Crosstalk between Phospholipase D and Sphingosine Kinase in Plant Stress Signaling

Abstract

The activation of phospholipase D (PLD) produces phosphatidic acid (PA), whereas plant sphingosine kinase (SPHK) phosphorylates long-chain bases to generate long-chain base-1-phosphates such as phytosphingosine-1-phosphate (phyto-S1P). PA and phyto-S1P have been identified as lipid messengers. Recent studies have shown that PA interacts directly with SPHKs in Arabidopsis, and that the interaction promotes SPHK activity. However, SPHK and phyto-S1P act upstream of PLDα1 and PA in the stomatal response to abscisic acid (ABA). These findings indicate that SPHK/phyto-S1P and PLD/PA are co-dependent in the amplification of lipid messengers, and that crosstalk between the sphingolipid- and phospholipid-mediated signaling pathways may play important roles in plant stress signaling.

Keywords: abscisic acid; lipid signaling; phosphatidic acid; phospholipase D; phytosphingosine; sphingosine kinase.

Figure 1

Generation of PA from phospholipids and PA target proteins functionally characterized in plants. PA is generated via two pathways during stress responses: PLD hydrolyzes phospholipid to generate PA, and PLC hydrolyzes phospholipid to generate DAG which can be phosphorylated by DAG kinase (DGK). PA has been found to interact with target proteins to regulate cellular functions. Examples of PA regulation of target proteins are discussed in the text and the references are cited in the text. *Indicates that PA is generated from PLD while others are not determined.

Figure 2

Phosphorylation of sphingosine and phytosphingosine by SPHK and the interaction SPHK and PA. (A) SPHK catalyzes the formation of S1P or phyto-S1P from sphingosine or phytosphingosine. S1P or phyto-S1P can be degraded by S1P phosphatase (SPP) or S1P lyase (not shown). (B) Surface plasmon resonance (SPR) analysis of interaction of PA with SPHK1. Liposomes containing PC only or PC plus 16:0/16:0 or 18:1/18:1 PA were used to analyze the interaction. Liposome containing of PC did not bind to SPHK1. Liposomes containing both PC and PA (16:0/16:0 or 18:1/18:1) bound to SPHK1. (B) is based on data from Guo et al., .

Figure 3

Proposed model for crosstalk between PLDα1/PA and SPHK/phyto-S1P in ABA-mediated stomatal closure signaling pathway. ABA may be perceived by the receptor (PYR/PYL/RCAR) in the cytosol, leading to activation of SPHK to produce phyto-S1P which initiates a cascade to activate PLDα1. PLDα1 hydrolyzes phospholipids to increase PA level in membrane (plasma membrane and tonoplast). PLDα1-deprived PA promotes the ABA effect through three targets: (i) PA binds to ABI1 and tethers ABI1 to the membrane to inhibit its negative effect; (ii) PA stimulates plasma membrane-localized NADPH oxidase to form secondary messenger: ROS; (iii) Increased PA in tonoplast interacts with SPHK and promotes its activity to form a positive loop. PLDα1/PA- and SPHK/phyto-S1P-mediated signaling pathway activates ion channel activity, leading to ion flux in guard cell and finally stomatal closure. Note that this model summarizes the crosstalk between PLDα1/PA and SPHK/phyto-S1P and their roles in ABA-mediated stomatal closure, not all ABA signaling components are included in this model. Arrow indicates positive regulation, bar indicates repression. Red arrow represents reactions which produce secondary signaling molecules.