Photosynthetic growth despite a broken Q-cycle

Central in respiration or photosynthesis, the cytochrome bc1 and b6f complexes are regarded as functionally similar quinol oxidoreductases. They both catalyse a redox loop, the Q-cycle, which couples electron and proton transfer. This loop involves a bifurcated electron transfer step considered as being mechanistically mandatory, making the Q-cycle indispensable for growth. Attempts to falsify this paradigm in the case of cytochrome bc1 have failed. The rapid proteolytic degradation of b6f complexes bearing mutations aimed at hindering the Q-cycle has precluded so far the experimental assessment of this model in the photosynthetic chain. Here we combine mutations in Chlamydomonas that inactivate the redox loop but preserve high accumulation levels of b6f complexes. The oxidoreductase activity of these crippled complexes is sufficient to sustain photosynthetic growth, which demonstrates that the Q-cycle is dispensable for oxygenic photosynthesis

Fast and slow responses of Southern Ocean sea surface temperature to SAM in coupled climate models

We investigate how sea surface temperatures (SSTs) around Antarctica respond to the Southern An- nular Mode (SAM) on multiple timescales. To that end we examine the relationship between SAM and SST within unperturbed preindustrial control simulations of coupled general circulation models (GCMs) included in the Climate Modeling Intercomparison Project phase 5 (CMIP5). We develop a technique to extract the re- sponse of the Southern Ocean SST (55◦S−70◦S) to a hypothetical step increase in the SAM index. We demonstrate that in many GCMs, the expected SST step re- sponse function is nonmonotonic in time. Following a shift to a positive SAM anomaly, an initial cooling regime can transition into surface warming around Antarctica. However, there are large differences across the CMIP5 ensemble. In some models the step response function never changes sign and cooling persists, while in other GCMs the SST anomaly crosses over from negative to positive values only three years after a step increase in the SAM. This intermodel diversity can be related to differences in the models’ climatological thermal ocean stratification in the region of seasonal sea ice around Antarctica. Exploiting this relationship, we use obser- vational data for the time-mean meridional and vertical temperature gradients to constrain the real Southern Ocean response to SAM on fast and slow timescales

Frequently asked questions about chlorophyll fluorescence, the sequel

[EN] Using chlorophyll (Chl) a fluorescence many aspects of the photosynthetic apparatus can be studied, both in vitro and, noninvasively, in vivo. Complementary techniques can help to interpret changes in the Chl a fluorescence kinetics. Kalaji et al. (Photosynth Res 122: 121-158, 2014a) addressed several questions about instruments, methods and applications based on Chl a fluorescence. Here, additionalChl a fluorescence-related topics are discussed again in a question and answer format. Examples are the effect of connectivity on photochemical quenching, the correction of F-V/F-M values for PSI fluorescence, the energy partitioning concept, the interpretation of the complementary area, probing the donor side of PSII, the assignment of bands of 77 K fluorescence emission spectra to fluorescence emitters, the relationship between prompt and delayed fluorescence, potential problems when sampling tree canopies, the use of fluorescence parameters in QTL studies, the use of Chl a fluorescence in biosensor applications and the application of neural network approaches for the analysis of fluorescence measurements. The answers draw on knowledge fromdifferent Chl a fluorescence analysis domains, yielding in several cases new insights.Kalaji, H.; Schansker, G.; Brestic, M.; Bussotti, F.; Calatayud, A.; Ferroni, L.; Goltsev, V.... (2017). Frequently asked questions about chlorophyll fluorescence, the sequel. Photosynthesis Research. 132(1):13-66. https://doi.org/10.1007/s11120-016-0318-yS13661321Adams WW III, Demmig-Adams B (1992) Operation of the xanthophyll cycle in higher plants in response to diurnal changes in incident sunlight. Plant 186:390–398Adams WW III, Demmig-Adams B (2004) Chlorophyll fluorescence as a tool to monitor plant response to the environment. In: Papageorgiou GC, Govindjee (eds) Advances in photosynthesis and respiration series chlorophyll fluorescence: a signature of photosynthesis, vol 19. Springer, Dordrecht, pp 583–604Adams WW III, Demmig-Adams B, Winter K, Schreiber U (1990a) The ratio of variable to maximum chlorophyll fluorescence from photosystem II, measured in leaves at ambient temperature and at 77 K, as an indicator of the photon yield of photosynthesis. Planta 180:166–174Adams WW III, Winter K, Schreiber U, Schramel P (1990b) Photosynthesis and chlorophyll fluorescence characteristics in relationship to changes in pigment and element composition of leaves of Platanus occidentalis L. during autumnal senescence. Plant Physiol 93:1184–1190Alfonso M, Montoya G, Cases R, Rodriguez R, Picorel R (1994) Core antenna complexes, CP43 and CP47, of higher plant photosystem II. Spectral properties, pigment stoichiometry, and amino acid composition. Biochemistry 33:10494–10500Allakhverdiev SI (2011) Recent progress in the studies of structure and function of photosystem II. J Photochem Photobiol B Biol 104:1–8Allakhverdiev SI, Klimov VV, Carpentier R (1994) Variable thermal emission and chlorophyll fluorescence in photosystem II particles. Proc Natl Acad Sci USA 491:281–285Allakhverdiev SI, Los DA, Mohanty P, Nishiyama Y, Murata N (2007) Glycinebetaine alleviates the inhibitory effect of moderate heat stress on the repair of photosystem II during photoinhibition. Biochim Biophys Acta 1767:1363–1371Allen JF (1992) Protein phosphorylation in regulation of photosynthesis. Biochim Biophys Acta 1098:275–335Allen JF, Bennett J, Steinback KE, Arntzen CJ (1981) Chloroplast protein phosphorylation couples platoquinone redox state to distribution of excitation energy between photosystems. Nature 291:21–25Amesz J, van Gorkom HJ (1978) Delayed fluorescence in photosynthesis. Annu Rev Plant Physiol 29:47–66Ananyev GM, Dismukes GC (1996) Assembly of the tetra-Mn site of photosynthetic water oxidation by photoactivation: Mn stoichiometry and detection of a new intermediate. Biochemistry 35:4102–4109Anderson JM, Chow WS, Goodchild DJ (1988) Thylakoid membrane organization in sun/shade acclimation. Aust J Plant Physiol 15:11–26Andrizhiyevskaya EG, Chojnicka A, Bautista JA, Diner BA, van Grondelle R, Dekker JP (2005) Origin of the F685 and F695 fluorescence in photosystem II. Photosynth Res 84:173–180Anithakumari AM, Nataraja KN, Visser RGF, van der Linden G (2012) Genetic dissection of drought tolerance and recovery potential by quantitative trait locus mapping of a diploid potato population. Mol Breed 30:1413–1429Antal TK, Krendeleva TE, Rubin AB (2007) Study of photosystem 2 heterogeneity in the sulfur-deficient green alga Chlamydomonas reinhardtii. Photosynth Res 94:13–22Antal TK, Matorin DN, Ilyash LV, Volgusheva AA, Osipov A, Konyuhow IV, Krendeleva TE, Rubin AB (2009) Probing of photosynthetic reactions in four phytoplanktonic algae with a PEA fluorometer. Photosynth Res 102:67–76Araus JL, Amaro T, Voltas J, Nakkoul H, Nachit MM (1998) Chlorophyll fluorescence as a selection criterion for grain yield in durum wheat under Mediterranean conditions. Field Crops Res 55:209–223Argyroudi-Akoyunoglou J (1984) The 77 K fluorescence spectrum of the Photosystem I pigment-protein complex CPIa. FEBS Lett 171:47–53Arnold WA (1991) Experiments. Photosynth Res 27:73–82Arnold WA, Thompson J (1956) Delayed light production by blue-green algae, red algae and purple bacteria. J Gen Physiol 39:311–318Aro EM, Hundal T, Carlberg I, Andersson B (1990) In vitro studies on light-induced inhibition of PSII and D1-protein degradation at low temperatures. Biochim Biophys Acta 1019:269–275Aro EM, Virgin I, Andersson B (1993) Photoinhibition of photosystem II. Inactivation protein damage and turnover. Biochim Biophys Acta 1143:113–134Arsalane W, Parésys G, Duval JC, Wilhelm C, Conrad R, Büchel C (1993) A new fluorometric device to measure the in vivo chlorophyll a fluorescence yield in microalgae and its use as a herbicide monitor. Eur J Phycol 28:247–252Asada K (1999) The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annu Rev Plant Physiol Plant Mol Biol 50:601–639Ashraf M, Harris PJC (2004) Potential biochemical indicators of salinity tolerance in plants. Plant Sci 166:3–16Bailey S, Walters RG, Jansson S, Horton P (2001) Acclimation of Arabidopsis thaliana to the light environment: the existence of separate low light and high light responses. Planta 213:794–801Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu Rev Plant Biol 59:659–668Baker NR, Rosenqvist E (2004) Applications of chlorophyll fluorescence can improve crop production strategies: an examination of future possibilities. J Exp Bot 55:1607–1621Ballottari M, Dall’Osto L, Morosinotto T, Bassi R (2007) Contrasting behavior of higher plant photosystem I and II antenna systems during acclimation. J Biol Chem 282:8947–8958Barbagallo RP, Oxborough K, Pallett KE, Baker NR (2003) Rapid, noninvasive screening for perturbations of metabolism and plant growth using chlorophyll fluorescence imaging. Plant Physiol 132:485–493Barber J, Malkin S, Telfer A (1989) The origin of chlorophyll fluorescence in vivo and its quenching by the photosystem II reaction centre. Philos Trans R Soc Lond B 323:227–239Barra M, Haumann M, Loja P, Krivanek R, Grundmeier A, Dau H (2006) Intermediates in assembly by photoactivation after thermally accelerated disassembly of the manganese complex of photosynthetic water oxidation. Biochemistry 45:14523–14532Baumann HA, Morrison L, Stengel DB (2009) Metal accumulation and toxicity measured by PAM-chlorophyll fluorescence in seven species of marine macroalgae. Ecotoxicol Environ Safe 72:1063–1075Bauwe H, Hagemann M, Fernie A (2010) Photorespiration: players, partners and origin. Trends Plant Sci 15:330–336Beck WF, Brudvig GW (1987) Reactions of hydroxylamine with the electron-donor side of photosystem II. Biochemistry 26:8285–8295Belgio E, Kapitonova E, Chmeliov J, Duffy CDP, Ungerer P, Valkunas L, Ruban AV (2014) Economic photoprotection in photosystem II that retains a complete light-harvesting system with slow energy traps. Nat Commun 5:4433. doi: 10.1038/ncomms5433Bell DH, Hipkins MF (1985) Analysis of fluorescence induction curves from pea chloroplasts: photosystem II reaction centre heterogeneity. Biochim Biophys Acta 807:255–262Bellafiore S, Barneche F, Peltier G, Rochaix J-D (2005) State transitions and light adaptation require chloroplast thylakoid protein kinase STN7. Nature 433:892–895Belyaeva NE, Schmitt F-J, Paschenko VZ, Riznichenko GY, Rubin AB (2015) Modeling of the redox state dynamics in photosystem II of Chlorella pyrenoidosa Chick cells and leaves of spinach and Arabidopsis thaliana from single flash-induced fluorescence quantum yield changes on the 100 ns–10 s time scale. Photosynth Res 125:123–140Bennett J (1977) Phosphorylation of chloroplast membrane polypeptides. Nature 269:344–346Bennett J (1983) Regulation of photosynthesis by reversible phosphorylation of the light-harvesting chlorophyll a/b protein. Biochem J 212:1–13Bennett J, Shaw EK, Michel H (1988) Cytochrome b6f complex is required for phosphorylation of light-harvesting chlorophyll a/b complex II in chloroplast photosynthetic membranes. Eur J Biochem 171:95–100Bennoun P (2002) The present model for chlororespiration. Photosynth Res 73:273–277Bennoun P, Li Y-S (1973) New results on the mode of action of 3,-(3,4-dichlorophenyl)-1,1-dimethylurea in spinach chloroplasts. Biochim Biophys Acta 292:162–168Berden-Zrimec M, Drinovec L, Zrimec A (2011) Delayed fluorescence. In: Suggett DJ, Borowitzka M, Prášil O (eds) Chlorophyll a fluorescence in aquatic sciences: methods and applications, developments in applied phycology, vol 4. Springer, The Netherlands, pp 293–309Berger S, Sinha AK, Roitsch T (2007) Plant physiology meets phytopathology: plant primary metabolism and plant-pathogen interactions. J Exp Bot 58:4019–4026Bernacchi CJ, Leakey ADB, Heady LE, Morgan PB, Dohleman FG, McGrath JM, Gillespie GM, Wittig VE, Rogers A, Long SP, Ort DR (2006) Hourly and seasonal variation in photosynthesis and stomatal conductance of soybean grown at future CO2 and ozone concentrations for 3 years under fully open-air field conditions. Plant Cell Environ 29:2077–2090Betterle N, Ballotari M, Zorzan S, de Bianchi S, Cazzaniga S, Dall’Osto L, Morosinotto T, Bassi R (2009) Light-induced dissociation of an antenna hetero-oligomer is needed for non-photochemical quenching induction. J Biol Chem 284:15255–15266Bielczynski LW, Schansker G, Croce R (2016) Effect of light acclimation on the organization of photosystem II super and sub-complexes in Arabidopsis thaliana. Front Plant Sci. doi: 10.3389/fpls.2016.00105Björkman O, Demmig-Adams B (1995) Regulation of photosynthetic light energy capture, conversion, and dissipation in leaves of higher plants. In: Schulze ED, Caldwell MM (eds) Ecophysiology of photosynthesis. Springer, Berlin, pp 17–47Blubaugh DJ, Cheniae GM (1990) Kinetics of photoinhibition in hydroxylamine-extracted photosystem II membranes: relevance to photoactivation and site of electron donation. Biochemistry 29:5109–5118Bock A, Krieger-Liszkay A, Ortiz de Zarate IB, Schönknecht G (2001) Cl—channel inhibitors of the arylaminobenzoate type act as photosystem II herbicides: a functional and structural study. Biochemistry 40:3273–3281Bode S, Quentmeier CC, Liao P-N, Hafi N, Barros T, Wilk L, Bittner F, Walla PJ (2009) On the regulation of photosynthesis by excitonic interactions between carotenoids and chlorophylls. Proc Natl Acad Sci USA 106:12311–12316Boekema EJ, Van Roon H, Van Breemen JFL, Dekker JP (1999) Supramolecular organization of photosystem II and its light-harvesting antenna in partially solubilized photosystem II membranes. Eur J Biochem 266:444–452Bolhar-Nordenkampf HR, Long SP, Baker NR, Öquist G, Schreiber U, Lechner EG (1989) Chlorophyll fluorescence as a probe of the photosynthetic competence of leaves in the field: a review of current Instrumentation. Funct Ecol 3:497–514Bonaventura C, Myers J (1969) Fluorescence and oxygen evolution from Chlorella pyrenoidosa. Biochim Biophys Acta 189:366–383Bonfig KB, Schreiber U, Gabler A, Roitsch T, Berger S (2006) Infection with virulent and avirulent P. syringae strains differentially affects photosynthesis and sink metabolism in Arabidopsis leaves. Planta 225:1–12Bouges-Bocquet B (1980) Kinetic models for the electron donors of photosystem II of photosynthesis. Biochim Biophys Acta 594:85–103Bradbury M, Baker NR (1981) Analysis of the slow phases of the in vivo chlorophyll fluorescence induction curve; changes in the redox state of photosystem II electron acceptors and fluorescence emission from photosystem I and II. Biochim Biophys Acta 635:542–551Brestič M, Živčák M (2013) PSII fluorescence techniques for measurement of drought and high temperature stress signal in crop plants: protocols and applications. In: Das AB, Rout GR (eds) Molecular stress physiology of plants. Springer, New Dehli, pp 87–131Brestič M, Cornic G, Fryer MJ, Baker NR (1995) Does photorespiration protect the photosynthetic apparatus in French bean leaves from photoinhibition during drought stress? Planta 196:450–457Brestič M, Živčák M, Kalaji HM, Allakhverdiev SI, Carpentier R (2012) Photosystem II thermo-stability in situ: environmentally induced acclimation and genotype-specific reactions in Triticum aestivum L. Plant Physiol Biochem 57:93–105Brody SS, Rabinowitch E (1957) Excitation lifetime of photosynthetic pigments in vitro and in vivo. Science 125:555–563Brudvig GW, Casey JL, Sauer K (1983) The effect of temperature on the formation and decay of the multiline EPR signal species associated with photosynthetic oxygen evolution. Biochim Biophys Acta 723:366–371Bukhov NG, Boucher N, Carpentier R (1997) The correlation between the induction kinetics of the photoacoustic signal and chlorophyll fluorescence in barley leaves is governed by changes in the redox state of the photosystem II acceptor side; a study under atmospheric and high CO2 concentrations. Can J Bot 75:1399–1406Bukhov N, Egorova E, Krendeleva T, Rubin A, Wiese C, Heber U (2001) Relaxation of variable chlorophyll fluorescence after illumination of dark-adapted barley leaves as influenced by the redox states of electron carriers. Photosynth Res 70:155–166Buschmann C, Koscányi L (1989) Light-induced heat production correlated with chlorophyll fluorescence and its quenching. Photosynth Res 21:129–136Bussotti F (2004) Assessment of stress conditions in Quercus ilex L. leaves by O-J-I-P chlorophyll a fluorescence analysis. Plant Biosystems 13:101–109Bussotti F, Agati G, Desotgiu R, Matteini P, Tani C (2005) Ozone foliar symptoms in woody plants assessed with ultrastructural and fluorescence analysis. New Phytol 166:941–955Bussotti F, Desotgiu R, Cascio C, Pollastrini M, Gravano E, Gerosa G, Marzuoli R, Nali C, Lorenzini G, Salvatori E, Manes F, Schaub M, Strasser RJ (2011a) Ozone stress in woody plants assessed with chlorophyll a fluorescence. A critical reassessment of existing data. Environ Exp Bot 73:19–30Bussotti F, Pollastrini M, Cascio C, Desotgiu R, Gerosa G, Marzuoli R, Nali C, Lorenzini G, Pellegrini E, Carucci MG, Salvatori E, Fusaro L, Piccotto M, Malaspina P, Manfredi A, Roccotello E, Toscano S, Gottardini E, Cristofori A, Fini A, Weber D, Baldassarre V, Barbanti L, Monti A, Strasser RJ (2011b) Conclusive remarks. Reliability and comparability of chlorophyll fluorescence data from several field teams. Environ Exp Bot 73:116–119Butler WL (1978) Energy distribution in the photochemical apparatus of photosynthesis. Annu Rev Plant Physiol 29:345–378Byrdin M, Rimke I, Schlodder E, Stehlik D, Roelofs TA (2000) Decay kinetics and quantum yields of fluorescence in photosystem I from Synechococcus elongatus with P700 in the reduced and oxidized state: Are the kinetics of excited state decay trap-limited or transfer-limited? Biophys J 79:992–1007Caffarri S, Croce R, Cattivelli L, Bassi R (2004) A look within LHCII: differential analysis of the Lhcb1-3 complexes building the major trimeric antenna complex of higher-plant photosynthesis. Biochemistry 43:9467–9476Calatayud A, Ramirez JW, Iglesias DJ, Barreno E (2002) Effects of ozone on photosynthetic CO2 exchange, chlorophyll a fluorescence and antioxidant systems in lettuce leaves. Physiol Plant 116:308–316Cascio C, Schaub M, Novak K, Desotgiu R, Bussotti F, Strasser RJ (2010) Foliar responses to ozone of Fagus sylvatica L. seedlings grown in shaded and in full sunlight conditions. Environ Exp Bot 68:188–197Cazzaniga S, Dall’Osto L, Kong S-G, Wada M, Bassi R (2013) Interaction between avoidance of photon absorption, excess energy dissipation and zeaxanthin synthesis against photooxidative stress in Arabidopsis. Plant J 76:568–579Ceppi MG, Oukarroum A, Çiçek N, Strasser RJ, Schansker G (2012) The IP amplitude of the fluorescence rise OJIP is sensitive to changes in the photosystem I content of leaves: a study on plants exposed to magnesium and sulfate deficiencies, drought stress and salt stress. Physiol Plant 144:277–288Chaudhary N, Singh S, Agrawal SB, Agrawal M (2013) Assessment of six Indian cultivars of mung bean against ozone by using foliar injury index and changes in carbon assimilation, gas exchange, chlorophyll fluorescence and photosynthetic pigments. Environ Monit Assess 185:7793–7807Chen J, Kell A, Acharya K, Kupitz C, Fromme P, Jankowiak R (2015) Critical assessment of the emission spectra of various photosystem II core complexes. Photosynth Res 124:253–265Cheng L, Fuchigami LH, Breen PJ (2000) Light absorption and partitioning in relation to nitrogen content ‘Fuji’ apple leaves. J Am Soc Hortic Sci 125:581–587Choi CJ, Berges JA, Young EB (2012) Rapid effects of diverse toxic water pollutants on chlorophyll a fluorescence: variable responses among freshwater microalgae. Water Res 46:2615–2626Chow WS, Aro EM (2005) Photoinactivation and mechanisms of recovery. In: Wydrzynski T, Satoh K (eds) Photosystem II: the light-driven water: plastoquinone oxidoreductase, advances in photosynthesis and respiration, vol 22. Springer, Dordrecht, pp 627–648Chow WS, Fan DY, Oguchi R, Jia H, Losciale P, Youn-Il P, He J, Öquist G, Shen YG, Anderson JM (2012) Quantifying and monitoring functional photosystem II and the stoichiometry of the two photosystems in leaf segments: approaches and approximations. Photosynth Res 113:63–74Christensen MG, Teicher HB, Streibig JC (2003) Linking fluorescence induction curve and biomass in herbicide screening. Pest Manag Sci 59:1303–1310Codrea CM, Aittokallio T, Keränen M, Tyystjärvi E, Nevalainen OS (2003) Feature learning with a genetic algorithm for fluorescence fingerprinting of plant species. Pattern Recognit Lett 24:2663–2673Conjeaud H, Mathis P (1980) The effect of pH on the reduction kinetics of P-680 in tris-treated chloroplasts. Biochim Biophys Acta 590:353–359Conrad R, Büchel C, Wilhelm C, Arsalane W, Berkaloff C, Duval JC (1993) Changes in yield of in-vivo fluorescence of chlorophyll a as a tool for selective herbicide monitoring. J Appl Phycol 5:505–516Cornic G, Massacci A (1996) Leaf photosynthesis under drought stress. In: Baker NR (ed) Photosynthesis and the environment. Kluwer Academic Publisher, Dordrecht, pp 347–366Cornic G, Fresneau C (2002) Photosynthetic carbon reduction and carbon oxidation cycles are the main electron sinks for photosystems II during a mild drought. Ann Bot 89:887–894Correia MJ, Chaves MMC, Pereira JS (1990) Afternoon depression in photosynthesis in grapevine leaves—evidence for a high light stress effect. J Exp Bot 41:417–426Cotrozzi L, Remorini D, Pellegrini E, Landi M, Massai R, Nali C, Guidi L, Lorenzini G (2016) Variations in physiological and biochemical traits of oak seedlings grown under drought and ozone stress. Physiol Plant 157:69–84Croce R, Zucchelli G, Garlaschi FM, Bassi R, Jennings RC (1997) Excited state equilibration in the photosystem I-light-harvesting I complex: P700 is almost isoenergetic with its antenna. Biochemistry 35:8572–8579Cser K, Vass I (2007) Radiative and non-radiative charge recombination pathways in photosystem II studied by thermoluminescence and chlorophyll fluorescence in the cyanobacterium Synechocystis 6308. Biochim Biophys Acta 1767:233–243Czyczyło-Mysza I, Tyrka M, Marcińska Skrzypek E, Karbarz M, Dziurka M, Hura T, Dziurka K, Quarrie SA (2013) Quantitative trait loci for leaf chlorophyll fluorescence parameters, chlorophyll and carotenoid contents in relation to biomass and yield in bread wheat and their chromosome deletion bin assignments. Mol Breed 32:189–210D’Haene SE, Sobotka R, Bučinská L, Dekker JP, Komenda J (2015) Interaction of the PsbH subunit with a chlorophyll bound to histidine 114 of CP47 is responsible for the red 77 K fluorescence of Photosystem II. Biochim Biophys Acta 1847:1327–1334Dang NC, Zazubovich V, Reppert M, Neupane B, Picorel R, Seibert M, Jankowiak R (2008) The CP43 proximal antenna complex of higher plant photosystem II revisited: modeling and hole burning study. J Phys Chem B 112:9921–9933Dau H (1994) Molecular mechanisms and quantitative models of variable Photosystem II fluorescence. Photochem Photobiol 60:1–23Dau H, Sauer K (1992) Electric field effect on the picosecond fluorescence of photosystem II and its relation to the energetics and kinetics of primary charge separation. Biochim Biophys Acta 1102:91–106Dau H, Zaharieva I, Haumann M (2012) Recent developments in research on water oxidation by photosystem II. Curr Opin Chem Biol 16:3–10de Wijn R, van Gorkom HJ (2001) Kinetics of electron transfer from QA to QB in photosystem II. Biochemistry 40:11912–11922de Wijn R, van Gorkom HJ (2002) The rate of charge recombination in photosystem II. Biochim Biophys Acta 1553:302–308Debus RJ (1992) The manganese and calcium ions of photosynthetic oxygen evolution. Biochim Biophys Acta 1102:269–352Degl’Innocenti E, Guidi L, Soldatini GF (2002) Characteriz

Observation of the Gamma-Ray Binary HESS J0632+057 with the HESS, MAGIC, and VERITAS Telescopes

The results of gamma-ray observations of the binary system HESS J0632 + 057 collected during 450 hr over 15 yr, between 2004 and 2019, are presented. Data taken with the atmospheric Cherenkov telescopes H.E.S.S., MAGIC, and VERITAS at energies above 350 GeV were used together with observations at X-ray energies obtained with Swift-XRT, Chandra, XMM-Newton, NuSTAR, and Suzaku. Some of these observations were accompanied by measurements of the H alpha emission line. A significant detection of the modulation of the very high-energy gamma-ray fluxes with a period of 316.7 +/- 4.4 days is reported, consistent with the period of 317.3 +/- 0.7 days obtained with a refined analysis of X-ray data. The analysis of data from four orbital cycles with dense observational coverage reveals short-timescale variability, with flux-decay timescales of less than 20 days at very high energies. Flux variations observed over a timescale of several years indicate orbit-to-orbit variability. The analysis confirms the previously reported correlation of X-ray and gamma-ray emission from the system at very high significance, but cannot find any correlation of optical H alpha parameters with fluxes at X-ray or gamma-ray energies in simultaneous observations. The key finding is that the emission of HESS J0632 + 057 in the X-ray and gamma-ray energy bands is highly variable on different timescales. The ratio of gamma-ray to X-ray flux shows the equality or even dominance of the gamma-ray energy range. This wealth of new data is interpreted taking into account the insufficient knowledge of the ephemeris of the system, and discussed in the context of results reported on other gamma-ray binary systems