Pathogen-derived mechanical cues potentiate the spatio-temporal implementation of plant defense.

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.

Expression polymorphism at the ARPC4 locus links the actin cytoskeleton with quantitative disease resistance to Sclerotinia sclerotiorum in Arabidopsis thaliana.

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 (ARPC4R ) showing a c. 1 kbp insertion in ARPC4 regulatory region and associated with higher level of QDR. Accessions from the ARPC4R 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.