Recruiting resistance: mobilizing the rhizosphere microbiome to reduce plant disease

Abstract

Soil-borne diseases are a growing threat to global agricultural production, a challenge further intensified by climate change. While chemical pesticides and fertilizers can offer short-term control over pathogen populations, their excessive use accelerates soil degradation, biodiversity loss, and environmental pollution. Due to these negative effects, there is an increasing demand for more sustainable alternatives. Breeding disease-resistant varieties is a widely recognized solution, and significant efforts have been made to develop, for instance, disease-resistant banana varieties. However, beyond the plant innate immune system encoded in the genome, increasing evidence has highlighted the plant microbiome as a functional extension of plant immunity. The rhizosphere microbiome, often described as a plant’s “second genome,” plays a central role in plant health and offers promising opportunities for sustainable disease suppression. However, optimizing plant-microbe interactions for disease resistance remains challenging due to the intricate interplay among environmental factors, plant traits, and microbiome dynamics. Therefore, this research investigates how disease-resistant plants shape rhizosphere microbial communities to suppress pathogens, using banana varieties with varying resistance to Fusarium wilt as a model. The study revealed that resistant banana varieties selectively enriched specific fungal taxa, particularly Trichoderma and Penicillium, which contributed to pathogen suppression. These beneficial fungi were stimulated by plant-secreted metabolites such as shikimic acid, D-(-)-ribofuranose, and propylene glycol. Applying these metabolites to soil enhanced the pathogen resistance of otherwise susceptible varieties, underscoring the role of metabolite-mediated recruitment in microbiome assembly. Further analysis demonstrated that the resistance of highly resistant variety was driven by the combined action of both bacteria and fungi. Synthetic cross-kingdom microbial communities, designed based on the natural recruitment patterns of highly resistant variety, significantly inhibited pathogen growth. Their suppressive effects were amplified when combined with metabolites like stearic acid and shikimic acid. The work also showed that transferring rhizosphere microbiomes from resistant to susceptible varieties effectively reduced pathogen densities, providing direct evidence that microbiome composition is a determinant of disease resistance. Moreover, soils previously cultivated with resistant varieties harbored beneficial microbial legacies that improved the resistance of subsequent susceptible plants, highlighting the potential for long-term microbiome-based disease management strategies. Overall, the findings demonstrate that a substantial component of plant disease resistance derives from the ability to recruit functional microbiomes. This shifts the breeding paradigm toward targeting microbiome recruitment traits as a means of improving plant health. By integrating ecological principles with plant–microbe interaction insights, this research lays a foundation for sustainable, microbiome-informed agricultural practices capable of enhancing resilience against soil-borne diseases.