Plastoglobules Are Lipoprotein Subcompartments of the Chloroplast That Are Permanently Coupled to Thylakoid Membranes and Contain Biosynthetic Enzymes

Abstract

Plastoglobules are lipoprotein particles inside chloroplasts. Their numbers have been shown to increase during the upregulation of plastid lipid metabolism in response to oxidative stress and during senescence. In this study, we used stateof-the-art high-pressure freezing/freeze-substitution methods combined with electron tomography as well as freeze-etch electron microscopy to characterize the structure and spatial relationship of plastoglobules to thylakoid membranes in developing, mature, and senescing chloroplasts. We demonstrate that plastoglobules are attached to thylakoids through a half-lipid bilayer that surrounds the globule contents and is continuous with the stroma-side leaflet of the thylakoid membrane. During oxidative stress and senescence, plastoglobules form linkage groups that are attached to each other and remain continuous with the thylakoid membrane by extensions of the half-lipid bilayer. Using three-dimensional tomography combined with immunolabeling techniques, we show that the plastoglobules contain the enzyme tocopherol cyclase (VTE1) and that this enzyme extends across the surface monolayer into the interior of the plastoglobules. These findings demonstrate that plastoglobules function as both lipid biosynthesis and storage subcompartments of thylakoid membranes. The permanent structural coupling between plastoglobules and thylakoid membranes suggests that the lipid molecules contained in the plastoglobule cores (carotenoids, plastoquinone, and tocopherol [vitamin E]) are in a dynamic equilibrium with those located in the thylakoid membranes.

A mechanism implicating plastoglobules in thylakoid disassembly during senescence and nitrogen starvation

“…Plastoquinol (PQH 2 ) and tocopherol (vitamin E) are the major constituents of the prenylquinone lipid family in plastoglobules, whereas phylloquinone (vitamin K) is also present but in minor concentrations (Lichtenthaler and Peveling 1966;Steinmuller and Tevini 1985;Austin et al 2006;Lohmann et al 2006;Gaude et al 2007;Zbierzak et al 2010;Lippold et al 2012).…”

Dual targeting of a mature plastoglobulin/fibrillin fusion protein to chloroplast plastoglobules and thylakoids in transplastomic tobacco plants

“…Plastoglobules are chloroplast lipid droplets that are attached to thylakoid membranes (Kessler et al 1999;Austin et al 2006) and function in diverse aspects of lipid metabolism (Eugeni Piller et al 2012). The proteome of plastoglobules has around two dozen proteins Ytterberg et al 2006;Lundquist et al 2012).…”

Not Just Fat: The Structure and Function of the Lipid Droplet

“…However, it has not been shown unequivocally that normal LDs retain membrane continuity with the ER as plastoglobules do with the thylakoid membrane ( Fig. 3C; Austin et al 2006). …”