Integrative transcriptomic analysis unveils lncRNA-miRNA-mRNA interplay in tomato plants responding to Ralstonia solanacearum

Ralstonia solanacearum, a bacterial plant pathogen, poses a significant threat to tomato (Solanum lycopersicum) production through destructive wilt disease. While noncoding RNA has emerged as a crucial regulator in plant disease, its specific involvement in tomato bacterial wilt remains limited. Here, we conducted a comprehensive analysis of the transcriptional landscape, encompassing both mRNAs and noncoding RNAs, in a tomato resistant line (‘ZRS_7’) and a susceptible line (‘HTY_9’) upon R. solanacearum inoculation using high-throughput RNA sequencing. Differential expression (DE) analysis revealed significant alterations in 7506 mRNAs, 997 lncRNAs, and 69 miRNAs between ‘ZRS_7’ and ‘HTY_9’ after pathogen exposure. Notably, 4548 mRNAs, 367 lncRNAs, and 26 miRNAs exhibited genotype-specific responses to R. solanacearum inoculation. GO and KEGG pathway analyses unveiled the potential involvement of noncoding RNAs in the response to bacterial wilt disease, targeting receptor-like kinases, cell wall-related genes, glutamate decarboxylases, and other key pathways. Furthermore, we constructed a comprehensive competing endogenous RNA (ceRNA) network incorporating 13 DE-miRNAs, 30 DE-lncRNAs, and 127 DEGs, providing insights into their potential contributions to the response against bacterial inoculation. Importantly, the characterization of possible endogenous target mimics (eTMs) of Sly-miR482e-3p via VIGS technology demonstrated the significant impact of eTM482e-3p-1 silencing on tomato's sensitivity to R. solanacearum. These findings support the existence of an eTM482e-3p-1-Sly-miR482e-3p-NBS-LRRs network in regulating tomato's response to the pathogen. Collectively, our findings shed light on the intricate interactions among lncRNAs, miRNAs, and mRNAs as underlying factors in conferring resistance to R. solanacearum in tomato.