Signals from the underground and their interplay with plant immunity

Abstract

The interface between roots and their adjacent soil layer, the rhizosphere, constitutes a hotspot of microbial activity and represents one of the most diverse ecosystems on Earth. The root-associated microbial community, the microbiome, contains rhizobacteria that can change the phenotypic plasticity of their hosts and trigger a broad-spectrum form of systemic immunity, known as induced systemic resistance (ISR). Although the effect of beneficial rhizobacteria on plant growth and plant health is relatively well studied, very little is known about the early molecular processes that occur at the root-microbiome interface. In this thesis, we investigated early changes in the root transcriptome and metabolome of plant roots in response to colonization of the roots by beneficial ISR-inducing Pseudomonas rhizobacteria. We discovered that ISR-inducing rhizobacteria suppress host immune responses that are triggered by their general microbial elicitors to subsequently allow root colonization and promotion of plant growth and protection. Moreover, we uncovered the iron-mobilizing coumarin scopoletin as a major player in the chemical dialogue between plants roots and ISR-inducing members in the root microbiome. Collectively, our results show that beneficial rhizobacteria are capable of suppressing root immune responses that are activated by their general elicitors, possibly via the action of immune-suppressive effectors. This paves the way to colonize the roots and provide beneficial functions to the host plant, such as enhanced growth and protection. Within the root, the transcription factor MYB72 regulates the biosynthesis of coumarins, such as scopolin. Due to the action of the MYB72-regulated β-glucosidase BGLU42, scopolin is hydrolyzed into scopoletin, which facilitates the excretion of this metabolite into the rhizosphere. Scopoletin has a differential antimicrobial activity to which ISR-inducing rhizobacteria WCS417 and WCS358 are insensitive, but which impacts the performance of selected soil-borne pathogens. Analysis of the root-associated microbiomes of Arabidopsis roots with different scopoletin exudation patterns demonstrated a role for scopoletin in microbiome assembly. Knowledge on the molecular mechanisms that play a role in the interaction between plant roots and beneficial members of the root microbiome is essential for the development of durable biological control strategies and crops with traits that can maximize the profitable functions the root microbiome.