Biogenesis of Green Plant Thylakoid Membranes

Abstract

Biogenesis of chloroplast thylakoid membranes involves the synthesis of proteins, lipids, and pigments and their assembly into an elaborate membrane system containing four different supramolecular photosynthetic complexes. In addition, because these biogenetic processes begin during early stages of plastid development, where plastids contain little internal membrane, thylakoid membrane formation also entails substantial membrane flow from the envelope. Most thylakoid proteins are encoded in the nucleus and synthesized in the cytosol—the remainder are encoded and synthesized in the plastid. Nuclear-encoded thylakoid proteins are imported into the plastid by a translocation apparatus that evolved after endosymbiosis, and the imported proteins are routed into thylakoids by translocation systems that evolved in prokaryotes prior to endosymbiosis. Four different translocation pathways have been described for thylakoids. The Sec pathway transports proteins in an unfolded conformation to the lumen; the ΔpH-dependent/Tat pathway transports folded proteins to the lumen; the spontaneous pathway integrates one class of membrane proteins; the cpSRP pathway appears dedicated to targeting and assembly of multispanning LHC proteins. Assembly of LHC proteins represents an interesting situation. A novel component of the cpSRP system has been employed to specifically adapt the SRP system to posttranslational integration. In addition, LHC proteins require chlorophyll for their integration and stability. Thus the site(s) of chlorophyll synthesis likely determine the exact site of LHC integration. Although the thylakoid membrane is the site of translocation/integration in immature and mature chloroplasts, evidence increasingly points to the inner envelope membrane as the site of insertion during very early plastid developmental stages, and envelope invagination combined with vesicular traffic as the vehicle for relocating lipids and proteins to the plastid interior. In such a scenario, the translocons and chlorophyll biosynthetic enzymes should be located in the envelope in developing proplastids. Recent cloning of the genes for these proteins should soon allow a test of this hypothetical mechanism.