The BZR1-BLH1-PIF4 feedback module acts as a molecular amplifier for precise thermomorphogenesis in Arabidopsis

Abstract

Global increases in the intensity and frequency of elevated temperatures is threatening ecosystem stability and crop yield. Understanding plant thermomorphogenesis is critical for developing climate-resilient crops, yet the underlying mechanisms remain to be clarified. Here, we identify the BEL1-LIKE HOMEODOMAIN transcription factor BLH1 as a critical negative regulator of thermomorphogenesis that modulates the key BRASSINAZOLE-RESISTANT 1 (BZR1)-PHYTOCHROME INTERACTING FACTOR 4 (PIF4) thermomorphogenic regulatory module. Overexpression of BLH1 or its homologs confers high-temperature (HT) insensitivity, whereas blh higher-order mutants exhibit HT hypersensitivity. BLH1 expression is directly repressed by BZR1 and is down-regulated by HT. We further demonstrate that BLH1 directly binds to the PIF4 promoter to repress its transcription and concurrently interacts with the PIF4 protein to inhibit its activity. Overexpression of BLH1 rescues the elongated hypocotyl phenotype in bzr1-1D or PIF4 overexpression plants. Our findings define a BZR1-BLH1-PIF4 regulatory axis that modulates the BZR1-PIF4-auxin-BR-BZR1 positive feedback loop, ensuring a balanced thermomorphogenic response to HT. High temperatures trigger plant growth responses that can compromise crop yield. Here the authors report that the BLH1 protein acts as a brake to fine-tune the heat response, offering a target for breeding climate-resilient crops.