β-cyclocitral (βCC), a major apocarotenoid of β-carotene, enhances plants’ defense against environmental stresses. However, the knowledge of βCC’s involvement in the complex stress-signaling network is limited. Here we demonstrate how βCC reprograms the transcriptional responses that enable Solanum lycopersicum L. (tomato) plants to endure a plethora of environmental stresses. Comparative transcriptome analysis of control and βCC-treated tomato plants was done by generating RNA sequences in the BGISEQ-500 platform. The trimmed sequences were mapped on the tomato reference genome that identifies 211 protein-coding differentially expressed genes. Gene ontology and Kyoto Encyclopedia of Genes and Genomes analysis and their enrichment uncovered that only upregulated genes are attributed to the stress response. Moreover, 80% of the upregulated genes are functionally related to abiotic and biotic stresses. Co-functional analysis of stress-responsive genes revealed a network of 18 genes that code for heat shock proteins, transcription factors (TFs), and calcium-binding proteins. The upregulation of jasmonic acid (JA)-dependent TFs (MYC2, MYB44, ERFs) but not the JA biosynthetic genes is surprising. However, the upregulation of DREB3, an abscisic acid (ABA)-independent TF, validates the unaltered expression of ABA biosynthetic genes. We conclude that βCC treatment upregulates multiple stress-responsive genes without eliciting JA and ABA biosynthesis.

β-cyclocitral (βCC) is one of the significant oxidative products of β-carotene. It primes plants for multiple stress acclimation without compromising plant growth. Metabolic reorganization is necessary to maintain a balance between growth and defense. However, the βCC-mediated changes in a plant’s metabolic network are unknown. Here, we demonstrate how βCC-induced metabolic changes enable Solanum lycopersicum L. (tomato) plants to promote defense and maintain growth under stress. An analysis of early (0–240 min) and late (72 h) changes in the tomato metabolome after βCC-treatment using liquid chromatography and tandem mass spectrometry identified 57 compounds. A principal coordinate analysis suggested that βCC treatment significantly changes the metabolite profile. A variable importance in projection (VIP) analysis revealed 16 and 19 discriminant metabolites from early and late samples, respectively (VIP ≥ 1.0). Upregulated metabolites were mainly amino acids and phytophenols. Pathway enrichment analysis showed that βCC treatment influenced amino acid metabolism at early and later times; however, phenylpropanoid and isoquinoline biosynthesis were influenced only at the later time. A 66.6% similarity in the upregulated metabolites of βCC- and simulated-herbivory-treated plants confirmed βCC’s role against herbivores. We conclude that βCC steers a temporal separation in amino acids and defense metabolite accumulation that optimizes resource allocation to growth and defense.