Abstract
The distribution of the two photosystems, PSI and PSII, in grana and stroma lamellae of the chloroplast membranes is not uniform. PSII are mainly concentrated in grana and PSI in stroma thylakoids. The dynamics and factors controlling the spatial segregation of PSI and PSII are generally not well understood, and here we address the segregation of photosystems in thylakoid membranes by means of a molecular dynamics method. The lateral segregation of photosystems was studied assuming a model comprising a two-dimensional (in-plane), two-component, many-body system with periodic boundary conditions and competing interactions between the photosystems in the thylakoid membrane. PSI and PSII are represented by particles with different values of negative charge. The pair interactions between particles include a screened Coulomb repulsive part and an exponentially decaying attractive part. The modeling results suggest a complicated phase behavior of the system, including quasi-crystalline phase of randomly distributed complexes of PSII and PSI at low ionic screening, well defined clustered state of segregated complexes at high screening, and in addition, an intermediate agglomerate phase where the photosystems tend to aggregate together without segregation. The calculations demonstrated that the ordering of photosystems within the membrane was the result of interplay between electrostatic and lipid-mediated interactions. At some values of the model parameters the segregation can be represented visually as well as by analyzing the correlation functions of the configuration.
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- Allen J. F. How does protein phosphorylation regulate photosynthesis? Trends Biochem Sci. 1992 Jan;17(1):12–17. doi: 10.1016/0968-0004(92)90418-9. [DOI] [PubMed] [Google Scholar]
- Andersson B., Anderson J. M. Lateral heterogeneity in the distribution of chlorophyll-protein complexes of the thylakoid membranes of spinach chloroplasts. Biochim Biophys Acta. 1980 Dec 3;593(2):427–440. doi: 10.1016/0005-2728(80)90078-x. [DOI] [PubMed] [Google Scholar]
- Barber J., Chow W. S., Scoufflaire C., Lannoye R. The relationship between thylakoid stacking and salt induced chlorophyll fluorescence changes. Biochim Biophys Acta. 1980 Jun 10;591(1):92–103. doi: 10.1016/0005-2728(80)90223-6. [DOI] [PubMed] [Google Scholar]
- Ben-Tal N., Honig B., Miller C., McLaughlin S. Electrostatic binding of proteins to membranes. Theoretical predictions and experimental results with charybdotoxin and phospholipid vesicles. Biophys J. 1997 Oct;73(4):1717–1727. doi: 10.1016/S0006-3495(97)78203-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Drepper F., Carlberg I., Andersson B., Haehnel W. Lateral diffusion of an integral membrane protein: Monte Carlo analysis of the migration of phosphorylated light-harvesting complex II in the thylakoid membrane. Biochemistry. 1993 Nov 9;32(44):11915–11922. doi: 10.1021/bi00095a022. [DOI] [PubMed] [Google Scholar]
- Dumas F., Lebrun M. C., Tocanne J. F. Is the protein/lipid hydrophobic matching principle relevant to membrane organization and functions? FEBS Lett. 1999 Sep 24;458(3):271–277. doi: 10.1016/s0014-5793(99)01148-5. [DOI] [PubMed] [Google Scholar]
- Gil T., Ipsen J. H., Mouritsen O. G., Sabra M. C., Sperotto M. M., Zuckermann M. J. Theoretical analysis of protein organization in lipid membranes. Biochim Biophys Acta. 1998 Nov 10;1376(3):245–266. doi: 10.1016/s0304-4157(98)00022-7. [DOI] [PubMed] [Google Scholar]
- Haworth P. Protein phosphorylation-induced State I-State II transitions are dependent on thylakoid membrane microviscosity. Arch Biochem Biophys. 1983 Oct 1;226(1):145–154. doi: 10.1016/0003-9861(83)90279-5. [DOI] [PubMed] [Google Scholar]
- Heimburg T., Biltonen R. L. A Monte Carlo simulation study of protein-induced heat capacity changes and lipid-induced protein clustering. Biophys J. 1996 Jan;70(1):84–96. doi: 10.1016/S0006-3495(96)79551-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hribar B., Vlachy V. Clustering of macroions in solutions of highly asymmetric electrolytes. Biophys J. 2000 Feb;78(2):694–698. doi: 10.1016/S0006-3495(00)76627-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Izawa S., Good N. E. Effect of Salts and Electron Transport on the Conformation of Isolated Chloroplasts. II. Electron Microscopy. Plant Physiol. 1966 Mar;41(3):544–552. doi: 10.1104/pp.41.3.544. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kleinschmidt J. H., Marsh D. Spin-label electron spin resonance studies on the interactions of lysine peptides with phospholipid membranes. Biophys J. 1997 Nov;73(5):2546–2555. doi: 10.1016/S0006-3495(97)78283-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Marcelja S. Lipid-mediated protein interaction in membranes. Biochim Biophys Acta. 1976 Nov 11;455(1):1–7. doi: 10.1016/0005-2736(76)90149-8. [DOI] [PubMed] [Google Scholar]
- Mouritsen O. G., Bloom M. Models of lipid-protein interactions in membranes. Annu Rev Biophys Biomol Struct. 1993;22:145–171. doi: 10.1146/annurev.bb.22.060193.001045. [DOI] [PubMed] [Google Scholar]
- Murata N. Control of excitation transfer in photosynthesis. II. Magnesium ion-dependent distribution of excitation energy between two pigment systems in spinach chloroplasts. Biochim Biophys Acta. 1969 Oct 21;189(2):171–181. doi: 10.1016/0005-2728(69)90045-0. [DOI] [PubMed] [Google Scholar]
- Ojakian G. K., Satir P. Particle movements in chloroplast membranes: quantitative measurements of membrane fluidity by the freeze-fracture technique. Proc Natl Acad Sci U S A. 1974 May;71(5):2052–2056. doi: 10.1073/pnas.71.5.2052. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rojdestvenski I., Ivanov A. G., Cottam M. G., Oquist G. A two-dimensional many-body system with competing interactions as a model for segregation of photosystems in thylakoids of green plants. Eur Biophys J. 2000;29(3):214–220. doi: 10.1007/s002490000080. [DOI] [PubMed] [Google Scholar]
- Sabra M. C., Uitdehaag J. C., Watts A. General model for lipid-mediated two-dimensional array formation of membrane proteins: application to bacteriorhodopsin. Biophys J. 1998 Sep;75(3):1180–1188. doi: 10.1016/S0006-3495(98)74037-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sintes T., Baumgärtner A. Protein attraction in membranes induced by lipid fluctuations. Biophys J. 1997 Nov;73(5):2251–2259. doi: 10.1016/S0006-3495(97)78257-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tieleman D. P., Marrink S. J., Berendsen H. J. A computer perspective of membranes: molecular dynamics studies of lipid bilayer systems. Biochim Biophys Acta. 1997 Nov 21;1331(3):235–270. doi: 10.1016/s0304-4157(97)00008-7. [DOI] [PubMed] [Google Scholar]
- Trissl H. W., Wilhelm C. Why do thylakoid membranes from higher plants form grana stacks? Trends Biochem Sci. 1993 Nov;18(11):415–419. doi: 10.1016/0968-0004(93)90136-b. [DOI] [PubMed] [Google Scholar]
- White S. H., Wimley W. C. Membrane protein folding and stability: physical principles. Annu Rev Biophys Biomol Struct. 1999;28:319–365. doi: 10.1146/annurev.biophys.28.1.319. [DOI] [PubMed] [Google Scholar]
- Wollman F. A., Diner B. A. Cation control of fluorescence emission, light scatter, and membrane stacking in pigment mutants of Chlamydomonas reinhardi. Arch Biochem Biophys. 1980 May;201(2):646–659. doi: 10.1016/0003-9861(80)90555-x. [DOI] [PubMed] [Google Scholar]
- Wollman FA, Minai L, Nechushtai R. The biogenesis and assembly of photosynthetic proteins in thylakoid membranes1 . Biochim Biophys Acta. 1999 Apr 21;1411(1):21–85. doi: 10.1016/s0005-2728(99)00043-2. [DOI] [PubMed] [Google Scholar]