Abstract
The structural reorganization of pea thylakoid systems in response to osmotic shock in a wide range of temperatures (36–70°C) was studied. At temperatures 40–46°C, the configuration of thylakoid systems changed from a flattened to a nearly round, whereas thylakoids themselves remained compressed. The percentage of thylakoids stacked into grana at 44°C decreased from 71 % in the control to 40 % in experimental samples, reaching 59 % at 48°C. At 44°C and above, thylakoid systems ceased to respond to the osmotic shock by disordering, in contrast to what happened at lower temperatures (36–43°C) and in the control, and retained the configuration inherent in thylakoid systems at these temperatures. At 50°C and above, the packing of thylakoids in grana systems changed, and thylakoids formed extended strands of pseudograna. Simultaneously, single thylakoids formed a network of anastomoses through local fusions. At temperatures of 60–70°C, thylakoid systems appeared as spherical clusters of membrane vesicles with different degree of separation.
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References
Armond, P.A., Björkman, O., Staehelin, L.A.: Dissociation of supramolecular complexes in chloroplast membranes. A manifestation of heat damage to the photosynthetic apparatus.–Biochim. biophys. Acta 601: 433–442, 1980.
Berry, J., Björkman, O.: Photosynthetic response and adaptation to temperature in higher plants.–Annu. Rev. Plant Physiol. 31: 491–543, 1980.
Bilger, W., Schreiber, U.: Chlorophyll luminescence as an indicator of stress-induced damage to the photosynthetic apparatus. Effects of heat stress in isolated chloroplasts.–Photosynth. Res. 25: 161–171, 1990.
Cao, J., Govindjee: Chlorophyll a fluorescence transient as an indicator of active and inactive Photosystem II in thylakoid membranes.–Biochim. biophys. Acta 1015: 180–188, 1990.
Cramer, W.A., Whitmarsh, J., Low, P.S.: Differential scanning calorimetry of chloroplast membranes: identification of an endothermic transition associated with the water-splitting complex of photosystem II.–Biochemistry 20: 157–162, 1981.
Gounaris, K., Brain, A.P.R., Quinn, P.J., Williams, W.P.: Structural and functional changes associated with heat-induced phase separations of non-bilayer lipids in chloroplast thylakoid membranes.–FEBS Lett. 153: 47–52, 1983.
Gounaris, K., Brain, A.P.R., Quinn, P.J., Williams, W.P.: Structural reorganisation of chloroplast thylakoid membranes in response to heat stress.–Biochim. biophys. Acta 766: 198–208, 1984.
Ignat’ev, A.P., Khorobrykh, S.A., Ivanov, B.N.: [Effect of high concentrations of magnesium ions on the rate of electron transport and proton exchange in thylakoid membranes of higher plants.]–Biofizika 46: 1075–1080, 2001. [In Russ.]
Kreslavskiï, V.D., Khristin, M.S.: [After-effect of heat shock on fluorescence induction and low-temperature fluorescence spectra in wheat leaves.]–Biofizika 45: 865–872, 2003. [In Russ.]
Lyutova, M.I., Tikhonov, A.N.: [After-effect of high temperature on photosynthesis and electron transport in wheat leaves.]–Biofizika 28: 284–287, 1983. [In Russ.]
Matos, M.C., Campos, P.S., Ramalho, J.C., Medeira, M.C., Maia, M.I., Semedo, J.M., Marques, N.M., Matos, A.: Photosynthetic activity and cellular integrity of the Andean legume Pachyrhizus ahipa (Wedd.) Parodi under heat and water stress.–Photosynthetica 40: 493–501, 2002.
Molotkovsky, Yu.G., Zheskova, I.M.: The influence of heating on the morphology and photochemical activity of isolated chloroplasts.–Biochem. biophys. Res. Commun. 20: 411–415, 1965.
Semenova, G.A.: The relationship between the transformation of thylakoid acyl lipids and the formation of tubular lipid aggregates visible on fracture faces.–J. Plant Physiol. 155: 669–677, 1999.
Semenova, G.A.: Effect of urea and distilled water on the structure of the thylakoid system.–J. Plant Physiol. 158: 1041–1050, 2001.
Semenova, G.A.: The thylakoid membrane in a wide pH range.–J. Plant Physiol. 159: 613–625, 2002.
Semenova, G.A., Agafonov, A.V., Opanasenko, V.K.: Light-induced reversible local fusions of thylakoid membranes in the presence of dibucaine or tetracaine.–Biochim. biophys. Acta 1285: 29–37, 1996.
Semenova, G.A., Khorobrykh, A.A.: [Structure, functional activity, and lipid composition of pea thylakoid systems during storage at–15 °C.]–Biol. Membr. 18: 259–264, 2001. [In Russ.]
Semenova, G.A., Vasilenko, I., Borovyagin, V.: Structural changes in thylakoid membranes of chilling-resistant and sensitive plants after heating and glycerol dehydration as revealed by 31P NMR and electron microscopy.–Biophys. Chem. 49: 59–69, 1994.
Shutilova, N.I.: [On the mechanism of photosynthetic oxidation of water in a dimeric oxygen-evolving complex of chloroplast photosystem II.]–Biofizika 45: 51–57, 2000. [In Russ.]
Shutilova, N.I., Klimov, V.V., Antropova, T.M., Shnyrov, V.L.: [On the mechanism of thermoinactivation of the oxygen-evolving photosystem II subchloroplast core complex.]–Biokhimiya 57: 1508–1518, 1992. [In Russ.]
Staehelin, L.A.: Chloroplast structure and supramolecular organization of photosynthetic membranes.–In: Staehelin, L.A., Arntzen, C.J. (ed.): Photosynthesis III. Pp. 1–84. Springer-Verlag, Berlin–Heidelberg–New York–Tokyo 1986.
Sundby, C., Melis, A., Mäenpää, P., Andersson, B.: Temperature-dependent changes in the antenna size of Photosystem II: Reversible conversion of Photosystem IIα to Photosystem IIβ.–Biochim. biophys. Acta 851: 475–483, 1986.
Thomas, P.G., Brain, A.P.R., Quinn, P.J., Williams, W.P.: Low pH and phospholipase A2 treatment induce the phase separation of non-bilayer lipids within pea chloroplast membranes.–FEBS Lett. 183: 161–166, 1985.
Thomas, P.G., Quinn, P.J., Williams, W.P.: The origin of photosystem I-mediated electron transport stimulation in heat-stressed chloroplasts.–Planta 167: 133–139, 1986.
Thompson, L.K., Blaylock, R., Sturtevant, J.M., Brudvig, G.W.: Molecular basis of the heat denaturation of photosystem II.–Biochemistry 28: 6686–6695, 1989.
Thompson, L.K., Sturtevant, J.M., Brudvig, G.W.: Differential scanning calorimetric studies of photosystem II: Evidence for a structural role of cytochrome b 559 in the oxygen evolving complex.–Biochemistry 25: 6161–6169, 1986.
Tikhonov, A.N., Ruuge, Ė.K.: [ESR study of electron transport in photosynthetic systems. VII. Effects of temperature on the processes of electron transport between two photosystems and the structural state of chloroplast membrane.]–Mol. Biol. 12: 1028–1036, 1978. [In Russ.]
Yamane, Y., Kashino, Y., Koike, H., Satoh, K.: Increases in the fluorescence F0 level and reversible inhibition of Photosystem II reaction center by high-temperature treatments in higher plants.–Photosynth. Res. 52: 57–64, 1997.
Yamane, Y., Kashino, Y., Koike, H., Satoh, K.: Effects of high temperatures on the photosynthetic systems in spinach: Oxygen-evolving activities, fluorescence characteristics and the denaturation process.–Photosynth. Res. 57: 51–59, 1998.
Yamashita, T., Butler, W.L.: Inhibition of chloroplasts by UV-irradiation and heat-treatment.–Plant Physiol. 43: 2037–2040, 1968.
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This revised version was published online in March 2005 with corrections to the page numbers.
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Semenova, G.A. Structural reorganization of thylakoid systems in response to heat treatment. Photosynthetica 42, 521–527 (2004). https://doi.org/10.1007/S11099-005-0008-z
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DOI: https://doi.org/10.1007/S11099-005-0008-z