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The BRASSINAZOLE‐RESISTANT 1 (BZR1) transcription factor family plays an essential role in plant brassinosteroid (BR) signaling, but the signaling mechanism through which BZR1 and its homologs cooperate with certain coactivators to facilitate transcription of target genes remains incompletely understood. In this study, we used an efficient protein interaction screening system to identify blue‐light inhibitor of cryptochromes 1 (BIC1) as a new BZR1‐interacting protein in Arabidopsis thaliana. We show that BIC1 positively regulates BR signaling and acts as a transcriptional coactivator for BZR1‐dependent activation of BR‐responsive genes. Simultaneously, BIC1 interacts with the transcription factor PIF4 to synergistically and interdependently activate expression of downstream genes including PIF4 itself, and to promote plant growth. Chromatin immunoprecipitation assays demonstrate that BIC1 and BZR1/PIF4 interdependently associate with the promoters of common target genes. In addition, we show that the interaction between BIC1 and BZR1 is evolutionally conserved in the model monocot plant Triticum aestivum (bread wheat). Together, our results reveal mechanistic details of BR signaling mediated by a transcriptional activation module BIC1/BZR1/PIF4 and thus provide new insights into the molecular mechanisms underlying the integration of BR and light signaling in plants. Synopsis: BZR1 and PIF4 are core transcription factors in brassinosteroid (BR) and light signaling, respectively. Here, Blue‐light Inhibitor of Cryptochromes 1 (BIC1) is found as a common coactivator linking BZR1 and PIF4 to synergistically and interdependently activate transcription of common target genes and promote cell elongation. BIC1 positively regulates BR responses.BIC1 interacts with BZR1 and PIF4 to synergistically co‐activate transcription of target genes, including PIF4 itself.BIC1 and BZR1/PIF4 interdependently associate with the promoters of common target genes.The interaction between BIC1 and BZR1 is evolutionally conserved in monocot and dicot plants. [ABSTRACT FROM AUTHOR]