Inhibition of SIZ1-mediated SUMOylation of HOOKLESS1 promotes light-induced apical hook opening in Arabidopsis

The apical hook protects cotyledons and the shoot apical meristem from mechanical injuries during seedling emergence from the soil. HOOKLESS1 (HLS1) is a central regulator of apical hook development, as a terminal signal onto which several pathways converge. However, how plants regulate the rapid opening of the apical hook in response to light by modulating HLS1 function remains unclear. In this study, we demonstrate that the small ubiquitin-like modifier (SUMO) E3 ligase SAP AND MIZ1 DOMAIN-CONTAINING LIGASE1 (SIZ1) interacts with HLS1 and mediates its SUMOylation in Arabidopsis thaliana. Mutating SUMO attachment sites of HLS1 results in impaired function of HLS1, indicating that HLS1 SUMOylation is essential for its function. SUMOylated HLS1 was more likely to assemble into oligomers, which are the active form of HLS1. During the dark-to-light transition, light induces rapid apical hook opening, concomitantly with a drop in SIZ1 transcript levels, resulting in lower HLS1 SUMOylation. Furthermore, ELONGATED HYPOCOTYL5 (HY5) directly binds to the SIZ1 promoter and suppresses its transcription. HY5-initiated rapid apical hook opening partially depended on HY5 inhibition of SIZ1 expression. Taken together, our study identifies a function for SIZ1 in apical hook development, providing a dynamic regulatory mechanism linking the post-translational modification of HLS1 during apical hook formation and light-induced apical hook opening. The E3 ligase SIZ1 regulates apical hook development by SUMOylating HOOKLESS1 in the dark, with light-induced ELONGATED HYPOCOTYL5 suppressing SIZ1 transcription to initiate apical hook unfolding.

Automated summary

HLS1 plays a key role in the development of the apical hook in plants, and SIZ1 regulates the rapid opening of the apical hook by mediating HLS1 SUMOylation. The opening of the apical hook is associated with a decrease in SIZ1 transcript levels, leading to reduced HLS1 SUMOylation. In addition, HY5 promotes the rapid opening of the apical hook by inhibiting SIZ1 transcription.