Local and Systemic Transcriptional Responses of Tomato to a Growth-Promoting Streptomyces Consortium

Members of the genus <i>Streptomyces</i> are prominent inhabitants of the plant rhizosphere and endosphere and are increasingly recognized for their roles in plant growth promotion and disease suppression. In this study, we isolated genetically distinct <i>Streptomyces</i> from the tomato (<i>Solanum lycopersicum</i> L.) rhizosphere, designated as TOM isolates, and assembled them into a defined 12-member TOM consortium. Application of the TOM consortium significantly promoted root and shoot growth in tomato. RNA-seq analysis revealed coordinated local and systemic transcriptional responses characterized by a predominance of down-regulated genes in both roots and leaves. In roots, differential gene expression reflected selective attenuation of defense- and cell wall-related processes, alongside increased expression of genes associated with phytoalexin biosynthesis, phosphate starvation responses, and hormonal regulation. In leaves, transcriptional reprogramming was dominated by reduced stress-related responses together with activation of metabolic and growth-associated functions. The TOM consortium also reduced disease severity caused by <i>Fusarium oxysporum</i> f. sp. <i>radicis-lycopersici</i> by approximately 60% compared to infected controls. To further characterize functional traits of individual consortium members, isolates were evaluated in vitro for antifungal activity and five strains displaying inhibition were selected for hybrid whole-genome sequencing. Genome analyses revealed diverse taxonomic affiliations and a rich repertoire of biosynthetic gene clusters, including clusters associated with known antimicrobial metabolites as well as numerous low-similarity clusters indicative of substantial unexplored biosynthetic potential. Collectively, this study provides new insights into plant interactions with beneficial <i>Streptomyces</i>, while revealing molecular signatures involved in <i>Streptomyces</i>-mediated plant growth promotion and pathogen suppression.