Photosynthesis Research

, Volume 44, Issue 3, pp 243–252 | Cite as

The unusually strong stabilizing effects of glycine betaine on the structure and function of the oxygen-evolving Photosystem II complex

  • George C. Papageorgiou
  • Norio Murata


Natural osmoregulatory substances (osmolytes) allow a wide variety of organisms to adjust to environments with high salt and/or low water content. In addition to their role in osmoregulation, some osmolytes protect proteins from denaturation and deactivation by, for example, elevated temperature and chaotropic compounds. A ubiquitous protein-stabilizing osmolyte is glycine betaine (N-trimethyl glycine). Its presence has been reported in bacteria, in particular cyanobacteria, in animals and in plants from higher plants to algae. In the present review we describe the experimental evidence related to the ability of glycine betaine to enhance and stabilize the oxygen-evolving activity of the Photosystem II protein complexes of higher plants and cyanobacteria. The osmolyte protects the Photosystem II complex against dissociation of the regulatory extrinsic proteins (the 18 kD, 23 kD and 33 kD proteins of higher plants and the 9 kD protein of cyanobacteria) from the intrinsic components of the Photosystem II complex, and it also stabilizes the coordination of the Mn cluster to the protein cleft. By contrast, glycine betaine has no stabilizing effect on partial photosynthetic processes that do not involve the oxygen-evolving site of the Photosystem II complex. It is suggested that glycine betaine might act, in part, as a solute that is excluded from charged surface domains of proteins and also as a contact solute at hydrophobic surface domains.

Key words

glycine betaine osmolyte oxygen-evolving complex photosynthesis 


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  1. Åkerlund HE and Jansson C (1981) Localization of a 34,000 and a 23,000 M r polypeptide to the lumenal side of the thylakoid membrane. FEBS Lett 124: 229–232Google Scholar
  2. Arakawa T and Timasheff SN (1982) Stabilization of protein structure by sugars. Biochemistry 21: 6536–6544Google Scholar
  3. Arakawa T and Timasheff SN (1983) Preferential interactions of proteins with solvent components in aqueous amino acid solutions. Arch Biochem Biophys 224: 169–177Google Scholar
  4. Arakawa T and Timasheff SN (1985) The stabilization of proteins by osmolytes. Biophys J 47: 411–414Google Scholar
  5. Azaria-Gabbay R, Tel-Or E and Schönfeld M (1988) Glycine betaine as an osmoregulant and compatible solute in the marine cyanobacterium Spirulina subsalsa. Arch Biochem Biophys 264: 333–339Google Scholar
  6. Bowlus RD and Somero GN (1979) Solute compatibility with enzyme function and structure: Rationales for the selection of osmotic agents and end-products of anaerobic metabolism in marine invertebrates. J Exp Zool 208: 137–152Google Scholar
  7. Brouquisse R, Weigel P, Rhodes D, Yocum CF and Hanson AD (1989) Evidence for a ferredoxin-dependent choline monooxygenase from spinach chloroplast stroma. Plant Physiol 90: 322–329Google Scholar
  8. Brown AD and Simpson JR (1972) Water relations of sugar-tolerant yeasts: The role of intracellular polyols. J Gen Microbiol 72: 589–591Google Scholar
  9. Burnap RL and Sherman LA (1991) Deletion mutagenesis in Synechocystis sp. PCC6803 indicates that the Mn-stabilizing protein of Photosystem II is not essential for O2 evolution. Biochemistry 30: 440–446Google Scholar
  10. Collins KD and Washabaugh MW (1985) The Hofmeister effect and the behaviour of water at interfaces. Quart Rev Biophys 18: 323–422Google Scholar
  11. Coughlan SJ and Heber U (1982) The role of glycine betaine in the protection of spinach thylakoids against freezing stress. Planta 156: 62–69Google Scholar
  12. Csonka LN (1989) Physiological and genetic responses of bacteria to osmotic stress. Microbiol Rev 53: 121–147Google Scholar
  13. Hanson AD, May AM, Grumet R, Bode J, Jamieson GC and Rhodes D (1985) Betaine synthesis in chenopods: Localization in chloroplasts. Proc Natl Acad Sci USA 82: 3678–3682Google Scholar
  14. Incharoensakdi A, Takabe T and Akazawa T (1986) Effect of betaine on enzyme activity and subunit interaction of ribulose-1,5-bisphosphate carboxylase/oxygenase from Aphanothece halophytica. Plant Physiol 81: 1044–1049Google Scholar
  15. Kalosaka K and Papageorgiou GC (1992) Differentiation between the structural and the catalytic roles of chloride in photosynthetic oxygen evolution. In: Murata N (ed) Research in Photosynthesis, Vol II, pp 349–352. Kluwer Academic Publishers, Dordrecht, the NetherlandsGoogle Scholar
  16. Klein MP, Sauer K, Yachandra VK (1993) Perspectives on the structure of the photosynthetic oxygen evolving manganese complex and its relation to the Kok cycle. Photosynth Res 38: 265–277Google Scholar
  17. Kuwabara T and Murata N (1983) Quantitative analysis of the inactivation of photosynthetic oxygen evolution and the release of polypeptides and manganese in the Photosystem II particles of spinach chloroplasts. Plant Cell Physiol 24: 741–747Google Scholar
  18. Ladyman JAR, Hitz WD and Hanson AD (1980) Translocation and metabolism of glycine betaine by barley plants in relation to water stress. Planta 150: 191–196Google Scholar
  19. Laurie S and Stewart GR (1990) The effects of compatible solutes on the heat stability of glutamine synthetase from chickpeas grown under different nitrogen and temperature regimes. J Exp Bot 41: 1415–1422Google Scholar
  20. Mackay MA, Norton R and Borowitzka LJ (1984) Organic osmoregulatory solutes in cyanobacteria. J Gen Microbiol 130: 2177–2191Google Scholar
  21. Mamedov M, Hayashi H, Wada H, Mohanty PS, Papageorgiou GC and Murata N (1991) Glycinebetaine enhances and stabilizes the evolution of oxygen and the synthesis of ATP by cyanobacterial thylakoid membranes. FEBS Lett 294: 271–274Google Scholar
  22. Mamedov M, Hayashi H and Murata N (1993) Effects of glycine betaine and unsaturation of membrane lipids on heat stability of photosynthetic electron-transport and phosphorylation reactions in Synechocystis PCC6803. Biochim Biophys Acta 1142: 1–5Google Scholar
  23. Manetas Y (1990) A re-examination of NaCl effects on phosphoenol pyruvate carboxylase at high (physiological) enzyme concentrations. Physiol Plant 78: 225–229Google Scholar
  24. Miyao M and Murata N (1983) Partial disintegration and reconstitution of the photosynthetic oxygen evolution system: Binding of the 24-kD and 18-kD polypeptides. Biochim Biophys Acta 725: 87–93Google Scholar
  25. Miyao M and Murata N (1984a) Effect of urea on Photosystem II particles: Evidence for an essential role of the 33 kDa polypeptide in photosynthetic oxygen evolution. Biochim Biophys Acta 765: 253–257Google Scholar
  26. Miyao M and Murata N (1984b) Calcium ions can be substituted for the 24-kDa polypeptide in photosynthetic oxygen evolution. FEBS Lett 168: 118–120Google Scholar
  27. Miyao M and Murata N (1984c) Role of the 33-kDa polypeptide in preserving Mn in the photosynthetic oxygen-evolution system and its replacement of chloride ions. FEBS Lett 170: 350–354Google Scholar
  28. Mohanty PS, Hayashi H, Papageorgiou GC and Murata N (1993) Stabilization of the Mn-cluster of the oxygen-evolving complex by glycinebetaine. Biochim Biophys Acta 1144: 92–96Google Scholar
  29. Murata N, Mohanty PS, Hayashi H and Papageorgiou GC (1992) Glycinebetaine stabilizes the association of extrinsic proteins with the photosynthetic oxygen-evolving complex. FEBS Lett 296: 187–189Google Scholar
  30. Nakaya S, Tanaka Y, Yoshioka Y and Yasuda N (1991) Interaction of water with nitrogenous compounds in human urine as studied by nuclear magnetic resonance spectroscopy. J Iwate Med Asc 43: 311–320Google Scholar
  31. Nishiyama Y, Kovacs E, Lee CB, Hayashi H, Watanabe T and Murata N (1993) Photosynthetic adaptation to high temperature associated with thylakoid membranes of Synechococcus PCC7002. Plant Cell Physiol 34: 337–343Google Scholar
  32. Ono T and Inoue Y (1984) Ca2+-dependent restoration of O2-evolving activity in CaCl2-washed PS II particles depleted of 33, 24 and 16 kDa proteins. FEBS Lett 168: 281–286Google Scholar
  33. Papageorgiou GC, Fujimura Y and Murata N (1991) Protection of the oxygen-evolving Photosystem II complex by glycine betaine. Biochim Biophys Acta 1057: 361–366Google Scholar
  34. Pollard A and Wyn Jones RG (1979) Enzyme activities in concentrated solutions of glycinebetaine and other solutes. Planta 144: 291–298Google Scholar
  35. Renger G (1993) Water cleavage by solar radiation — an inspiring challenge of photosynthesis research. Photosynth Res 38: 229–247Google Scholar
  36. Santoro MM, Liu Y, Khan SMA, Hou L-X and Bolen DW (1992) Increased thermal stability of proteins in the presence of naturally occurring osmolytes. Biochemistry 31: 5278–5283Google Scholar
  37. Schobert (1977) Is there an osmotic regulatory mechanism in algae and higher plants? J Theor Biol 68: 17–26Google Scholar
  38. Schopf JW and Walter MR (1982) Origin and early evolution of cyanobacteria: The geological evidence. In: Carr NG and Whitton BA (eds) The Biology of Cyanobacteria, pp 543–564. Blackwell Scientific Publications, OxfordGoogle Scholar
  39. Shen JR and Inoue Y (1993) Binding and functional properties of two new extrinsic components, cytochrome C 550 and a 12-kDa protein, is cynobacterial Photosystem II. Biochemistry 32: 1825–1832Google Scholar
  40. Shen JR, Ikeuchi M and Inoue Y (1992) Stoichiometric association of extrinsic cytochrome C 550 and 12 kDa protein with a highly purified oxygen-evolving Photosystem II core complex from Synechococcus vulcanus. FEBS Lett 301: 145–149Google Scholar
  41. Stamatakis C and Papageorgiou GC (1993) Stabilization of Photosystem II particles isolated from the thermophilic cyanobacterium Phormidium laminosum with glycinebetaine and glycerol. Biochim Biophys Acta 1183: 333–338Google Scholar
  42. Stewart AC, Ljungberg U, Åkerlund HE and Andersson B (1985a) Studies on the polypeptide composition of the cyanobacterial oxygen-evolving complex. Biochim Biophys Acta 808: 353–362Google Scholar
  43. Stewart AC, Siczkowski M and Ljungberg U (1985b) Glycerol stabilizes oxygen evolution and maintains binding of a 9 kDa polypeptide in Photosystem II particles from the cyanobacterium Phormidium laminosum. FEBS Lett 193: 175–179Google Scholar
  44. Tinoco IJr, Sauer K and Wang JC (1978) Physical Chemistry: Principles and Applications in Biological Sciences, Prentice Hall Inc, Englewood Cliffs, NJ, USAGoogle Scholar
  45. Van Gorkom HJ and Schelvis JPM (1993) Kok's oxygen clock: what makes it tick? The structure of P680 and consequences of its oxidizing power. Photosynth Res 38: 297–301Google Scholar
  46. Vermaas WFJ, Styring S, Schröder WP and Andersson B (1993) Photosynthetic water oxidation: The protein framework. Photosynth Res 38: 249–263Google Scholar
  47. Warr SRC, Reed RH and Stewart WDP (1984) Osmotic adjustment of cyanobacteria: the effects of NaCl, KCl, sucrose and glycine betaine on glutamine synthetase activity in a marine and a halotolerant strain. J Gen Microbiol 130: 2169–2175Google Scholar
  48. Weigel P, Weretilnyk EA and Hanson AD (1986) Betaine aldehyde oxidation by spinach chloroplasts. Plant Physiol 82: 753–759Google Scholar
  49. Weretilnyk EA and Hanson AD (1990) Molecular cloning of a plant betaine aldehyde dehydrogenase in an enzyme implicated in adaptation to salinity and drought. Proc Natl Acad Sci USA 87: 2475–2749Google Scholar
  50. Williams WP and Gounaris K (1992) Stabilisation of PS-II-mediated electron transport in oxygen-evolving PS II core preparations by the addition of compatible co-solutes. Biochim Biophys Acta 1100: 92–97Google Scholar
  51. Wyn Jones RG and Storey R (1981) Betaines. In: Paleg LG and Aspinal D (eds) The Physiology and Biochemistry of Draught Resistance in Plants, pp 171–204. Academic Press, Sydney, AustraliaGoogle Scholar
  52. Yancey PH, Clark ME, Hand SC, Bowlus RD and Somero GN (1982) Living with water stress: Evolution of the osmolyte systems. Science 217: 1214–1222Google Scholar

Copyright information

© Kluwer Academic Publishers 1995

Authors and Affiliations

  • George C. Papageorgiou
    • 1
  • Norio Murata
    • 1
  1. 1.National Institute for Basic BiologyOkazakiJapan

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