Revising the Role of Cortical Cytoskeleton during Secretion: Actin and Myosin XI Function in Vesicle Tethering

In plants, secretion of cell wall components and membrane proteins plays a fundamental role in growth and development as well as survival in diverse environments. Exocytosis, as the last step of the secretory trafficking pathway, is a highly ordered and precisely controlled process involving tetheri...

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Main Authors: Weiwei Zhang, Christopher J. Staiger
Format: Article
Language:English
Published: MDPI AG 2021-12-01
Series:International Journal of Molecular Sciences
Subjects:
Online Access:https://www.mdpi.com/1422-0067/23/1/317
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author Weiwei Zhang
Christopher J. Staiger
author_facet Weiwei Zhang
Christopher J. Staiger
author_sort Weiwei Zhang
collection DOAJ
description In plants, secretion of cell wall components and membrane proteins plays a fundamental role in growth and development as well as survival in diverse environments. Exocytosis, as the last step of the secretory trafficking pathway, is a highly ordered and precisely controlled process involving tethering, docking, and fusion of vesicles at the plasma membrane (PM) for cargo delivery. Although the exocytic process and machinery are well characterized in yeast and animal models, the molecular players and specific molecular events that underpin late stages of exocytosis in plant cells remain largely unknown. Here, by using the delivery of functional, fluorescent-tagged cellulose synthase (CESA) complexes (CSCs) to the PM as a model system for secretion, as well as single-particle tracking in living cells, we describe a quantitative approach for measuring the frequency of vesicle tethering events. Genetic and pharmacological inhibition of cytoskeletal function, reveal that the initial vesicle tethering step of exocytosis is dependent on actin and myosin XI. In contrast, treatments with the microtubule inhibitor, oryzalin, did not significantly affect vesicle tethering or fusion during CSC exocytosis but caused a minor increase in transient or aborted tethering events. With data from this new quantitative approach and improved spatiotemporal resolution of single particle events during secretion, we generate a revised model for the role of the cortical cytoskeleton in CSC trafficking.
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spelling doaj.art-74ffd22163a9420495a81a1cb47831842023-11-23T11:38:08ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672021-12-0123131710.3390/ijms23010317Revising the Role of Cortical Cytoskeleton during Secretion: Actin and Myosin XI Function in Vesicle TetheringWeiwei Zhang0Christopher J. Staiger1Department of Biological Sciences, Purdue University, West Lafayette, IN 47907, USADepartment of Biological Sciences, Purdue University, West Lafayette, IN 47907, USAIn plants, secretion of cell wall components and membrane proteins plays a fundamental role in growth and development as well as survival in diverse environments. Exocytosis, as the last step of the secretory trafficking pathway, is a highly ordered and precisely controlled process involving tethering, docking, and fusion of vesicles at the plasma membrane (PM) for cargo delivery. Although the exocytic process and machinery are well characterized in yeast and animal models, the molecular players and specific molecular events that underpin late stages of exocytosis in plant cells remain largely unknown. Here, by using the delivery of functional, fluorescent-tagged cellulose synthase (CESA) complexes (CSCs) to the PM as a model system for secretion, as well as single-particle tracking in living cells, we describe a quantitative approach for measuring the frequency of vesicle tethering events. Genetic and pharmacological inhibition of cytoskeletal function, reveal that the initial vesicle tethering step of exocytosis is dependent on actin and myosin XI. In contrast, treatments with the microtubule inhibitor, oryzalin, did not significantly affect vesicle tethering or fusion during CSC exocytosis but caused a minor increase in transient or aborted tethering events. With data from this new quantitative approach and improved spatiotemporal resolution of single particle events during secretion, we generate a revised model for the role of the cortical cytoskeleton in CSC trafficking.https://www.mdpi.com/1422-0067/23/1/317plant exocytosisactin cytoskeletonmicrotubulescellulose synthasevesicle traffickingcell wall biosynthesis
spellingShingle Weiwei Zhang
Christopher J. Staiger
Revising the Role of Cortical Cytoskeleton during Secretion: Actin and Myosin XI Function in Vesicle Tethering
International Journal of Molecular Sciences
plant exocytosis
actin cytoskeleton
microtubules
cellulose synthase
vesicle trafficking
cell wall biosynthesis
title Revising the Role of Cortical Cytoskeleton during Secretion: Actin and Myosin XI Function in Vesicle Tethering
title_full Revising the Role of Cortical Cytoskeleton during Secretion: Actin and Myosin XI Function in Vesicle Tethering
title_fullStr Revising the Role of Cortical Cytoskeleton during Secretion: Actin and Myosin XI Function in Vesicle Tethering
title_full_unstemmed Revising the Role of Cortical Cytoskeleton during Secretion: Actin and Myosin XI Function in Vesicle Tethering
title_short Revising the Role of Cortical Cytoskeleton during Secretion: Actin and Myosin XI Function in Vesicle Tethering
title_sort revising the role of cortical cytoskeleton during secretion actin and myosin xi function in vesicle tethering
topic plant exocytosis
actin cytoskeleton
microtubules
cellulose synthase
vesicle trafficking
cell wall biosynthesis
url https://www.mdpi.com/1422-0067/23/1/317
work_keys_str_mv AT weiweizhang revisingtheroleofcorticalcytoskeletonduringsecretionactinandmyosinxifunctioninvesicletethering
AT christopherjstaiger revisingtheroleofcorticalcytoskeletonduringsecretionactinandmyosinxifunctioninvesicletethering