Deciphering of benzothiadiazole (BTH)-induced response of tomato (Solanum lycopersicum L.) and its effect on early response to virus infection through the multi-omics approach

Background and aims One of the preventive methods used to limit the losses caused by viruses is the application of synthetic immunity inducers, such as benzo(1,2,3)-thiadiazole-7-carbothioic acid S-methyl ester (BTH). This study aimed at explaining how the BTH treatment affects the defence and developmental processes in tomato plants (Solanum lycopersicum L.) as well as plant response to virus infection. Method The comparative multi-omics analyses concerning tomato plants treated with BTH were performed, including transcriptomics (RNA-Seq), proteomics (Liquid Chromatography-Mass Spectrometry), and metabolomics (targeted hormonal analysis). To confirm the priming effect of BTH on tomato resistance, the plants were infected with tomato mosaic virus (ToMV) seven days post-BTH treatment. Results The combined functional analysis indicated the high impact of BTH on the plant's developmental processes and activation of the immune response early after the treatment. In the presented experimental model, the increased level of WRKY TRANSCRIPTION FACTORS, ARGONAUTE 2A, thiamine and glutathione metabolism, cell wall reorganization, and detoxification processes, as well as accumulation of three phytohormones: abscisic acid, jasmonic acid-isoleucine (JA-Ile), and indole-3-carboxylic acid (I3CA), were observed upon BTH application. Conclusion The immune response activated by BTH was related to increased expression of genes associated with the cellular detoxification process, systemic acquired resistance, and induced systemic resistance as well as post-transcriptional gene silencing. Increased levels of I3CA and JA-Ile might explain the BTH's effectiveness in the induction of the plant defence against a broad spectrum of pathogens. For the first time, the BTH involvement in the induction of the thiamine metabolism was revealed in tomatoes.

Automated summary

This study investigated the effects of benzo(1,2,3)-thiadiazole-7-carbothioic acid S-methyl ester (BTH) treatment on the defense and developmental processes in tomato plants. Multi-omics analyses revealed that BTH treatment significantly influenced the plant's immune response and activation of certain genes, as well as the accumulation of important phytohormones. The study also uncovered the involvement of BTH in the induction of thiamine metabolism in tomatoes. These findings provide valuable insights into the plant's defense mechanisms against virus infections.