The protein homeostasis of SPATULA coordinates seed thermoinhibition response in Arabidopsis thaliana

Supraoptimal temperature (SOT) suppresses the completion of seed germination (termed thermoinhibition) to ensure seedling establishment under favorable environmental conditions. SOMNUS (SOM) plays a crucial role in suppressing seed germination completion under SOT, although the underlying regulatory mechanism governing this process remains elusive. In this study, we identified that a bHLH transcription factor SPATULA (SPT) directly binds to the promoter region of SOM, thereby activating its expression. Notably, knockout mutants of SPT enhanced the completion of seed germination under SOT, characterized by increased GA and decreased ABA biosynthesis. In contrast, SPT overexpression reduced the completion of seed germination, leading to decreased GA and increased ABA biosynthesis. These results suggest that SPT negatively controls the seed thermoinhibition response. Genetic analyses further showed that SOM acts epistatically to SPT in suppressing the completion of seed germination under SOT conditions. Furthermore, our findings suggest that the E3 ligase COP1 possibly mediates the degradation of SPT in the nucleus. Under SOT conditions, COP1 is translocated from the nucleus to the cytoplasm, stabilizing nuclear SPT and activating SOM expression to initiate seed thermoinhibition. In a DEX-inducible system, artificial retention of nuclear COP1 induced the degradation of nuclear SPT, limiting SOM expression and subsequently attenuating the seed thermoinhibition response under SOT conditions. These findings reveal a critical function of SPT in controlling the seed thermoinhibition response via SOM activation.