Single-cell RNA-seq uncovers landscape of tomato metabolic rewiring mediated by plant growth-promoting rhizobacteria

Tomato contains various classes of metabolites conferring benefits to human health and plant defense. Metabolic reprogramming of tomato induced by plant growth-promoting rhizobacteria (PGPR), such as Streptomyces spp., provides a feasible solution to enhance fruit quality and plant performance. However, the spatiotemporal and intensity characteristics of plant metabolism rewired following PGPR inoculation remain largely uncovered. Here, we characterized the landscape of PGPR-mediated metabolic reprogramming in whole plants of tomato. Large-scale single-cell transcriptomic and metabolomic analyses were performed using leaf, stem, root, flower, and fruit samples from potted plants inoculated or not with Streptomyces rochei D74. The accumulation of flavonoids, sugars, vitamins, and phenolic acids in fruits was enhanced upon inoculation, accompanied by increased contents of phenolic acids and flavonoids in vegetative tissues. We observed strong metabolic responses to PGPR in fruits, as indicated by upregulated relative abundances of many flavonoids and high expression levels of related biosynthetic genes located in the exocarp. Cell subclustering coupled with trajectory construction revealed three distinct states of exocarp cells, i.e., precursor metabolite mobilization-flavonoid biosynthesis-post-synthetic transport. PGPR inoculation promoted flavonoid accumulation in fruits by upregulating the expression of genes related to flavonoid and phenylpropanoid biosynthesis. We additionally identified phytohormone- and transcription factor-associated regulatory genes specific to cell states upon inoculation. Our findings unravel dynamic changes in PGPR-mediated plant metabolism at single-cell resolution. This study provides a multi-omic data resource for identifying the key molecular mechanisms that regulate flavonoid metabolism in tomato.