The yeast H+-ATPase Pma1 promotes Rag/Gtr-dependent TORC1 activation in response to H+-coupled nutrient uptake

  1. Elie Saliba
  2. Minoas Evangelinos
  3. Christos Gournas
  4. Florent Corrillon
  5. Isabelle Georis
  6. Bruno Andre  Is a corresponding author
  1. Université Libre de Bruxelles (ULB), Belgium
  2. Institut de Recherches Microbiologiques Jean-Marie Wiame, Belgium

Abstract

The yeast Target of Rapamycin Complex 1 (TORC1) plays a central role in controlling growth. How amino acids and other nutrients stimulate its activity via the Rag/Gtr GTPases remains poorly understood. We here report that the signal triggering Rag/Gtr-dependent TORC1 activation upon amino-acid uptake is the coupled H+ influx catalyzed by amino-acid/H+ symporters. H+-dependent uptake of other nutrients, ionophore-mediated H+ diffusion, and inhibition of the vacuolar V-ATPase also activate TORC1. As the increase in cytosolic H+ elicited by these processes stimulates the compensating H+-export activity of the plasma membrane H+-ATPase (Pma1), we have examined whether this major ATP-consuming enzyme might be involved in TORC1 control. We find that when the endogenous Pma1 is replaced with a plant H+-ATPase, H+ influx or increase fails to activate TORC1. Our results show that H+ influx coupled to nutrient uptake stimulates TORC1 activity and that Pma1 is a key actor in this mechanism.

Article and author information

Author details

  1. Elie Saliba

    IBMM - Molecular Physiology of the Cell, Université Libre de Bruxelles (ULB), Gosselies, Belgium
    Competing interests
    The authors declare that no competing interests exist.
  2. Minoas Evangelinos

    IBMM - Molecular Physiology of the Cell, Université Libre de Bruxelles (ULB), Gosselies, Belgium
    Competing interests
    The authors declare that no competing interests exist.
  3. Christos Gournas

    IBMM - Molecular Physiology of the Cell, Université Libre de Bruxelles (ULB), Gosselies, Belgium
    Competing interests
    The authors declare that no competing interests exist.
  4. Florent Corrillon

    IBMM - Molecular Physiology of the Cell, Université Libre de Bruxelles (ULB), Gosselies, Belgium
    Competing interests
    The authors declare that no competing interests exist.
  5. Isabelle Georis

    Institut de Recherches Microbiologiques Jean-Marie Wiame, Anderlecht, Belgium
    Competing interests
    The authors declare that no competing interests exist.
  6. Bruno Andre

    IBMM - Molecular Physiology of the Cell, Université Libre de Bruxelles (ULB), Gosselies, Belgium
    For correspondence
    Bruno.Andre@ulb.ac.be
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7683-9150

Funding

Fonds De La Recherche Scientifique - FNRS (3.4.592.08.F)

  • Bruno Andre

Fonds pour la Formation à la Recherche dans l'Industrie et dans l'Agriculture (21074048)

  • Elie Saliba

Fonds De La Recherche Scientifique - FNRS (22396499)

  • Christos Gournas

Fonds De La Recherche Scientifique - FNRS (30274494)

  • Minoas Evangelinos

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

Reviewing Editor

  1. Michael N Hall, University of Basel, Switzerland

Publication history

  1. Received: September 13, 2017
  2. Accepted: March 22, 2018
  3. Accepted Manuscript published: March 23, 2018 (version 1)
  4. Version of Record published: April 24, 2018 (version 2)

Copyright

© 2018, Saliba 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. Elie Saliba
  2. Minoas Evangelinos
  3. Christos Gournas
  4. Florent Corrillon
  5. Isabelle Georis
  6. Bruno Andre
(2018)
The yeast H+-ATPase Pma1 promotes Rag/Gtr-dependent TORC1 activation in response to H+-coupled nutrient uptake
eLife 7:e31981.
https://doi.org/10.7554/eLife.31981
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