qo site of cytochrome b6f complexes controls the activation of the LHCII kinase EMBO J. 18 1999 2961 2969 (Pubitemid 29255605)
N. Depege, S. Bellafiore, and J. Rochaix Role of chloroplast protein kinase stt7 in LHCII phosphorylation and state transition in chlamydomonas Science 299 2003 1572 1575 (Pubitemid 36297706)
A. Shapiguzov, B. Ingelsson, I. Samol, C. Andres, F. Kessler, J. Rochaix, A.V. Vener, and M. Goldschmidt-Clermont The PPH1 phosphatase is specifically involved in LHCII dephosphorylation and state transitions in arabidopsis PNAS 107 2010 4782 4787
M. Pribil, P. Pesaresi, A. Hertle, R. Barbato, and D. Leister Role of plastid protein phosphatase TAP38 in LHCII dephosphorylation and thylakoid electron flow PLoS Biol. 8 2010 e1000288
E. Rintamäki, P. Martinsuo, S. Pursiheimo, and E.M. Aro Cooperative regulation of light-harvesting complex II phosphorylation via the plastoquinol and ferredoxin-thioredoxin system in chloroplasts PNAS 97 2000 11644
G. Finazzi, A. Furia, R.P. Barbagallo, and G. Forti State transitions, cyclic and linear electron transport and photophosphorylation in chlamydomonas reinhardtii BBA-Bioenergetics 1413 1999 117 129 (Pubitemid 29507551)
F.A. Wollman State transitions reveal the dynamics and flexibility of the photosynthetic apparatus EMBO J. 20 2001 3623 3630
D.I. Arnon, H.Y. Tsujimoto, and B.D. Mcswain Ferredoxin and photosynthetic phosphorylation Nature 214 1967 562 566
D.I. Arnon, and R.K. Chain Regulation of ferredoxin-catalyzed photosynthetic phosphorylations PNAS 72 1975 4961 4965
P. Joliot, and A. Joliot Cyclic electron transfer in plant leaf PNAS 99 2002 10209 10214 (Pubitemid 34831197)
J.M. Anderson, and A. Melis Localization of different photosystems in separate regions of chloroplast membranes PNAS 80 1983 745
O. Vallon, F. Wollman, and J. Olive Lateral distribution of the main protein complexes of the photosynthetic apparatus in chlamydomonas reinhardtii and in spinach: an immunocytochemical study using intact thylakoid membranes and a psii enriched membrane preparation Photobiochem. Photobiophys. 12 1986 203 220
A. Melis, and P.H. Homann Kinetic analysis of the fluorescence induction in 3-(3,4-dichlorophenyl)-1,1-dimethylurea poisoned chloroplasts Photochem. Photobiol. 21 1975 431 437
P. Joliot, and A. Joliot Etude cinétique de la réaction photochimique libérant de l'oxygène au cours de la photosynthèse CR Acad. Sci. Paris 258 1964 4622 4625
W.W. Doschek, and B. Kok Photon trapping in photosystem II of photosynthesis: the fluorescence rise curve in the presence of 3-(3,4-Dichlorophenyl)-1,1-dimethylurea Biophys. J. 12 1972 832 838
A. Melis, and P.H. Homann Heterogeneity of the photochemical centers in system II of chloroplasts Photochem. Photobiol. 23 1976 343 350
N. Murata, M. Nishimura, and A. Takamiya Fluorescence of chlorophyll in photosynthetic systems II. Induction of fluorescence in isolated spinach chloroplasts BBA - Biophys. Incl. Photosynth. 120 1966 23 33
P. Bennoun, and Y.-s. Li New results on the mode of action of 3,-(3,4-dichlorophenyl)-1,1-dimethylurea in spinach chloroplasts BBA-Bioenergetics 292 1973 162 168
S. Malkin, and B. Kok Fluorescence induction studies in isolated chloroplasts. i. Number of components involved in the reaction and quantum yields BBA 126 1966 413
B. Hsu, and J. Lee A study on the fluorescence induction curve of the DCMU-poisoned chloroplast BBA-Bioenergetics 1056 1991 285 292
B. Hsu, Y. Lee, and Y. Jang A method for analysis of fluorescence induction curve from DCMU-poisoned chloroplasts BBA-Bioenergetics 975 1989 44 49
A. Melis, and J.M. Anderson Structural and functional organization of the photosystems in spinach chloroplasts. Antenna size, relative electron-transport capacity, and chlorophyll composition BBA-Bioenergetics 724 1983 473 484
D. Lazár, P. Tomek, P. Ilik, and J. Nauš Determination of the antenna heterogeneity of photosystem II by direct simultaneous fitting of several fluorescence rise curves measured with DCMU at different light intensities Photosynth. Res. 68 2001 247 257 (Pubitemid 34009601)
J. Sinclair, and S.M. Spence Heterogeneous photosystem 2 activity in isolated spinach chloroplasts Photosynth. Res. 24 1990 209 220
J. Lavergne, and J.-M. Briantais Photosystem II heterogeneity Oxygenic photosynthesis: The light reactions 2004 Springer 265 287
L. Duysens, and H. Sweers Mechanism of two photochemical reactions in algae as studied by means of fluorescence Studies on microalgae and photosynthetic bacteria 1963 353 372
A. Stirbet Chlorophyll a fluorescence induction: a personal perspective of the thermal phase, the j-i-p rise Photosynth. Res. 113 2012 15 61
N. Moise, and I. Moya Correlation between lifetime heterogeneity and kinetics heterogeneity during chlorophyll fluorescence induction in leaves: 1. mono-frequency phase and modulation analysis reveals a conformational change of a PSII pigment complex during the ip thermal phase BBA-Bioenergetics 1657 2004 33 46 (Pubitemid 38823042)
N. Moise, and I. Moya Correlation between lifetime heterogeneity and kinetics heterogeneity during chlorophyll fluorescence induction in leaves: 2. multi-frequency phase and modulation analysis evidences a loosely connected PSII pigment-protein complex BBA-Bioenergetics 1657 2004 47 60 (Pubitemid 38823043)
G. Schansker, S.Z. Tóth, L. Kovács, A.R. Holzwarth, and G. Garab Evidence for a fluorescence yield change driven by a light-induced conformational change within photosystem II during the fast chlorophyll a fluorescence rise BBA-Bioenergetics 1807 2011 1032 1043
A. Melis, and L.N.M. Duysens Biphasic energy conversion kinetics and absorbance difference spectra of photosystem II of chloroplasts. Evidence for two different photosystem II reaction centers Photochem. Photobiol. 29 1979 373 382
J. Lavergne, and F. Rappaport Stabilization of charge separation and photochemical misses in photosystem II Biochemistry-US 37 1998 7899 7906 (Pubitemid 28248651)
P. Joliot, and A. Joliot Evidence for a double hit process in photosystem II based on fluorescence studies BBA-Bioenergetics 462 1977 559 574 (Pubitemid 8242338)
A. Thielen, and H. van Gorkom Quantum efficiency and antenna size of photosystems IIα, IIβ and i in tobacco chloroplasts BBA-Bioenergetics 635 1981 111 120
T.A. Roelofs, C.-H. Lee, and A.R. Holzwarth Global target analysis of picosecond chlorophyll fluorescence kinetics from pea chloroplasts: a new approach to the characterization of the primary processes in photosystem II α- and β-units Biophys. J. 61 1992 1147 1163
U. Schreiber, and K. Pfister Kinetic analysis of the light-induced chlorophyll fluorescence rise curve in the presence of dichlorophenyldimethylurea: dependence of the slow-rise component on the degree of chloroplast intactness BBA-Bioenergetics 680 1982 60 68
M.T. Black, T.H. Brearley, and P. Horton Heterogeneity in chloroplast photosystem II Photosynth. Res. 8 1986 193 207
D.J. Kyle, P. Haworth, and C.J. Arntzen Thylakoid membrane protein phosphorylation leads to a decrease in connectivity between photosystem II reaction centers BBA-Bioenergetics 680 1982 336 342
P. Horton, and M.T. Black Light-dependent quenching of chlorophyll fluorescence in pea chloroplasts induced by adenosine 5′-triphosphate BBA-Bioenergetics 635 1981 53 62
P. Horton, and M.T. Black A comparison between cation and protein phosphorylation effects on the fluorescence induction curve in chloroplasts treated with 3-(3,4-dichlorophenyl)-1,1-dimethylurea BBA-Bioenergetics 722 1983 214 218 (Pubitemid 13165728)
L. Nedbal, M. Trtílek, and D. Kaftan Flash fluorescence induction: a novel method to study regulation of photosystem II J. Photochem. Photobiol. B 48 1999 154 157 (Pubitemid 29195443)
S. Mathur, S. Allakhverdiev, and A. Jajoo Analysis of high temperature stress on the dynamics of antenna size and reducing side heterogeneity of photosystem II in wheat leaves triticum aestivum BBA-Bioenergetics 1807 2011 22 29
N.G. Bukhov, and R. Carpentier Heterogeneity of photosystem II reaction centers as influenced by heat treatment of barley leaves Physiol. Plant. 110 2000 279 285
A. Melis, and G. Akoyunoglou Development of the two heterogeneous photosystem II units in etiolated bean leaves Plant Physiol. 59 1977 1156
X. Barthélemy, R. Popovic, and F. Franck Studies on the o-j-i-p transient of chlorophyll fluorescence in relation to photosystem II assembly and heterogeneity in plastids of greening barley J. Photochem. Photobiol. B 39 1997 213 218 (Pubitemid 27356832)
E.J. Boekema, J.F. van Breemen, H. van Roon, and J.P. Dekker Arrangement of photosystem II supercomplexes in crystalline macrodomains within the thylakoid membrane of green plant chloroplasts J. Mol. Biol. 301 2000 1123 1133
R. Kouřil, J.P. Dekker, and E.J. Boekema Supramolecular organization of photosystem II in green plants Biochim. Biophys. Acta 1817 2012 2 12
J. Nield, K. Redding, and M. Hippler Remodeling of light-harvesting protein complexes in chlamydomonas in response to environmental changes Eukaryot. Cell 3 2004 1370 1380 (Pubitemid 40025096)
M. Iwai, Y. Takahashi, and J. Minagawa Molecular remodeling of photosystem II during state transitions in chlamydomonas reinhardtii Plant Cell 20 2008 2177
J. Minagawa State transitions - the molecular remodeling of photosynthetic supercomplexes that controls energy flow in the chloroplast BBA-Bioenergetics 1807 2011 897 905
D. Kyle, L. Staehelin, and C. Arntzen Lateral mobility of the light-harvesting complex in chloroplast membranes controls excitation energy distribution in higher plants Arch. Biochem. Biophys. 222 1983 527 541
M.T. Black, P. Lee, and P. Horton Changes in topography and function of thylakoid membranes following membrane protein phosphorylation Planta 168 1986 330 336
U.K. Larsson, B. Jergil, and B. Andersson Changes in the lateral distribution of the light-harvesting chlorophyll-a/b - protein complex induced by its phosphorylation Eur. J. Biochem. 136 1983 25 29
H. Takahashi, M. Iwai, Y. Takahashi, and J. Minagawa Identification of the mobile light-harvesting complex II polypeptides for state transitions in chlamydomonas reinhardtii PNAS 103 2006 477 482 (Pubitemid 43122426)
A.V. Ruban, and M.P. Johnson Dynamics of higher plant photosystem cross-section associated with state transitions Photosynth. Res. 99 2008 173 183
R. Tokutsu, M. Iwai, and J. Minagawa CP29, a monomeric light-harvesting complex II protein, is essential for state transitions in chlamydomonas reinhardtii J. Biol. Chem. 284 2009 7777 7782
J. García-Cerdán, L. Kovács, T. Tóth, S. Kereïche, E. Aseeva, E. Boekema, F. Mamedov, C. Funk, and W. Schröder The psbw protein stabilizes the supramolecular organization of photosystem ii in higher plants Plant J. 65 2011 368 381
L. Dietzel, K. Brautigam, S. Steiner, K. Schuffler, B. Lepetit, B. Grimm, M.A. Schottler, and T. Pfannschmidt Photosystem II supercomplex remodeling serves as an entry mechanism for state transitions in arabidopsis Plant Cell 23 2011 2964 2977
M.M. Fleischmann, S. Ravanel, R. Delosme, J. Olive, F. Zito, F.A. Wollman, and J.D. Rochaix Isolation and characterization of photoautotrophic mutants of Chlamydomonas reinhardtii deficient in state transition J. Biol. Chem. 274 1999 30987 30994
D.S. Gorman, and R.P. Levine Cytochrome f and plastocyanin: their sequence in the photosynthetic electron transport chain PNAS 54 1965 1665
D.R. Davies, and A. Plaskitt Genetical and structural analyses of cell-wall formation in chlamydomonas reinhardi Genet. Res. 17 1971 33 43
E.H. Harris The Chlamydomonas Sourcebook: A Comprehensive Guide to Biology and Laboratory Use 1989 Academic Press Inc
Lichtenthaler Chlorophylls and carotenoids: pigment of photosynthetic biomembranes Methods Enzymol. 148 1987 350 382
R.D.C. Team R: A Language and Environment for Statistical Computing, Vienna, Austria 2011 3-900051-07-0
J. Pinheiro, D. Bates, S. DebRoy, D. Sarkar, and R.D.C. Team nlme: Linear and Nonlinear Mixed Effects Models R package version 3.1-102 2011
M.L. Johnson, and L.M. Faunt Parameter estimation by least-squares methods Methods Enzymol. 210 1992 37
D.H. Bell, and M.F. Hipkins Analysis of fluorescence induction curves from pea chloroplasts: Photosystem II reaction centre heterogeneity BBA-Bioenergetics 807 1985 255 262
J. Lavergne, and H. Trissl Theory of fluorescence induction in photosystem II: derivation of analytical expressions in a model including exciton-radical-pair equilibrium and restricted energy transfer between photosynthetic units Biophys. J. 68 1995 2474 2492
H. Trissl, and J. Lavergne Fluorescence induction from photosystem II: analytical equations for the yields of photochemistry and fluorescence derived from analysis of a model including exciton-radical pair equilibrium and restricted energy transfer between photosynthetic units Aust. J. Plant Physiol. 22 1995 183 193
H. Akaike A new look at the statistical model identification IEEE Trans. Autom. Control 19 1974 716 723
K.P. Burnham, and D.R. Anderson Model Selection and Multimodel Inference: A Practical Information-theoretic Approach 2002 Springer
J. Lavaud, B. Rousseau, H.J. Van Gorkom, and A.L. Etienne Influence of the diadinoxanthin pool size on photoprotection in the marine planktonic diatom phaeodactylum tricornutum Plant Physiol. 129 2002 1398 1406 (Pubitemid 34801107)
M. Havaux, and F. Tardy Loss of chlorophyll with limited reduction of photosynthesis as an adaptive response of syrian barley landraces to high-light and heat stress Aust. J. Plant Physiol. 26 1999 569 578 (Pubitemid 129711967)
J.-C. Cadoret, R. Demoulière, J. Lavaud, H.J. van Gorkom, J. Houmard, and A.-L. Etienne Dissipation of excess energy triggered by blue light in cyanobacteria with CP43 isiA BBA-Bioenergetics 1659 2004 100 104 (Pubitemid 39423612)
L. Dall'Osto, C. Lico, J. Alric, G. Giuliano, M. Havaux, and R. Bassi Lutein is needed for efficient chlorophyll triplet quenching in the major LHCII antenna complex of higher plants and effective photoprotection in vivo under strong light BMC Plant Biol. 6 2006 32
J.M. Anderson Photoregulation of the composition, function, and structure of thylakoid membranes Annu. Rev. Plant Physiol. 37 1986 93 136
L. Bulté, P. Gans, F. Rebéillé, and F. Wollman ATP control on state transitions in vivo in chlamydomonas reinhardtii BBA-Bioenergetics 1020 1990 72 80
B. Velthuys, and J. Amesz Charge accumulation at the reducing side of system 2 of photosynthesis BBA-Bioenergetics 333 1974 85 94
L. Bulté, and F. Wollman Stabilization of states I and II by p-benzoquinone treatment of intact cells of chlamydomonas reinhardtii BBA-Bioenergetics 1016 1990 253 258
