The signaling lipid phosphatidylinositol-3,5-bisphosphate targets plant CLC-a anion/H+ exchange activity

EMBO Rep. 2017 Jul;18(7):1100-1107. doi: 10.15252/embr.201643814. Epub 2017 May 23.

Abstract

Phosphatidylinositol-3,5-bisphosphate (PI(3,5)P2) is a low-abundance signaling lipid associated with endo-lysosomal and vacuolar membranes in eukaryotic cells. Recent studies on Arabidopsis indicated a critical role of PI(3,5)P2 in vacuolar acidification and morphology during ABA-induced stomatal closure, but the molecular targets in plant cells remained unknown. By using patch-clamp recordings on Arabidopsis vacuoles, we show here that PI(3,5)P2 does not affect the activity of vacuolar H+-pyrophosphatase or vacuolar H+-ATPase. Instead, PI(3,5)P2 at low nanomolar concentrations inhibited an inwardly rectifying conductance, which appeared upon vacuolar acidification elicited by prolonged H+ pumping activity. We provide evidence that this novel conductance is mediated by chloride channel a (CLC-a), a member of the anion/H+ exchanger family formerly implicated in stomatal movements in Arabidopsis H+-dependent currents were absent in clc-a knock-out vacuoles, and canonical CLC-a-dependent nitrate/H+ antiport was inhibited by low concentrations of PI(3,5)P2 Finally, using the pH indicator probe BCECF, we show that CLC-a inhibition contributes to vacuolar acidification. These data provide a mechanistic explanation for the essential role of PI(3,5)P2 and advance our knowledge about the regulation of vacuolar ion transport.

Keywords: patch‐clamp; phosphoinositide; proton antiport; vacuolar acidification.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Anions
  • Arabidopsis / metabolism*
  • Arabidopsis Proteins / metabolism
  • Biological Transport
  • Chloride Channels / metabolism*
  • Hydrogen-Ion Concentration
  • Ion Transport
  • Lysosomes / metabolism
  • Phosphatidylinositol Phosphates / metabolism*
  • Signal Transduction*
  • Vacuolar Proton-Translocating ATPases / metabolism
  • Vacuoles / metabolism

Substances

  • Anions
  • Arabidopsis Proteins
  • Chloride Channels
  • Phosphatidylinositol Phosphates
  • phosphatidylinositol 3,5-diphosphate
  • Vacuolar Proton-Translocating ATPases