Plant phospholipid signaling: "in a nutshell"

Abstract

Since the discovery of the phosphoinositide/phospholipase C (PI/PLC) system in animal systems, we know that phospholipids are much more then just structural components of biological membranes. In the beginning, this idea was fairly straightforward. Receptor stimulation activates PLC, which hydrolyses phosphatidylinositol4,5-bisphosphate [PtdIns(4,5)P2] into two second messengers: inositol 1,4,5-trisphosphate (InsP3) and diacylglycerol (DG). While InsP3 difuses into the cytosol and triggers the release of calcium from an internal store via ligand-gated calcium channels, DG remains in the membrane where it recruits and activates members of the PKC family. The increase in calcium, together with the change in phosphorylation status, (in)activates a variety of protein targets, leading to a massive reprogramming, allowing the cell to appropriately respond to the extracellular stimulus. Later, it became obvious that not just PLC, but a variety of other phospholipid-metabolizing enzymes were activated, including phospholipase A, phospholipase D, and PI 3-kinase. More recently, it has become apparent that PtdIns4P and PtdIns(4,5)P2 are not just signal precursors but can also function as signaling molecules themselves. While plants contain most of the components described above, and evidence for their role in cell signaling is progressively increasing, major differences between plants and the mammalian paradigms exist. Below, these are described "in a nutshell."

Fig. 1.

Plant PI/PLC signaling: Differences and similarities to the mammalian paradigm. Higher plants lack both InsP₃ receptor, a ligand-gated Ca²⁺ channel, and PKC; hence, these are striked-out (X). Instead, plants seem to use their phosphorylated products, InsP₆ and PA, as signaling molecules. PA can also be generated by PLD and is attenuated by PA kinase (PAK), a novel lipid kinase that is absent from mammalian cells. PAK generates diacylglycerolpyrophosphate (DGPP), which might function as a signaling molecule itself (19). Plant PLCs belong to the PLCζ subfamily. It is not known how they are regulated but not through heterotrimeric G-proteins (G), which is therefore striked out. Plant PtdIns(4,5)P₂ (PIP₂) quantities are extremely low, and plant PLCs lack the PH domain (Fig. 2). Instead, PtdIns4P (PIP) is a better candidate to be the in vivo PLC substrate. The resulting InsP₂ can be phosphoryated to InsP₆ via two dual-specificity inositolpolyphosphate kinases (IPK), while DG is phosphorylated to PA via DGK. Evidence is also emerging that PtdIns4P and PtdIns(4,5)P₂ themselves function as signaling molecules, involving membrane trafficking, organization of the cytoskeleton, and regulation of ion channels. In such a scenario, PLC would function as an attenuator of PIP and PIP₂ signaling. Solid arrows indicate metabolic conversions. Dashed arrows represent mechanisms of regulation.

Fig. 2.

Domain structure and organization of PI/PLC isozymes. Plant PLCs belong to the most simple group, the PLCζs. PLCη undergoes alternative splicing, generating variable C termini with a PDZ binding motif being only present in the longer forms. Adapted from (11).