Cargando…

Sucrose targets clathrin-mediated endocytosis kinetics supporting cell elongation in Arabidopsis thaliana

Sucrose is a central regulator of plant growth and development, coordinating cell division and cell elongation according to the energy status of plants. Sucrose is known to stimulate bulk endocytosis in cultured cells; however, its physiological role has not been described to date. Our work shows th...

Descripción completa

Detalles Bibliográficos
Autores principales: Osorio-Navarro, Claudio, Toledo, Jorge, Norambuena, Lorena
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9623095/
https://www.ncbi.nlm.nih.gov/pubmed/36330253
http://dx.doi.org/10.3389/fpls.2022.987191
_version_ 1784821919166496768
author Osorio-Navarro, Claudio
Toledo, Jorge
Norambuena, Lorena
author_facet Osorio-Navarro, Claudio
Toledo, Jorge
Norambuena, Lorena
author_sort Osorio-Navarro, Claudio
collection PubMed
description Sucrose is a central regulator of plant growth and development, coordinating cell division and cell elongation according to the energy status of plants. Sucrose is known to stimulate bulk endocytosis in cultured cells; however, its physiological role has not been described to date. Our work shows that sucrose supplementation induces root cell elongation and endocytosis. Sucrose targets clathrin-mediated endocytosis (CME) in epidermal cells. Its presence decreases the abundance of both the clathrin coating complex and phosphatidylinositol 4,5-biphosphate at the plasma membrane, while increasing clathrin complex abundance in intracellular spaces. Sucrose decreases the plasma membrane residence time of the clathrin complex, indicating that it controls the kinetics of endocytic vesicle formation and internalization. CME regulation by sucrose is inducible and reversible; this on/off mechanism reveals an endocytosis-mediated mechanism for sensing plant energy status and signaling root elongation. The sucrose monosaccharide fructose also induces CME, while glucose and mannitol have no effect, demonstrating the specificity of the process. Overall, our data show that sucrose can mediate CME, which demonstrates that sucrose signaling for plant growth and development is dependent on endomembrane trafficking.
format Online
Article
Text
id pubmed-9623095
institution National Center for Biotechnology Information
language English
publishDate 2022
publisher Frontiers Media S.A.
record_format MEDLINE/PubMed
spelling pubmed-96230952022-11-02 Sucrose targets clathrin-mediated endocytosis kinetics supporting cell elongation in Arabidopsis thaliana Osorio-Navarro, Claudio Toledo, Jorge Norambuena, Lorena Front Plant Sci Plant Science Sucrose is a central regulator of plant growth and development, coordinating cell division and cell elongation according to the energy status of plants. Sucrose is known to stimulate bulk endocytosis in cultured cells; however, its physiological role has not been described to date. Our work shows that sucrose supplementation induces root cell elongation and endocytosis. Sucrose targets clathrin-mediated endocytosis (CME) in epidermal cells. Its presence decreases the abundance of both the clathrin coating complex and phosphatidylinositol 4,5-biphosphate at the plasma membrane, while increasing clathrin complex abundance in intracellular spaces. Sucrose decreases the plasma membrane residence time of the clathrin complex, indicating that it controls the kinetics of endocytic vesicle formation and internalization. CME regulation by sucrose is inducible and reversible; this on/off mechanism reveals an endocytosis-mediated mechanism for sensing plant energy status and signaling root elongation. The sucrose monosaccharide fructose also induces CME, while glucose and mannitol have no effect, demonstrating the specificity of the process. Overall, our data show that sucrose can mediate CME, which demonstrates that sucrose signaling for plant growth and development is dependent on endomembrane trafficking. Frontiers Media S.A. 2022-10-18 /pmc/articles/PMC9623095/ /pubmed/36330253 http://dx.doi.org/10.3389/fpls.2022.987191 Text en Copyright © 2022 Osorio-Navarro, Toledo and Norambuena. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Plant Science
Osorio-Navarro, Claudio
Toledo, Jorge
Norambuena, Lorena
Sucrose targets clathrin-mediated endocytosis kinetics supporting cell elongation in Arabidopsis thaliana
title Sucrose targets clathrin-mediated endocytosis kinetics supporting cell elongation in Arabidopsis thaliana
title_full Sucrose targets clathrin-mediated endocytosis kinetics supporting cell elongation in Arabidopsis thaliana
title_fullStr Sucrose targets clathrin-mediated endocytosis kinetics supporting cell elongation in Arabidopsis thaliana
title_full_unstemmed Sucrose targets clathrin-mediated endocytosis kinetics supporting cell elongation in Arabidopsis thaliana
title_short Sucrose targets clathrin-mediated endocytosis kinetics supporting cell elongation in Arabidopsis thaliana
title_sort sucrose targets clathrin-mediated endocytosis kinetics supporting cell elongation in arabidopsis thaliana
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9623095/
https://www.ncbi.nlm.nih.gov/pubmed/36330253
http://dx.doi.org/10.3389/fpls.2022.987191
work_keys_str_mv AT osorionavarroclaudio sucrosetargetsclathrinmediatedendocytosiskineticssupportingcellelongationinarabidopsisthaliana
AT toledojorge sucrosetargetsclathrinmediatedendocytosiskineticssupportingcellelongationinarabidopsisthaliana
AT norambuenalorena sucrosetargetsclathrinmediatedendocytosiskineticssupportingcellelongationinarabidopsisthaliana