Contribution of galactoglycerolipids to the 3-dimensional architecture of thylakoids

FASEB Journal

Volumn 28, Issue 8, 2014, Pages 3373-3383

  Demé, Bruno ^a   Cataye, Céline ^b,c,d,e   Block, Maryse A ^b,c,d,e   Maréchal, Eric ^b,c,d,e   Jouhet, Juliette ^b,c,d,e  

^a INSTITUT LAUE LANGEVIN   (France)

^b LEGI   (France)

^c UNIV GRENOBLE ALPES   (France)

^d DIF   (France)

^e Laboratoire de Physiologie Cellulaire Vegetale Grenoble   (France)

Author keywords

Glycolipid; Hexagonal II phase; Lamellar phase; Membrane stacking; Neutron diffraction

Indexed keywords

DIACYLGLYCEROL; DIGALACTOSYLDIGLYCERIDE; GALACTOGLYCEROLIPID; GALACTOSYLDIACYLGLYCEROL; GLYCEROLIPID; LIPID; SULFOQUINOVOSEDIACYLGLYCEROL; UNCLASSIFIED DRUG;

ARTICLE; DISPERSION; ENDODONTIC FILE; HUMIDITY; HYDRATION; HYDROGEN BOND; LIPID BILAYER; LIPID COMPOSITION; LIPID MEMBRANE; NEUTRON DIFFRACTION; NONHUMAN; PERIODICITY; PRIORITY JOURNAL; SPINACH; SURFACE PROPERTY; THYLAKOID; THYLAKOID MEMBRANE; WATER TRANSPORT;

GLYCOLIPID; HEXAGONAL II PHASE; LAMELLAR PHASE; MEMBRANE STACKING; NEUTRON DIFFRACTION;

ADAPTATION, PHYSIOLOGICAL; COLD TEMPERATURE; DROUGHTS; GALACTOLIPIDS; GLYCOLIPIDS; HYDROGEN BONDING; LIPID BILAYERS; MEMBRANE LIPIDS; NEUTRON DIFFRACTION; PHOSPHATIDYLGLYCEROLS; PLANT DEVELOPMENT; PLANT LEAVES; SALINITY; SPINACIA OLERACEA; STATIC ELECTRICITY; STRUCTURE-ACTIVITY RELATIONSHIP; THYLAKOIDS; WATER;

EID: 84905241632     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.13-247395     Document Type: Article

References (82)

1. Austin, J. R., 2nd, and Staehelin, L. A. (2011) Three-dimensional architecture of grana and stroma thylakoids of higher plants as determined by electron tomography. Plant Physiol. 155, 1601-1611
2. Gounaris, K., and Barber, J. (1983) Monogalactosyldiacylglycerol: the most abundant polar lipid in nature. Trends Biochem. Sci. 8, 378-381
3. Boudiere, L., Michaud, M., Petroutsos, D., Rebeille, F., Falconet, D., Bastien, O., Roy, S., Finazzi, G., Rolland, N., Jouhet, J., Block, M. A., and Marechal, E. (2014) Glycerolipids in photosynthesis: composition, synthesis and trafficking. Biochim. Biophys. Acta 1837, 470-480
4. Shipley, G. G., Green, J. P., and Nichols, B. W. (1973) The phase behavior of monogalactosyl, digalactosyl, and sulphoquinovosyl diglycerides. Biochim. Biophys. Acta 311, 531-544
5. Mustardy, L., and Garab, G. (2003) Granum revisited: A three-dimensional model - where things fall into place. Trends Plant. Sci. 8, 117-122 (Pubitemid 36726467)
6. Dekker, J. P., and Boekema, E. J. (2005) Supramolecular organization of thylakoid membrane proteins in green plants. Biochim. Biophys. Acta 1706, 12-39 (Pubitemid 40044704)
7. Chow, W. S., Kim, E. H., Horton, P., and Anderson, J. M. (2005) Granal stacking of thylakoid membranes in higher plant chloroplasts: the physicochemical forces at work and the functional consequences that ensue. Photochem. Photobiol. Sci. 4, 1081-1090 (Pubitemid 41811373)
8. Ladygin, V. G., and Semenova, G. A. (2005) The involvement of the complexes of photosystems in the organization of chloroplast ultrastructure in pea mutants. Russ. J. Plant Physiol. 52, 596-605 (Pubitemid 41414300)
9. Endow, J. K., Ruppel, N. J., and Inoue, K. (2010) Keep the balloon deflated: the significance of protein maturation for thylakoid flattening. Plant Signal. Behav. 5, 721-723
10. Gruszecki, W. I., and Strzalka, K. (2005) Carotenoids as modulators of lipid membrane physical properties. Biochim. Biophys. Acta 1740, 108-115 (Pubitemid 40798219)
11. Aronsson, H., Schottler, M. A., Kelly, A. A., Sundqvist, C., Dormann, P., Karim, S., and Jarvis, P. (2008) Monogalactosyldiacylglycerol deficiency in Arabidopsis affects pigment composition in the prolamellar body and impairs thylakoid membrane energization and photoprotection in leaves. Plant Physiol. 148, 580-592 (Pubitemid 352847592)
12. Kobayashi, K., Kondo, M., Fukuda, H., Nishimura, M., and Ohta, H. (2007) Galactolipid synthesis in chloroplast inner envelope is essential for proper thylakoid biogenesis, photosynthesis, and embryogenesis. Proc. Natl. Acad. Sci. U.S.A. 104, 17216-17221 (Pubitemid 350211017)
13. Botte, C. Y., Deligny, M., Roccia, A., Bonneau, A. L., Saidani, N., Hardre, H., Aci, S., Yamaryo-Botte, Y., Jouhet, J., Dubots, E., Loizeau, K., Bastien, O., Brehelin, L., Joyard, J., Cintrat, J. C., Falconet, D., Block, M. A., Rousseau, B., Lopez, R., and Marechal, E. (2011) Chemical inhibitors of monogalactosyldiacylglycerol synthases in Arabidopsis thaliana. Nat. Chem. Biol. 7, 834-842
14. Dormann, P., Hoffmann-Benning, S., Balbo, I., and Benning, C. (1995) Isolation and characterization of an Arabidopsis mutant deficient in the thylakoid lipid digalactosyl diacylglycerol. Plant Cell 7, 1801-1810 (Pubitemid 3019799)
15. Holzl, G., Witt, S., Gaude, N., Melzer, M., Schottler, M. A., and Dormann, P. (2009) The role of diglycosyl lipids in photosynthesis and membrane lipid homeostasis in Arabidopsis. Plant Physiol. 150, 1147-1159
16. Webb, M. S., Tilcock, C. P. S., and Green, B. R. (1988) Salt-mediated interactions between vesicles of the thylakoid lipid digalactosyldiacylglycerol. Biochim. Biophys. Acta 938, 323-333
17. Armbruster, U., Labs, M., Pribil, M., Viola, S., Xu, W., Scharfenberg, M., Hertle, A. P., Rojahn, U., Jensen, P. E., Rappaport, F., Joliot, P., Dormann, P., Wanner, G., and Leister, D. (2013) Arabidopsis CURVATURE THYLAKOID1 proteins modify thylakoid architecture by inducing membrane curvature. Plant Cell 25, 2661-2678
18. Murphy, D. J. (1982) The importance of non-planar bilayer regions in photosynthetic membranes and their stabilization by galactolipids. FEBS Lett. 150, 19-26
19. Dubois, M., Deme, B., Gulik-Krzywicki, T., Dedieu, J. C., Vautrin, C., Desert, S., Perez, E., and Zemb, T. (2001) Self-assembly of regular hollow icosahedra in salt-free catanionic solutions. Nature 411, 672-675 (Pubitemid 32531666)
20. Zemb, T., Dubois, M., Deme, B., and Gulik-Krzywicki, T. (1999) Self-assembly of flat nanodiscs in salt-free catanionic surfactant solutions. Science 283, 816-819
21. Gounaris, K., Barber, J., and Harwood, J. L. (1986) The thylakoid membranes of higher plant chloroplasts. Biochem. J. 237, 313-326
22. Gounaris, K., Sundby, C., Andersson, B., and Barber, J. (1983) Lateral heterogeneity of polar lipids in the thylakoid membranes of spinach- chloroplasts. FEBS Lett. 156, 170-174
23. Gounaris, K., Sen, A., Brain, A. P. R., Quinn, P. J., and Williams, W. P. (1983) The formation of non-bilayer structures in total polar lipid extracts of chloroplast membranes. Biochim. Biophys. Acta 728, 129-139
24. Krumova, S. B., Dijkema, C., de Waard, P., Van As, H., Garab, G., and van Amerongen, H. (2008) Phase behavior of phosphatidylglycerol in spinach thylakoid membranes as revealed by 31P-NMR. Biochim. Biophys. Acta 1778, 997-1003
25. Nevo, R., Charuvi, D., Tsabari, O., and Reich, Z. (2012) Composition, architecture and dynamics of the photosynthetic apparatus in higher plants. Plant J. 70, 157-176
26. Tikkanen, M., and Aro, E. M. (2012) Thylakoid protein phosphorylation in dynamic regulation of photosystem II in higher plants. Biochim. Biophys. Acta 1817, 232-238
27. McDonnel, A., and Staehelin, L. A. (1980) Adhesion between liposomes mediated by the chlorophyll a/b light-harvesting complex isolated from chloroplast membranes. J. Cell Biol. 84, 40-56
28. Ryrie, I. J., Anderson, J. M., and Goodchild, D. J. (1980) The role of the light-harvesting chlorophyll a/b protein complex in chloroplast membrane stacking. Cation-induced aggregation of reconstituted proteoliposomes. Eur. J. Biochem. 107, 345-354
29. Nakanishi, H., Nozue, H., Suzuki, K., Kaneko, Y., Taguchi, G., and Hayashida, N. (2005) Characterization of the Arabidopsis thaliana mutant pcb2 which accumulates divinyl chlorophylls. Plant Cell Physiol. 46, 467-473
30. Cui, Y. L., Jia, Q. S., Yin, Q. Q., Lin, G. N., Kong, M. M., and Yang, Z. N. (2011) The GDC1 gene encodes a novel ankyrin domain-containing protein that is essential for grana formation in Arabidopsis. Plant Physiol. 155, 130-141
31. Schaller, S., Latowski, D., Jemiola-Rzeminska, M., Dawood, A., Wilhelm, C., Strzalka, K., and Goss, R. (2011) Regulation of LHCII aggregation by different thylakoid membrane lipids. Biochim. Biophys. Acta 1807, 326-335
32. Krumova, S. B., Laptenok, S. P., Kovacs, L., Toth, T., van Hoek, A., Garab, G., and van Amerongen, H. (2010) Digalactosyldiacylglycerol-deficiency lowers the thermal stability of thylakoid membranes. Photosynth. Res. 105, 229-242
33. Liberton, M., Page, L. E., O'Dell, W. B., O'Neill, H., Mamontov, E., Urban, V. S., and Pakrasi, H. B. (2013) Organization and flexibility of cyanobacterial thylakoid membranes examined by neutron scattering. J. Biol. Chem. 288, 3632-3640
34. Dobrikova, A. G., Domonkos, I., Sozer, O., Laczko-Dobos, H., Kis, M., Parducz, A., Gombos, Z., and Apostolova, E. L. (2013) Effect of partial or complete elimination of light-harvesting complexes on the surface electric properties and the functions of cyanobacterial photosynthetic membranes. Physiol. Plant. 147, 248-260
35. Webb, M. S., and Green, B. R. (1990) Effects of neutral and anionic lipids on digalactosyldiacylglycerol vesicle aggregation. Biochim. Biophys. Acta 1030, 231-237
36. Schneck, E., Rehfeldt, F., Oliveira, R. G., Gege, C., Deme, B., and Tanaka, M. (2008) Modulation of intermembrane interaction and bending rigidity of biomembrane models via carbohydrates investigated by specular and off-specular neutron scattering. Phys. Rev. E 78, 061924
37. McDaniel, R. V. (1988) Neutron diffraction studies of digalactosyldiacylglycerol. Biochim. Biophys. Acta 940, 158-164
38. Douce, R., Holtz, R. B., and Benson, A. A. (1973) Isolation and properties of the envelope of spinach chloroplasts. J. Biol. Chem. 248, 7215-7222
39. Douce, R., and Joyard, J. (1982) Purification of the chloroplast envelope. In Methods in Chloroplast Molecular Biology (Edelman, M., Hallick, R., and Chua, N.-H., eds) pp. 239-256, Elsevier, Amsterdam
40. Bligh, E. G., and Dyer, W. J. (1959) A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37, 911-917
41. Jouhet, J., Marechal, E., Bligny, R., Joyard, J., and Block, M. A. (2003) Transient increase of phosphatidylcholine in plant cells in response to phosphate deprivation. FEBS Lett. 544, 63-68 (Pubitemid 36628037)
42. Schneck, E., Deme, B., Gege, C., and Tanaka, M. (2011) Membrane adhesion via homophilic saccharide-saccharide interactions investigated by neutron scattering. Biophys. J. 100, 2151-2159
43. Schneck, E., Oliveira, R. G., Rehfeldt, F., Deme, B., Brandenburg, K., Seydel, U., and Tanaka, M. (2009) Mechanical properties of interacting lipopolysaccharide membranes from bacteria mutants studied by specular and off-specular neutron scattering. Phys. Rev. E 80, 041929
44. Richard, D., Ferrand, M., and Kearley, G. J. (1996) Analysis and visualisation of neutron-scattering data. J. Neutron. Res. 4, 33-39
45. Miller, W. H. (1839) A Treatise on Crystallography, J. & J. J. Deighton, Cambridge
46. Block, M. A., Dorne, A. J., Joyard, J., and Douce, R. (1983) Preparation and characterization of membrane fractions enriched in outer and inner envelope membranes from spinach chloroplasts. I. Electrophoretic and immunochemical analyses. J. Biol. Chem. 258, 13273-13280 (Pubitemid 14237297)
47. Douce, R., Block, M. A., Dorne, A. J., and Joyard, J. (1984) The plastid envelope membranes: their structure, composition, and role in chloroplast biogenesis. Subcell. Biochem. 10, 1-84
48. Jacrot, B. (1976) Study of biological structures by neutron-scattering from solution. Rep. Prog. Phys. 39, 911-953
49. Ding, L., Weiss, T. M., Fragneto, G., Liu, W., Yang, L., and Huang, H. W. (2005) Distorted hexagonal phase studied by neutron diffraction: lipid components demixed in a bent monolayer. Langmuir 21, 203-210 (Pubitemid 40086965)
50. Groen, D., Gooris, G. S., Barlow, D. J., Lawrence, M. J., van Mechelen, J. B., Deme, B., and Bouwstra, J. A. (2011) Disposition of ceramide in model lipid membranes determined by neutron diffraction. Biophys. J. 100, 1481-1489
51. Sen, A., Williams, W. P., Brain, A. P., Dickens, M. J., and Quinn, P. J. (1981) Formation of inverted micelles in dispersions of mixed galactolipids. Nature 293, 488-490
52. Sen, A., Brain, A. P., Quinn, P. J., and Williams, W. P. (1982) Formation of inverted lipid micelles in aqueous dispersions of mixed sn-3- galactosyldiacylglycerols induced by heat and ethylene glycol. Biochim. Biophys. Acta 686, 215-224
53. Rivas, E., and Luzzati, V. (1969) [Polymorphism of polar lipids and galacto-lipids of maize chloroplasts, in the presence of water]. J. Mol. Biol. 41, 261-275
54. McIntosh, T. J., and Simon, S. A. (1994) Hydration and steric pressures between phospholipid bilayers. Annu. Rev. Biophys. Biomol. Struct. 23, 27-51 (Pubitemid 24217361)
55. Deme, B., Dubois, M., and Zemb, T. (2002) Swelling of a lecithin lamellar phase induced by small carbohydrate solutes. Biophys. J. 82, 215-225 (Pubitemid 34289796)
56. Deme, B., Dubois, M., Gulik-Krzywicki, T., and Zemb, T. (2002) Giant collective fluctuations of charged membranes at the lamellar-to-vesicle unbinding transition. 1. Characterization of a new lipid morphology by SANS, SAXS, and electron microscopy. Langmuir 18, 997-1004 (Pubitemid 35384020)
57. Schaller, S., Latowski, D., Jemiola-Rzeminska, M., Wilhelm, C., Strzalka, K., and Goss, R. (2010) The main thylakoid membrane lipid monogalactosyldiacylglycerol (MGDG) promotes the de-epoxidation of violaxanthin associated with the light-harvesting complex of photosystem II (LHCII). Biochim. Biophys. Acta 1797, 414-424
58. Jahns, P., Latowski, D., and Strzalka, K. (2009) Mechanism and regulation of the violaxanthin cycle: the role of antenna proteins and membrane lipids. Biochim. Biophys. Acta 1787, 3-14
59. Latowski, D., Akerlund, H. E., and Strzalka, K. (2004) Violaxanthin de-epoxidase, the xanthophyll cycle enzyme, requires lipid inverted hexagonal structures for its activity. Biochemistry 43, 4417-4420 (Pubitemid 38500569)
60. Gunning, B. E. (2001) Membrane geometry of "open" prolamellar bodies. Protoplasma 215, 4-15
61. Williams, W. P., Selstam, E., and Brain, T. (1998) X-ray diffraction studies of the structural organisation of prolamellar bodies isolated from Zea mays. FEBS Lett. 422, 252-254 (Pubitemid 28064554)
62. Siegel, D. P. (1999) The modified stalk mechanism of lamellar/inverted phase transitions and its implications for membrane fusion. Biophys. J. 76, 291-313
63. Bottier, C., Gean, J., Artzner, F., Desbat, B., Pezolet, M., Renault, A., Marion, D., and Vie, V. (2007) Galactosyl headgroup interactions control the molecular packing of wheat lipids in Langmuir films and in hydrated liquid-crystalline mesophases. Biochim. Biophys. Acta 1768, 1526-1540 (Pubitemid 46782702)
64. Selstam, E., and Sandelius, A. S. (1984) A comparison between prolamellar bodies and prothylakoid membranes of etioplasts of dark-grown wheat concerning lipid and polypeptide composition. Plant Physiol. 76, 1036-1040
65. Torres-Franklin, M. L., Gigon, A., de Melo, D. F., Zuily-Fodil, Y., and Pham-Thi, A. T. (2007) Drought stress and rehydration affect the balance between MGDG and DGDG synthesis in cowpea leaves. Physiol. Plant 131, 201-210 (Pubitemid 47367727)
66. Browse, J. (2010) Plant science: saving the bilayer. Science 330, 185-186
67. Moellering, E. R., Muthan, B., and Benning, C. (2010) Freezing tolerance in plants requires lipid remodeling at the outer chloroplast membrane. Science 330, 226-228
68. Lindblom, G., Oradd, G., Rilfors, L., and Morein, S. (2002) Regulation of lipid composition in Acholeplasma laidlawii and Escherichia coli membranes: NMR studies of lipid lateral diffusion at different growth temperatures. Biochemistry 41, 11512-11515
69. Jouhet, J. (2013) Importance of the hexagonal lipid phase in biological membrane organization. Front. Plant Sci. 4, 494
70. Garab, G., Lohner, K., Laggner, P., and Farkas, T. (2000) Self-regulation of the lipid content of membranes by non-bilayer lipids: a hypothesis. Trends Plant Sci. 5, 489-494
71. De Kruijff, B. (1997) Biomembranes: lipids beyond the bilayer. Nature 386, 129-130
72. Harauz, G., Ladizhansky, V., and Boggs, J. M. (2009) Structural polymorphism and multifunctionality of myelin basic protein. Biochemistry 48, 8094-8104
73. Stewart, R. J., and Boggs, J. M. (1993) A carbohydrate-carbohydrate interaction between galactosylceramide-containing liposomes and cerebroside sulfate-containing liposomes: dependence on the glycolipid ceramide composition. Biochemistry 32, 10666-10674 (Pubitemid 23327799)
74. Koshy, K. M., and Boggs, J. M. (1996) Investigation of the calcium-mediated association between the carbohydrate head groups of galactosylceramide and galactosylceramide I3 sulfate by electrospray ionization mass spectrometry. J. Biol. Chem. 271, 3496-3499 (Pubitemid 26065658)
75. Koshy, K. M., Wang, J., and Boggs, J. M. (1999) Divalent cation-mediated interaction between cerebroside sulfate and cerebrosides: an investigation of the effect of structural variations of lipids by electrospray ionization mass spectrometry. Biophys. J. 77, 306-318 (Pubitemid 29305230)
76. Boggs, J. M., Menikh, A., and Rangaraj, G. (2000) Trans interactions between galactosylceramide and cerebroside sulfate across apposed bilayers. Biophys. J. 78, 874-885 (Pubitemid 30211845)
77. Menikh, A., and Fragata, M. (1993) Fourier transform infrared spectroscopic study of ion binding and intramolecular interactions in the polar head of digalactosyldiacylglycerol. Eur. Biophys. J. 22, 249-258 (Pubitemid 23337922)
78. Hincha, D. K. (2003) Effects of calcium-induced aggregation on the physical stability of liposomes containing plant glycolipids. Biochim. Biophys. Acta 1611, 180-186
79. Hartel, H., and Benning, C. (2000) Can digalactosyldiacylglycerol substitute for phosphatidylcholine upon phosphate deprivation in leaves and roots of Arabidopsis? Biochem. Soc. Trans. 28, 729-732 (Pubitemid 32163248)
80. Daum, B., Nicastro, D., Austin, J., 2nd, McIntosh, J. R., and Kuhlbrandt, W. (2010) Arrangement of photosystem II and ATP synthase in chloroplast membranes of spinach and pea. Plant Cell 22, 1299-1312
81. Collins, A. M., Liberton, M., Jones, H. D., Garcia, O. F., Pakrasi, H. B., and Timlin, J. A. (2012) Photosynthetic pigment localization and thylakoid membrane morphology are altered in Synechocystis 6803 phycobilisome mutants. Plant Physiol. 158, 1600-1609
82. Allen, K. D., Duysen, M. E., and Staehelin, L. A. (1988) Biogenesis of thylakoid membranes is controlled by light intensity in the conditional chlorophyll b-deficient CD3 mutant of wheat. J. Cell Biol. 107, 907-919