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In higher plants, S₁-basic region-leucine zipper (S₁-bZIP) transcription factors fulfill crucial roles in the physiological homeostasis of carbon and amino acid metabolisms and stress responses. However, very little is known about the physiological role of S₁-bZIP in cruciferous vegetables. Here, we analyzed the physiological function of S₁-bZIP from <i>Brassica rapa</i> (BrbZIP-S) in modulating proline and sugar metabolism. Overexpression of <i>BrbZIP-S</i> in <i>Nicotiana benthamiana</i> resulted in delayed chlorophyll degradation during the response to dark conditions. Under heat stress or recovery conditions, the transgenic lines exhibited a lower accumulation of H₂O₂, malondialdehyde, and protein carbonyls compared to the levels in transgenic control plants. These results strongly indicate that BrbZIP-S regulates plant tolerance against dark and heat stress. We propose that BrbZIP-S is a modulator of proline and sugar metabolism, which are required for energy homeostasis in response to environmental stress conditions.