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Title: The Plant Actin Cytoskeleton Responds to Signals from Microbe-Associated Molecular Patterns

Abstract

Plants are constantly exposed to a large and diverse array of microbes; however, most plants are immune to the majority of potential invaders and susceptible to only a small subset of pathogens. The cytoskeleton comprises a dynamic intracellular framework that responds rapidly to biotic stresses and supports numerous fundamental cellular processes including vesicle trafficking, endocytosis and the spatial distribution of organelles and protein complexes. For years, the actin cytoskeleton has been assumed to play a role in plant innate immunity against fungi and oomycetes, based largely on static images and pharmacological studies. To date, however, there is little evidence that the host-cell actin cytoskeleton participates in responses to phytopathogenic bacteria. Here, we quantified the spatiotemporal changes in host-cell cytoskeletal architecture during the immune response to pathogenic and non-pathogenic strains of Pseudomonas syringae pv. tomato DC3000. Two distinct changes to host cytoskeletal arrays were observed that correspond to distinct phases of plant-bacterial interactions i.e. the perception of microbe-associated molecular patterns (MAMPs) during pattern-triggered immunity (PTI) and perturbations by effector proteins during effector-triggered susceptibility (ETS). We demonstrate that an immediate increase in actin filament abundance is a conserved and novel component of PTI. Notably, treatment of leaves with a MAMP peptide mimicmore » was sufficient to elicit a rapid change in actin organization in epidermal cells, and this actin response required the host-cell MAMP receptor kinase complex, including FLS2, BAK1 and BIK1. Finally, we found that actin polymerization is necessary for the increase in actin filament density and that blocking this increase with the actin-disrupting drug latrunculin B leads to enhanced susceptibility of host plants to pathogenic and non-pathogenic bacteria.« less

Authors:
; ; ; ; ; ;
Publication Date:
Research Org.:
Energy Frontier Research Centers (EFRC) (United States). Center for Direct Catalytic Conversion of Biomass to Biofuels (C3Bio)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22)
OSTI Identifier:
1385374
DOE Contract Number:  
SC000997
Resource Type:
Journal Article
Journal Name:
PLoS Pathogens
Additional Journal Information:
Journal Volume: 9; Journal Issue: 4; Related Information: C3Bio partners with Purdue University (lead); Argonne National Laboratory; National Renewable Energy Laboratory; Northeastern University; University of Tennessee; Journal ID: ISSN 1553-7374
Publisher:
Public Library of Science
Country of Publication:
United States
Language:
English
Subject:
60 APPLIED LIFE SCIENCES; catalysis (homogeneous), catalysis (heterogeneous), biofuels (including algae and biomass), bio-inspired, materials and chemistry by design, synthesis (self-assembly), synthesis (scalable processing)

Citation Formats

Henty-Ridilla, Jessica L., Shimono, Masaki, Li, Jiejie, Chang, Jeff H., Day, Brad, Staiger, Christopher J., and Zhou, Jian-Min. The Plant Actin Cytoskeleton Responds to Signals from Microbe-Associated Molecular Patterns. United States: N. p., 2013. Web. doi:10.1371/journal.ppat.1003290.
Henty-Ridilla, Jessica L., Shimono, Masaki, Li, Jiejie, Chang, Jeff H., Day, Brad, Staiger, Christopher J., & Zhou, Jian-Min. The Plant Actin Cytoskeleton Responds to Signals from Microbe-Associated Molecular Patterns. United States. https://doi.org/10.1371/journal.ppat.1003290
Henty-Ridilla, Jessica L., Shimono, Masaki, Li, Jiejie, Chang, Jeff H., Day, Brad, Staiger, Christopher J., and Zhou, Jian-Min. Thu . "The Plant Actin Cytoskeleton Responds to Signals from Microbe-Associated Molecular Patterns". United States. https://doi.org/10.1371/journal.ppat.1003290.
@article{osti_1385374,
title = {The Plant Actin Cytoskeleton Responds to Signals from Microbe-Associated Molecular Patterns},
author = {Henty-Ridilla, Jessica L. and Shimono, Masaki and Li, Jiejie and Chang, Jeff H. and Day, Brad and Staiger, Christopher J. and Zhou, Jian-Min},
abstractNote = {Plants are constantly exposed to a large and diverse array of microbes; however, most plants are immune to the majority of potential invaders and susceptible to only a small subset of pathogens. The cytoskeleton comprises a dynamic intracellular framework that responds rapidly to biotic stresses and supports numerous fundamental cellular processes including vesicle trafficking, endocytosis and the spatial distribution of organelles and protein complexes. For years, the actin cytoskeleton has been assumed to play a role in plant innate immunity against fungi and oomycetes, based largely on static images and pharmacological studies. To date, however, there is little evidence that the host-cell actin cytoskeleton participates in responses to phytopathogenic bacteria. Here, we quantified the spatiotemporal changes in host-cell cytoskeletal architecture during the immune response to pathogenic and non-pathogenic strains of Pseudomonas syringae pv. tomato DC3000. Two distinct changes to host cytoskeletal arrays were observed that correspond to distinct phases of plant-bacterial interactions i.e. the perception of microbe-associated molecular patterns (MAMPs) during pattern-triggered immunity (PTI) and perturbations by effector proteins during effector-triggered susceptibility (ETS). We demonstrate that an immediate increase in actin filament abundance is a conserved and novel component of PTI. Notably, treatment of leaves with a MAMP peptide mimic was sufficient to elicit a rapid change in actin organization in epidermal cells, and this actin response required the host-cell MAMP receptor kinase complex, including FLS2, BAK1 and BIK1. Finally, we found that actin polymerization is necessary for the increase in actin filament density and that blocking this increase with the actin-disrupting drug latrunculin B leads to enhanced susceptibility of host plants to pathogenic and non-pathogenic bacteria.},
doi = {10.1371/journal.ppat.1003290},
url = {https://www.osti.gov/biblio/1385374}, journal = {PLoS Pathogens},
issn = {1553-7374},
number = 4,
volume = 9,
place = {United States},
year = {2013},
month = {4}
}

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