RNA interference-mediated c-MYC inhibition prevents cell growth and decreases sensitivity to radio- and chemotherapy in childhood medulloblastoma cells

BACKGROUND: With current treatment strategies, nearly half of all medulloblastoma (MB) patients die from progressive tumors. Accordingly, the identification of novel therapeutic strategies remains a major goal. Deregulation of c-MYC is evident in numerous human cancers. In MB, over-expression of c-MYC has been shown to cause anaplasia and correlate with unfavorable prognosis. METHODS: To study the role of c-MYC in MB biology, we down-regulated c-MYC expression by using small interfering RNA (siRNA) and investigated changes in cellular proliferation, cell cycle analysis, apoptosis, telomere maintenance, and response to ionizing radiation (IR) and chemotherapeutics in a representative panel of human MB cell lines expressing different levels of c-MYC (DAOY wild-type, DAOY transfected with the empty vector, DAOY transfected with c-MYC, D341, and D425). RESULTS: siRNA-mediated c-MYC down-regulation resulted in an inhibition of cellular proliferation and clonogenic growth, inhibition of G1-S phase cell cycle progression, and a decrease in human telomerase reverse transcriptase (hTERT) expression and telomerase activity. On the other hand, down-regulation of c-MYC reduced apoptosis and decreased the sensitivity of human MB cells to IR, cisplatin, and etoposide. This effect was more pronounced in DAOY cells expressing high levels of c-MYC when compared with DAOY wild-type or DAOY cells transfected with the empty vector. CONCLUSION: In human MB cells, in addition to its roles in growth and proliferation, c-MYC is also a potent inducer of apoptosis. Therefore, targeting c-MYC might be of therapeutic benefit when used sequentially with chemo- and radiotherapy rather than concomitantly

Convergent functional genomics of anxiety disorders: translational identification of genes, biomarkers, pathways and mechanisms

Anxiety disorders are prevalent and disabling yet understudied from a genetic standpoint, compared with other major psychiatric disorders such as bipolar disorder and schizophrenia. The fact that they are more common, diverse and perceived as embedded in normal life may explain this relative oversight. In addition, as for other psychiatric disorders, there are technical challenges related to the identification and validation of candidate genes and peripheral biomarkers. Human studies, particularly genetic ones, are susceptible to the issue of being underpowered, because of genetic heterogeneity, the effect of variable environmental exposure on gene expression, and difficulty of accrual of large, well phenotyped cohorts. Animal model gene expression studies, in a genetically homogeneous and experimentally tractable setting, can avoid artifacts and provide sensitivity of detection. Subsequent translational integration of the animal model datasets with human genetic and gene expression datasets can ensure cross-validatory power and specificity for illness. We have used a pharmacogenomic mouse model (involving treatments with an anxiogenic drug—yohimbine, and an anti-anxiety drug—diazepam) as a discovery engine for identification of anxiety candidate genes as well as potential blood biomarkers. Gene expression changes in key brain regions for anxiety (prefrontal cortex, amygdala and hippocampus) and blood were analyzed using a convergent functional genomics (CFG) approach, which integrates our new data with published human and animal model data, as a translational strategy of cross-matching and prioritizing findings. Our work identifies top candidate genes (such as FOS, GABBR1, NR4A2, DRD1, ADORA2A, QKI, RGS2, PTGDS, HSPA1B, DYNLL2, CCKBR and DBP), brain–blood biomarkers (such as FOS, QKI and HSPA1B), pathways (such as cAMP signaling) and mechanisms for anxiety disorders—notably signal transduction and reactivity to environment, with a prominent role for the hippocampus. Overall, this work complements our previous similar work (on bipolar mood disorders and schizophrenia) conducted over the last decade. It concludes our programmatic first pass mapping of the genomic landscape of the triad of major psychiatric disorder domains using CFG, and permitted us to uncover the significant genetic overlap between anxiety and these other major psychiatric disorders, notably the under-appreciated overlap with schizophrenia. PDE10A, TAC1 and other genes uncovered by our work provide a molecular basis for the frequently observed clinical co-morbidity and interdependence between anxiety and other major psychiatric disorders, and suggest schizo-anxiety as a possible new nosological domain

Deciphering the Preference and Predicting the Viability of Circular Permutations in Proteins

Circular permutation (CP) refers to situations in which the termini of a protein are relocated to other positions in the structure. CP occurs naturally and has been artificially created to study protein function, stability and folding. Recently CP is increasingly applied to engineer enzyme structure and function, and to create bifunctional fusion proteins unachievable by tandem fusion. CP is a complicated and expensive technique. An intrinsic difficulty in its application lies in the fact that not every position in a protein is amenable for creating a viable permutant. To examine the preferences of CP and develop CP viability prediction methods, we carried out comprehensive analyses of the sequence, structural, and dynamical properties of known CP sites using a variety of statistics and simulation methods, such as the bootstrap aggregating, permutation test and molecular dynamics simulations. CP particularly favors Gly, Pro, Asp and Asn. Positions preferred by CP lie within coils, loops, turns, and at residues that are exposed to solvent, weakly hydrogen-bonded, environmentally unpacked, or flexible. Disfavored positions include Cys, bulky hydrophobic residues, and residues located within helices or near the protein's core. These results fostered the development of an effective viable CP site prediction system, which combined four machine learning methods, e.g., artificial neural networks, the support vector machine, a random forest, and a hierarchical feature integration procedure developed in this work. As assessed by using the hydrofolate reductase dataset as the independent evaluation dataset, this prediction system achieved an AUC of 0.9. Large-scale predictions have been performed for nine thousand representative protein structures; several new potential applications of CP were thus identified. Many unreported preferences of CP are revealed in this study. The developed system is the best CP viability prediction method currently available. This work will facilitate the application of CP in research and biotechnology

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