Mechanosensory trichome cells evoke a mechanical stimuli–induced immune response in Arabidopsis thaliana

Abstract

Perception of pathogen-derived ligands by corresponding host receptors is a pivotal strategy in eukaryotic innate immunity. In plants, this is complemented by circadian anticipation of infection timing, promoting basal resistance even in the absence of pathogen threat. Here, we report that trichomes, hair-like structures on the epidermis, directly sense external mechanical forces, including raindrops, to anticipate pathogen infections in Arabidopsis thaliana. Exposure of leaf surfaces to mechanical stimuli initiates the concentric propagation of intercellular calcium waves away from trichomes to induce defence-related genes. Propagating calcium waves enable effective immunity against pathogenic microbes through the CALMODULIN-BINDING TRANSCRIPTION ACTIVATOR 3 (CAMTA3) and mitogen-activated protein kinases. We propose an early layer of plant immunity in which trichomes function as mechanosensory cells that detect potential risks.

Single-cell profiling of complex plant responses toPseudomonas syringaeinfection

“…A second independent transgenic line of pLipoP1∷NLS-3xmCitrine exhibited a similar expression pattern, but had more robust expression at 72h (Figure S6A). A previous transcriptional reporter CBP60gpro:EYFP-NLS has been characterized and this line exhibited similar baseline expression as well as expression in skirt cells (see below, Matsumura et al, 2022). Together, these data highlight activation of immune marker genes at early infection stages and downregulation at late stages, consistent with the pseudotime trajectory.…”

How the sensory system of carnivorous plants has evolved

“…(2022) are not surprising in the context of another recent study, which may help us to understand how this sensory system may have evolved. When the leaf trichome of non-carnivorous Arabidopsis thaliana transformed with the same Ca 2+ sensor (GCaMP3) was mechanically stimulated, a Ca 2+ wave was triggered, beginning at the trichome base before propagating away from the trichome as a concentric wave ( Matsumura et al., 2022 ). In the cells that received a Ca 2+ signal, the immune response was initiated in a phytohormone (e.g., JA)-dependent and independent manner.…”

“…These findings suggest that the prerequisite for the sensory system of Droseraceae was already present in non-carnivorous plants and that evolution only fine-tuned the process for botanical carnivory. Because the Ca 2+ wave in the Arabidopsis trichome does not enter neighboring trichomes ( Matsumura et al., 2022 ), an increase in tentacle density or a decrease in the resistance to Ca 2+ wave propagation may lead to coordination and complex trap behavior. Presumably, this hypothesis can be tested using mutants of transgenic GCaMP3 Arabidopsis with increased trichome density.…”

Efficient Isolation and Purification of High‐Quality Arabidopsis thaliana Trichomes

“…Concerning the latter, the secretion of, for instance, phenolic substances (mainly by glandular trichomes) and the deployment of an initial physical barrier (mainly by non‐glandular trichomes) have been identified as pivotal strategies to prevent herbivore attack (Karabourniotis, Liakopoulos, Nikolopoulos, & Bresta, 2020). Moreover, non‐glandular trichomes of the model plant Arabidopsis thaliana were recently described as mechanosensors that initiate immune responses upon rainfall, to preempt attacks by rain‐dispersed fungal spores or bacteria (Matsumura et al., 2022).…”