Abstract
The effect of alterations of lipid phase order of thylakoid membranes on the thermosensitivity of photosystem I (PS I) and photosystem II (PS II) was studied. Plant sterols stigmasterol and cholesterol were applied to decrease the fluidity in isolated membranes. After sterol treatment, a decrease of the temperature of 50 % inhibition of PSII activity was observed. Heat stress-induced stimulation of PSI-mediated electron transport rate was registered for control, but not for sterol-treated membranes. Effect of altered lipid order on oxygen evolving complex was evaluated by means of flash oxygen yields revealing changes in the stoichiometry of PSIIα and PSIIβ centers. The effect of sterol incorporation on the changes in the thermotropic behavior of the main pigment-protein complexes was studied by differential scanning calorimetry (DSC). DSC traces of control thylakoids in the temperature range 20–98 °C exhibited several irreversible endothermic transitions. Incorporation of cholesterol and stigmasterol results in superimposition of the transitions and only two main bands could be resolved. While high temperature band peaks at the same temperature after treatment with both sterols, the band that combines low temperature transitions shows different melting temperature (Tm): 70 °C for stigmasterol- and 65 °C for cholesterol-treated membranes. The data presented here emphasise the crucial role of lipid order for the response of thylakoids to high temperatures, mediated not only by changes in the fluidity of bulk lipid phase as result of sterol incorporation but also by changes in the thermotropic properties of pigment-protein complexes.
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References
Bernsdorff C and Winter R (2003). Differential properties of the sterols cholesterol, ergosterol, β—sitosterol, trans-7-dehydrocholesterol, stigmasterol and lanosterol on DPPC bilayer order. J. Phys. Chem. 107: 10658–10664.
Bukhov NG and Carpentier R (2000). Heterogeneity of photosystem II reaction centers as influenced by heat treatment of barley leaves. Physiol. Plant. 110: 279–285.
Bukhov NG and Mohanty P (1999). Elevated temperature stress effects on photosystems: Characterization and evaluation of the nature of heat induced impairments. In: Concepts of Photobiology: Photosynthesis and Photomorphogenesis (Eds. Singhal G.S., Renger G., Sopory S.K., Irgang K-D., Govindjee ), Narosa Publishing House, New Delhi, India, pp. 617–648.
Busheva M, Velitchkova M, Markova Tz and Zanev Y (1998). Effects of cholesterol and benzyl alcohol on fluorescence transients of thylakoids. J. Photochem. Photobiol. B 42: 240–244.
Dobrikova A, Tuparev N, Krasteva I, Busheva M and Velitchkova M (1997). Artificial alteration of fluidity of pea thylakoid membranes and its effect on energy distribution between both photosystems. Z. Naturforsch. 52c: 475–480.
Cramer WA, Whitmarsh J and Low PS (1981). Differential scanning calorimetry of chloroplast membranes: Identification of an endothermic transition associated with the water-splitting complex of photosystem II, Biochemistry 20: 157–162.
Ford RC and Barber J (1980). The use of diphenylhexatriene to monitor the fluidity of the thylakoid membrane. Photobiochem. Photobiophys. 1: 263–270.
Ford RC and Barber J (1983). Incorporation of sterols into chloroplast thylakoid membranes and its effect on fluidity and function. Planta 158: 35–41.
Ford RC, Yamamoto Y and Barber J (1981). Lipid fluidity and photosynthetic electron flow: Effect of cholesterol. In: Photosynthesis I. Photophysical Processes-Membrane Energization (Ed. Akoyunoglou G), Balaban International Science Services, Philadelphia, Pa., vol. 1, pp. 617–626.
Gounaris K, Brian APR, Quinn PJ and Williams WP (1983). Structural reorganization and functional changes associated with heat-induced phase separation of nonbilayer lipids in chloroplast thylakoid membranes. FEBS Lett. 153: 47–52.
Halling KK and Slotte JP (2004). Membrane properties of plant sterols in phospholipid bilayers as determined by differential scanning calorimetry, resonance energy transfer and detergent-induced solubilization. Biochim. Biophys. Acta 1664: 161–171.
Harwood J (1999). Involvement of chloroplast lipids in the reaction of plants submitted to stress. In: Lipids in Photosynthesis: Structure, Function and Genetics (Eds. Siegenthaler P-A, Murata N), Kluwer Publishers, Dordrecht, Boston, London, pp. 287–302.
Horvath G, Melis A, Hideg E, Droppa M and Vigh L (1987). Role of lipids in the organization and function of photosystem II studied by homogeneous catalytic hydrogenation of thylakoid membranes in situ. Biochim. Biophys. Acta 891: 68–74.
Ivanov A and Velitchkova M (1990). Heat-induced changes in the efficiency of P700 photo-oxidation in pea chloroplast membranes. J. Photochem. Photobiol. B 4: 307–320.
Kanavero E, Tasaka Y, Murata N and Aro E-M (1997). Membrane lipid unsaturation modulates processing of the photosystem II reaction center protein D1 at low temperature. Plant Physiol. 114: 841–849.
Kinosita K, Kataoka R, Kimura Y, Gotoh O and Ikegami A (1981). Dynamic structure of biological membranes as probed by DPH: a nanosecond depolarization study, Biochemistry 20: 4270–4277.
Klyachko-Gurvich GL, Tzoglin LN, Doucha J, Kopetski J, Shebatina (Ryabych) IB and Semenenko VE (1999). Desaturation of fatty acids as an adaptive response to shifts in light intensity. Physiol. Plant. 74: 566–574.
Kok B, Forbush B and McGloin M (1970). Co-operation of charges in photosynthetic O2. I. A linear four step mechanism. Photochem. Photobiol. 11: 457–475.
Kota Z, Horvath LI, Droppa M, Horvath G, Farkas T and Pali T (2002). Protein assembly and heat stability in developing thylakoid membranes during greening. Proc. Natl. Acad. Sci. USA, 99: 12149–12154.
Lichtenthaler HK (1987). Chlorophylls and carotenoids: Pigments of photosynthetic membranes. Methods Enzym. 148:350–382.
Loll B, Kern J, Saenger W, Zouni A and Biesiadka J (2005). Towards complete cofactor arrangement in the 3.0 A resolution structure of photosystem II. Nature 438: 1040–1044.
Moon BY, Higasshi ST, Gombos Z and Murata N (1995). Unsaturation of the membrane lipids of chloroplasts stabilizes the photosynthetic machinery against low-temperature photoinhibition in transgenic tobacco plants. Proc. Natl. Acad. Sci. USA 92: 6219–6223.
Nolan WG, Hopkins JrHP and Kalini SAM (1992). Differential scanning calorimetric investigation of pea chloroplast thylakoids and thylakoid fractions. Arch. Biochem. Biophys. 297: 19–27.
Popova A, Velitchkova M and Zanev Y (2007). Effect of membrane fluidity on photosynthetic oxygen production reactions. Z. Naturforsch. 62c: 253–260.
Raison JK, Roberts JKM and Berry JA (1982). Correlation between the thermal stability of chloroplast (thylakoid) membrane and the composition and fluidity of their polar lipids upon acclimation of the higher plant, Nerium oleander, to growth temperature. Biochim. Biophys. Acta 688: 218–228.
Siegenthaler P-A and Tremolieres A (1998). Role of acyl lipids in the function of photosynthetic membranes in higher plants. In: Lipids in Photosynthesis: Structure, Function and Genetics (Eds. Siegenthaler P-A, Murata N), Kluwer Publishers, Dordrecht, Boston, London, pp. 145–173.
Smith KA, Ardelt BK, Huner NPA, Krol M, Myscich E and Low PS (1989). Identification and partial characterization of the denaturation transition of the light harvesting complex II of spinach chloroplast membrane. Plant Physiol. 90: 492–499.
Smith KA and Low PS (1989). Identification and partial characterization of the denaturation transition of the photosystem II reaction center of spinach chloroplast membranes. Plant Physiol. 90: 575–581.
Sundby C and Andersson B (1985). Temperature induced reversible migration along thylakoid membranes of photosystem II regulates its association with LHCII. FEBS Lett. 191: 24–28.
Sundby S, Melis A, Maenpaa P and Andersson B (1986). Temperature-dependent changes in the antenna size of Photosystem II. Reversible conversion of Photosystem IIa to Photosystem IIb. Biochim. Biophys. Acta 851: 475–483.
Thomas PG, Dominy PJ, Vigh L, Mansourian AR, Quinn PJ and Williams WP (1986). Increased thermal stability of pigment protein complexes of pea thylakoids following catalytic hydrogenation of membrane lipids. Biochim. Biophys. Acta, 849: 131–140.
Thomas PG, Quinn PJ and Williams WP (1986). The origin of photosystem I-mediated electron transport stimulation in heat-stressed chloroplasts. Planta 167: 133–139.
Thompson LK, Sturtevant JM and Brudvig GW (1986). Differential scanning calorimetric studies of photosystem II: Evidence for a structural role for cytochrome b559 in the oxygen-evolving complex. Biochemistry 25: 6161–6169.
Velitchkova M, Popova A and Markova Tz (2001). Effect of membrane fluidity on photoinhibition of isolated thylakoid membranes at room and low temperature. Z. Naturforsch. 56c: 369–374.
Vigh L, Gombos Z, Horvath I and Joo F (1989). Saturation of membrane lipids by hydrogenation induces thermal stability in chloroplast inhibiting the heat-dependent stimulation of photosystem I-mediated electron transport. Biochim. Biophys. Acta, 979: 361–364.
Williams WP (1998). The physical properties of thylakoid membrane lipids and their relation to photosynthesis. In: Lipids in Photosynthesis: Structure, Function and Genetics (Eds. Siegenthaler P-A, Murata N), Kluwer Publishers, Dordrecht, Boston, London, pp. 103–118.
Yamamoto Y, Ford RC and Barber J (1981). Relationship between thylakoid membrane fluidity and the functioning of pea chloroplasts. Effects of cholesteryl hemisuccinate. Plant Physiol. 67: 1069–1072.
Yang C, Boggasch S, Haase W and Paulsen H (2006). Thermal stability of trimeric light-harvesting chlorophyll a/b complex (LHCIIb) in liposomes of thylakoid lipids. Biochim. Biophys. Acta 1757: 1642–1648.
Zeinalov Y (1982). Existence of two different ways for oxygen evolution in photosynthesis and photosynthetic unit concept. Photosynthetica 16: 27–35.
Zeinalov Y (2002). An equipment for investigation of photosynthetic oxygen production reactions. Bulg. J. Plant Physiol. 28: 57–67.
Zeinalov Y (2005). Mechanisms of photosynthetic oxygen evolution and the fundamental hypothesis of photosynthesis. In: Handbook of photosynthesis (Ed. Pessarakly M.), 2nd ed. CRC Press, Taylor and Francis Group, Boca Raton, FL, USA, pp. 3–19.
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Velitchkova, M., Lazarova, D. & Popova, A. Response of isolated thylakoid membranes with altered fluidity to short term heat stress. Physiol Mol Biol Plants 15, 43–52 (2009). https://doi.org/10.1007/s12298-009-0004-z
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DOI: https://doi.org/10.1007/s12298-009-0004-z