Phosphatidic Acid Directly Regulates PINOID-Dependent Phosphorylation and Activation of the PIN-FORMED2 Auxin Efflux Transporter in Response to Salt Stress

Abstract

Remodeling of auxin distribution during the integration of plant growth responses with the environment requires the precise control of auxin influx and efflux transporters. The plasma membrane-localized PIN-FORMED (PIN) proteins facilitate auxin efflux from cells, and their activity is regulated by reversible phosphorylation. How PIN modulates plant cellular responses to external stresses and whether its activity is coordinated by phospholipids remain unclear. Here, we reveal that, in Arabidopsis (Arabidopsis thaliana), the phosphatidic acid (PA)-regulated PINOID (PID) kinase is a crucial modulator of PIN2 activity and auxin redistribution in response to salt stress. Under salt stress, loss of phospholipase D function impaired auxin redistribution and resulted in markedly reduced primary root growth; these effects were reversed by exogenous PA. The phospholipase D-derived PA interacted with PID and increased PID-dependent phosphorylation of PIN2, which activated auxin efflux and altered auxin accumulation, promoting root growth when exposed to salt stress. Ablation of the PA binding motif not only diminished PID accumulation at the plasma membrane but also abolished PA-promoted PID phosphorylation of PIN2 and its function in coping with salt stress; however, this ablation did not affect inflorescence and cotyledon development or PIN2-dependent gravitropic and halotropic responses. Our data indicate a role for PA in coupling extracellular salt signaling to PID-directed PIN2 phosphorylation and polar auxin transport, highlighting the importance of lipid-protein interactions in the spatiotemporal regulation of auxin signaling.

Phospholipase D‐derived phosphatidic acid promotes root hair development under phosphorus deficiency by suppressing vacuolar degradation of PIN‐FORMED2

“…PLD‐derived PA plays crucial roles in plant responses to various environmental stresses, such as salinity and P deficiency (Li et al , ; Wang et al , ). PA interacts with protein kinase PID and increases the PID‐dependent phosphorylation of PIN2, which enhances the auxin efflux activity and PIN2 accumulation at the plasma membrane under salt stress (Wang et al , ). Our results demonstrated that PLDζ2‐derived PA that is induced by P deficiency mediates the vacuolar degradation of PIN2 to increase the plant response to low P tolerance.…”

“…PLD-derived PA plays crucial roles in plant responses to various environmental stresses, such as salinity and P deficiency (Li et al, 2006;Wang et al, 2019). PA interacts with protein kinase PID and increases the PID-dependent phosphorylation of PIN2, which enhances the auxin efflux activity and PIN2 accumulation at the plasma membrane under salt stress (Wang et al, 2019).…”

Root Growth Adaptation is Mediated by PYLs ABA Receptor‐PP2A Protein Phosphatase Complex

“…[55,57,58] Besides, PIN proteins have also been reported to be phosphorylated by MITOGEN-ACTIVATED PRO-TEIN KINASEs (MPKs), which inhibit the polar targeting and thus the function of PINs. [55,57,58] Besides, PIN proteins have also been reported to be phosphorylated by MITOGEN-ACTIVATED PRO-TEIN KINASEs (MPKs), which inhibit the polar targeting and thus the function of PINs.…”

A lipid code-dependent phosphoswitch directs PIN-mediated auxin efflux in Arabidopsis development

“…Multiple lines of genetic evidence suggest that the local membrane status regulates polar localization and recycling of PIN proteins. For example, mutants defective in phospholipid biosynthesis or metabolism exhibit strong defects in various growth and developmental processes, for which mislocalization of PIN proteins account for many of those phenotypes 19, 48–53 . Our studies uncover a novel layer of participation of lipids, in regulating PIN transporters, at the level of activity via polarizing a PDK1-mediated phosphorylation cascade.…”

“…In contrast to PID, D6PKs and PAX phosphorylate basal-localized PINs to regulate their activity 17 . To date, little is known about the upstream regulatory mechanism by which this phosphorylation increases or declines, except for that both PID 18, 19 and D6PK 20 have been reported to bind phospholipids, which might determine their subcellular localizations.…”