Pseudomonas syringaepv. tomato exploits light signals to optimize virulence and colonization of leaves

Abstract

Light is pervasive in the leaf environment, creating opportunities for both plants and pathogens to cue into light as a signal to regulate plant-microbe interactions. Light enhances plant defences and regulates opening of stomata, an entry point for foliar bacterial pathogens such as Pseudomonas syringae pv. tomato DC3000 (PsPto). The effect of light perception on gene expression and virulence was investigated in PsPto. Light induced genetic reprogramming in PsPto that entailed significant changes in stress tolerance and virulence. Blue light-mediated up-regulation of type three secretion system genes and red light-mediated down-regulation of coronatine biosynthesis genes. Cells exposed to white light, blue light or darkness before inoculation were more virulent when inoculated at dawn than dusk probably due to an enhanced entry through open stomata. Exposure to red light repressed coronatine biosynthesis genes which could lead to a reduced stomatal re-opening and PsPto entry. Photoreceptor were required for the greater virulence of light-treated and dark-treated PsPto inoculated at dawn as compared to dusk, indicating that these proteins sense the absence of light and contribute to priming of virulence in the dark. These results support a model in which PsPto exploits light changes to maximize survival, entry and virulence on plants.

Blue‐light perception by epiphytic Pseudomonas syringae drives chemoreceptor expression, enabling efficient plant infection

“…Although our previous results showed that light had a regulatory effect on the above-mentioned categories in PsPto in vitro populations (Santamaria-Hernando et al, 2018), we show here that the contact with the leaf triggers a regulatory response that is upstream to the regulatory effect exerted by light. Interestingly, we have found that following contact with the leaf surface, and regardless of light conditions, all genes that encode the chemosensory cluster III are up-regulated in PsPto (Tables S1 and S2).…”

“…Record GSE10 1783 (Santamaria-Hernando et al, 2018) previously generated in our laboratory has been used for comparisons.…”

“…Control of motility and chemotaxis towards plant compounds facilitates bacterial access to the apoplast through stomata or wounds on the leaf surface (Matilla and Krell, 2018). Both motility and chemotaxis during the initial stages of plant colonization are required for a subsequent successful infection (Rio‐Alvarez et al ., 2014; Matilla and Krell, 2018; Santamaria‐Hernando et al ., 2018). Chemoreceptors or methyl‐accepting chemotaxis proteins (MCPs) are particularly abundant in phytopathogenic bacteria as compared to bacteria living in other habitats (Matilla and Krell, 2018).…”

“…The PsPto genome encodes a single blue‐light‐sensing light oxygen voltage (LOV)‐domain protein and two red‐light‐sensing bacteriophytochromes, BphP1 and BphP2 (Figure ). Light perception through these photosensory proteins, especially during the initial stages of plant colonization, affects adhesion, motility, and virulence in PsPto (Moriconi et al ., 2013; Rio‐Alvarez et al ., 2014; Santamaria‐Hernando et al ., 2018). Interestingly, we found that light functions as a global signal in PsPto.…”

“…A short light treatment prior to challenge induces a genetic reprogramming that involves significant changes in subsequent leaf colonization and virulence‐related traits. These changes at the transcriptomic level were correlated with alterations in the virulence outcome depending on the wavelength of the light applied to bacteria before plant inoculation (Santamaria‐Hernando et al ., 2018). These findings highlight the relevance of light as a signal in the early stages of plant colonization and prompted us to evaluate the effect of light perception on gene expression in PsPto epiphytic populations during the initial contact with the tomato leaf surface.…”