Modulation of non-bilayer lipid phases and the structure and functions of thylakoid membranes: effects on the water-soluble enzyme violaxanthin de-epoxidase

Abstract

the role of non-bilayer lipids and non-lamellar lipid phases in biological membranes is an enigmatic problem of membrane biology. non-bilayer lipids are present in large amounts in all membranes; in energy-converting membranes they constitute about half of their total lipid content-yet their functional state is a bilayer. in vitro experiments revealed that the functioning of the water-soluble violaxanthin de-epoxidase (VDE) enzyme of plant thylakoids requires the presence of a non-bilayer lipid phase. 31 p-nMR spectroscopy has provided evidence on lipid polymorphism in functional thylakoid membranes. Here we reveal reversible pH-and temperature-dependent changes of the lipid-phase behaviour, particularly the flexibility of isotropic non-lamellar phases, of isolated spinach thylakoids. these reorganizations are accompanied by changes in the permeability and thermodynamic parameters of the membranes and appear to control the activity of VDE and the photoprotective mechanism of non-photochemical quenching of chlorophyll-a fluorescence. The data demonstrate, for the first time in native membranes, the modulation of the activity of a water-soluble enzyme by a non-bilayer lipid phase. The primary function of biological membranes is to allow compartmentalization of cells and cellular organelles and, in general, the separation of two aqueous phases with different compositions. The functioning of these membranes, at the basic level, depends on the organization of their lipid molecules into bilayer structures 1-3. These structures provide a two-dimensional matrix, which is capable of embedding intrinsic proteins and permits the lateral diffusion of mobile compounds inside the 2D matrix of the membrane. By acting as highly selective barrier, the bilayer membrane allows the formation of concentration gradients of ions and other water-soluble compounds across them. The generation and utilization of the transmembrane electrochemical potential gradient for protons, Δµ H + or proton-motive force, is of pivotal importance in biological energy conversion 4. Most membrane lipids readily form bilayers. However, biological membranes also contain non-bilayer lipid species-which do not self-assemble into bilayers 5. Their role in the biomembranes is still enigmatic. Most noteworthy, in energy-converting membranes non-bilayer lipids constitute about half of their total lipid content,

Hot topic: Thermosensing in plants

“…Thylakoid membranes are always close to HII phase transition and, as HII phases emerge, they must be controlled to avoid damage, which involves the function of sHSPs (Tsvetkova et al, 2002). HII phases are however key to chloroplast heat acclimation because when they emerge under stress, they recruit and activate the xanthophyll cycle enzyme, violaxanthin deepoxidase (VDE) (Dlouhý et al, 2020). VDE synthesizes zeaxanthin which quenches excess excitation energy and enhances membrane F I G U R E 3 Sensing and signalling of heat stress at the chloroplast.…”

Cardiolipin, Non-Bilayer Structures and Mitochondrial Bioenergetics: Relevance to Cardiovascular Disease

“…According to this model, bilayer and non-bilayer phases co-exist as a dynamic equilibrium between the different lipid phases [ 71 , 72 , 73 , 74 ]. This is most clearly indicated by reversible co-solute-, temperature- and pH-dependent changes in the lipid-phase behavior of thylakoid membranes [ 73 , 75 ]. The shifts in equilibrium may represent states of various physiological activities in these light-energy converting membranes.…”

Lipids Composition in Plant Membranes

“…Fatty acids composition (with the proportion of saturated and unsaturated fatty acids) influences lipid composition (specific proportions) and organization in plant membranes. For example, the percentage content of lipids in the thylakoid membranes of green plants is as follows: MGDG~50%, DGDG~25-30%, SQDG~5-15%, PG~5-15% [70,71]. The most popular fatty acids in the skeleton of plant galactolipids are 18:3/16:3 as 34:6 MGDG, 18:3/18:3 as 36:6 MGDG, 18:3/16:0 as 34:3 DGDG, and 18:3/18:3 DGDG in the approximate proportion: 80%, 16%, 16%, 70%, respectively [72].…”

“…The studies concerning the location of the xanthophyll cycle in the transient membrane domain combined with LHCII, MGDG, VDE allowed to prove that MGDG have a crucial function in the stabilization of the structure of the LHCII protein in prevention its aggregation in PSII [71].…”

“…The important functions of MGDG are to promote membrane stacking, stabilizing the inner membrane leaflet in grana disc [ 88 ] and conservation of photosynthetic energy [ 94 ]. Furthermore, the proportion of the thylakoid nonbilayer lipids are crucial, because the higher content of the MGDG is responsible for the membrane permeability and thermal stability of PSII [ 71 ].

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