Plants perceive information from the surroundings and elicit appropriate molecular responses. How plants dynamically respond to combinations of external inputs is yet to be revealed, despite the detailed current knowledge of intracellular signalling pathways. We measured dynamics of Response-to-Dehydration 29A (RD29A) expression induced by single or combined NaCl and ABA treatments in Arabidopsis thaliana. RD29A expression in response of combination of NaCl and ABA leads to unique dynamical behaviours that cannot be explained by the sum of responses to individual NaCl and ABA. To explore the potential mechanisms responsible for the observed synergistic response, we developed a mathematical model of the DREB2 and AREB pathways based upon the existing knowledge, where NaCl and ABA act as the cognate inputs, respectively, and examined various system structures with cross-input modulation, where non-cognate input affects expression of the genes involved in adjacent signalling pathways. The results from the analysis of system structures, combined with the insights from microarray expression profiles and model-guided experiments, predicted that synergistic activation of RD29A originates from enhancement of DREB2 activity by ABA. Our analysis of RD29A expression profiles demonstrates that a simple mathematical model can be used to extract information from temporal dynamics induced by combinatorial stimuli and produce experimentally testable hypotheses.