Salicylic Acid and Jasmonic Acid Pathways are Activated in Spatially Different Domains Around the Infection Site During Effector-Triggered Immunity in Arabidopsis thaliana

Abstract

The innate immune response is, in the first place, elicited at the site of infection. Thus, the host response can be different among the infected cells and the cells surrounding them. Effector-triggered immunity (ETI), a form of innate immunity in plants, is triggered by specific recognition between pathogen effectors and their corresponding plant cytosolic immune receptors, resulting in rapid localized cell death known as hypersensitive response (HR). HR cell death is usually limited to a few cells at the infection site, and is surrounded by a few layers of cells massively expressing defense genes such as Pathogenesis-Related Gene 1 (PR1). This virtually concentric pattern of the cellular responses in ETI is proposed to be regulated by a concentration gradient of salicylic acid (SA), a phytohormone accumulated around the infection site. Recent studies demonstrated that jasmonic acid (JA), another phytohormone known to be mutually antagonistic to SA in many cases, is also accumulated in and required for ETI, suggesting that ETI is a unique case. However, the molecular basis for this uniqueness remained largely to be solved. Here, we found that, using intravital time-lapse imaging, the JA signaling pathway is activated in the cells surrounding the central SA-active cells around the infection sites in Arabidopsis thaliana. This distinct spatial organization explains how these two phythormone pathways in a mutually antagonistic relationship can be activated simultaneously during ETI. Our results re-emphasize that the spatial consideration is a key strategy to gain mechanistic insights into the apparently complex signaling cross-talk in immunity.

MdWRKY15 improves resistance of apple to Botryosphaeria dothidea via the salicylic acid‐mediated pathway by directly binding the MdICS1 promoter

“…As a plant hormone, SA plays a significant role in fighting disease (Shirasu et al 1997; Betsuyaku et al 2017). With increasing concentrations of SA, plants increase resistance to pathogens by triggering defense gene expression and H 2 O 2 accumulation (Shirasu et al 1997).…”

Molecular networks in plant–pathogen holobiont

“…During ETI, a concentration gradient of SA is formed around the pathogen infection site that eventually undergoes HR cell death . Intravital time‐lapse imaging of the promoter activities of the SA maker gene PR1 and the JA marker gene VSP1 during Pto AvrRpt2‐triggered ETI showed that JA signaling is activated in a spatial domain surrounding the HR area at an early stage, which is followed by activation of SA signaling in the region between the HR‐ and JA‐active domains . This temporally dynamic and spatially separated activation of JA and SA signaling during ETI could be interpreted as a plant strategy to locally confine the SA‐active cells via JA‐SA antagonism and to create JA‐active cells for preventing secondary infection by necrotrophic pathogens that are sensitive to JA‐mediated immunity .…”

“…However, it was shown that prior ETI activation in one half of a leaf has no effect on promoting the growth of the necrotrophic fungus Alternaria brassicicola in the other leaf half . Furthermore, ETI‐associated cell death and defense responses are tightly regulated in a spatiotemporal manner . Therefore, it may be possible that spatiotemporal regulation of ETI responses including cell death provides certain tolerance against exploitation by necrotrophic pathogens.…”

“…Thus, this “incoherent feed‐forward loop” consisting of JA, PAD4, and EDS5 coordinates SA‐mediated immunity with plant growth and high‐temperature response during PTI . Another excellent example of the biological significance of JA‐SA crosstalk was recently proposed . During ETI, a concentration gradient of SA is formed around the pathogen infection site that eventually undergoes HR cell death .…”

On plant defense signaling networks and early land plant evolution

“…Liu et al [145] showed that SA promotes the synthesis of JA and the activation of its signaling during ETI. However, a recent study by Betsuyaku et al [146] showed that SA and JA act antagonistically during ETI on a narrow spatial scale. So far, spatial information on JA responses in non-flowering plants is only available for conifers, where MeJA treatment results in cell type-specific PAL activation [17].…”