Formin nanoclustering-mediated actin assembly during plant flagellin and DSF signaling

Plants respond to bacterial infection acutely with actin remodeling during plant immune responses. The mechanisms by which bacterial virulence factors (VFs) modulate plant actin polymerization remain enigmatic. Here, we show that plant-type-I formin serves as the molecular sensor for actin remodelin...

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Published in:	Cell reports (Cambridge) 2021-03, Vol.34 (13), p.108884-108884, Article 108884
Main Authors:	Ma, Zhiming, Liu, Xiaolin, Nath, Sangeeta, Sun, He, Tran, Tuan Minh, Yang, Liang, Mayor, Satyajit, Miao, Yansong
Format:	Article
Language:	eng
Subjects:	actin nucleation actin remodeling Actins - metabolism Arabidopsis - microbiology Bacterial Proteins - metabolism BASIC BIOLOGICAL SCIENCES Cell Wall - metabolism Cellulose - metabolism diffusible signal factor Flagellin - metabolism formin Formins - metabolism Host-Pathogen Interactions Models, Biological nanoclustering Nanoparticles - chemistry PAMP Pathogen-Associated Molecular Pattern Molecules - metabolism Protein Binding PTI quorum sensing Signal Transduction Xanthomonas campestris - metabolism
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Summary:	Plants respond to bacterial infection acutely with actin remodeling during plant immune responses. The mechanisms by which bacterial virulence factors (VFs) modulate plant actin polymerization remain enigmatic. Here, we show that plant-type-I formin serves as the molecular sensor for actin remodeling in response to two bacterial VFs: Xanthomonas campestris pv. campestris (Xcc) diffusible signal factor (DSF), and pathogen-associated molecular pattern (PAMP) flagellin in pattern-triggered immunity (PTI). Both VFs regulate actin assembly by tuning the clustering and nucleation activity of formin on the plasma membrane (PM) at the nano-sized scale. By being integrated within the cell-wall-PM-actin cytoskeleton (CW-PM-AC) continuum, the dynamic behavior and function of formins are highly dependent on each scaffold layer’s composition within the CW-PM-AC continuum during both DSF and PTI signaling. Our results reveal a central mechanism for rapid actin remodeling during plant-bacteria interactions, in which bacterial signaling molecules fine tune plant formin nanoclustering in a host mechanical-structure-dependent manner. [Display omitted] •Plant actin remodeling is triggered by the molecular condensation of surface formins•PAMPs stimulate nanoclustering of host surface formin to enhance actin nucleation•Plant surface scaffolding structures control formin dynamics and functions•DSF elevates cellulose production and constrains formin dynamics on the plant surface Ma et al. describe a molecular switcher of actin remodeling during plant immune responses. These findings provide a mechanism by which molecular condensation of plant-type-I formin responds to bacterial signaling biomolecules. These plant-surface formins are tightly regulated by the cell-wall-plasma-membrane-actin-cytoskeleton continuum during bacterial-host communication.
ISSN:	2211-1247 2211-1247