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...

Full description

Bibliographic Details
Main Authors: Claudio Osorio-Navarro, Jorge Toledo, Lorena Norambuena
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-10-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2022.987191/full
_version_ 1798030135010525184
author Claudio Osorio-Navarro
Jorge Toledo
Lorena Norambuena
author_facet Claudio Osorio-Navarro
Jorge Toledo
Lorena Norambuena
author_sort Claudio Osorio-Navarro
collection DOAJ
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.
first_indexed 2024-04-11T19:36:25Z
format Article
id doaj.art-9bc9b0ec59fb4319b149fb3ade8054f6
institution Directory Open Access Journal
issn 1664-462X
language English
last_indexed 2024-04-11T19:36:25Z
publishDate 2022-10-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Plant Science
spelling doaj.art-9bc9b0ec59fb4319b149fb3ade8054f62022-12-22T04:06:51ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2022-10-011310.3389/fpls.2022.987191987191Sucrose targets clathrin-mediated endocytosis kinetics supporting cell elongation in Arabidopsis thalianaClaudio Osorio-Navarro0Jorge Toledo1Lorena Norambuena2Department of Biology, Facultad de Ciencias, Plant Molecular Biology Centre, Universidad de Chile, Santiago, ChileRed de Equipamiento Científico Avanzado (REDECA), Faculty of Medicine, Universidad de Chile, Santiago, ChileDepartment of Biology, Facultad de Ciencias, Plant Molecular Biology Centre, Universidad de Chile, Santiago, ChileSucrose 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.https://www.frontiersin.org/articles/10.3389/fpls.2022.987191/fullsucrosecell elongationclathrin-mediated endocytosis (CME)traffickingclathrin
spellingShingle Claudio Osorio-Navarro
Jorge Toledo
Lorena Norambuena
Sucrose targets clathrin-mediated endocytosis kinetics supporting cell elongation in Arabidopsis thaliana
Frontiers in Plant Science
sucrose
cell elongation
clathrin-mediated endocytosis (CME)
trafficking
clathrin
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 sucrose
cell elongation
clathrin-mediated endocytosis (CME)
trafficking
clathrin
url https://www.frontiersin.org/articles/10.3389/fpls.2022.987191/full
work_keys_str_mv AT claudioosorionavarro sucrosetargetsclathrinmediatedendocytosiskineticssupportingcellelongationinarabidopsisthaliana
AT jorgetoledo sucrosetargetsclathrinmediatedendocytosiskineticssupportingcellelongationinarabidopsisthaliana
AT lorenanorambuena sucrosetargetsclathrinmediatedendocytosiskineticssupportingcellelongationinarabidopsisthaliana