For the successful completion of their life cycle plants need strategies for successful growth and defense. This need for phenotypic plasticity requires the reconfiguration of plants’ transcriptome, proteome, and hence the metabolome to optimize resource use during stress, whose regulators remain largely unknown. We explored the possibility of small-RNAs (smRNAs) as regulators of plants’ induced stress responses. Because RNA-directed RNA polymerases (RdRs) are central to smRNA biogenesis, especially the biogenesis of siRNAs, they can be manipulated in order to study the smRNA response of the whole organism. Combining large-scale pyro-sequencing, computational predictions, RdR-silencing, field studies, and assays that are molecular, biochemical, and glasshouse based, we determined that the induced physiological responses of plants to stress are under smRNA control.