Plants with lowered activity of enzymes catalyzing the final step of ascorbate synthesis or the equilibrium between reduced and oxidized forms have highly pleiotropic phenotypes suggesting regulatory roles for ascorbate and its oxidized forms. Network analysis of the transcriptome, proteome and key metabolites of RNAi lines for ascorbate oxidase, monodehydroascorbate reductase and galactonolactone dehydrogenase has been carried out in orange fruit pericarp of tomato (Solanum lycopersicum). We show a transcriptional switch-type response with expression profiles in ascorbate oxidase lines being inversed compared to the monodehydroascorbate reductase and galactonolactone dehydrogenase lines. Differentially expressed genes are linked to ribosome biogenesis and translation. The inversion between the transcriptome signatures is not specific to tomato fruit as it is conserved in Arabidopsis. The transcriptome response is not correlated with accumulated proteins which, with the metabolites, are correlated to the activity of the ascorbate redox enzymes. Differentially accumulated proteins include metacaspase, protein disulphide isomerase, chaperone DnaK and carbonic anhydrase and the metabolites chlorogenic acid, dehydroascorbate and alanine. Hub genes are related to signaling, the heat-shock response and ribosome biogenesis. This study in a non-photosynthetic tissue reveals signaling from the ascorbate pool related to the heat-shock response, translation and protein synthesis.