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      Biogenesis and Function of Multivesicular Bodies in Plant Immunity

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          Abstract

          Multivesicular bodies (MVBs) are specialized endosomes that contain intraluminal vesicles generated from invagination and budding of the limiting membrane. In the endocytic pathway, MVBs are late endosomes whose content can be degraded through fusion with lysosomes/vacuoles or released into the extracellular space after fusion with the plasma membrane (PM). The proteins retained on the limiting membrane of MVBs are translocated to the membrane of lysosomes/vacuoles or delivered back to the PM. It has been long suspected that MVBs might fuse with the PM to form paramural bodies in plant cells, possibly leading to release of building blocks for deposition of papillae and antimicrobial molecules against invading pathogens. Over the past decade or so, major progress has been made in establishing the critical roles of MVBs and associated membrane trafficking in pathogen recognition, defense signaling, and deployment of defense-related molecules during plant immune responses. Regulatory proteins and signaling pathways associated with induced biogenesis and trafficking of MVBs during plant immune responses have also been identified and characterized. Recent successful isolation of plant extracellular vesicles and proteomic profiling of their content have provided additional support for the roles of MVBs in plant–pathogen interactions. In this review, we summarize the important progress and discuss how MVBs, particularly through routing of cellular components to different destinations, contribute to the complex network of plant immune system.

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          Most cited references43

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          Molecular Mechanism of Multivesicular Body Biogenesis by ESCRT Complexes

          When internalized receptors and other cargo are destined for lysosomal degradation, they are ubiquitinated and sorted by the ESCRT complexes 0, I, II, and III into multivesicular bodies. Multivesicular bodies are formed when cargo-rich patches of the limiting membrane of endosomes bud inward by an unknown mechanism and are then cleaved to yield cargo-bearing intralumenal vesicles. The biogenesis of multivesicular bodies was reconstituted and visualized using giant unilamellar vesicles, fluorescent ESCRT-0, I, II, and III complexes, and a membrane-tethered fluorescent ubiquitin fusion as a model cargo. ESCRT-0 forms domains of clustered cargo but does not deform membranes. ESCRT-I and II in combination deform the membrane into buds, in which cargo is confined. ESCRT-I and II localize to the bud necks, and recruit ESCRT-0-ubiquitin domains to the buds. ESCRT-III subunits localize to the bud neck and efficiently cleave the buds to form intralumenal vesicles. Intralumenal vesicles produced in this reaction contain the model cargo but are devoid of ESCRTs. The observations explain how the ESCRTs direct membrane budding and scission from the cytoplasmic side of the bud without being consumed in the reaction.
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            Extracellular Vesicles Isolated from the Leaf Apoplast Carry Stress-Response Proteins.

            Exosomes are extracellular vesicles (EVs) that play a central role in intercellular signaling in mammals by transporting proteins and small RNAs. Plants are also known to produce EVs, particularly in response to pathogen infection. The contents of plant EVs have not been analyzed, however, and their function is unknown. Here, we describe a method for purifying EVs from the apoplastic fluids of Arabidopsis (Arabidopsis thaliana) leaves. Proteomic analyses of these EVs revealed that they are highly enriched in proteins involved in biotic and abiotic stress responses. Consistent with this finding, EV secretion was enhanced in plants infected with Pseudomonas syringae and in response to treatment with salicylic acid. These findings suggest that EVs may represent an important component of plant immune responses.
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              Ligand-induced endocytosis of the pattern recognition receptor FLS2 in Arabidopsis.

              Pattern-recognition receptors (PRRs) trigger innate immune responses in animals and plants. One such PRR is the flagellin receptor FLS2 in Arabidopsis. Here, we demonstrate that a functional fusion of FLS2 to the green fluorescent protein (GFP) resides in cell membranes of most tissues. Stimulation with the flagellin epitope flg22 induces its transfer into intracellular mobile vesicles, followed by degradation. FLS2 internalization depends on cytoskeleton and proteasome functions, and receptor activation. A variant FLS2 mutated in Thr 867, a potential phosphorylation site, binds flg22 normally, but is impaired in flg22 responses and FLS2 endocytosis. We propose that plant cells regulate pathogen-associated molecular pattern (PAMP)-mediated PRR activities by subcellular compartmentalization.

                Author and article information

                Contributors
                Journal
                Front Plant Sci
                Front Plant Sci
                Front. Plant Sci.
                Frontiers in Plant Science
                Frontiers Media S.A.
                1664-462X
                09 July 2018
                2018
                : 9
                : 979
                Affiliations
                [1] 1Department of Horticulture, Zhejiang University , Hangzhou, China
                [2] 2College of Life Sciences, China Jiliang University , Hangzhou, China
                [3] 3Department of Botany and Plant Pathology, Center for Plant Biology, Purdue University , West Lafayette, IN, United States
                Author notes

                Edited by: Thomas Mitchell, The Ohio State University, United States

                Reviewed by: Roger W. Innes, Indiana University Bloomington, United States; Xiaohong Zhuang, The Chinese University of Hong Kong, Hong Kong

                These authors have contributed equally to this work.

                This article was submitted to Plant Microbe Interactions, a section of the journal Frontiers in Plant Science

                Article
                10.3389/fpls.2018.00979
                6047128
                30038635
                6a12394f-d442-41cd-a535-62b096169959
                Copyright © 2018 Li, Bao, Wang, Wang, Fan, Zhu and Chen.

                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.

                History
                : 02 March 2018
                : 15 June 2018
                Page count
                Figures: 2, Tables: 0, Equations: 0, References: 52, Pages: 7, Words: 0
                Funding
                Funded by: National Science Foundation 10.13039/100000001
                Award ID: IOS-0958066
                Award ID: IOS1456300
                Categories
                Plant Science
                Mini Review

                Plant science & Botany
                mvbs,plant immunity,lip5,endocytosis,endosomal trafficking
                Plant science & Botany
                mvbs, plant immunity, lip5, endocytosis, endosomal trafficking

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