Potentiation of plant defense by bacterial outer membrane vesicles is mediated by membrane nanodomains

Outer membrane vesicles (OMVs) are released from the outer membranes of Gram-negative bacteria during infection and modulate host immunity during host-pathogen interactions. The mechanisms by which OMVs are perceived by plants and affect host immunity are unclear. Here, we used the pathogen Xanthomo...

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Main Authors: Tran, Tuan Minh, Chng, Choon-Peng, Pu, Xiaoming, Ma, Zhiming, Han, Xiao, Liu, Xiaolin, Yang, Liang, Huang, Changjin, Miao, Yansong
Other Authors: School of Biological Sciences
Format: Article
Language:English
Published: 2022
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Online Access:https://hdl.handle.net/10356/162116
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Institution: Nanyang Technological University
Language: English
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spelling sg-ntu-dr.10356-1621162022-10-04T07:38:16Z Potentiation of plant defense by bacterial outer membrane vesicles is mediated by membrane nanodomains Tran, Tuan Minh Chng, Choon-Peng Pu, Xiaoming Ma, Zhiming Han, Xiao Liu, Xiaolin Yang, Liang Huang, Changjin Miao, Yansong School of Biological Sciences School of Mechanical and Aerospace Engineering School of Chemical and Biomedical Engineering Singapore Centre for Environmental Life Sciences and Engineering (SCELSE) Science::Biological sciences Bacterial Outer Membrane Plant Immunity Outer membrane vesicles (OMVs) are released from the outer membranes of Gram-negative bacteria during infection and modulate host immunity during host-pathogen interactions. The mechanisms by which OMVs are perceived by plants and affect host immunity are unclear. Here, we used the pathogen Xanthomonas campestris pv. campestris to demonstrate that OMV-plant interactions at the Arabidopsis thaliana plasma membrane (PM) modulate various host processes, including endocytosis, innate immune responses, and suppression of pathogenesis by phytobacteria. The lipid phase of OMVs is highly ordered and OMVs directly insert into the Arabidopsis PM, thereby enhancing the plant PM's lipid order; this also resulted in strengthened plant defenses. Strikingly, the integration of OMVs into the plant PM is host nanodomain- and remorin-dependent. Using coarse-grained simulations of molecular dynamics, we demonstrated that OMV integration into the plant PM depends on the membrane lipid order. Our computational simulations further showed that the saturation level of the OMV lipids could fine-tune the enhancement of host lipid order. Our work unraveled the mechanisms underlying the ability of OMVs produced by a plant pathogen to insert into the host PM, alter host membrane properties, and modulate plant immune responses. Ministry of Education (MOE) Nanyang Technological University This study was supported by Nanyang Technological University startup grant (M4081533), Ministry of Education (MOE) Tier 1 (RG32/20; RT11/20), and Tier 3 (MOE2019-T3- 1-012) grants to YM; Nanyang Technological University startup grant (M4082352), MOE Tier 1 (RG92/19), and Accelerating Creativity and Excellence grant (NTU-ACE2020-07) to CH. 2022-10-04T07:38:16Z 2022-10-04T07:38:16Z 2022 Journal Article Tran, T. M., Chng, C., Pu, X., Ma, Z., Han, X., Liu, X., Yang, L., Huang, C. & Miao, Y. (2022). Potentiation of plant defense by bacterial outer membrane vesicles is mediated by membrane nanodomains. The Plant Cell, 34(1), 395-418. https://dx.doi.org/10.1093/plcell/koab276 1040-4651 https://hdl.handle.net/10356/162116 10.1093/plcell/koab276 34791473 2-s2.0-85123377331 1 34 395 418 en M4081533 RG32/20 RT11/20 MOE 2019-T3-1-012 M4082352 RG92/19 NTU-ACE2020-07 The Plant Cell © 2021 American Society of Plant Biologists. All rights reserved.
institution Nanyang Technological University
building NTU Library
continent Asia
country Singapore
Singapore
content_provider NTU Library
collection DR-NTU
language English
topic Science::Biological sciences
Bacterial Outer Membrane
Plant Immunity
spellingShingle Science::Biological sciences
Bacterial Outer Membrane
Plant Immunity
Tran, Tuan Minh
Chng, Choon-Peng
Pu, Xiaoming
Ma, Zhiming
Han, Xiao
Liu, Xiaolin
Yang, Liang
Huang, Changjin
Miao, Yansong
Potentiation of plant defense by bacterial outer membrane vesicles is mediated by membrane nanodomains
description Outer membrane vesicles (OMVs) are released from the outer membranes of Gram-negative bacteria during infection and modulate host immunity during host-pathogen interactions. The mechanisms by which OMVs are perceived by plants and affect host immunity are unclear. Here, we used the pathogen Xanthomonas campestris pv. campestris to demonstrate that OMV-plant interactions at the Arabidopsis thaliana plasma membrane (PM) modulate various host processes, including endocytosis, innate immune responses, and suppression of pathogenesis by phytobacteria. The lipid phase of OMVs is highly ordered and OMVs directly insert into the Arabidopsis PM, thereby enhancing the plant PM's lipid order; this also resulted in strengthened plant defenses. Strikingly, the integration of OMVs into the plant PM is host nanodomain- and remorin-dependent. Using coarse-grained simulations of molecular dynamics, we demonstrated that OMV integration into the plant PM depends on the membrane lipid order. Our computational simulations further showed that the saturation level of the OMV lipids could fine-tune the enhancement of host lipid order. Our work unraveled the mechanisms underlying the ability of OMVs produced by a plant pathogen to insert into the host PM, alter host membrane properties, and modulate plant immune responses.
author2 School of Biological Sciences
author_facet School of Biological Sciences
Tran, Tuan Minh
Chng, Choon-Peng
Pu, Xiaoming
Ma, Zhiming
Han, Xiao
Liu, Xiaolin
Yang, Liang
Huang, Changjin
Miao, Yansong
format Article
author Tran, Tuan Minh
Chng, Choon-Peng
Pu, Xiaoming
Ma, Zhiming
Han, Xiao
Liu, Xiaolin
Yang, Liang
Huang, Changjin
Miao, Yansong
author_sort Tran, Tuan Minh
title Potentiation of plant defense by bacterial outer membrane vesicles is mediated by membrane nanodomains
title_short Potentiation of plant defense by bacterial outer membrane vesicles is mediated by membrane nanodomains
title_full Potentiation of plant defense by bacterial outer membrane vesicles is mediated by membrane nanodomains
title_fullStr Potentiation of plant defense by bacterial outer membrane vesicles is mediated by membrane nanodomains
title_full_unstemmed Potentiation of plant defense by bacterial outer membrane vesicles is mediated by membrane nanodomains
title_sort potentiation of plant defense by bacterial outer membrane vesicles is mediated by membrane nanodomains
publishDate 2022
url https://hdl.handle.net/10356/162116
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