Heritability of tomato rhizobacteria resistant to Ralstonia solanacearum

BACKGROUND: Ralstonia solanacearum (Rs) is a soilborne phytopathogen that causes bacterial wilt and substantial yield losses in many plants, such as tomatoes. A resistant tomato cultivar can recruit a beneficial microbiome from soil to resist Rs. However, whether this recruitment is inheritable from resistant parent to progeny has not been determined. RESULTS: In the present study, we investigated the rhizosphere microbiomes of tomatoes with clear kinship and different resistance against Rs. Resistant tomatoes grown with the additions of natural soil or its extract showed lower disease indexes than those grown in the sterile soil, demonstrating the importance of soil microbiome in resisting Rs. The results of 16S ribosomal RNA gene amplicon sequencing revealed that the resistant cultivars had more robust rhizosphere microbiomes than the susceptible ones. Besides, the resistant progeny HF12 resembled its resistant parent HG64 in the rhizosphere microbiome. The rhizosphere microbiome had functional consistency between HF12 and HG64 as revealed by metagenomics. Based on multi-omics analysis and experimental validation, two rhizobacteria (Sphingomonas sp. Cra20 and Pseudomonas putida KT2440) were enriched in HF12 and HG64 with the ability to offer susceptible tomatoes considerable protection against Rs. Multiple aspects were involved in the protection, including reducing the virulence-related genes of Rs and reshaping the transcriptomes of the susceptible tomatoes. CONCLUSIONS: We found promising bacteria to suppress the tomato bacterial wilt in sustainable agriculture. And our research provides insights into the heritability of Rs-resistant tomato rhizobacteria, echoing the inheritance of tomato genetic material. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40168-022-01413-w.