Connection matters: Pi Sensing and ER Quality Control

Abstract:

Limited access to inorganic phosphate (Pi), often restricted by Pi-metal (Fe, Al) inter­actions in soil, guides root development. Growing root tips scout the essential but immobile mineral nutrient; however, the mechanisms monitoring external Pi status are unknown. In Arabidopsis thaliana root meristems, two inter­acting genes, PDR2 (P5-type ATPase AtP5A) and LPR1 (ferroxidase), are central to Fe-depen­dent Pi sensing. While LPR1, a specific bacterial-type ferroxidase, is key to local Pi monitoring, PDR2 restricts LPR1 function by maintaining root tip Fe homeostasis. Our comparative genetic and biochemical studies of Arabidopsis mutants defective in Pi deficiency response, ER stress response, and autophagy indicate that ER stress-dependent autophagy is rapidly activated as part of the developmental response of the root apex to Pi limitation and implicates PDR2/AtP5A as a central mediator of this process. Recent biochemical and genetic data on PDR2/AtP5A orthologues in S. cere­visiae and C. elegans uncovered ER-resident P5A-type ATPases to act as trans­mem­­brane helix dislocases, which facilitate the extraction of mistargeted tail-an­chored mem­brane proteins, to enforce ER protein quality control. To dissect the link between PDR2/AtP5A and the autophagic pathway and to understand the significance of Pi limitation-induced autophagy in plants, we used Tandem Mass Tag (TMT) mass spec­tro­metry as a first, untargeted approach to monitor global changes in the proteome of root tips. In addition to core autophagy proteins, which are known to be involved in and degraded by autophagy, our results indicate that Pi deprivation acts as a potent inducer of ER stress and ER stress-mediated autophagy, and therefore specifically influences proteostasis. The comparative proteomic data in combination with the recently obtained Pi-dependent PDR2-interactome point to PDR2 as a major mediator for coordinating local root Pi sensing, ER quality control, and ER stress-activated autophagy in Arabidopsis roots