Plant trans-golgi network/early endosome pH regulation requires cation chloride cotransporter (CCC1)

  1. Daniel Walter McKay
  2. Heather E McFarlane
  3. Yue Qu
  4. Apriadi Situmorang
  5. Matthew Gilliham
  6. Stefanie Wege  Is a corresponding author
  1. University of Adelaide, Australia
  2. University of Toronto, Canada

Abstract

Plant cells maintain a low luminal pH in the Trans-Golgi-Network/Early Endosome (TGN/EE), the organelle in which the secretory and endocytic pathways intersect. Impaired TGN/EE pH regulation translates into severe plant growth defects. The identity of the proton pump and proton/ion antiporters that regulate TGN/EE pH have been determined, but an essential component required to complete the TGN/EE membrane transport circuit remains unidentified - a pathway for cation and anion efflux. Here, we have used complementation, genetically encoded fluorescent sensors, and pharmacological treatments to demonstrate that Arabidopsis Cation Chloride Cotransporter (CCC1) is this missing component necessary for regulating TGN/EE pH and function. Loss of CCC1 function leads to alterations in TGN/EE-mediated processes including endocytic trafficking, exocytosis and response to abiotic stress, consistent with the multitude of phenotypic defects observed in ccc1 knockout plants. This discovery places CCC1 as a central component of plant cellular function.

Data availability

Data generated or analysed during this study are included in the manuscript and supporting file; Source Data files have been provided for Figures 2-7. Original images files can be accesses here: https://doi.org/10.25909/17256545https://doi.org/10.25909/17256515https://doi.org/10.25909/17256467https://doi.org/10.25909/17256428

Article and author information

Author details

  1. Daniel Walter McKay

    ARC Centre of Excellence in Plant Energy Biology, University of Adelaide, Glen Osmond, Australia
    Competing interests
    No competing interests declared.
  2. Heather E McFarlane

    Department of Cell and Systems Biology, University of Toronto, Toronto, Canada
    Competing interests
    Heather E McFarlane, Reviewing editor, eLife.
  3. Yue Qu

    ARC Centre of Excellence in Plant Energy Biology, University of Adelaide, Glen Osmond, Australia
    Competing interests
    No competing interests declared.
  4. Apriadi Situmorang

    ARC Centre of Excellence in Plant Energy Biology, University of Adelaide, Glen Osmond, Australia
    Competing interests
    No competing interests declared.
  5. Matthew Gilliham

    ARC Centre of Excellence in Plant Energy Biology, University of Adelaide, Adelaide, Australia
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0666-3078
  6. Stefanie Wege

    ARC Centre of Excellence in Plant Energy Biology, University of Adelaide, Glen Osmond, Australia
    For correspondence
    stefanie.wege@adelaide.edu.au
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7232-5889

Funding

Australian Research Council (DE160100804)

  • Stefanie Wege

Australian Research Council (FT130100709)

  • Matthew Gilliham

Australian Research Council (CE140100008)

  • Matthew Gilliham

Australian Research Council (DE170100054)

  • Heather E McFarlane

Canada Research Chairs Program

  • Heather E McFarlane

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Copyright

© 2022, McKay et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Daniel Walter McKay
  2. Heather E McFarlane
  3. Yue Qu
  4. Apriadi Situmorang
  5. Matthew Gilliham
  6. Stefanie Wege
(2022)
Plant trans-golgi network/early endosome pH regulation requires cation chloride cotransporter (CCC1)
eLife 11:e70701.
https://doi.org/10.7554/eLife.70701

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https://doi.org/10.7554/eLife.70701