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Gibberellin DELLA signaling targets the retromer complex to redirect protein trafficking to the plasma membrane

The plant hormone gibberellic acid (GA) is a crucial regulator of growth and development. The main paradigm of GA signaling puts forward transcriptional regulation via the degradation of DELLA transcriptional repressors. GA has also been shown to regulate tropic responses by modulation of the plasma...

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Autores principales: Salanenka, Yuliya, Verstraeten, Inge, Löfke, Christian, Tabata, Kaori, Naramoto, Satoshi, Glanc, Matouš, Friml, Jiří
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5889667/
https://www.ncbi.nlm.nih.gov/pubmed/29463731
http://dx.doi.org/10.1073/pnas.1721760115
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author Salanenka, Yuliya
Verstraeten, Inge
Löfke, Christian
Tabata, Kaori
Naramoto, Satoshi
Glanc, Matouš
Friml, Jiří
author_facet Salanenka, Yuliya
Verstraeten, Inge
Löfke, Christian
Tabata, Kaori
Naramoto, Satoshi
Glanc, Matouš
Friml, Jiří
author_sort Salanenka, Yuliya
collection PubMed
description The plant hormone gibberellic acid (GA) is a crucial regulator of growth and development. The main paradigm of GA signaling puts forward transcriptional regulation via the degradation of DELLA transcriptional repressors. GA has also been shown to regulate tropic responses by modulation of the plasma membrane incidence of PIN auxin transporters by an unclear mechanism. Here we uncovered the cellular and molecular mechanisms by which GA redirects protein trafficking and thus regulates cell surface functionality. Photoconvertible reporters revealed that GA balances the protein traffic between the vacuole degradation route and recycling back to the cell surface. Low GA levels promote vacuolar delivery and degradation of multiple cargos, including PIN proteins, whereas high GA levels promote their recycling to the plasma membrane. This GA effect requires components of the retromer complex, such as Sorting Nexin 1 (SNX1) and its interacting, microtubule (MT)-associated protein, the Cytoplasmic Linker-Associated Protein (CLASP1). Accordingly, GA regulates the subcellular distribution of SNX1 and CLASP1, and the intact MT cytoskeleton is essential for the GA effect on trafficking. This GA cellular action occurs through DELLA proteins that regulate the MT and retromer presumably via their interaction partners Prefoldins (PFDs). Our study identified a branching of the GA signaling pathway at the level of DELLA proteins, which, in parallel to regulating transcription, also target by a nontranscriptional mechanism the retromer complex acting at the intersection of the degradation and recycling trafficking routes. By this mechanism, GA can redirect receptors and transporters to the cell surface, thus coregulating multiple processes, including PIN-dependent auxin fluxes during tropic responses.
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spelling pubmed-58896672018-04-09 Gibberellin DELLA signaling targets the retromer complex to redirect protein trafficking to the plasma membrane Salanenka, Yuliya Verstraeten, Inge Löfke, Christian Tabata, Kaori Naramoto, Satoshi Glanc, Matouš Friml, Jiří Proc Natl Acad Sci U S A Biological Sciences The plant hormone gibberellic acid (GA) is a crucial regulator of growth and development. The main paradigm of GA signaling puts forward transcriptional regulation via the degradation of DELLA transcriptional repressors. GA has also been shown to regulate tropic responses by modulation of the plasma membrane incidence of PIN auxin transporters by an unclear mechanism. Here we uncovered the cellular and molecular mechanisms by which GA redirects protein trafficking and thus regulates cell surface functionality. Photoconvertible reporters revealed that GA balances the protein traffic between the vacuole degradation route and recycling back to the cell surface. Low GA levels promote vacuolar delivery and degradation of multiple cargos, including PIN proteins, whereas high GA levels promote their recycling to the plasma membrane. This GA effect requires components of the retromer complex, such as Sorting Nexin 1 (SNX1) and its interacting, microtubule (MT)-associated protein, the Cytoplasmic Linker-Associated Protein (CLASP1). Accordingly, GA regulates the subcellular distribution of SNX1 and CLASP1, and the intact MT cytoskeleton is essential for the GA effect on trafficking. This GA cellular action occurs through DELLA proteins that regulate the MT and retromer presumably via their interaction partners Prefoldins (PFDs). Our study identified a branching of the GA signaling pathway at the level of DELLA proteins, which, in parallel to regulating transcription, also target by a nontranscriptional mechanism the retromer complex acting at the intersection of the degradation and recycling trafficking routes. By this mechanism, GA can redirect receptors and transporters to the cell surface, thus coregulating multiple processes, including PIN-dependent auxin fluxes during tropic responses. National Academy of Sciences 2018-04-03 2018-02-20 /pmc/articles/PMC5889667/ /pubmed/29463731 http://dx.doi.org/10.1073/pnas.1721760115 Text en Copyright © 2018 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/ This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle Biological Sciences
Salanenka, Yuliya
Verstraeten, Inge
Löfke, Christian
Tabata, Kaori
Naramoto, Satoshi
Glanc, Matouš
Friml, Jiří
Gibberellin DELLA signaling targets the retromer complex to redirect protein trafficking to the plasma membrane
title Gibberellin DELLA signaling targets the retromer complex to redirect protein trafficking to the plasma membrane
title_full Gibberellin DELLA signaling targets the retromer complex to redirect protein trafficking to the plasma membrane
title_fullStr Gibberellin DELLA signaling targets the retromer complex to redirect protein trafficking to the plasma membrane
title_full_unstemmed Gibberellin DELLA signaling targets the retromer complex to redirect protein trafficking to the plasma membrane
title_short Gibberellin DELLA signaling targets the retromer complex to redirect protein trafficking to the plasma membrane
title_sort gibberellin della signaling targets the retromer complex to redirect protein trafficking to the plasma membrane
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5889667/
https://www.ncbi.nlm.nih.gov/pubmed/29463731
http://dx.doi.org/10.1073/pnas.1721760115
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