Regulatory roles of phosphoinositides in membrane trafficking and their potential impact on cell-wall synthesis and re-modelling

Abstract

Background: Plant cell walls are complex matrices of carbohydrates and proteins that control cell morphology and provide protection and rigidity for the plant body. The construction and maintenance of this intricate system involves the delivery and recycling of its components through a precise balance of endomembrane trafficking, which is controlled by a plethora of cell signalling factors. Phosphoinositides (PIs) are one class of signalling molecules with diverse roles in vesicle trafficking and cytoskeleton structure across different kingdoms. Therefore, PIs may also play an important role in the assembly of plant cell walls.

Scope: The eukaryotic PI pathway is an intricate network of different lipids, which appear to be divided in different pools that can partake in vesicle trafficking or signalling. Most of our current understanding of how PIs function in cell metabolism comes from yeast and mammalian systems; however, in recent years significant progress has been made towards a better understanding of the plant PI system. This review examines the current state of knowledge of how PIs regulate vesicle trafficking and their potential influence on plant cell-wall architecture. It considers first how PIs are formed in plants and then examines their role in the control of vesicle trafficking. Interactions between PIs and the actin cytoskeleton and small GTPases are also discussed. Future challenges for research are suggested.

Keywords: PI; Phosphoinositide; actin; cytoskeleton; endocytosis; exocytosis; plant cell wall; small GTPase; vesicle trafficking.

Fig. 1.

The plant PI pathway. The plant PI pathway consists of different PIs, and the kinases and phosphatases involved in their formation. The kinases are named depending on the carbon head group they phosphorylate. For example, the kinase PI3 K converts the hydroxyl group on the 3rd position of the head group of PtdIns to form PtdIns3P, and PtdIns(4,5)P₂ is formed by phosphorylation of PtdIns4P at the 5th head group in the presence of PI4P 5-kinases. PI3P 5-kinases phosphorylate the 5th head group of PtdIns3P to give rise to PtdIns(3,5)P₂. PtdIns5P is present in plants but an enzyme capable of producing it has not yet been identified. Some phosphatases have also been identified that are capable of dephosphorylation of some bi-phosphates to give PtdIns3P and PtdIns4P.

Fig. 2.

Potential functions of PIs in endomembrane trafficking and in actin organization in plant cells. (A) Endocytosis: RAC GTPases may recruit PI4P 5-kinases to the PM where they start producing PtdIns(4,5)P₂ (yellow line). At the initial stages of clathrin-mediated endocytosis (CME), AP2 complex and other accessory proteins may hypothetically bind to PtdIns(4,5)P₂ at the PM, as this has been shown in animal cells. This could initiate cargo recognition and vesicle nucleation with the help of clathrin triskelia. One of the cargoes presumably internalized via CME is cellulose synthase (CesA). (B) Secretion: PtdIns4P at the TGN can aid in the formation of secretory vesicles (SVs) and, along with ECHIDNIA/YIP-related vesicles, may secrete pectins/hemicelluloses to the apoplast. On the other hand, PtdIns3P appears to be involved in trafficking between the TGN and vacuole. It is plausible that one of the tethering factors, the exocyst complex, can bind to the PtdIns(4,5)P₂ at the PM, as shown in other eukaryotic systems. In these studies, the binding may occur via the SEC3A and EXO70 subunits, which then facilitate secretion of different cargoes to the cell surface. (C) Actin cytoskeleton: PtdIns(4,5)P₂ can bind to actin depolymerization factor (ADF) and prevent actin depolymerization, which may in turn have an effect on exocytosis of CesAs to the plasma membrane.