Local traveling waves of cytosolic calcium elicited by defense signals or wounding are propagated by distinct mechanisms

Abstract

Cytosolic Ca2+ signatures with specific spatiotemporal patterns play crucial roles in plant responses to biotic and abiotic stresses. Perception of microbe- or damage-associated molecular patterns (MAMPs or DAMPs) initiates signaling cascades that represent the first layer of plant defense against pathogens known as pattern-triggered immunity (PTI). During PTI, MAMP/DAMP-induced cytosolic Ca2+ fluxes serve as essential messengers in the initiation and transmission of defense signals at the cellular, whole organ, and systemic levels. However, the specific patterns of these Ca2+ signatures in response to different pathogen cues, and the mechanisms that encode them, remain largely unexplored. In this study, we quantitatively assessed Ca2+ signatures at the single-cell level as well as the local traveling Ca2+ waves induced by global treatment of Arabidopsis cotyledons with MAMPs or DAMPs. We demonstrated that MAMPs induced distinct local spatiotemporal Ca2+ responses in epidermal pavement cells, with Ca2+ traveling waves consistently initiated from a subset of cells and spreading in an approximately radial pattern. These local traveling waves propagated at a slow but constant speed of approximately 1 {micro}m/s and spread to a limited number of neighboring cells. In contrast, wound-induced traveling waves displayed a diffusion-like decay pattern that moved rapidly away from the wounded cell but with diminishing speed over time and distance. Mathematical modeling supported a calcium-induced calcium release mechanism that could recapitulate the constant wave speed induced by MAMPs. These findings contribute to a deeper understanding of plant defense-related Ca2+ signaling mechanisms as well as how defense responses are spatially restricted within tissues. One Sentence SummaryA slow, local traveling wave of calcium is initiated from a subset of epidermal cells during plant immune signaling.