Abstract
Thermo-optically induced structural reorganizations have earlier been identified in isolated LHCII, the main chlorophyll a/b light harvesting complexes of Photosystem II, and in granal thylakoid membranes [Cseh et al. (2000) Biochemistry 39: 15250–15257; Garab et al. (2002) Biochemistry 41: 15121–15129]. According to the thermo-optic mechanism, structural changes can be induced by fast, local thermal transients due to the dissipation of excess excitation energy. In this paper, we analyze the temperature and light-intensity dependencies of thermo-optically induced reversible and irreversible reorganizations in the chiral macrodomains of lamellar aggregates of isolated LHCII and of granal thylakoid membranes. We show that these structural changes exhibit non-Arrhenius type of temperature dependencies, which originate from the ‘combination’ of the ambient temperature and the local thermal transient. The experimental data can satisfactorily be simulated with the aid of a simple mathematical model based on the thermo-optic effect. The model also predicts, in good accordance with experimental data published earlier and presented in this paper, that the reorganizations depend linearly on the intensity of the excess light, a unique property that is probably important in light adaptation and photoprotection of plants.
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Abbreviations
- CD:
-
circular dichroism
- Chl:
-
chlorophyll
- LHC II:
-
light-harvesting chlorophyll a/b pigment-protein complex
- NPQ:
-
non-photochemical quenching
- psi:
-
polymer- and salt-induced
- PS II:
-
Photosystem II
References
JF Allen J Forsberg (2001) ArticleTitleMolecular recognition in thylakoid structure and function Trends Plant Sci 6 317–326 Occurrence Handle10.1016/S1360-1385(01)02010-6 Occurrence Handle11435171
JM Anderson B Andersson (1988) ArticleTitleThe dynamic photosynthetic membrane and regulation of solar-energy conversion Trends Biochem Sci 13 351–355 Occurrence Handle10.1016/0968-0004(88)90106-5 Occurrence Handle3072714
JF Anderson J Forsberg (2003) ArticleTitleRedox regulation of thylakoid protein phosphorylation Antioxidants Redox Signaling 5 55–67 Occurrence Handle10.1089/152308603321223540 Occurrence Handle12626117
V Barzda A Istokovics I Simidjiev G Garab (1996) ArticleTitleStructural flexibility of chiral macroaggregates of light-harvesting chlorophyll a/b pigment-protein complexes. Light-induced reversible structural changes associated with energy dissipation Biochemistry 35 8981–8985 Occurrence Handle10.1021/bi960114g Occurrence Handle8688435
V Barzda RC Jennings G Zucchelli G Garab (1999) ArticleTitleKinetic analysis of the light-induced fluorescence quenching in light-harvesting chlorophyll a/b pigment–protein complex of Photosystem II Photochem Photobiol 70 751–759 Occurrence Handle10.1562/0031-8655(1999)070<0751:KAOTLI>2.3.CO;2
V Barzda L Mustárdy G Garab (1994) ArticleTitleSize dependency of circular-dichroism in macroaggregates of photosynthetic pigment–protein complexes Biochemistry 33 10837–10841 Occurrence Handle10.1021/bi00201a034 Occurrence Handle8075086
V Barzda CJ Grauw Particlede J Vroom FJ Kleima R Grondelle Particlevan H Amerongen Particlevan HC Gerritsen (2001) ArticleTitleFluorescence lifetime heterogeneity in aggregates of LHCII revealed by time-resolved microscopy Biophys J 81 538–546 Occurrence Handle11423435
EJ Boekema JFL Breemen Particlevan H Roon Particlevan JP Dekker (2000) ArticleTitleArrangement of Photosystem II supercomplexes in crystalline macrodomains within the thylakoid membrane of green plant chloroplasts J Mol Biol 301 1123–1133 Occurrence Handle10.1006/jmbi.2000.4037 Occurrence Handle10966810
Z Cseh S Rajagopal T Tsonev M Busheva E Papp G Garab (2000) ArticleTitleThermooptic effect in chloroplast thylakoid membranes. Thermal and light stability of pigment arrays with different levels of structural complexity Biochemistry 39 15250–15257 Occurrence Handle10.1021/bi001600d Occurrence Handle11106505
JP Dekker EJ Boekema (2005) ArticleTitleSupramolecular organization of thylakoid membrane proteins in green plants Biochim Biophys Acta 1706 12–39 Occurrence Handle15620363
AG Dobrikova Z Várkonyi SB Krumova L Kovács GK Kostov SJ Todinova MC Busheva SG Taneva G Garab (2003) ArticleTitleStructural Rearrangements in chloroplast thylakoid membranes revealed by differential scanning calorimetry and circular dichroism spectroscopy. Thermo-optic effect Biochemistry 42 11272–11280 Occurrence Handle10.1021/bi034899j Occurrence Handle14503877
G Garab A Faludi-Dániel JC Sutherland G Hind (1988a) ArticleTitleMacroorganization of chlorophyll a/b light harvesting complex in thylakoids and aggregates-information from circular differential scattering Biochemistry 27 2425–2430 Occurrence Handle10.1021/bi00407a027
G Garab RC Leegood DA Walker JC Sutherland G Hind (1988b) ArticleTitleReversible changes in macroorganization of the light-harvesting chlorophyll a/b pigment protein comlex detected by circular dichroism Biochemistry 27 2430–2434 Occurrence Handle10.1021/bi00407a028
G Garab Z Cseh L Kovács S Rajagopal Z Várkonyi M Wentworth L Mustárdy A Dér AV Ruban E Papp A Holzenburg P Horton (2002) ArticleTitleLight-induced trimer to monomer transition in the main light-harvesting antenna complex of plants: Thermo-optic mechanism Biochemistry 41 15121–15129 Occurrence Handle12484748
W Grudzinski Z Krupa M Garstka W Maksymiec TE Swartz WI Gruszecki (2002) ArticleTitleConformational rearrangements in light-harvesting complex II accompanying light-induced chlorophyll a fluorescence quenching Biochim Biophys Acta 1554 108–117 Occurrence Handle12034476
W Grudzinski M Matula J Sielewiesiuk P Kernen Z Krupa WI Gruszecki (2001) ArticleTitleEffect of 13-cis violaxanthin on organization of light harvesting complex II in monomolecular layers Biochim Biophys Acta 1503 2091–302
EE Gussakovsky V Barzda Y Shahak G Garab (1997) ArticleTitleIrreversible disassembly of chiral macrodomains in thylakoids due to photoinhibition Photosynth Res 51 119–126 Occurrence Handle10.1023/A:1005775720376
JK Holm Z Várkonyi L Kovács D Posselt G Garab (2005) ArticleTitleThermo-optically induced reorganizations in the main light harvesting antenna of plants. II: indications for the role of LHCII-only macrodomains in thylakoids Photosynth Res 86 275–282
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
P Horton AV Ruban AJ Young (1999) Regulation of the structure and function of the light-harvesting complexes of Photosystem II by the xanthophyll cycle Frank HA (Eds) Advances in Photosynthesis. The Photochemistry of Carotenoids Kluwer Academic Publishers Dordrecht/Boston/London 271–291
A Istokovics I Simidjiev F Lajkó G Garab (1997) ArticleTitleCharacterization of the light induced reversible changes in the chiral macroorganization of the chromophores in chloroplast thylakoid membranes. Temperature dependence and effect of inhibitors Photosynth Res 54 45–53 Occurrence Handle10.1023/A:1005891708054
E Iwaszko A Wardak Z Krupa WI Gruszecki (2004) ArticleTitleIon transport across model lipid membranes containing light-harvesting complex II: an effect of light J Photochem Photobiol 74 13–21 Occurrence Handle10.1016/j.jphotobiol.2004.01.005
RC Jennings FM Garlaschi G Zucchelli (1991) ArticleTitleLight-induced fluorescence quenching in the light-harvesting chlorophyll a/b protein complex Photosynth Res 27 57–64 Occurrence Handle10.1007/BF00029976
J Leng LB Li TY Kuang (2003) ArticleTitleThe composition and spectral properties of three different forms of light-harvesting complex II Sci China C-Life Sci 46 464–473 Occurrence Handle10.1360/02yc0195
XP Li O Bjorkman C Shih AR Grossman M Rosenquist S Jansson KK Niyogi (2000) ArticleTitleA pigment-binding protein essential for regulation of photosynthetic light harvesting Nature 403 391–395 Occurrence Handle10667783
C Lunde PE Jensen A Haldrup J Knoetzel HV Scheller (2000) ArticleTitleThe PSI-H subunit of Photosystem I is essential for state transitions in plant Photosynthesis Nature 408 613–615 Occurrence Handle11117752
A Pandit HR Ma IHM Stokkum Particlevan M Gruebele R Grondelle Particlevan (2002) ArticleTitleTime-resolved dissociation of the light-harvesting 1 complex of Rhodospirillum rubrum, studied by infrared laser temperature jump Biochemistry 41 15115–15120 Occurrence Handle10.1021/bi0269005 Occurrence Handle12484747
H Rogl W Kühlbrandt A Barth (2003) ArticleTitleLight-induced changes in the chemical bond structure of light-harvesting complex II probed by FTIR spectroscopy Biochemistry 42 10223–10228 Occurrence Handle10.1021/bi034114+ Occurrence Handle12939150
D Rutkauskas V Novoderezkhin RJ Cogdell R Grondelle Particlevan (2004) ArticleTitleFluorescence spectral fluctuations of single LH2 complexes from Rhodopseudomonas acidophila strain 10050 Biochemistry 43 4431–4438 Occurrence Handle10.1021/bi0497648 Occurrence Handle15078088
I Simidjiev V Barzda L Mustárdy G Garab (1997) ArticleTitleIsolation of lamellar aggregates of the light-harvesting chlorophyll a/b protein complex of Photosystem II with long-range chiral order and structural flexibility Anal Biochem 250 169–175 Occurrence Handle10.1006/abio.1997.2204 Occurrence Handle9245435
I Simidjiev V Barzda L Mustárdy G Garab (1998) ArticleTitleRole of thylakoid lipids in the structural flexibility of lamellar aggregates of the isolated light-harvesting chlorophyll a/b complex of Photosystem II Biochemistry 37 4169–4173 Occurrence Handle10.1021/bi972726m Occurrence Handle9521738
I Simidjiev Z Várkonyi G Garab (2004) Aggregates of LHCII, LHCII-lipid macro-assemblies with light-inducible structural transition Carpentier R (Eds) Photosynthesis Research Protocols Humana Press Totowa 105–115
SG Taneva I Simidjiev G Garab A Muga (1998) Thermal stability and conformational properties of lamellar macroaggregats of LHCII Garab G (Eds) Photosynthesis: Mechanisms and effects Kluwer Academic Publishers Dordrecht, The Netherlands 325–328
SZ Tóth G Schansker J Kissimon L Kovács G Garab RJ Strasser (2005) ArticleTitleBiophysical studies of Photosystem II-related recovery processes after a heat pulse in barley seedlings (Hordeum vulgare L.) J Plant Phys 162 181–194 Occurrence Handle10.1016/j.jplph.2004.06.010
M Wentworth AV Ruban P Horton (2004) ArticleTitleThe functional significance of the monomeric and trimeric states of the Photosystem II light harvesting complexes Biochemistry 43 501–509 Occurrence Handle10.1021/bi034975i Occurrence Handle14717605
WP Williams (1998) The physical properties of thylakoid membrane lipids and their relation to photosynthesis P-A Siegenthaler N Murata (Eds) Advances in Photosynthesis. Lipids in Photosynthesis Kluwer Academic Publishers Dordrecht, The Netherlands 103–118
DH Yang H Paulsen B Andersson (2000) ArticleTitleThe N-terminal domain of the light-harvesting chlorophyll a/b-binding protein complex (LHCII) is essential for its acclimative proteolysis FEBS Lett 466 385–388 Occurrence Handle10.1016/S0014-5793(00)01107-8 Occurrence Handle10682866
H Zer M Vink N Keren HG Dilly-Hartwig H Paulsen RG Herrmann B Andersson I Ohad (1999) ArticleTitleRegulation of thylakoid protein phosphorylation at the substrate level: reversible light-induced conformational changes expose the phosphorylation site of the light-harvesting complex II Proc Natl Acad Sci USA 96 8277–8282 Occurrence Handle10.1073/pnas.96.14.8277 Occurrence Handle10393985
H Zer M Vink S Shochat RG Herrmann B Andersson I Ohad (2003) ArticleTitleLight affects the accessibility of the thylakoid light harvesting complex II, (LHCII) phosphorylation site to the membrane protein kinase(s) Biochemistry 42 728–738 Occurrence Handle10.1021/bi020451r Occurrence Handle12534285
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Cseh, Z., Vianelli, A., Rajagopal, S. et al. Thermo-optically Induced Reorganizations in the Main Light Harvesting Antenna of Plants. I. Non-Arrhenius Type of Temperature Dependence and Linear Light-intensity Dependencies. Photosynth Res 86, 263–273 (2005). https://doi.org/10.1007/s11120-005-5104-1
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DOI: https://doi.org/10.1007/s11120-005-5104-1