The plant actin cytoskeleton responds to signals from microbe-associated molecular patterns

PLoS Pathog. 2013;9(4):e1003290. doi: 10.1371/journal.ppat.1003290. Epub 2013 Apr 4.

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 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.

Publication types

  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Actin Cytoskeleton* / drug effects
  • Actin Cytoskeleton* / metabolism
  • Actin Cytoskeleton* / microbiology
  • Arabidopsis / immunology*
  • Arabidopsis / metabolism*
  • Arabidopsis / microbiology
  • Arabidopsis Proteins / metabolism
  • Bridged Bicyclo Compounds, Heterocyclic / pharmacology
  • Immunity, Innate
  • Plant Diseases / immunology
  • Plant Diseases / microbiology
  • Plant Leaves / immunology
  • Protein Kinases / metabolism
  • Protein-Serine-Threonine Kinases / metabolism
  • Pseudomonas syringae / immunology*
  • Pseudomonas syringae / metabolism
  • Pseudomonas syringae / pathogenicity
  • Receptors, Pattern Recognition*
  • Signal Transduction
  • Thiazolidines / pharmacology
  • Virulence Factors / metabolism

Substances

  • Arabidopsis Proteins
  • Bridged Bicyclo Compounds, Heterocyclic
  • Receptors, Pattern Recognition
  • Thiazolidines
  • Virulence Factors
  • Protein Kinases
  • BAK1 protein, Arabidopsis
  • FLS2 protein, Arabidopsis
  • BIK1 protein, Arabidopsis
  • Protein-Serine-Threonine Kinases
  • latrunculin B

Grant support

This research was supported by a collaborative grant from the US National Science Foundation-Arabidopsis 2010 Program (IOS-1021185; IOS-1021463; and IOS-1021044) to CJS, JHC, and BD. The SDCM facility was funded in part by the Department of Energy-sponsored Center for Direct Catalytic Conversion of Biomass to Biofuels (C3Bio) an Energy Frontiers Research Center (DE-SC0000997) and an NSF-MEU grant (IBN-0217552). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.