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Salicylic acid-mediated plasmodesmal closure via Remorin-dependent lipid organization

Plasmodesmata (PD) are plant-specific membrane-lined channels that create cytoplasmic and membrane continuities between adjacent cells, thereby facilitating cell–cell communication and virus movement. Plant cells have evolved diverse mechanisms to regulate PD plasticity in response to numerous envir...

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Autores principales: Huang, Dingquan, Sun, Yanbiao, Ma, Zhiming, Ke, Meiyu, Cui, Yong, Chen, Zichen, Chen, Chaofan, Ji, Changyang, Tran, Tuan Minh, Yang, Liang, Lam, Sin Man, Han, Yanhong, Shui, Guanghou, Wei, Zhuang, Tan, Shutang, Liao, Kan, Friml, Jiří, Miao, Yansong, Jiang, Liwen, Chen, Xu
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6800329/
https://www.ncbi.nlm.nih.gov/pubmed/31575745
http://dx.doi.org/10.1073/pnas.1911892116
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author Huang, Dingquan
Sun, Yanbiao
Ma, Zhiming
Ke, Meiyu
Cui, Yong
Chen, Zichen
Chen, Chaofan
Ji, Changyang
Tran, Tuan Minh
Yang, Liang
Lam, Sin Man
Han, Yanhong
Shui, Guanghou
Wei, Zhuang
Tan, Shutang
Liao, Kan
Friml, Jiří
Miao, Yansong
Jiang, Liwen
Chen, Xu
author_facet Huang, Dingquan
Sun, Yanbiao
Ma, Zhiming
Ke, Meiyu
Cui, Yong
Chen, Zichen
Chen, Chaofan
Ji, Changyang
Tran, Tuan Minh
Yang, Liang
Lam, Sin Man
Han, Yanhong
Shui, Guanghou
Wei, Zhuang
Tan, Shutang
Liao, Kan
Friml, Jiří
Miao, Yansong
Jiang, Liwen
Chen, Xu
author_sort Huang, Dingquan
collection PubMed
description Plasmodesmata (PD) are plant-specific membrane-lined channels that create cytoplasmic and membrane continuities between adjacent cells, thereby facilitating cell–cell communication and virus movement. Plant cells have evolved diverse mechanisms to regulate PD plasticity in response to numerous environmental stimuli. In particular, during defense against plant pathogens, the defense hormone, salicylic acid (SA), plays a crucial role in the regulation of PD permeability in a callose-dependent manner. Here, we uncover a mechanism by which plants restrict the spreading of virus and PD cargoes using SA signaling by increasing lipid order and closure of PD. We showed that exogenous SA application triggered the compartmentalization of lipid raft nanodomains through a modulation of the lipid raft-regulatory protein, Remorin (REM). Genetic studies, superresolution imaging, and transmission electron microscopy observation together demonstrated that Arabidopsis REM1.2 and REM1.3 are crucial for plasma membrane nanodomain assembly to control PD aperture and functionality. In addition, we also found that a 14-3-3 epsilon protein modulates REM clustering and membrane nanodomain compartmentalization through its direct interaction with REM proteins. This study unveils a molecular mechanism by which the key plant defense hormone, SA, triggers membrane lipid nanodomain reorganization, thereby regulating PD closure to impede virus spreading.
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spelling pubmed-68003292019-10-24 Salicylic acid-mediated plasmodesmal closure via Remorin-dependent lipid organization Huang, Dingquan Sun, Yanbiao Ma, Zhiming Ke, Meiyu Cui, Yong Chen, Zichen Chen, Chaofan Ji, Changyang Tran, Tuan Minh Yang, Liang Lam, Sin Man Han, Yanhong Shui, Guanghou Wei, Zhuang Tan, Shutang Liao, Kan Friml, Jiří Miao, Yansong Jiang, Liwen Chen, Xu Proc Natl Acad Sci U S A Biological Sciences Plasmodesmata (PD) are plant-specific membrane-lined channels that create cytoplasmic and membrane continuities between adjacent cells, thereby facilitating cell–cell communication and virus movement. Plant cells have evolved diverse mechanisms to regulate PD plasticity in response to numerous environmental stimuli. In particular, during defense against plant pathogens, the defense hormone, salicylic acid (SA), plays a crucial role in the regulation of PD permeability in a callose-dependent manner. Here, we uncover a mechanism by which plants restrict the spreading of virus and PD cargoes using SA signaling by increasing lipid order and closure of PD. We showed that exogenous SA application triggered the compartmentalization of lipid raft nanodomains through a modulation of the lipid raft-regulatory protein, Remorin (REM). Genetic studies, superresolution imaging, and transmission electron microscopy observation together demonstrated that Arabidopsis REM1.2 and REM1.3 are crucial for plasma membrane nanodomain assembly to control PD aperture and functionality. In addition, we also found that a 14-3-3 epsilon protein modulates REM clustering and membrane nanodomain compartmentalization through its direct interaction with REM proteins. This study unveils a molecular mechanism by which the key plant defense hormone, SA, triggers membrane lipid nanodomain reorganization, thereby regulating PD closure to impede virus spreading. National Academy of Sciences 2019-10-15 2019-10-01 /pmc/articles/PMC6800329/ /pubmed/31575745 http://dx.doi.org/10.1073/pnas.1911892116 Text en Copyright © 2019 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/ 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
Huang, Dingquan
Sun, Yanbiao
Ma, Zhiming
Ke, Meiyu
Cui, Yong
Chen, Zichen
Chen, Chaofan
Ji, Changyang
Tran, Tuan Minh
Yang, Liang
Lam, Sin Man
Han, Yanhong
Shui, Guanghou
Wei, Zhuang
Tan, Shutang
Liao, Kan
Friml, Jiří
Miao, Yansong
Jiang, Liwen
Chen, Xu
Salicylic acid-mediated plasmodesmal closure via Remorin-dependent lipid organization
title Salicylic acid-mediated plasmodesmal closure via Remorin-dependent lipid organization
title_full Salicylic acid-mediated plasmodesmal closure via Remorin-dependent lipid organization
title_fullStr Salicylic acid-mediated plasmodesmal closure via Remorin-dependent lipid organization
title_full_unstemmed Salicylic acid-mediated plasmodesmal closure via Remorin-dependent lipid organization
title_short Salicylic acid-mediated plasmodesmal closure via Remorin-dependent lipid organization
title_sort salicylic acid-mediated plasmodesmal closure via remorin-dependent lipid organization
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6800329/
https://www.ncbi.nlm.nih.gov/pubmed/31575745
http://dx.doi.org/10.1073/pnas.1911892116
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