Phospholipids in Salt Stress Response

Abstract

High salinity threatens crop production by harming plants and interfering with their development. Plant cells respond to salt stress in various ways, all of which involve multiple components such as proteins, peptides, lipids, sugars, and phytohormones. Phospholipids, important components of bio-membranes, are small amphoteric molecular compounds. These have attracted significant attention in recent years due to the regulatory effect they have on cellular activity. Over the past few decades, genetic and biochemical analyses have partly revealed that phospholipids regulate salt stress response by participating in salt stress signal transduction. In this review, we summarize the generation and metabolism of phospholipid phosphatidic acid (PA), phosphoinositides (PIs), phosphatidylserine (PS), phosphatidylcholine (PC), phosphatidylethanolamine (PE) and phosphatidylglycerol (PG), as well as the regulatory role each phospholipid plays in the salt stress response. We also discuss the possible regulatory role based on how they act during other cellular activities.

Keywords: phosphatidic acid; phosphatidylcholine; phosphatidylethanolamine; phosphatidylglycerol; phosphatidylserine; phosphoinositide; phospholipids; salt stress.

Figure 1

The regulatory role of PLD-derived PA in the salt stress response of plants. PA level is induced by salt stress. PLDα1-derived PA binds and activates MPK6, MKK7, and MKK9 to phosphorylate SOS1 and activate its activity in extruding excess Na⁺ out of the cells under salt stress; PLDα1-derived PA can bind MAP65-1 and regulate it activity in microbutule polymerization and bundling process under salt stress, and this process may regulate cellulose synthesis in salt stress; PLDα-1- and PLDδ-derived PA also binds PINOID and stimulates its activity in phosphorylating PIN2 to participate in salt stress response through the regulation of auxin signaling; PA regulates root growth and architecture through the interaction of Snrk2.4; PA also regulates PM H⁺-ATPase activity, K⁺-Na⁺ homeostasis, proline and sugar synthesis through the unidentified proteins. PM, plasma membrane; PA, phosphatidic acid; SOS1, salt overly sensitive 1; PIN2, PIN-FORMED 2; MPK, mitogen-activated protein kinase; MKK, mitogen-activated protein kinase kinase; MAP65-1, microtubule-associated protein 65-1; SnRK2.4, SNF1-related protein kinase 2.4.

Figure 2

The regulatory role of PI4P in the salt stress response of plants. PI4P level is induced by salt stress. PI binds PM H⁺-ATPase and inhibits its activity under normal conditions without salt stress; however, under salt stress condition, PI4P derived from PI stimulates SOS1 activity and excludes excess Na⁺ from plant cells; PI4P also mediates the internalization of CESA3 and KORRIGAN1 from the plasma membrane, which may participate in salt stress response through the regulation of cellulose synthesis; PI4P at the plasma membrane generates an electrostatic field, which may interact with PINOID, BKI1, MAKRs, and PUB13, and participate in salt stress response. PI, phosphatidylinositol; PI4P, PI 4-phosphate; PS, phosphatidylserine; PM: plasma membrane; SOS1, salt overly sensitive 1; BKI1, BRI1 kinase inhibitor 1; MAKRs, membrane associated kinase regulators; PUB13: PLANT U-BOX13; BR, brassinosteroid; SA, salicylic acid.

Figure 3

The regulatory role of PI(4,5)P₂ in the salt stress response of plants. PI(4,5)P₂ level is induced by salt stress. PI(4,5)P₂ at the plasma membrane interacts with SYT1 and mediates the salt stress-induced ER and plasma membrane connectivity. The membrane trafficking regulation of PIN2 by PI(4,5)P₂ may participate in salt stress response through the regulation of auxin signaling. PUT3, a polyamine uptake transporter, interacts with SOS1 and SOS2 under salt stress condition, and the application of spermine can induce PI(4,5)P₂ accumulation, which indicate a possible link between polyamine, PI(4,5)P₂ and Na⁺ extrusion under salt stress condition. The hydrolysis of PI(4,5)P₂ by PI-PLC can produce inositol phosphates, which is involved in Ca²⁺ stimulation under salt stress condition, and ABA may participate in this process by the regulation of PLC activity. PI-PLC may also participate in salt stress response by the regulation of proline synthesis and ER stress response, and the further catalysis by DGK can improve plant salt tolerance through PA signaling. PI, phosphatidylinositol; PI(4,5)P₂, PI 4,5-bisphosphate; PM, plasma membrane; SYT1, synaptotagmin 1; PM, plasma membrane; ER, endoplasmic reticulum; ABA, abscisic acid; PI-PLC, phosphatidylinositol-phospholipase C; PIN2, PIN-FORMED 2; DGK, diacylglycerol kinase; PUT3: polyamine uptake transporter 3; SOS, salt overly sensitive.

Figure 4

The regulatory role of PI3P and PI(3,5)P₂ in the salt stress response of plants. PI3P and PI(3,5)P 2 mainly reside in late endosomes. PI3K and its product PI3P play a role in ROS production under salt stress, and rbohD/F may mediate this process. PI3P interacts with SH3P2, which may mediate autophagosome formation under salt stress. PI3K may also participate in salt stress response by its regulation function on ethylene, GA, and MeJA signalings, and proline biosynthesis. PI3P and PI(3,5)P₂ regulate plant salt tolerance by their regulatory roles on the recycling of PINs and CESA from late endosomes under salt stress. PI(3,5)P₂ can interact with ROF1 and regulate plant seed germination under salt stress. The hydrolysis of PI(3,5)P₂ by PI-PLC can produce inositol phosphates, which is involved in Ca²⁺ stimulation under salt stress condition, and ABA may participate in this process by the regulation of PLC activity. The hydrolysis of PI(3,5)P₂ by PI-PLC and the further catalysis by DGK can improve plant salt tolerance through PA signaling. PI3P, PI 3-phosphate; PI(3,5)P₂, PI 3,5-bisphosphate; PM, plasma membrane; PIN, PIN-FORMED; CESA: cellulose synthase; SH3P2, SH3 domain-containing protein 2; PI-PLC, phosphatidylinositol-phospholipase C; DGK, diacylglycerol kinase; PA, phosphatidic acid; GA, gibberellin; MeJA, methyl jasmonic acid; ROS, reactive oxygen species; rbohD/F, respiratory burst oxidase homolog D/F.

Figure 5

The regulatory role of PS in the salt stress response of plants. PS level is induced by salt stress. PS regulates K⁺/Na⁺ homeostasis by regulating PM H⁺-ATPase activity and SOS1 activity under salt stress. PS, together with PI4P and PA, regualtes the electronegative features of plasma membrane in plants, which may participate in salt stress response through the unknown proteins not identified yet. PS, phosphatidylserine; PA, phosphatidic acid; PI4P, PI 4-phosphate; PM, plasma membrane; SOS, salt overly sensitive.

Figure 6

The regulatory role of PC and PE in the salt stress response of plants. PC improves plant salt tolerance by stabilizing the cell membrane through its conversion to PE, PS, PG, and ACBP1 and PLDδ mediate this process; The biosynthesis of PC can be regulated by SnRK1 and ER stress; The further hydrolysis of PC and PE can improce plant salt tolerance through the PA signaling and the glycine betaine signaling. PG, phosphatidylglycerol; PS, phosphatidylserine; PC, phosphatidylcholine; PE, phosphatidylethanolamine; PM, plasma membrane; ACBP1, Acyl-CoA-binding protein 1; PLD, phospholipase D; ER, endoplasmic reticulum; CEK1, choline/ethanolamine kinase 1; SnRK1; NPC, non-specific phospholipase C; DGK, diacylglycerol kinase.