Chloroplast envelope membranes: a dynamic interface between plastids and the cytosol

Abstract

Chloroplasts are bounded by a pair of outer membranes, the envelope, that is the only permanent membrane structure of the different types of plastids. Chloroplasts have had a long and complex evolutionary past and integration of the envelope membranes in cellular functions is the result of this evolution. Plastid envelope membranes contain a wide diversity of lipids and terpenoid compounds serving numerous biochemical functions and the flexibility of their biosynthetic pathways allow plants to adapt to fluctuating environmental conditions (for instance phosphate deprivation). A large body of knowledge has been generated by proteomic studies targeted to envelope membranes, thus revealing an unexpected complexity of this membrane system. For instance, new transport systems for metabolites and ions have been identified in envelope membranes and new routes for the import of chloroplast-specific proteins have been identified. The picture emerging from our present understanding of plastid envelope membranes is that of a key player in plastid biogenesis and the co-ordinated gene expression of plastid-specific protein (owing to chlorophyll precursors), of a major hub for integration of metabolic and ionic networks in cell metabolism, of a flexible system that can divide, produce dynamic extensions and interact with other cell constituents. Envelope membranes are indeed one of the most complex and dynamic system within a plant cell. In this review, we present an overview of envelope constituents together with recent insights into the major functions fulfilled by envelope membranes and their dynamics within plant cells.

Figure 1. Lipid metabolism and trafficking connected to galactolipid synthesis in the chloroplast envelope

Whereas prokaryotic type galactolipids are issued from phosphatidate (PAP) synthesized in the chloroplast, formation of eukaryotic type galactolipids is dependent on the supply to the envelope of some PC derivatives formed in the ER: either diacylglycerol (DAG_E) or phosphatidate (PA_E). PAP converting PA to DAG is present in the envelope but only in the inner membrane. Altogether, a number of lipid transfers noted by dashed arrows are important to build plastid membranes. Under phosphate deprivation, DGDG formation is stimulated corresponding to activation or stimulation of a part of the galactolipid synthesis pathway indicated in red. Under these conditions, DGDG is transferred through membrane contact between chloroplast and mitochondria.