Soil microbiota influences clubroot disease by modulating Plasmodiophora brassicae and Brassica napus transcriptomes

The contribution of surrounding plant microbiota to disease development has led to the postulation of the ‘pathobiome’ concept, which represents the interaction between the pathogen, the host-plant, and the associated biotic microbial community, resulting or not in plant disease. The structure, composition and assembly of different plant-associated microbial communities (soil, rhizosphere, leaf, root) are more and more described, both in healthy and infected plants. A major goal is now to shift from descriptive to functional studies of the interaction, in order to gain a mechanistic understanding of how microbes act on plant growth and defense, and/or on pathogen development and pathogenicity. The aim herein is to understand how the soil microbial environment may influence the functions of a pathogen and its pathogenesis, as well as the molecular response of the plant to the infection, with a dual-RNAseq transcriptomics approach. We address this question using Brassica napus and Plasmodiophora brassicae, the pathogen responsible for clubroot. A time-course experiment was conducted to study interactions between P. brassicae, two B. napus genotypes, and three soils harboring High (H), Medium (M) or Low (L) microbiota diversities and displaying different levels of richness and diversity. The soil microbial diversity levels had an impact on disease development (symptom levels and pathogen quantity). The P. brassicae and B. napus transcriptional patterns were modulated by these microbial diversities, and the modulations were dependent of the host genotype plant and the kinetic time. The functional analysis of gene expressions allowed the identification of pathogen and plant-host functions potentially involved in the change of plant disease level, such as pathogenicity-related genes (NUDIX effector) in P. brassicae and plant defense-related genes (glucosinolate metabolism) in B. napus. Author summary The untapped soil microbiota diversity can influence plant tolerance and resistance to several pests. A better understanding of the mechanisms underlying the plant / pests / microbiota interaction is required to contribute to the improvement of new plant protection methods taking into account sustainability, respect for the environment, and low input utilization. Our work showed that in the Plasmodiophora brassicae / Brassica napus pathosystem, the soil microbiota diversity modulated the disease symptom level and the pathogen development. We discovered that soil microbial composition modulated both the pathogen and the plant expression genes profiles. On one hand, the pathogen transcriptome was mainly modulated by the microbial communities at the end of infection, when the pathogen infects a susceptible plant genotype, and the expression of genes potentially involved in growth and pathogenicity was affected. On the other hand, the plant transcriptome was more modulated by the microbial communities at the early step of infection, in the most resistant genotype and the expression of genes potentially involved in defense was affected. This study provides new insights into the molecular basis of soil microbiota-mediated modulation of plant pest diseases.