Granum revisited. A three-dimensional model--where things fall into place.

The complex structure of higher plant chloroplasts has fascinated researchers for many years. Although the spatial relationship between granum and stroma thylakoids has been known for more than 20 years, most textbooks and research papers continue to include erroneous 3D models and simplified schemes. Here we present a simple computer model, based on electron micrographs from serial section of granum-stroma assemblies, showing the striking 3D structure of the stroma membrane wound around the granum. This model also provides an insight into some previously unknown functions of this intriguing multilamellar membrane system. However, many areas, such as self-assembly, structural flexibility and evolutionary niche, still remain to be explored.

[1]  Reinhard Lipowsky,et al.  Structure and dynamics of membranes , 1995 .

[2]  L. Mustárdy,et al.  Development of Thylakoid Membrane Stacking , 1996 .

[3]  B. Ninham,et al.  An ion‐exchange model for thylakoid stacking in chloroplasts , 1981 .

[4]  H. Matthijs,et al.  Supramolecular structure of the thylakoid membrane of Prochlorothrix hollandica: a chlorophyll b-containing prokaryote. , 1988, Journal of cell science.

[5]  P Albertsson,et al.  A quantitative model of the domain structure of the photosynthetic membrane. , 2001, Trends in plant science.

[6]  N. Boardman,et al.  Isolation from Spinach Chloroplasts of Particles Containing Different Proportions of Chlorophyll a and Chlorophyll b and their Possible Role in the Light Reactions of Photosynthesis , 1964, Nature.

[7]  G. Meszéna,et al.  Trapping magnetically oriented chloroplast thylakoid membranes in gels for electric measurements. , 1994, Journal of photochemistry and photobiology. B, Biology.

[8]  U. Hinz,et al.  The role of the light harvesting complex and photosystem II in thylakoid stacking in thechlorina-f2 barley mutant , 1985 .

[9]  L. Staehelin,et al.  Photosynthesis III. Photosynthetic membranes and light harvesting systems. , 1986 .

[10]  Jan M. Anderson Insights into the consequences of grana stacking of thylakoid membranes in vascular plants: a personal perspective , 1999 .

[11]  G. Garab,et al.  Role of thylakoid lipids in the structural flexibility of lamellar aggregates of the isolated light-harvesting chlorophyll a/b complex of photosystem II. , 1998, Biochemistry.

[12]  Numerical Taxonomy and Comparative Elaborateness, with a Speculation on Unused Genes , 1965, Nature.

[13]  H. Westerhoff,et al.  Light intensity distribution in thylakoids and the polarity of the photovoltaic effect , 1994 .

[14]  L. Mustárdy,et al.  Evidence of helical thylakoid arrangement by scanning electron microscopy , 1979 .

[15]  C. Wilhelm,et al.  Why do thylakoid membranes from higher plants form grana stacks? , 1993, Trends in biochemical sciences.

[16]  A. Holzenburg,et al.  An alternative model for photosystem II/light harvesting complex II in grana membranes based on cryo-electron microscopy studies. , 2002, European journal of biochemistry.

[17]  C. Sundby,et al.  A model for the topology of the chloroplast thylakoid membrane , 1999 .

[18]  J. Anderson,et al.  The dynamic photosynthetic membrane and regulation of solar energy conversion. , 1988, Trends in biochemical sciences.

[19]  J. Sutherland,et al.  ORGANIZATION OF PIGMENT‐PROTEIN COMPLEXES INTO MACRODOMAINS IN THE THYLAKOID MEMBRANES OF WILD‐TYPE and CHLOROPHYLL fo‐LESS MUTANT OF BARLEY AS REVEALED BY CIRCULAR DICHROISM , 1991 .

[20]  J. Allen,et al.  Protein phosphorylation in regulation of photosynthesis. , 1992, Biochimica et biophysica acta.

[21]  G. Garab,et al.  Size dependency of circular dichroism in macroaggregates of photosynthetic pigment-protein complexes. , 1994, Biochemistry.

[22]  J. Anderson,et al.  Lateral heterogeneity in the distribution of chlorophyll-protein complexes of the thylakoid membranes of spinach chloroplasts. , 1980, Biochimica et biophysica acta.

[23]  P. Sitte Zellfeinbau bei Plasmolyse , 1963, Protoplasma.

[24]  L. Staehelin Chloroplast Structure and Supramolecular Organization of Photosynthetic Membranes , 1986 .

[25]  W. Menke Das allgemeine Bauprinzip des Lamellarsystems der Chloroplasten , 1960, Experientia.

[26]  P. Horton Hypothesis: Are grana necessary for regulation of light harvesting? , 1999 .

[27]  K. Diederichs,et al.  Determination of interaction forces between higher plant thylakoids and electron-density-profile evaluation using small-angle X-ray scattering , 1985 .

[28]  H. Scheller,et al.  The PSI-H subunit of photosystem I is essential for state transitions in plant photosynthesis , 2000, Nature.

[29]  C. Stocking,et al.  The grana as structural units of chloroplasts of mesophyll of Nicotiana rustica and Phaseolus vulgaris , 1963 .

[30]  G. Garab,et al.  Structural flexibility of chiral macroaggregates of light-harvesting chlorophyll a/b pigment-protein complexes. Light-induced reversible structural changes associated with energy dissipation. , 1996, Biochemistry.

[31]  K. Steinback,et al.  Chloroplast protein phosphorylation couples plastoquinone redox state to distribution of excitation energy between photosystems , 1981, Nature.

[32]  C F Fowler,et al.  Direct observation of a light-induced electric field in chloroplasts. , 1974, Biochimica et biophysica acta.

[33]  E. Boekema,et al.  Arrangement of photosystem II supercomplexes in crystalline macrodomains within the thylakoid membrane of green plant chloroplasts. , 2000, Journal of molecular biology.

[34]  D. Paolillo The localization of ultraviolet-induced excision repair in the nucleus and the distribution of repair events in higher order chromatin loops in mammalian cells. , 1987 .

[35]  G. Meszéna Wavelength dependence and kinetics of the photovoltaic effects in chloroplast suspensions , 1994 .

[36]  R. Park Advances in photosynthesis , 1962 .

[37]  P. Gustafsson,et al.  Chlorophyll a/b-Binding Proteins, Pigment Conversions, and Early Light-Induced Proteins in a Chlorophyll b-less Barley Mutant , 1995, Plant physiology.

[38]  W Leibl,et al.  Why does the light-gradient photovoltage from photosynthetic organelles show a wavelength-dependent polarity? , 1993, Biophysical journal.

[39]  J. Briantais,et al.  Kinetics of cation-induced changes of Photosystem II fluorescence and of lateral distribution of the two photosystems in the thylakoid membranes of pea chloroplasts , 1984 .

[40]  C. Bustamante,et al.  Theory of the interaction of light with large inhomogeneous molecular aggregates. I. Absorption , 1986 .

[41]  G. Garab,et al.  Role of LHCII-containing macrodomains in the structure, function and dynamics of grana , 2000 .

[42]  S. Izawa,et al.  Effect of Salts and Electron Transport on the Conformation of Isolated Chloroplasts. II. Electron Microscopy. , 1966, Plant physiology.

[43]  T G Frey,et al.  The internal structure of mitochondria. , 2000, Trends in biochemical sciences.

[44]  E. Aro,et al.  Photoinhibition of Photosystem II. Inactivation, protein damage and turnover. , 1993, Biochimica et biophysica acta.

[45]  J. Barber Influence of Surface Charges on Thylakoid Structure and Function , 1982 .

[46]  Reinhard Lipowsky,et al.  Generic interactions of flexible membranes , 1995 .

[47]  L. Staehelin,et al.  Adhesion between liposomes mediated by the chlorophyll a/b light- harvesting complex isolated from chloroplast membranes , 1980, The Journal of cell biology.

[48]  J F Allen,et al.  Molecular recognition in thylakoid structure and function. , 2001, Trends in plant science.