Role of Acyl Lipids in the Function of Photosynthetic Membranes in Higher Plants

Summary

The great diversity of thylakoid acyl lipids and their unique (physico)chemical characteristics as well as their peculiar topology in the membrane strongly suggest that specific functions and distinct domains of acyl lipids exist in the thylakoid membrane.

To investigate the functional significance of thylakoid lipid composition, several approaches have been adopted which are presented in this chapter. The functional alterations occurring in aged thylakoids and during leaf senescence can be attributed, at least in part, to a release of free fatty acids and/or to the loss or modification of the parent lipids which are essential for the functioning of the thylakoid membrane. The effects of aging are strikingly similar to those of exogenous free unsaturated fatty acids. Controlled lipolytic treatment of thylakoid membranes is another approach allowing the stepwise digestion of specific acyl lipids, first in the thylakoid outer monolayer, then in the inner one. These topological lipid depletions show that only certain lipid populations (e.g. located in one of the two membrane monolayers) are able to sustain photochemical reactions. The removal of thylakoid acyl lipids by cyclodextrins (cyclic oligosaccharides consisting of six to eight glucopyranose units linked by α(1–4)bonds) represents a potentially interesting depletion technique, since no detergents are used as in the preparation of subchloroplast particles and no free fatty acids and lysolipids are produced as in the enzymatic approach. The modulation of thylakoid membrane fluidity by homogenous catalytic hydrogenation in situ shows quite clearly the importance of the lipid unsaturation for optimal photochemical reactions. In addition, alteration in membrane fluidity may be the first signal in the perception of temperature changes in the plant environment. Another interesting approach is to use antibodies directed to specific membrane lipids and measure the photochemical reactions which are impaired in thylakoids. Lipids are also involved in the mode of action of herbicides by mediating the accessibility of these compounds to their binding site, for instance to the Q_B protein level. Finally, a number of Arabidopsis and Chlamydomonas mutants have been characterized as being deficient in desaturases or glycerol-3-phosphate acyltransferases. The availability of these mutants provides another tool in determining the physiological consequences of variations in lipid unsaturation, though information concerning photosynthetic activity is still rather scarce. All these approaches present advantages and drawbacks.

In spite of considerable effort, the structure/function relationship of acyl lipids in the thylakoid membrane remains ambiguous and elusive. This is due probably to the fact that, in contrast to proteins, lipids have by themselves no recognized catalytic properties. They allow the maintenance of an appropriate conformation and orientation of proteins which may express their function only in the presence of specific lipids. This function is expected to require only a few specific lipid molecules as it appears to be the case for phosphatidylglycerol containing trans-Δ³-hexadecenoic acid in the formation of the trimeric chlorophyll a/b light-harvesting protein of Photosystem II and the development of grana stacks. In the literature, there is no clear distinction between the role of these specific lipids and the general physicochemical properties of the membrane bulk lipids which are likely to be involved in structural aspects of the membrane such as the mode of herbicide action, chilling injury, photoinhibition and, in general, responses to environmental changes.