GIGANTEA shapes diurnal seedling growth by sequestering SMAX1 and SMXL2

Abstract

The circadian clock regulates diurnal growth by integrating external signals and phytohormonal pathways in a time-specific manner. Our previous work demonstrated that the karrikin signaling components, SUPPRESSOR OF MAX2 1 (SMAX1) and SMAX1-LIKE2 (SMXL2), promote seedling growth by modulating the growth-promoting transcription factor PHYTOCHROME INTERACTING FACTOR 4 (PIF4)-mediated auxin signaling in Arabidopsis (Arabidopsis thaliana). However, the genetic and molecular links between the circadian clock and SMAX1/SMXL2 remain poorly understood. In this study, we show that the core clock protein GIGANTEA (GI) influences rhythmic growth by inhibiting the functions of SMAX1 and SMXL2. Our findings reveal that GI directly interacts with SMAX1 and SMXL2, thereby preventing their association with PIF4. This interaction leads to the destabilization of PIF4 protein and alters transcriptomic patterns, including those related to auxin signaling, ultimately suppressing hypocotyl elongation. Furthermore, under warm long-day conditions, elevated GI abundance enhances its interaction with SMAX1/SMXL2 during the night, thereby attenuating nighttime thermomorphogenic growth rhythms. We propose that the regulation of SMAX1 and SMXL2 by GI is essential for the precise modulation of growth rhythms in response to environmental changes.