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However, within a class of lipids, fatty acids can also influence the lipid architecture; the effect of increasing chain length and of unsaturation number is expected to favor in general the formation of HII phase. For instance, saturated PE form a lamellar phase whereas unsaturated PE form an HII phase (for a review, see Seddon, 1990). Furthermore, HII forming lipids are able to switch from a HII phase to a lamellar phase sometimes through an intermediate cubic phase (Figure 1) by lowering the temperature ( Tenchov and Koynova, 2012). Proteins and pigments might also be involved in cubic phase formation ( Wang and Quinn, 1999; Almsherqi et al., 2006; Tenchov et al., 2013). All these phase transitions are spontaneous and reversible ( Siegel and Tenchov, 2008). de Physiologie Cellulaire et Végétale, USC1359, Institut National de la Recherche Agronomique, Grenoble, France Plant pots are a great way to make your home look even more stylish and there's something for all tastes at Dunelm. From small plant pots to large ornamental planters, we have an extensive range that you'll need to keep an eye on! For the preservation of cell structure and compartmentalization, the membrane needs to be in a lamellar phase but, for membrane architecture and for some enzyme activities, HII phase domains must be present. It was shown that bacteria cells are able to keep the membrane lipids in a “window” between lamellar phases and HII phases. For example, E. coli or A. laidlawii maintain a balance between HII forming lipids and bilayer forming lipids by adjusting the composition of the polar head group ( A. laidlawii) or the acyl chains ( E. coli; Lindblom et al., 2002). This lead to the hypothesis that biomembranes homeostatically adjust their intrinsic curvatures to maintain a constant net spontaneous curvature in each leaflet of the bilayer ( Gruner, 1985). Activation of the CTP: phosphocholine cytidylyltransferase by HII phase might be a key factor for this kind of adaptability ( Attard et al., 2000). On this model, it was postulated that several enzymes involved in lipid biosynthesis could also be regulated by membrane stored curvature elastic energy. Kinetic simulations of the eukaryotic lipid biosynthetic pathway were used to show how this elastic energy was homeostatically maintained through a HII/bilayer ratio control mechanism ( Alley et al., 2008; Beard et al., 2008) similarly to what was proposed for A. laidlawii ( Vikstrom et al., 2000). Domains are present in every natural membrane. They are characterized by a distinctive protein and/or lipid composition and they confer specific properties to the membrane leading to original structure and function. Plasmodesmata, a highly specialized membrane organization that connects two plant cells, involves membrane domains. This typical plant structure is composed of two membranes: the plasma membrane and the desmotubule, a narrow tube in continuity with the endoplasmic reticulum (ER). Membrane domains described as lipid raft were found in the plasma membrane of plasmodesmata and might be involved in plasmodesmata scaffolding but nothing is known about the lipid organization of the desmotubule. The diameter of the membrane desmotubule is between 10 and 15 nm, which is highly constricted for a bilayer ( Tilsner et al., 2011). Continuity of the membrane and of the luminal space between reticulum and desmotubule is now clearly established ( Tilsner et al., 2011) but the organization of the desmotubule membrane as a bilayer has never been demonstrated. The presence of non-bilayer phase in desmotubule as a hypothesis may provide a new angle for desmotubule model establishment. This review presents how the ability of lipids to organize into non-lamellar phases, particularly hexagonal II (HII) phase, can promote specific local structures within membranes.

Biological membranes of course contain complex mixtures of lipids, and so it is of great importance to understand the polymorphic phase behavior of such mixtures in well-defined model systems. The use of synthetic lipid mixture and the development of techniques, such as electron microscopy, nuclear magnetic resonance (NMR), X-ray, and neutron diffraction, helped a lot to characterize the parameters that trigger the transition from lamellar phase toward HII phase. Lipid membrane composition, hydration, pH, and presence of cations contribute to lipid organization. For example, an equimolar mixture of PE and PC at low hydration pressure is organized in HII phase whereas at high hydration pressure it adopts a bilayer conformation ( Ding et al., 2005). Lowering the pH induces lamellar toward HII transition phase in charged phospholipid system such as PS and PA ( Seddon, 1990). Furthermore, transition of DPG from lamellar phase to HII phase is induced either upon lowering pH to below 2.8, or upon increasing NaCl concentration to above 1.6 M at pH 7 ( Seddon et al., 1983).

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Works on lipid membrane organization were first done by physical chemistry using synthetic lipids and model membranes but they gave us the premises for apprehending the biology of cell membrane structure. According to the Singer and Nicholson’s model ( Singer and Nicolson, 1972), cell membranes are viewed as proteins embedded in a lipid matrix. This so-called mosaic fluid model includes two basic postulates referring to the “lipid phase” state – liquid crystalline and bilayer, both of which are of vital importance for the proper functioning of membranes. In in vitro systems, aqueous dispersions of lipids are however able to form a large variety of other phases such as non-liquid crystalline and non-bilayer phases. These “solid phases” (also called “gel phases”) are favored by low temperature and long and saturated fatty acid chains. They were mainly characterized on model membranes of saturated phosphatidylcholine (PC; for example, see Mason, 1998). However, natural lipids are mostly unsaturated and organisms adapt their fatty acid composition to the environment to prevent the formation of gel phases. Moreover, even though gel phase domains were detected in biological membranes in very specific cases such as the myelin sheath ( Ruocco and Shipley, 1984) or in the stratum corneum ( Norlen, 2001b), most biological membranes are organized in liquid phase. Therefore gel phases will not be described further in this review.

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