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Heat drives tomato bacterial wilt through enhanced pathogen virulence and rhizosphere microbiome and metabolic shifts

ABSTRACT: Bacterial wilt caused by Ralstonia solanacearum is globally widespread and strongly associated with elevated temperature, yet the ecological mechanisms underlying temperature-driven disease outbreaks remains unclear. Here, we show that high temperature promotes bacterial wilt by reconfiguring the tomato rhizosphere system across multiple biological scales. High temperature enhanced pathogen growth and virulence, accompanied by transcriptional activation of motility, quorum sensing, and environmental sensing pathways. Concurrently, heat stress suppressed plant performance and destabilized the rhizosphere microbiome, leading to reduced diversity and depletion of beneficial taxa. Metabolomic analyses further revealed a temperature-driven shift from defense-associated metabolites to amino acids and nucleosides, creating a metabolically permissive niche for pathogen establishment. Guided by these insights, a heat-adapted synthetic microbial community effectively suppressed disease and restored plant growth under high-temperature conditions. Together, our findings reveal temperature as a central driver of rhizosphere reprogramming and highlight microbiome engineering as a promising strategy for climate-resilient disease control.

INSTRUMENT(S): Liquid Chromatography MS - positive - hilic, Liquid Chromatography MS - negative - hilic

PROVIDER: MTBLS14437 | MetaboLights | 2026-05-31

REPOSITORIES: MetaboLights

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			Action	DRS
	a_MTBLS14437_LC-MS_negative_hilic.txt	Txt
	a_MTBLS14437_LC-MS_positive_hilic.txt	Txt
	i_Investigation.txt	Txt
	m_MTBLS14437_LC-MS_negative_hilic_v2_maf.tsv	Tabular
	m_MTBLS14437_LC-MS_positive_hilic_v2_maf.tsv	Tabular

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Project description:Background Crop continuous cropping obstacles (CCO) severely threaten soil ecosystem health and sustainable agricultural production. Although bio-organic fertilizer (BF) has been widely applied to mitigate crop CCO, the underlying mechanisms remain poorly understood. Herein, an Aspergillus-amended BF was developed using an antagonistic strain isolated from tobacco rhizosphere. By integrating plant physiological responses with plant and rhizosphere metabolomics and microbiome analyses, we investigated the mechanisms underlying BF-mediated alleviation of tobacco CCO. Results We show that novel Aspergillus-amended BF markedly alleviates tobacco CCO by coordinately reprogramming host metabolism and the rhizosphere microbiome. BF application activated tobacco systemic acquired resistance through phenylalanine-derived salicylic acid signaling, as evidenced by the induction of PR genes, reactive oxygen species accumulation, and redox homeostasis regulation. Concurrently, BF significantly reshaped the composition, functional potential, and interaction networks of the rhizosphere microbiome, suppressing pathogen survival and virulence while enriching beneficial taxa, including Aspergillus, Flavobacterium, Pseudomonas, and Galbibacter, along with functional pathways related to quorum sensing and ABC transporters. BF also enhanced positive microbial interactions, thereby strengthening microbial network stability. Critically, microbiome reconstitution assays demonstrated that this protective effect depended on viable rhizosphere microbial communities, highlighting a causal role of the microbiome. Field trials further confirmed the efficacy of BF in mitigating tobacco CCO, resulting in a 31.0% reduction in disease incidence and significant improvements in economic traits compared with chemical fertilizer alone. Conclusions Collectively, our findings reveal a coordinated host-microbiome mechanism underlying BF-mediated alleviation of tobacco CCO and highlight microbiome priming as a promising strategy for microbiome-based disease suppression and sustainable agricultural production.

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Heat drives tomato bacterial wilt through enhanced pathogen virulence and rhizosphere microbiome and metabolic shifts

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