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 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.

Nuclear Function of Subclass I Actin-Depolymerizing Factor Contributes to Susceptibility in Arabidopsis to an Adapted Powdery Mildew Fungus

“…S14). Actin microfilaments regulate the movement of organelles, such as mitochondria (Henty-Ridilla et al, 2013). GFP-labeled mitochondria showed dynamic movement in ADF1-4Ri at a speed comparable with that of the wild type (Supplemental Movies S1 and S2).…”

“…The organization and dynamics of AFs are regulated by a number of actin-binding proteins, among which actin-depolymerizing factors (ADFs) play a conserved role in actin destabilization by severing and depolymerizing microfilaments at the minus end in eukaryotes, including yeast, mammals, and plants (Maciver and Hussey, 2002;Henty-Ridilla et al, 2013). The Arabidopsis genome contains 11 members of the ADF gene family, which are classified into four subclasses (Ruzicka et al, 2007).…”

Live cell imaging approaches reveal actin cytoskeleton-induced self-association of the actin-bundling protein WLIM1

“…The creation and turnover of actin filaments, as well as their assembly into higherorder structures, are tightly regulated at spatial and temporal levels by a plethora of actin-binding proteins, which control nucleation, polymerization, capping, severing and crosslinking (dos Remedios et al, 2003;Higaki et al, 2007;Staiger and Blanchoin, 2006;Thomas et al, 2009;Winder and Ayscough, 2005). Recent live cell studies combining reliable fluorescent actin markers with novel high-resolution imaging techniques such as spinning-disc confocal microscopy and variable-angle epifluorescence microscopy (VAEM) have provided key insights into actin cytoskeleton dynamics at the cell cortex of plant cells (Augustine et al, 2011;Era et al, 2009;Henty et al, 2011;Henty-Ridilla et al, 2013;Khurana et al, 2010;Konopka and Bednarek, 2008;Li et al, 2012;Smertenko et al, 2010;Staiger et al, 2009;Tóth et al, 2012). In striking contrast to in vitro actin treadmilling (Bugyi and Carlier, 2010;Selve and Wegner, 1986), in vivo remodeling of plant cortical actin arrays was found to follow a socalled 'stochastic dynamics' process that is dominated by fast elongation and prolific severing of single filaments Okreglak and Drubin, 2010;Staiger et al, 2009).…”

“…Additional, more specific, roles have been assigned to actin bundling during guard cell and chloroplast movements (Higaki et al, 2010b), cell growth and morphogenesis (Baluska et al, 2001;Higaki et al, 2010a;Nick, 2010;Nick et al, 2009;Smith and Oppenheimer, 2005) and the set-up of plant defense responses against pathogens (Clément et al, 2009;Day et al, 2011;Hardham et al, 2007;Henty-Ridilla et al, 2013;Opalski et al, 2005;Schmidt and Panstruga, 2007;Takemoto et al, 2006).…”

Capping Protein Modulates Actin Remodeling in Response to Reactive Oxygen Species during Plant Innate Immunity

“…In Arabidopsis epidermal cells, the density of cortical actin filament arrays increases within minutes after infection with pathogenic and nonpathogenic bacteria as well as elicitation by diverse MAMPs (Henty-Ridilla et al, 2013bLi et al, 2015b). This actin remodeling is required for defense responses such as callose deposition in the cell wall, transcriptional reprogramming of defense genes, and subsequently contributes to plant resistance against virulent and avirulent microbes (Henty-Ridilla et al, 2013bLi et al, 2015b). Quantitative analyses of actin dynamics in live cells have uncovered the potential molecular mechanisms that contribute to increased filament abundance.…”