Abstract
The carotenoid triplet populations associated with the fluorescence emission chlorophyll forms of Photosystem II have been investigated in isolated spinach thylakoid membranes by means of fluorescence detected magnetic resonance in zero field (FDMR). The spectra collected in the 680–690 nm emission range, have been fitted by a global analysis procedure. At least five different carotenoid triplet states coupled to the terminal emitting chlorophyll forms of PS II, peaking at 682 nm, 687 nm and 692 nm, have been characterised. The triplets associated with the outer antenna emission forms, at 682 nm, have zero field splitting parameters |D| = 0.0385 cm−1, |E| = 0.00367 cm−1; |D| = 0.0404 cm−1, |E| = 0.00379 cm−1 and |D| = 0.0386 cm−1, |E| = 0.00406 cm−1 which are very similar to those previously reported for the xanthophylls of the isolated LHC II complex. Therefore the FDMR spectra recorded in this work provide insights into the organisation of the LHC II complex in the unperturbed environment represented by thylakoid membranes. The additional carotenoid triplet populations, detected by monitoring the chlorophyll emission at 687 and 692 nm, are assigned to carotenoids bound to inner antenna complexes and hence attributed to β-carotene molecules.
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Abbreviations
- ADMR:
-
absorbance detected magnetic resonance
- Car:
-
carotenoid
- Chl:
-
chlorophyll
- FDMR:
-
fluorescence detected magnetic resonance
- MIF:
-
microwave induced fluorescence
- ODMR:
-
optically detected magnetic resonance
- PS I:
-
Photosystem I
- PS II:
-
Photosystem II
- ZFS:
-
zero field splitting
References
V Barzda EJG Peterman R Grondelle Particlevan H Amerongen Particlevan (1998) ArticleTitleThe influence on triplet formation in light-harvesting chlorophyll a/b pigment-protein complex II of green plants Biochemistry 37 546–551 Occurrence Handle10.1021/bi972123a Occurrence Handle9425075
R Bassi B Pineau P Dainese J Marquardt (1993) ArticleTitleCarotenoid-binding proteins of Photosystem II J Eur J Biochem 212 297–303 Occurrence Handle8444169
A Ben-Shem F Frolow N Nelson (2003) ArticleTitleCrystal structure of plant Photosystem I Nature 426 630–635 Occurrence Handle14668855
PG Bowers G Porter (1967) ArticleTitleQuantum yield of triplet formation in solutions of chlorophylls Proc R Soc A 296 435–441
WL Butler (1978) ArticleTitleEnergy distribution in the photochemical apparatus of photosyntesis Ann Rev Plant Physiol 29 345–378 Occurrence Handle10.1146/annurev.pp.29.060178.002021
D Carbonera G Giacometti G Agostini (1992a) ArticleTitleFDMR of carotenoid and chlorophyll triplets in light harvesting complex LHC II of spinach Appl Magn Res 3 859–872
D Carbonera G Giacometti G Agostini A Angerhofer V Aust (1992b) ArticleTitleODMR of carotenoid and chlorophyll triplets in CP43 and CP47 complexes of spinach Chem Phys Lett 194 275–281 Occurrence Handle10.1016/0009-2614(92)86051-I
D Carbonera P Collareta G Giacometti (1997) ArticleTitleThe P700 triplet state in intact environment Biochim Biophys Acta Bioenerg 1322 115–128 Occurrence Handle10.1016/S0005-2728(97)00068-6
R Croce G Zucchelli FM Garlaschi RC Jennings (1998) ArticleTitleA thermal broadening study of the antenna chlorophylls in PS I-200, LHC I, and PS I core Biochemistry 37 17355–17360 Occurrence Handle9860850
DL Dexter (1953) ArticleTitleA theory of sensitised luminescence in solids J Chem Phys 21 836–850 Occurrence Handle10.1063/1.1699044
ML Groot EJ Peterman IHM Stokkum Particlevan JP Dekker R Grondelle Particlevan (1994) ArticleTitleTemperature dependent triplet and fluorescence quantum yield of Photosystem II described in a thermodynamic model Biophys J 67 318–330 Occurrence Handle7919002
ML Groot RN Frese F Weerd Particlede K Bromek Å Petterson EJG Peterman IHM Stokkum Particlevan R Grondelle Particlevan JP Dekker (1999) ArticleTitleSpectroscopic properties of the CP43 core antenna protein of Photosystem II Biophys J 77 3328–3340 Occurrence Handle10585955
Hoff AJ (1986) Optically detected magnetic resonance (ODMR) of triplet states in vivo. In: Staehlin LA and Arntzen CJ (eds) Encyclopaedia of Plant Physiology, Photosynthesis II, Vol.13, pp 400–421. New Series.
P Horton AV Ruban RG Walters (1996) ArticleTitleRegulation of light harvesting in green plants Ann Rev Plant Physiol Plant Mol Biol 47 655–684 Occurrence Handle10.1146/annurev.arplant.47.1.655
JA Ihalainen B Gobets K Sznee M Brazzoli R Croce R Bassi R Grondelle Particlevan JE Korppi-Tommola JP Dekker (2000) ArticleTitleEvidence for two spectroscopically different dimers of light-harvesting complex I from green plants Biochemistry 39 8625–8631 Occurrence Handle10913270
T Javorfi G Garab KR Naqvi (2000) ArticleTitleReinvestigation of the triplet-minus-singlet spectrum of chloroplasts Spectrochim Acta A 56 211–214
RC Jennings FM Garlaschi PD Gerola R Etzion-Katz G Forti (1981) ArticleTitleProton-induced grana formation in chloroplast. Distribution of chlorophyll–protein complexes amd Photosystem II photochemistry Biochim Biophys Acta Bionerg 638 100–107 Occurrence Handle10.1016/0005-2728(81)90191-2
R Jennings G Zucchelli R Bassi (1996) Antenna structure and energy transfer in higher plant photosystems J Mattay (Eds) Topics in Current Chemistry NumberInSeriesVol. 177 Spinger-Verlag Berlin, Heidelberg 147–181
H Kramer P Mathis (1980) ArticleTitleQuantum yield and rate of formation of the carotenoid triplet state in photosynthetic structure Biochim Biophys Acta Bioenerg 593 319–329 Occurrence Handle10.1016/0005-2728(80)90069-9
AA Krasnowsky (1992) ArticleTitleDelayed luminescence and phosphorescence of plant pigments Photochem Photobiol 36 733–741
AA Krasnowsky (1994) Biophysics 39 197–211
W Kühlbrandt ND Wang Y Fujiyoshi (1994) ArticleTitleAtomic model of plant light-harvesting complex by electron crystallography Nature 367 614–621 Occurrence Handle8107845
SS Lampoura V Barzda GM Owen AJ Hoff H Amerongen Particlevan (2002) ArticleTitleAggregation of LHC II leads to a redistribution of the triplets over the central xanthophylls in LHC II Biochemistry 41 9139–9144 Occurrence Handle10.1021/bi025724x Occurrence Handle12119029
Z Liu H Yan T Kuang J Zhang L Gui X An W Chang (2004) ArticleTitleCrystal structure of spinach major light-harvesting complex at 2.72 Å resolution Nature 428 287–292 Occurrence Handle15029188
P Mathis WL Butler K Satoh (1979) ArticleTitleCarotenoid triplet state and chlorophyll fluorescence quenching in chloroplasts and subchloroplast particles Photochem Photobiol 30 603–614
E Papagiannakis JT Kennis IHM Stokkum Particlevan RJ Cogdell R van Grondelle (2002) ArticleTitleAn alternative carotenoid-to-bacteriochlorophyll energy transfer pathway in photosynthetic light harvesting Proc Natl Acad Sci USA 99 6017–6022 Occurrence Handle10.1073/pnas.092626599 Occurrence Handle11972067
H Paulsen B Finkenzeller N Kuhlein (1993) ArticleTitlePigments induce folding of light-harvesting chlorophyll a/b-binding protein Eur J Biochem 215 809–816 Occurrence Handle10.1111/j.1432-1033.1993.tb18096.x Occurrence Handle8354287
EJG Peterman FM Dekker R Grondelle Particlevan H Amerongen Particlevan (1995) ArticleTitleChlorophyll a and carotenoid states in light harvesting complex II of higher plants Biophys J 59 2670–3678
EJG Peterman SF Hobe F Calkoen R Grondelle Particlevan H Paulsen H van Amerongen (1996) ArticleTitleLow temperature spectroscopy of monomeric and trimeric form of reconstituted light-harvesting chlorophyll a/b complex Biochim Biophys Acta Bioenerg 1273 171–174 Occurrence Handle10.1016/0005-2728(95)00139-5
FG Plumley GW Schmidt (1987) ArticleTitleReconstitution of Chl a/b light-harvesting complexes. Xanthophyll-dependent reconstitution and energy transfer Proc Nat Acad Sci USA 84 145–150
CP Rijgersberg J Amesz AP Thielen JA Swager (1981) ArticleTitleFluorescence emission spectra of chloroplasts and subchloroplast preparations at low temperature Biochim Biophys Acta Bioenerg 637 272–277 Occurrence Handle10.1016/0005-2728(81)90166-3
AV Ruban JP Dekker P Horton R Grondelle Particlevan (1995) ArticleTitleTemperature dependence of chlorophyll fluorescence from the light harvesting complex II of higher plants Photochem Photobiol 61 216–221
Santabarbara S. and Carbonera D (2005) The carotenoid triplet state associated with the long wavelength emitting chlorophyll forms of Photosystem I in isolated thylakoid membranes. J. Phys. Chem. B in press.
S Santabarbara FM Garlaschi G Zucchelli RC Jennings (1999) ArticleTitleThe effect of excited state population in Photosystem II on the photoinhibition-induced changes in chlorophyll fluorescence parameters Biochim Biophys Acta Bioenerg 1409 165–170 Occurrence Handle10.1016/S0005-2728(98)00159-5
S Santabarbara KV Neverov FM Garlaschi G Zucchelli RC Jennings (2001) ArticleTitleInvolvement of uncoupled antenna chlorophylls in photoinhibition in thylakoids FEBS Lett 491 109–113 Occurrence Handle11226430
S Santabarbara I Cazzalini A Rivadossi FM Garlaschi G Zucchelli RC Jennings (2002a) ArticleTitlePhotoinhibition in vivo and in vitro involves weakly coupled chlorophyll-protein complexes Photochem Photobiol 75 613–618 Occurrence Handle10.1562/0031-8655(2002)075<0613:PIVAIV>2.0.CO;2
S Santabarbara E Bordignon RC Jennings D Carbonera (2002b) ArticleTitleChlorophyll triplet states associated with Photosystem II of thylakoids Biochemistry 41 8184–8194 Occurrence Handle10.1021/bi0201163
S Santabarbara RC Jennings D Carbonera (2003) ArticleTitleAnalysis of Photosystem II triplet states in thylakoids by fluorescence detected magnetic resonance as a function of the reduction state of the primary quinone acceptor Q A Chem Phys 2003 IssueID294 257–267 Occurrence Handle10.1016/S0301-0104(03)00279-9
R Schodel KD Irrgang J Voigt G Renger (1998) ArticleTitleRate of carotenoid triplet formation in solubilised light-harvesting complex II (LHC II) from spinach Biophys J 75 3143–3153 Occurrence Handle9826635
GW Searle TJ Schaafsma (1992) ArticleTitleFluorescence detected magnetic resonance of the primary donor and inner core antenna chlorophyll in Photosystem I reaction centres protein: sign inversion and energy transfer Photosynth Res 32 193–206 Occurrence Handle10.1007/BF00034795
D Siefermann-Harms (1985) ArticleTitleCarotenoids in photosynthesis. I. Location in photosynthetic membranes and light- harvesting function Biochim Biophys Acta 811 325–355
J Sinclair YI Park WS Chow J Anderson (1996) ArticleTitleTarget theory and the photoinactivation of Photosystem II Photos Res 50 33–40 Occurrence Handle10.1007/BF00018219
PJ Smith S Peterson VM Masters T Wydrzynski S Styring E Krausz RJ Pace (2002) ArticleTitleMagneto-optical measurements of the pigments in fully active Photosystem II core complexes from plants Biochemistry 41 1981–1989 Occurrence Handle11827545
R Strasser WL Butler (1977) ArticleTitleFluorescence emission spectra of Photosystem I, Photosystem II and the light-harvesting chlorophyll a/b complex of higher plants Biochim Biophys Acta 462 307–313 Occurrence Handle588570
E Tyystjarvi N King M Hakala EM Aro (1999) ArticleTitleArtificial quenchers of chlorophyll fluorescence do not protect against photoinhibition J Photochem Photobiol B Biol 48 142–147 Occurrence Handle10.1016/S1011-1344(99)00022-6
R Grondelle Particlevan JP Dekker T Gillbro V Sündstrom (1994) ArticleTitleEnergy transfer and trapping in photosynthesis Biochim Biophys Acta Bioenerg 1187 1–65 Occurrence Handle10.1016/0005-2728(94)90166-X
R Vos ParticleVan der D Carbonera AJ Hoff (1991) ArticleTitleMicrowave and optical spectroscopy of carotenoid triplets in light-harvesting complex LHC II of spinach by absorbance-detected magnetic resonance Appl Magn Res 2 179–202
R Vos ParticleVan der EM Franken AJ Hoff (1994) ArticleTitleADMR study of the effect of oligomerisation on the carotenoid triplet and triplet–triplet energy transfer in light harvesting complex II (LHC II) of spinach Biochim Biophys Acta Biogen 1188 243–250
C Wolff HT Witt (1969) ArticleTitleOn metastable states of carotenoids in primary events of photosynthesis Z Naturforsch 24b 1031–1037
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Santabarbara, S., Agostini, G., Heathcote, P. et al. A Fluorescence Detected Magnetic Resonance Investigation of the Carotenoid Triplet States Associated with Photosystem II of Isolated Spinach Thylakoid Membranes. Photosynth Res 86, 283–296 (2005). https://doi.org/10.1007/s11120-005-2840-1
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DOI: https://doi.org/10.1007/s11120-005-2840-1