Calcium-containing inorganic immunity booster drives the enrichment of specific root endophytic microbiota against Ralstonia solanacearum

BACKGROUND: Engineering root microbiomes holds great promise to enhance plant health. Enhanced plant resistance via breeding or genetic modification can promote recruiting beneficial microbes, but is challenging to achieve. RESULTS: Here we showed that calcium (Ca) addition caused significant changes in tomato physiology, resulting in enhanced immunity towards the pathogen Ralstonia solanacearum along with increased levels of salicylic acid (SA), sugar content, and defense enzyme activities in roots. High Ca levels significantly altered the root microbiomes, enriching sixteen bacterial genera, including Dyella japonica, Rhodanobacter glycinis, Paenibacillus polymyxa, and Pseudomonas aeruginosa, with the mostly enriched genus showing a 16.5-fold increase in the relative abundance compared to no Ca addition. Associated with the enhancement of these bacterial genera, tomato wilt incidence was reduced from 80 to 0%. The growth of these four bacterial strains was promoted to varying extent by the addition of SA, sucrose, trehalose, and Ca in vitro. All the four bacterial strains had antagonistic ability against R. solanacearum. A synthetic microbial community (SynCom) of these four strains significantly inhibited R. solanacearum growth in whole root exudates treated with Ca, and the combination of SynCom and Ca addition resulted in nearly eradication of the tomato bacterial wilt. CONCLUSIONS: Our findings revealed an effective and simple method for enriching beneficial microbiomes to protect plants against pathogens. Our results also suggested that combination of immunity boosters and beneficial microbes offers a novel strategy to combat soil-borne diseases. Video Abstract.