The bacterial quorum sensing signal DSF hijacks Arabidopsis thaliana sterol biosynthesis to suppress plant innate immunity

Abstract

Quorum sensing (QS) is a recognized phenomenon that is crucial for regulating population-related behaviors in bacteria. However, the direct specific effect of QS molecules on host biology is largely understudied. In this work, we show that the QS molecule DSF (cis-11-methyl-dodecenoic acid) produced by Xanthomonas campestris pv. campestris can suppress pathogen-associated molecular pattern–triggered immunity (PTI) in Arabidopsis thaliana, mediated by flagellin-induced activation of flagellin receptor FLS2. The DSF-mediated attenuation of innate immunity results from the alteration of FLS2 nanoclusters and endocytic internalization of plasma membrane FLS2. DSF altered the lipid profile of Arabidopsis, with a particular increase in the phytosterol species, which impairs the general endocytosis pathway mediated by clathrin and FLS2 nano-clustering on the plasma membrane. The DSF effect on receptor dynamics and host immune responses could be entirely reversed by sterol removal. Together, our results highlighted the importance of sterol homeostasis to plasma membrane organization and demonstrate a novel mechanism by which pathogenic bacteria use their communicating molecule to manipulate pathogen-associated molecular pattern–triggered host immunity.

Regulation of immune receptor kinase plasma membrane nanoscale organization by a plant peptide hormone and its receptors

“…Two lines expressing FLS2-GFP under the control of its native promoter were crossed with FER knock-out alleles fer-2 and fer-4 . In line with previous reports ( Bücherl et al, 2017 ; Tran et al, 2020 ), we observed that FLS2-GFP localized to laterally stable foci in wild-type (WT) ( Figure 1—video 1 ). Consistently, FLS2-GFP single-particle trajectories exhibited a confined mobility behavior ( Figure 1—figure supplement 1 , Figure 1—video 1 ).…”

“…Using this approach, we found that FLS2-GFP fluorescence was maintained into well-defined and static structures in WT, while it appeared more disperse and more mobile in both fer mutants ( Figure 1A and B , Figure 1—figure supplement 2 ). To substantiate these observations, we used the previously established spatial clustering index (SCI), which describes protein lateral organization ( Gronnier et al, 2017 ; Tran et al, 2020 ). As expected, SCI of FLS2-GFP was lower in fer-4 than in WT ( Figure 1C ), indicating disturbance in FLS2-GFP lateral organization.…”

Regulation of immune receptor kinases plasma membrane nanoscale landscape by a plant peptide hormone and its receptors

“…Two lines expressing FLS2-GFP under the control of its native promoter were crossed with two FER knock-out alleles, fer-2 and fer-4. In line with previous reports (Bücherl et al, 2017;Tran et al, 2020), we observed that FLS2-GFP localizes to static foci in the wild-type (WT) (Movie S1). Consistently, FLS2-GFP single particle trajectories exhibit a confined mobility behavior (Fig.…”

“…1A-B and S2). To substantiate these observations, we used previously established spatial clustering index (SCI) which describes protein lateral organization (Gronnier et al, 2017;Tran et al, 2020). As expected, SCI of FLS2-GFP was lower in fer-4 than in WT (Fig.…”

Pathogens and Elicitors Induce Local and Systemic Changes in Triacylglycerol Metabolism in Roots and in Leaves of Arabidopsis thaliana

“…This is especially relevant since the activity of receptors might be dependent on nanodomains. The liquid-ordered phases of nanodomains comprise a particular lipid composition and, e.g., are enriched in sterols and sphingolipids [ 47 , 48 ]. In addition, early responses such as extracellular alkalinization and ion fluxes are associated with the plasma membrane, and membrane dynamics have been shown to regulate the response to flagellin by internalizing the receptor FLS2 [ 49 ].…”