Vacuolar Sorting Receptor-Mediated Trafficking of Soluble Vacuolar Proteins in Plant Cells

Abstract

Vacuoles are one of the most prominent organelles in plant cells, and they play various important roles, such as degradation of waste materials, storage of ions and metabolites, and maintaining turgor. During the past two decades, numerous advances have been made in understanding how proteins are specifically delivered to the vacuole. One of the most crucial steps in this process is specific sorting of soluble vacuolar proteins. Vacuolar sorting receptors (VSRs), which are type I membrane proteins, are involved in the sorting and packaging of soluble vacuolar proteins into transport vesicles with the help of various accessory proteins. To date, large amounts of data have led to the development of two different models describing VSR-mediated vacuolar trafficking that are radically different in multiple ways, particularly regarding the location of cargo binding to, and release from, the VSR and the types of carriers utilized. In this review, we summarize current literature aimed at elucidating VSR-mediated vacuolar trafficking and compare the two models with respect to the sorting signals of vacuolar proteins, as well as the molecular machinery involved in VSR-mediated vacuolar trafficking and its action mechanisms.

Keywords: molecular machinery; protein trafficking to vacuoles; soluble vacuolar proteins; sorting signals; vacuolar sorting receptors.

Figure 1

Vacuolar sorting receptor (VSR)-mediated soluble cargo transport from the trans-Golgi network (TGN) to the prevacuolar compartment (PVC): Model I. Nascent soluble vacuolar proteins are initially targeted to the endoplasmic reticulum (ER). Subsequently, they are transported to the Golgi apparatus in a COPII-dependent manner. Traveling from cis-Golgi to the TGN occurs via cisternal maturation. At the TGN, VSRs recognize their cargoes and receptor-cargo complexes are packaged into clathrin-coated vesicles with the help of AP-1 and/or EpsinR1. Clathrins and adaptor proteins dissociate from the clathrin-coated vesicles (CCVs) after vesicle release. After fusion of vesicles harboring vacuolar cargoes with the PVC, VSRs release their cargoes. VSRs are recognized by VPS29-containing retromers and recycle back to the TGN for the next round of cargo sorting. The exact mechanism of how retromers recognizes VSRs at the PVC remains elusive. It is also unknown whether retromers dissociate from the recycling vesicles in plants; thus retromers on the recycling vesicle are indicated with dotted lines. VSRs are also involved in trafficking of proteins to the PSV at the TGN via CCVs. However, it is not known which adaptors are involved in this pathway. It is also not clear whether the PVCs for the lytic vacuole and PSV are the same compartment or two different organelles. m, process occurring through maturation.

Figure 2

Vacuolar sorting receptor (VSR)-mediated cargo trafficking from the endoplasmic reticulum (ER) to the trans-Golgi network (TGN): Model II. After targeting of nascent vacuolar proteins to the ER, the folded vacuolar proteins bind to VSRs in the ER. Ca²⁺ plays a critical role in this binding. VSR-cargo complexes are transported to the cis-Golgi via COPII vesicles. The complexes are maintained until they reach the TGN, where the cargoes are released from the VSR due to the low concentrations of Ca²⁺. VSRs are selectively recycled back to the ER by retromer. Vacuolar cargo-enriched domains of the TGN mature into the prevacuolar compartment (PVC). The endosomal sorting complexes required for transport (ESCRT) machinery might be involved in this maturation step. m, process occurring through maturation.