Lipid Signaling Requires ROS Production to Elicit Actin Cytoskeleton Remodeling during Plant Innate Immunity.

Lingyan Cao,Weiwei Zhang,Wenyi Wang,Christopher J. Staiger

doi:10.3390/ijms23052447

Abstract

In terrestrial plants a basal innate immune system, pattern-triggered immunity (PTI), has evolved to limit infection by diverse microbes. The remodeling of actin cytoskeletal arrays is now recognized as a key hallmark event during the rapid host cellular responses to pathogen attack. Several actin binding proteins have been demonstrated to fine tune the dynamics of actin filaments during this process. However, the upstream signals that stimulate actin remodeling during PTI signaling remain poorly characterized. Two second messengers, reactive oxygen species (ROS) and phosphatidic acid (PA), are elevated following pathogen perception or microbe-associated molecular pattern (MAMP) treatment, and the timing of signaling fluxes roughly correlates with actin cytoskeletal rearrangements. Here, we combined genetic analysis, chemical complementation experiments, and quantitative live-cell imaging experiments to test the role of these second messengers in actin remodeling and to order the signaling events during plant immunity. We demonstrated that PHOSPHOLIPASE Dβ (PLDβ) isoforms are necessary to elicit actin accumulation in response to flg22-associated PTI. Further, bacterial growth experiments and MAMP-induced apoplastic ROS production measurements revealed that PLDβ-generated PA acts upstream of ROS signaling to trigger actin remodeling through inhibition of CAPPING PROTEIN (CP) activity. Collectively, our results provide compelling evidence that PLDβ/PA functions upstream of RBOHD-mediated ROS production to elicit actin rearrangements during the innate immune response in Arabidopsis.

Highlights

Plants lack an adaptive immune response and rely on the machinery of innate immunity to sense and respond to extracellular danger signals, such as microbe-associated molecular patterns (MAMPs) and damage-associated molecular patterns (DAMP) [1].Recognition of MAMPs or DAMPs by cognate pattern recognition receptors (PRRs) activates basal defense responses, referred to as pattern-triggered immunity (PTI), and protects plants from pathogen infection
We investigated whether actin filament arrays from the epidermal pavement cells of cotyledons respond to MAMP treatment in a similar fashion to rosette leaves and dark-grown hypocotyls
Actin cytoskeleton remodeling in response to short-term (15–20 min) MAMP or DAMP treatment was examined by collecting z-series images from the abaxial epidermal cells of seven-day-old light-grown cotyledons by spinning disk confocal microscopy (SDCM), and actin array organization was analyzed with tools described previously [16,22]

Summary

Introduction

Plants lack an adaptive immune response and rely on the machinery of innate immunity to sense and respond to extracellular danger signals, such as microbe-associated molecular patterns (MAMPs) and damage-associated molecular patterns (DAMP) [1]. Recognition of MAMPs or DAMPs by cognate pattern recognition receptors (PRRs) activates basal defense responses, referred to as pattern-triggered immunity (PTI), and protects plants from pathogen infection. Several cognate pairs of MAMP/PRR have been well characterized; for example, bacterial flagellin and elongation factor EF-Tu, or their peptide mimics flg and elf26/ac-elf, are recognized by leucine-rich repeat receptor kinases (LRR-RK), FLAGELLIN-SENSING2 (FLS2) [2] and EF-TU RECEPTOR (EFR) [3], respectively. Endogenous secreted polypeptides or molecules released from damaged host cells act as danger signals upon plant infection. Oligogalacturonides (OGs) [6] released from the plant cell wall and

Methods

Results

Conclusion