Quantitative disease resistance (QDR) is a form of plant immunity widespread in nature, and the only one active against broad host range fungal pathogens. The genetic determinants of QDR are complex and largely unknown, and are thought to rely partly on genes controlling plant morphology and development.We used genome-wide association mapping in Arabidopsis thaliana to identify ARPC4 as associated with QDR against the necrotrophic fungal pathogen Sclerotinia sclerotiorum. Mutants impaired in ARPC4 showed enhanced susceptibility to S. sclerotiorum, defects in the structure of the actin filaments and in their responsiveness to S. sclerotiorum. Disruption of ARPC4 also alters callose deposition and the expression of defense-related genes upon S. sclerotiorum infection.Analysis of ARPC4 diversity in A. thaliana identified one haplotype (ARPC4 R ) showing a c. 1 kbp insertion in ARPC4 regulatory region and associated with higher level of QDR. Accessions from the ARPC4 R haplotype showed enhanced ARPC4 expression upon S. sclerotiorum challenge, indicating that polymorphisms in ARPC4 regulatory region are associated with enhanced QDR.This work identifies a novel actor of plant QDR against a fungal pathogen and provides a prime example of genetic mechanisms leading to the recruitment of cell morphology processes in plant immunity.480 New Phytologist (2019) 222: 480-496

Background The ongoing adaptation of plants to their environment is the basis for their survival. In this adaptation, mechanoperception of gravity and local curvature plays a role of prime importance in finely regulating growth and ensuring a dynamic balance preventing buckling. However, the abiotic environment is not the exclusive cause of mechanical stimuli. Biotic interactions between plants and microorganisms also involve physical forces and potentially mechanoperception. Whether pathogens trigger mechanoperception in plants and the impact of mechanotransduction on the regulation of plant defense remains however elusive. Results Here, we found that the perception of pathogen-derived mechanical cues by microtubules potentiates the spatio-temporal implementation of plant immunity to fungus. By combining biomechanics modeling and image analysis of the post-invasion stage, we reveal that fungal colonization releases plant cell wall-born tension locally, causing fluctuations of tensile stress in walls of healthy cells distant from the infection site. In healthy cells, the pathogen-derived mechanical cues guide the reorganization of mechanosensing cortical microtubules (CMT). The anisotropic patterning of CMTs is required for the regulation of immunity-related genes in distal cells. The CMT-mediated mechanotransduction of pathogen-derived cues increases Arabidopsis disease resistance by 40% when challenged with the fungus Sclerotinia sclerotiorum. Conclusions CMT anisotropic patterning triggered by pathogen-derived mechanical cues activates the implementation of early plant defense in cells distant from the infection site. We propose that the mechano-signaling triggered immunity (MTI) complements the molecular signals involved in pattern and effector-triggered immunity.

How immune responses are activated and regulated is a central question in immunology. In addition to molecular signaling, recent work has shown that physical forces regulate the immune response of vertebrates by modifying transmembrane protein conformation and cell contact. Mechanical stress and strain produced by forces constitute physical cues perceived by cells instructing gene expression. Whether mechanical cues generated by pathogens during host colonization can trigger adaptive responses in plant cells remains elusive. We found that local and progressive variations of plant cell wall tension caused by fungal pathogen attacks are transmitted to neighboring healthy tissue around the infection site and trigger immunity in distal cells. This thigmoimmunity process requires the reorganization of cortical microtubules and contributes strongly to Arabidopsis disease resistance.