Recruitment of microbial communities involved in the soil borne legacy of disease

Abstract

Plants host an immense and diverse community of microbes, throughout their leaves to the roots and into the surrounding soil. These complex communities provide many benefits to their hosts in exchange for nutrient. For example, plants can actively recruit beneficial microbiomes through the secretion of exudates upon pathogen challenge, resulting in reduced susceptibility to disease. This heightened resistance to a pathogen can be inherited via the soil to future populations of plants as a soil-borne legacy of disease (SBL). Here, we use 16S amplicon sequencing to investigate the spatial and temporal colonisation patterns of a set of consistently recruited Hpa-associated microbes that we suspect play a role the establishment of an SBL in Arabidopsis thaliana. We provide evidence that this Hpa-associated microbiome (HAM) can colonise both the phyllosphere and endosphere of the plant, and furthermore, that they can be inherited in these compartments to a subsequent population of A. thaliana growing on the same soil. These findings support the hypothesis that these beneficial microbes migrate within the plant, explaining how they travel from the phyllosphere to the soil to mediate soil-borne inheritance. In a parallel line of questioning, we investigate the role of plant exudates in the establishment of the SBL. Using A. thaliana mutant genotypes impaired in the secretion of specific metabolites, we implicate two new exudate biosynthesis pathways in this phenomenon – camalexins and flavonoids. This brings us closer to understanding the complex network of interactions required for Hpa-induced recruitment of the protective microbiome and the maintenance of this defensive community for subsequent populations. Together, our results contribute to an emerging model of how active plant-microbe interactions foster beneficial microbiomes that protect against disease, a better understanding of which will unlock further research avenues and facilitate advances in crop protection techniques for sustainable agriculture.