The puzzle of chloroplast vesicle transport - involvement of GTPases

Abstract

In the cytosol of plant cells vesicle transport occurs via secretory pathways among the endoplasmic reticulum network, Golgi bodies, secretory granules, endosome, and plasma membrane. Three systems transfer lipids, proteins and other important molecules through aqueous spaces to membrane-enclosed compartments, via vesicles that bud from donor membranes, being coated and uncoated before tethered and fused with acceptor membranes. In addition, molecular, biochemical and ultrastructural evidence indicates presence of a vesicle transport system in chloroplasts. Little is known about the protein components of this system. However, as chloroplasts harbor the photosynthetic apparatus that ultimately supports most organisms on the planet, close attention to their pathways is warranted. This may also reveal novel diversification and/or distinct solutions to the problems posed by the targeted intra-cellular trafficking of important molecules. To date two homologs to well-known yeast cytosolic vesicle transport proteins, CPSAR1 and CPRabA5e (CP, chloroplast localized), have been shown to have roles in chloroplast vesicle transport, both being GTPases. Bioinformatic data indicate that several homologs of cytosolic vesicle transport system components are putatively chloroplast-localized and in addition other proteins have been implicated to participate in chloroplast vesicle transport, including vesicle-inducing protein in plastids 1, thylakoid formation 1, snowy cotyledon 2/cotyledon chloroplast biogenesis factor, curvature thylakoid 1 proteins, and a dynamin like GTPase FZO-like protein. Several putative potential cargo proteins have also been identified, including building blocks of the photosynthetic apparatus. Here we discuss details of the largely unknown putative chloroplast vesicle transport system, focusing on GTPase-related components.

Keywords: COPI/II; GTPase; Rab; SAR1; cargo protein; chloroplast; clathrin; vesicle transport.

FIGURE 1

Detection of CPSAR1 in Arabidopsis chloroplasts. Transmission electron micrograph of immunogold-labeled sections of leaves after low temperature incubation (Garcia et al., 2010) showing the presence of CPSAR1 in the stroma (white arrow) and at both the envelope and vesicle membranes (black arrows). E, envelope; V, vesicle; T, thylakoids. Bar 0.5 μm.

FIGURE 2

Schematic diagram of vesicle formation and movement in chloroplasts. Proteins included are those with suggested involvement in chloroplast vesicle transport, and verified to be chloroplast localized. VIPP1 (pink), FZL (green), and THF1 (yellow) are located both at the donor membrane (inner envelope) and the acceptor membrane (thylakoids), and could thus participate in both fission and fusion of vesicles. CPSAR1 (violet) is located at the donor membrane, the vesicle and in the stroma, indicating that it plays a similar role as the cytosolic Sar1, i.e., in an active GTP-bound state it helps to form vesicles, and in an inactive GDP-bound state it is recycled back to the donor membrane for a subsequent cycle. THF1 (yellow) and CPRabA5e (blue) are both located in the stroma and the acceptor membrane (thylakoids) may interact with the vesicle just prior to fusion and facilitating this step. SCO2/CYO1 (turquoise) and CURT1 (black) are located at the acceptor membrane and may interact with vesicles for the transport of molecules, e.g., cargo protein(s; red) and facilitating the fusion (delivery) step.