Streptomyces violaceoruber induces root morphological changes in Solanum lycopersicum via early epigenetic and transcriptional reprogramming

The increasing demand for sustainable agricultural practices has highlighted the potential of Plant Growth-Promoting Bacteria (PGPB) as eco-friendly tools to enhance crop productivity while minimizing environmental impact. Among PGPBs, members of the Actinomycetota phylum (formerly known as actinobacteria), and particularly Streptomyces violaceoruber, have emerged as promising candidates due to their ability to produce bioactive metabolites, promote plant growth, and modulate plant physiological responses. In this work, we investigated the effects of S. violaceoruber on tomato (Solanum lycopersicum) in vitro - grown seedlings using an integrated phenotypic, volatilomic, transcriptomic, and epigenetic approach. Seedlings were analyzed at seven (T1) and fifteen days (T2) post-inoculation with S. violaceoruber. Phenotypic assessment of inoculated seedlings revealed no significant alterations in shoot length or biomass, while a remarkable increase in seedling root diameter and the formation of aerial roots was observed. Transcriptomic analyses showed substantial transcriptional reprogramming, with a greater number of differentially expressed genes (DEGs) at T1, in particular involved in the regulation of biological processes, metabolic pathways, and responses to external stimuli, such as light. Co-expression network analysis of four root-associated bait genes further confirmed that these pathways are primary targets of S. violaceoruber effects. Epigenetic profiling of treated plant roots revealed an increase in global DNA methylation (5-methylcytosine) levels, along with a significant enrichment of histone post-translational modifications associated with permissive chromatin at the bait gene loci. Overall, S. violaceoruber inoculation induced notable molecular and developmental changes in tomato seedlings, reinforcing its potential as a sustainable biofertilizer. These findings provide new insights into PGPB–plant interactions and contribute to the development of environmentally-friendly strategies for crop improvement.