Transport from the endoplasmic reticulum to the Golgi in plants: Where are we now?

Abstract

The biogenesis of about one third of the cellular proteome is initiated in the endoplasmic reticulum (ER), which exports proteins to the Golgi apparatus for sorting to their final destination. Notwithstanding the close proximity of the ER with other secretory membranes (e.g., endosomes, plasma membrane), the ER is also important for the homeostasis of non-secretory organelles such as mitochondria, peroxisomes, and chloroplasts. While how the plant ER interacts with most of the non-secretory membranes is largely unknown, the knowledge on the mechanisms for ER-to-Golgi transport is relatively more advanced. Indeed, over the last fifteen years or so, a large number of exciting results have contributed to draw parallels with non-plant species but also to highlight the complexity of the plant ER-Golgi interface, which bears unique features. This review reports and discusses results on plant ER-to-Golgi traffic, focusing mainly on research on COPII-mediated transport in the model species Arabidopsis thaliana.

Figure 1. Organization of ER and Golgi in plant cells

A. Diagram depicting the distribution of Golgi stacks (GA) with respect to the ER, which is distributed to the cell cortex beneath the plasma membrane and through the cytoplasm enveloping the vacuole (V) in the transvacuolar strands. B. Confocal image of an ER (ER-YK; red network) and Golgi marker (ST-GFP; green structures) in a tobacco leaf epidermal cell shows the close vicinity of the two organelles (Scale bar = 5 μm). Image courtesy of Dr. Giovanni Stefano, MSU-DOE PRL. C. Diagram depicting a Golgi stack with cis, medial and trans-cisternae. COPI vesicle deliver cargo from the Golgi to the ER while COPII carriers, whose morphology is still under discussion, facilitate ER protein export to the Golgi.

Figure 2. Models for ERES and Golgi organization in highly vacuolated cells

The kiss-and-run model predicts that Golgi stacks (GA) and ERES are not continuously associated and that ERES are stable. The model also predicts that Golgi stacks pick up cargo from ERES onto which they associate in a non-continuous fashion (blue arrow) (A). The secretory model unit predicts that a Golgi stack and an ERES are continuously associated. The existence of punctate structures labelled by COPII markers that are not in association with Golgi stacks (here indicated as mini-ERES) may be interpreted as sites for the biogenesis of new Golgi stacks or as sites that contribute to ER export to the Golgi. The verified continuous association of COPII coat markers with the Golgi stacks may indicate the partially uncoated COPII carriers at the Golgi. However, as discussed in the main text, the FRAP experiments with SEC16 indicate that the Golgi stacks are associated with bona-fide ERES. In the figure the large and small green ribbons at the ERES and Golgi stacks represent COPII labelling.