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The contribution of glutathione (GSH) in combating environmental stress in plants has long been known. Previous reports have pointed to the involvement of GSH in inducing various heat shock proteins (HSPs), but the molecular mechanism is yet to be explored. Here, we investigate how GSH induces the expression of important HSP genes in Arabidopsis. Expression of HSP genes BiP3, HSP70B, and HSP90.1 was positively regulated by GSH, and a promoter activation assay suggested a role for GSH in their induction. Lower expression of BiP3 and HSP70B in the GSH-fed Atmyb21 mutant and of HSP90.1 in the GSH-fed Atbzip10 mutant, in comparison with GSH-fed Col-0, revealed a role for GSH in activating their promoters through the transcription factors MYB21 and BZIP10. Co-transfection of transcription factor mutant protoplasts with transcription factor constructs and HSP promoters confirmed the results. Comparative proteomics also revealed proteins whose expression was controlled by MYB21 and BZIP10 in response to GSH feeding. A co-immunoprecipitation assay demonstrated a role for GSH in modulating the level of interaction of glutathione-S-transferase with HSP70. Collectively, our results demonstrate a role for GSH in activating the promoters of BiP3 and HSP70B via MYB21 and of HSP90.1 via BZIP10. [ABSTRACT FROM AUTHOR]