Abstract
Singlet-excited oxygen (1O *2 ) has been recognized as the most destructive member of the reactive oxygen species (ROS) which are formed during oxygenic photosynthesis by plants, algae, and cyanobacteria. ROS and 1O *2 are known to damage protein and phospholipid structures and to impair photosynthetic electron transport and de novo protein synthesis. Partial protection is afforded to photosynthetic organism by the β-carotene (β-Car) molecules which accompany chlorophyll (Chl) a in the pigment-protein complexes of Photosystem II (PS II). In this paper, we studied the effects of exogenously added β-Car on the initial kinetic rise of Chl a fluorescence (10–1000 μs, the OJ segment) from the unicellular cyanobacterium Synechococcus sp. PCC7942. We show that the added β-Car enhances Chl a fluorescence when it is excited at an intensity of 3000 μmol photons m−2 s−1 but not when excited at 1000 μmol photons m−2 s−1. Since β-Car is an efficient scavenger of 1O *2 , as well as a quencher of 3Chl a * (precursor of 1O *2 ), both of which are more abundant at higher excitations, we assume that the higher Chl a fluorescence in its presence signifies a protective effect against photo-oxidative damages of Chl proteins. The protective effect of added β-Car is not observed in O2-depleted cell suspensions. Lastly, in contrast to β-Car, a water-insoluble molecule, a water-soluble scavenger of 1O *2 , histidine, provides no protection to Chl proteins during the same time period (10–1000 μs).
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Abbreviations
- β-Car:
-
β-Carotene
- Chl:
-
Chlorophyll
- DCMU:
-
3-(3,4-Dichlorophenyl)-1,1-dimethylurea
- DMSO:
-
Dimethyl sulfoxide
- GO:
-
Glucose oxidase
- PS I, PS II:
-
Photosystem I, photosystem II
- PQ-pool:
-
Plastoquinones shuttling electrons between PS II and PS I
- ROS:
-
Reactive oxygen species
References
Allakhverdiev SI, Murata N (2004) Environmental stress inhibits the synthesis de novo of proteins involved in the photodamage-repair cycle of photosystem II in Synechocystis sp. PCC 6803. Biochim Biophys Acta 1657:23–32
Asada K (1999) The water–water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Ann Rev Plant Physiol Plant Mol Biol 50:601–639
Belyaeva NE, Schmitt F-J, Steffen R, Paschenko VZ, Riznichenko GY, Chemeris YK, Renger G, Rubin AB (2008) PS II model-based simulations of single turnover flash-induced transients of fluorescence yield monitored within the time domain of 100 ns-10 s on dark-adapted Chlorella pyrenoidosa cells. Photosynth Res 98:105–119
Belyaeva NE, Schmitt F-J, Paschenko VZ, Riznichenko GY, Rubin AB, Renger G (2011) PS II model based analysis of transient fluorescence yield measured on whole leaves of Arabidopsis thaliana after excitation with light flashes of different energies. BioSystems 103:188–195
Belyaeva NE, Schmitt F-J, Pachenko VZ, Riznichenko GY, Rubin AB (2015) Modeling of the redox state dynamics 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 125:123–140
Blankenship R, McGuire A, Sauer K (1975) Chemically induced dynamic electron polarization in chloroplasts at room temperature: evidence for triplet state participation in photosynthesis. Proc Natl Acad Sci USA 72:4943–4947
Broser M, Gabdulkhakov A, Kern J, Guskov A, Müh F, Saenger W, Zouni A (2010) Crystal structure of monomeric photosystem II from Thermosynechococcus elongatus at 3.6-Å resolution. J Biol Chem 285:26255–26262
Carbonera D, Agostini G, Morosinotto T, Bassi R (2005) Quenching of chlorophyll triplet states by carotenes in reconstituted Lhca4 subunit of peripheral light-harvesting complex of photosystem I. Biochemistry 44:8337–8346
Cazzaniga S, Li Z, Niyogi KK, Bassi R, Dall’Osto L (2012) The Arabidopsis szl1 mutant reveals a critical role of β-carotene in photosystem I photoprotection. Plant Physiol 159:1745–1758
Croce R, Mozzo M, Morosinotto T, Romeo A, Hienerwadel R, Bassi R (2007) Singlet and triplet state transitions of carotenoids in antenna complexes of higher-plant photosystem I. Biochemistry 46:3846–3855
Demmig-Adams B, Stewart JJ, Adams WW III (2014) Chloroplast photoprotection and the trade-off between abiotic and biotic defense. In: Demmig-Adams B, Garab G, Adams W, Govindjee (eds) Non-photochemical quenching and energy dissipation in plants, algae and cyanobacteria. Advances in photosynthesis and respiration, vol 40. Springer, Dordrecht, pp 632–643
Di Mascio P, Kaiser S, Sies H (1989) Lycopene as the most efficient biological carotenoid singlet oxygen quencher. Arch Biochem Biophys 274:532–538
Dominy P, Williams WP (1987) The role of respiratory electron flow in the control of excitation energy distribution in blue-green algae. Biochim Biophys Acta 982:264–274
Domonkos I, Kis M, Gombos Z, Ughy B (2013) Carotenoids, versatile components of oxygenic photosynthesis. Prog Lipid Res 52:539–561
Edelman M, Mattoo AK (2008) D1-protein dynamics in photosystem II: the lingering enigma. Photosynth Res 98:609–620
Edge R, Truscott DG (1999) Carotenoid radicals and the interaction of carotenoids with active oxygen species. In: Frank HA, Young AJ, Britton G, Cogdell RJ (eds) The photochemistry of carotenoids. Advances in photosynthesis and respiration, vol 8. Springer, Dordrecht, pp 223–244
Edge R, Land EJ, McGarvey DJ, Burke M, Truscott TG (2000) The reduction potential of the β-carotene•+/β-carotene couple in an aqueous micro-heterogeneous environment. FEBS Lett 471:125–127
Flors C, Fryer MJ, Waring J, Reeder B, Bechtold U, Mullinaux PM, Nonell S, Wilson MT, Baker NR (2006) Imaging the production of singlet oxygen in vivo using a new fluorescent sensor, Singlet Oxygen Sensor Green. J Exp Bot 57:1725–1734
Frank HA, McLean MB, Sauer K (1979) Triplet states in photosystem I of spinach chloroplasts and subchloroplast particles. Proc Natl Acad Sci USA 76:5124–5128
Fryer MJ, Oxborough K, Mullineaux PM, Baker NR (2002) Imaging of photo-oxidative stress responses in leaves. J Exp Bot 53:1249–1254
Govindjee (1995) Sixty-three years since Kautsky: chlorophyll a fluorescence. Aust J Plant Physiol (Funct Plant Biol) 22:131–160
Hanley J, Deligiannakis Y, Pascal A, Faller P, Rutherford AW (1999) Carotenoid oxidation in photosystem II. Biochemistry 38:8189–8195
Hideg E, Vass I (1995) Singlet oxygen is not produced in photosystem I under photoinhibitory conditions. Photochem Photobiol 62:949–952
Hideg E, Barta C, Kalai T, Vass I, Hideg K, Asada K (2002) Detection of singlet oxygen and superoxide with fluorescent sensors in leaves under stress by photoinhibition or UV radiation. Plant Cell Physiol 43:1154–1164
Ishikita H, Knapp E-W (2005) Redox potentials of chlorophylls and β-carotene in the antenna complexes of photosystem II. J Am Chem Soc 127:1963–1968
Keren N, Berg A, van Kan PJM, Levanon H, Ohad I (1997) Mechanism of photosystem II photo-inactivation and D1 protein degradation at low light: the role of back electron flow. Proc Natl Acad Sci USA 19:1579–1584
Knox JP, Dodge AD (1985) Singlet oxygen and plants. Phytochemistry 24:889–896
Kreslavski VD, Zorina AA, Los DA, Fomina IR, Allakhverdiev SI (2013) Molecular mechanisms of stress resistance of photosynthetic machinery. In: Rout GR, Das AB (eds) Molecular stress physiology of plants, chap 2. Springer, New Delhi, pp 21–51
Krieger-Liszkay A, Fufezan C, Trebst A (2008) Singlet oxygen production in photosystem II and related protection mechanism. Photosynth Res 98:551–564
Lazar D, Jablonsky J (2009) On the approaches in the formulation of a kinetic model of photosystem II. Different approaches lead to different simulations of the chlorophyll a fluorescence transients. J Theor Biol 257:260–269
Mamedov M, Govindjee, Nadtochenko V, Semenov A (2015) Primary electron transfer processes in photosynthetic reaction centers from oxygenic organisms. Photosynth Res 125:51–63
Murata N, Allakhverdiev SI, Nishiyama Y (2012) The mechanism of photoinhibition in vivo: re-evaluation of the roles of catalase, α-tocopherol, non-photochemical quenching, and electron transport. Biochim Biophys Acta 1817:1127–1133
Nishiyama Y, Allakhverdiev SI, Yamamoto H, Hayashi H, Murata N (2004) Singlet oxygen inhibits the repair of photosystem II by suppressing the translation elongation of the D1 protein in Synechocystis sp. PCC 6803. Biochemistry 43:11321–11330
Ostrumov EE, Scholes GD, Govindjee (2014) Photophysics of photosynthetic pigment–protein complexes. In: Demmig-Adams B, Garab G, Adams W, Govindjee (eds) Non-photochemical quenching and energy dissipation in plants, algae and cyanobacteria. Advances in photosynthesis and respiration, vol 40. Springer, Dordrecht, pp 97–128
Papageorgiou GC (2012) Fluorescence emission from the photosynthetic apparatus. In: Eaton-Rye JJ, Tripathy BC, Sharkey TD (eds) Photosynthesis: plastid biology, energy conversion and carbon assimilation. Advances in photosynthesis and respiration, vol 34. Springer, Dordrecht, pp 415–443
Papageorgiou GC, Govindjee (2014) The non-photochemical quenching of the electronically excited state of chlorophyll a in plants: definitions, timelines, viewpoints, open questions. In: Demmig-Adams B, Garab G, Adams WW Jr, Govindjee (eds) Non-photochemical quenching and energy dissipation in plants, algae and cyanobacteria. Advances in photosynthesis and respiration, vol 40. Springer, Dordrecht, pp 1–44
Papageorgiou G, Isaakidou J, Argoudelis C (1972) Structure-dependent control of chlorophyll a excitation density: the role of oxygen. FEBS Lett 25:139–142
Papageorgiou GC, Tsimilli-Michael M, Stamatakis K (2007) The fast and slow kinetics of chlorophyll a fluorescence induction in plants, algae and cyanobacteria: a viewpoint. Photosynth Res 94:275–290
Pospišil P, Prasad A (2014) Formation of singlet oxygen and protection against its oxidative damage in photosystem II under abiotic stress. J Photochem Photobiol B 137:39–48
Ramel F, Mialoundama AS, Havaux M (2013) Nonenzymic carotenoid oxidation and photooxidative stress signaling in plants. J Exp Bot 64:799–805
Rehman AU, Cser K, Sass L, Vass I (2013) Characterization of singlet oxygen production and its involvement in photodamage of photosystem II in the cyanobacterium Synechocystis PCC 6803 by histidine-mediated chemical trapping. Biochim Biophys Acta 1827:689–698
Rippka R, Deruelles J, Waterbury JB, Herdman M, Stanier RT (1979) Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J Gen Microbiol 111:1–61
Schansker G, Tóth SZ, Holzwarth AR, Garab G (2014) Chlorophyll a fluorescence: beyond the limits of the Q(A) model. Photosynth Res 120:43–58
Schlodder E, Cetin M, Byrdin M, Terekhova I, Karapetyan NV (2005) P700+-and 3P700-induced quenching of the fluorescence at 760 nm in trimeric photosystem I complexes from the cyanobacterium Arthrospira platensis. Biochim Biophys Acta 1706:53–67
Schlodder E, Shubin VV, El-MohsnawyE Roegner M, Karapetyan NV (2007) Steady-state and transient polarized absorption spectroscopy of photosystem I complexes from the cyanobacteria Arthrospira platensis and Thermosynechococcus elongatus. Biochim Biophys Acta 1767:732–741
Shuvalov VA (1976) The study of the primary photoprocesses in photosystem I of chloroplasts. Recombination luminescence, Chl triplet state and triplet-triplet annihilation. Biochim Biophys Acta 430:113–121
Sinha RK, Komenda J, Knoppova J, Sedlanova M, Pospisil P (2011) Small CAB-like proteins prevent formation of singlet oxygen in the damaged photosystem II complex of the cyanobacterium Synechocystis sp. PCC 6803. J Exp Bot 35:806–818
Stamatakis K, Tsimilli-Michael M, Papageorgiou GC (2014) On the question of the light-harvesting role of β-carotene in photosystem II and photosystem I core complexes. Plant Physiol Biochem 81:121–127
Stirbet A, Govindjee (2011) On the relation between the Kautsky effect (chlorophyll a fluorescence induction) and photosystem II: basics and applications of the OJIP fluorescence transient. J Photochem Photobiol B: Biol 104:236–257
Strasser RJ, Srivastava A, Tsimilli-Michael M (2004) The fluorescence transient as a tool to characterize and screen photosynthetic samples. In: Papageorgiou GC, Govindjee (eds) Chlorophyll a fluorescence: a signature of photosynthesis, vol 19., Advances in photosynthesis and respirationSpringer, Dordrecht, pp 321–362
Telfer A (2014) Singlet oxygen production by photosystem II under light stress: mechanism, detection and the protective role of β-carotene. Plant Cell Physiol 55:1216–1223
Telfer A, Bishop SM, Phillips D, Barber J (1994) Isolated photosynthetic reaction center of photosystem II as a sensitizer for the formation of singlet oxygen. Detection and quantum yield determination using a chemical trapping technique. J Biol Chem 269:13244–13253
Triantaphyllidès C, Havaux M (2009) Singlet oxygen in plants: production, detoxification and signaling. Trends Plant Sci 14:219–228
Tsimilli-Michael M, Stamatakis K, Papageorgiou GC (2009) Dark-to-light transition in Synechococcus sp. PCC 7942 cells studied by fluorescence kinetics assesses plastoquinone redox poise in the dark and photosystem II fluorescence component and dynamics during state 2 to state 1 transition. Photosynth Res 99:243–255
Tyystjaervi E (2013) Photoinhibition of photosystem II. Int Rev Cell Mol Biol 300:243–303
Van Mieghem FJE, Nitschke W, Mathis P, Rutherford AW (1989) The influence of the quinone–iron electron acceptor complex on the reaction centre photochemistry of photosystem II. Biochim Biophys Acta 977:207–214
Vass I (2012) Molecular mechanisms of photodamage in the photosystem II complex. Biochim Biophys Acta 1817:209–217
Vass I, Styring S, Hundal T, Koivuniemi A, Aro EM, Andersson B (1992) Reversible and irreversible intermediates during photoinhibition of photosystem II: stable reduced Q A species promote chlorophyll triplet formation. Proc Natl Acad Sci USA 89:1408–1412
Velthuys BR (1981) Electron-dependent competition between plastoquinone and inhibitors for binding to photosystem II. FEBS Lett 126:277–281
Vredenberg W (2015) A simple routine for the quantitative analysis of light and dark kinetics of photochemical and non-photochemical quenching of chlorophyll fluorescence in intact leaves. Photosynth Res 124:87–106
Vrettos JS, Stewart DH, de Paula JC, Brudwig GW (1999) Low temperature optical and resonance Raman spectra of a carotenoid cation radical in Photosystem II. J Phys Chem B 103:6403–6406
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Govindjee thanks for a visiting professorship at the School of Life Sciences, Jawaharlal Nehru University, New Delhi, during the preparation of this manuscript.
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Stamatakis, K., Papageorgiou, G.C. & Govindjee Effects of exogenous β-carotene, a chemical scavenger of singlet oxygen, on the millisecond rise of chlorophyll a fluorescence of cyanobacterium Synechococcus sp. PCC 7942. Photosynth Res 130, 317–324 (2016). https://doi.org/10.1007/s11120-016-0255-9
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DOI: https://doi.org/10.1007/s11120-016-0255-9