Abstract
In their natural environment, plants are exposed to varying light conditions, which can lead to a build-up of excitation energy in photosystem (PS) II. Non-photochemical quenching (NPQ) is the primary defence mechanism employed to dissipate this excess energy. Recently, we developed a fluorescence-quenching analysis procedure that enables the protective effectiveness of NPQ in intact Arabidopsis leaves to be determined. However, pulse-amplitude modulation measurements do not currently allow distinguishing between PSII and PSI fluorescence levels. Failure to account for PSI contribution is suggested to lead to inaccurate measurements of NPQ and, particularly, maximum PSII yield (F v/F m). Recently, Pfündel et al. (Photosynth Res 114:189–206, 2013) proposed a method that takes into account PSI contribution in the measurements of F o fluorescence level. However, when PSI contribution was assumed to be constant throughout the induction of NPQ, we observed lower values of the measured minimum fluorescence level (\({F_{{\text{o}}_{\text{calc.}}^{^\prime }}}\)) than those calculated according to the formula of Oxborough and Baker (Photosynth Res 54:135–142 1997) (\({F_{{\text{o}}_{\text{calc.}}^{^\prime } }}\)), regardless of the light intensity. Therefore, in this work, we propose a refined model to correct for the presence of PSI fluorescence, which takes into account the previously observed NPQ in PSI. This method efficiently resolves the discrepancies between measured and calculated F o′ produced by assuming a constant PSI fluorescence contribution, whilst allowing for the correction of the maximum PSII yield.
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References
Adams WW, Zarter CR, Mueh KE, Amiard V, Demmig-Adams B (2006) Energy dissipation and photoinhibition: a continuum of photoprotection. In: Demmig-Adams B, Adams WW, Mattoo AK (eds) Photoprotection, photoinhibition, gene regulation, and environment. Springer, Dordrecht, pp 49–64
Aro E-M, McCaffery S, Anderson JM (1993) Photoinhibition and D1 protein degradation in peas acclimated to different growth irradiances. Plant Physiol 130:835–843
Ballottari M, Alcocer MJP, D’Andrea C, Viola D, Ahn TK, Petrozza A, Polli D, Fleming GR, Cerullo G, Bassi R (2014) Regulation of photosystem I light harvesting by zeaxanthin. Proc Natl Acad Sci USA 111:E2431–E2438
Barber J (1995) Molecular basis of the vulnerability of photosystem II to damage by light. Aust J Plant Physiol 22:201–208
Barber J (2002) Photosystem II: a multisubunit membrane protein that oxidises water. Curr Opin Struct Biol 12:523–530
Barber J (2009) Photosynthetic energy conversion: natural and artificial. Chem Soc Rev 38:185–196
Bassi R, HØyer-Hansen G, Barbato R, Giacometti GM, Simpson DJ (1987) Chlorophyll-proteins of the photosystem II antenna system. J Biol Chem 27:13333–13341
Bassi R, Pineau B, Dainese P, Marquardt J (1993) Carotenoid-binding proteins of photosystem II. Eur J Biochem 212:297–303
Becker B, Marin B (2009) Streptophyte algae and the origin of embryophytes. Ann Bot 103:999–1004
Belgio E, Johnson MP, Jurić S, Ruban AV (2012) Higher plant photosystem II light-harvesting antenna, not the reaction center, determines the excited state lifetime-both the maximum and the nonphotochemically quenched. Biophys J 102:2761–2771
Bellafiore S, Barneche F, Peltier G, Rochaix J-D (2005) State transitions and light adaptation require chloroplast thylakoid protein kinase STN7. Nature 433:892–895
Blankenship RE (2002) Molecular mechanisms of photosynthesis. Wiley, London
Briantais J-M, Vemotte C, Picaud M, Krause GH (1979) A quantitative study of the slow decline of chlorophyll a fluorescence in isolated chloroplasts. Biochim Biophys Acta 548:128–138
Brooks MD, Sylak-Glassman EJ, Fleming GR, Niyogi KK (2013) A thioredoxin-like/β-propeller protein maintains the efficiency of light harvesting in Arabidopsis. Proc Natl Acad Sci USA 110:E2733–E2740
Brugnoli E, Björkman O (1992) Chloroplast movements in leaves: Influence on chlorophyll fluorescence and measurements of light-induced absorbance changes related to ΔpH and zeaxanthin formation. Photosynth Res 32:23–35
Caffarri S, Tibiletti T, Jennings RC, Santabarbara S (2014) A comparison between plant photosystem I and photosystem II architecture and functioning. Curr Protein Pept Sci 15:296–331
Dall’Osto L, Cazzaniga S, Wada M, Bassi R (2014) On the origin of a slowly reversible fluorescence decay component in the Arabidopsis npq4 mutant. Phil Trans R Soc B 369:20130221
Dau H (1994) Molecular mechanism and quantitative models of variable photosystem II fluorescence. Photochem Photobiol 60:1–23
Dekker JP, Boekema EJ (2005) Supramolecular organization of thylakoid membrane proteins in green plants. Biochim Biophys Acta 1706:12–39
Demmig-Adams B (1990) Carotenoids and photoprotection: a role for the xanthophyll zeaxanthin. Biochim Biophys Acta 1020:1–24
Engelmann EC, Zucchelli G, Garlaschi FM, Casazza AP, Jennings RC (2005) The effect of outer antenna complexes on the photochemical trapping rate in barley thylakoid Photosystem II. Biochim Biophys Acta 1706:276–286
Falkowski PG, Katz ME, Knoll AH, Quigg A, Raven JA, Schofield O, Taylor FRJ (2004) The evolution of modern phytoplankton. Science 305:354–360
Farber A, Young AJ, Ruban AV, Horton P, Jahns P (1997) Dynamics of xanthophyll-cycle activity in different antenna subcomplexes in the photosynthetic membranes of higher plants: the relationship between zeaxanthin conversion and nonphotochemical fluorescence quenching. Plant Physiol 115:1609–1618
Goral TK, Johnson MP, Duffy CD, Brain AP, Ruban AV, Mullineaux CW (2012) Light-harvesting antenna composition controls the macrostructure and dynamics of thylakoid membranes in Arabidopsis. Plant J 69:289–301
Goss R, Lepetit B (2014) Biodiversity of NPQ. J Plant Physiol 172:13–32
Holzwarth AR, Miloslavina Y, Nilkens M, Jahns P (2009) Identification of two quenching sites active in the regulation of photosynthetic light-harvesting studied by time-resolved fluorescence. Chem Phys Lett 483:262–267
Horton P, Ruban AV (1992) Regulation of photosystem II. Photosynth Res 34:375–385
Horton P, Ruban AV (2004) Molecular design of the photosystem II light harvesting antenna: photosynthesis and photoprotection. J Exp Bot 56:365–373
Horton P, Ruban AV, Wentworth M (2000) Allosteric regulation of the light harvesting system of photosystem II. Phil Trans R Soc B 355:1361–1370
Jahns P, Holzwarth AR (2012) The role of the xanthophyll cycle and of lutein in photoprotection of photosystem II. Biochim Biophys Acta 1817:182–193
Johnson MP, Ruban AV (2009) Photoprotective energy dissipation in higher plants involves alteration of the excited state energy of the emitting chlorophyll(s) in the light harvesting antenna II (LHCII). J Biol Chem 284:23592–23601
Johnson MP, Ruban AV (2010) Arabidopsis plants lacking PsbS protein possess photoprotective energy dissipation. Plant J 61:283–289
Johnson MP, Goral TK, Duffy CDP, Brain APR, Mullineaux CW, Ruban AV (2011) Photoprotective energy dissipation involves the reorganization of photosystem II light harvesting complexes in the grana membranes of spinach chloroplasts. Plant Cell 23:1468–1479
Krause GH (1988) Photoinhibition of photosynthesis. An evaluation of damaging and protective mechanisms. Physiol Plant 74:566–574
Krause GH, Behrend U (1986) ΔpH-dependent chlorophyll fluorescence quenching indicating a mechanism of protection against photoinhibition of chloroplasts. FEBS Lett 200:298–302
Krause GH, Weis E (1991) Chlorophyll fluorescence and photosynthesis: the basics. Annu Rev Plant Physiol Plant Mol Biol 42:313–349
Lazár D (2013) Simulations show that a small part of variable chlorophyll a fluorescence originates in photosystem I and contributes to overall fluorescence rise. J Theor Biol 335:249–264
Li X-P, Björkman O, Shih C, Grossman AR, Rosenquist M, Jansson S, Niyogi KK (2000) A pigment-binding protein essential for regulation of photosynthetic light harvesting. Nature 403:391–395
Miloslavina Y, de Bianchi S, Dall’Osto L, Bassi R, Holzwarth AR (2011) Quenching in Arabidopsis thaliana mutants lacking monomeric antenna proteins of photosystem II. J Biol Chem 286:36830–36840
Moise N, Moya I (2004) 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. Biochim Biophys Acta 1657:47–60
Müller P, Li X-P, Niyogi KK (2001) Non-photochemical quenching. A response to excess light energy. Plant Physiol 125:1558–1566
Nelson N (2011) Photosystems and global effects of oxygenic photosynthesis. Biochim Biophys Acta 1807:856–863
Nilkens M, Kress E, Lambrev P, Miloslavina Y, Müller M, Holzwarth AR, Jahns P (2010) Identification of a slowly inducible zeaxanthin-dependent component of non-photochemical quenching of chlorophyll fluorescence generated under steady-state conditions in Arabidopsis. Biochim Biophys Acta 1797:466–475
Niyogi KK, Truong TB (2013) Evolution of flexible non-photochemical quenching mechanisms that regulate light harvesting in oxygenic photosynthesis. Curr Opin Plant Biol 16:307–314
Noctor G, Ruban AV, Horton P (1993) Modulation of ΔpH-dependent nonphotochemical quenching of chlorophyll fluorescence in spinach chloroplasts. Biochim Biophys Acta 1183:339–344
Osmond CB (1994) What is photoinhibition? Some insights from comparisons of shade and sun plants. In: Baker NR, Bowyer JR (eds) Photoinhibition of photosynthesis. Bios Scientific, Lancaster, pp 1–24
Oxborough K, Baker NR (1997) Resolving chlorophyll a fluorescence of photosynthetic efficiency into photochemical components—calculation of qP and F v′/F m′ without measuring F o′. Photosynth Res 54:135–142
Peterson RB, Oja V, Eichelmann H, Bichele I, Dall’Osto L, Laisk A (2014) Fluorescence F0 of photosystems II and I in developing C3 and C4 leaves, and implications on regulation of excitation balance. Photosynth Res 122:41–56
Pfündel EE, Klughammer C, Meister A, Cerovic ZG (2013) Deriving fluorometer- specific values of relative PSI fluorescence intensity from quenching of F o fluorescence in leaves of Arabidopsis thaliana and Zea mays. Photosynth Res 114:189–206
Porra RJ, Thompson WA, Kriedemann PE (1989) Determination of accurate extinction coefficients and simultaneous-equations for assaying chlorophyll-a and chlorophyll-b extracted with 4 different solvents-verification of the concentration of chlorophyll standards by atomic-absorption spectroscopy. Biochim Biophys Acta 975:384–394
Powles SB (1984) Photoinhibition of photosynthesis induced by visible light. Ann Rev Plant Physiol 35:15–44
Richter M, Goss R, Wagner B, Holzwarth AR (1999) Characterization of the fast and slow reversible components of non-photochemical quenching in isolated pea thylakoids by picosecond time-resolved chlorophyll fluorescence analysis. Biochemistry 38:12718–12726
Rintamäki E, Martinsuo P, Pursiheimo S, Aro E-M (2000) Cooperative regulation of light-harvesting complex II phosphorylation via the plastoquinol and ferredoxin-thioredoxin system in chloroplasts. Proc Natl Acad Sci USA 97:11644–11649
Ruban A (2012) The photosynthetic membrane: molecular mechanisms and biophysics of light harvesting. Wiley-Blackwell, Oxford
Ruban AV, Belgio E (2014) The relationship between maximum tolerated light intensity and photoprotective energy dissipation in the photosynthetic antenna: chloroplast gains and losses. Phil Trans R Soc B 369:20130222
Ruban AV, Horton P (1999) The xanthophyll cycle modulates the kinetics of nonphotochemical energy dissipation in isolated light harvesting complexes, intact chloroplasts and leaves. Plant Physiol 119:531–542
Ruban AV, Murchie EH (2012) Assessing the photoprotective effectiveness of non-photochemical chlorophyll fluorescence quenching: a new approach. Biochim Biophys Acta 1817:977–982
Ruban AV, Rees D, Noctor GD, Young A, Horton P (1991) Long-wavelength chlorophyll species are associated with amplification of high-energy-state excitation quenching in higher plants. Biochim Biophys Acta 1059:355–360
Ruban AV, Young A, Horton P (1993) Induction of nonphotochemical energy dissipation and absorbance changes in leaves; evidence for changes in the state of the light harvesting system of photosystem II in vivo. Plant Physiol 102:741–750
Ruban AV, Young AJ, Pascal AA, Horton P (1994) The effects of illumination on the xanthophyll composition of the photosystem II light harvesting complexes of spinach thylakoid membranes. Plant Physiol 104:227–234
Ruban AV, Johnson MP, Duffy CDP (2012) The photoprotective molecular switch in the photosystem II antenna. Biochim Biophys Acta 1817:167–181
Sylak-Glassman EJ, Malnoë A, De Re E, Brooks MD, Fischer AL, Niyogi KK, Fleming GR (2014) Distinct roles of the photosystem II protein PsbS and zeaxanthin in the regulation of light harvesting in plants revealed by fluorescence lifetime snapshots. Proc Natl Acad Sci USA. doi:10.1073/pnas.1418317111
Tikkanen M, Piippo M, Suorsa M, Sirpio S, Mulo P, Vainonen J, Vener AV, Allahverdiyeva Y, Aro EM (2006) State transitions revisited—a buffering system for dynamic low light acclimation of Arabidopsis. Plant Mol Biol 62:779–793
Triantaphylidès C, Havaux M (2009) Singlet oxygen in plants: production, detoxification and signalling. Trends Plant Sci 14:219–228
Trissl HW, Gao Y, Wulf K (1993) Theoretical fluorescence induction curves derived from coupled differential equations describing the primary photochemistry of photosystem II by an exciton-radical pair equilibrium. Biophys J 64:974–988
Tyystjärvi E, Aro EM (1996) The rate constant of photoinhibition, measured in lincomycin-treated leaves, is directly proportional to light intensity. Proc Natl Acad Sci USA 93:2213–2218
van Amerongen H, van Grondelle R (2001) Understanding the energy transfer function of LHCII, the major light-harvesting complex of green plants. J Phys Chem B 105:604–617
Vass I (2012) Molecular mechanisms of photodamage in the photosystem II complex. Biochim Biophys Acta 1817:209–217
Wagner B, Goss R, Richter M, Wild A, Holzwarth AR (1996) Picosecond time-resolved study on the nature of high-energy-state quenching in isolated pea thylakoids. Different localization of zeaxanthin dependent and independent mechanisms. J Photochem Photobiol B Biol 36:339–350
Ware MA, Belgio E, Ruban AV (2014) Comparison of the protective effectiveness of NPQ in Arabidopsis plants deficient in PsbS protein and zeaxanthin. J Exp Bot. doi:10.1093/jxb/eru477
Waters ER (2003) Molecular adaptation and the origin of land plants. Mol Phylogenet Evol 29:456–463
Wientjes E, van Amerongen H, Croce R (2013) Quantum yield of charge separation in photosystem II: functional effect of changes in the antenna size upon light acclimation. J Phys Chem 117:11200–11208
Yamamoto HY (1979) Biochemistry of the violaxanthin cycle in higher plants. Pure Appl Chem 51:639–648
Yamamoto HY, Kamite L (1972) The effects of dithiothreitol on violaxanthin de-epoxidation and absorbance changes in the 500-nm region. Biochim Biophys Acta 267:538–543
Acknowledgments
We would like to thank Dr Christopher Duffy for the critical reading of the manuscript, and Dr Erica Belgio for helpful discussions. This work was supported by the UK Biotechnology and Biological Sciences Research Council and The Leverhulme Trust to AVR and Queen Mary Principal’s research studentship to MAW.
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Giovagnetti, V., Ware, M.A. & Ruban, A.V. Assessment of the impact of photosystem I chlorophyll fluorescence on the pulse-amplitude modulated quenching analysis in leaves of Arabidopsis thaliana . Photosynth Res 125, 179–189 (2015). https://doi.org/10.1007/s11120-015-0087-z
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DOI: https://doi.org/10.1007/s11120-015-0087-z