A PIF4-PUB9-DSK2A signaling loop integrates skotomorphogenesis and carbon starvation response in Arabidopsis

When seeds germinate under soil, the emerging seedlings undergo a period of darkness. Short-term darkness promotes skotomorphogenesis, whereas prolonged darkness leads to carbon starvation, triggering a transition from growth to autophagy-mediated survival. The molecular mechanism by which plants coordinate skotomorphogenesis and carbon starvation response remains unclear. Here, we show that the ubiquitin receptor protein DOMINANT SUPPRESSOR OF KAR2 (DSK2) negatively regulates skotomorphogenesis, and the E3 ubiquitin ligase PLANT U-BOX 9 (PUB9) interacts with and ubiquitinates DSK2 for proteasomal degradation during skotomorphogenesis, thereby inhibiting the carbon starvation response. Moreover, PUB9 is a direct target of PHYTOCHROME-INTERACTING FACTOR 4 (PIF4), which promotes PUB9 expression during skotomorphogenesis. Upon carbon starvation, PIF4 is primarily degraded via DSK2A-dependent autophagy, leading to reduced PUB9 expression and consequently weakened DSK2A degradation. This feedback loop enables plants to shift from skotomorphogenesis toward carbon starvation response. Collectively, our work reveals that plants coordinate skotomorphogenesis and carbon starvation through the PIF4-PUB9-DSK2A signaling loop, providing a molecular link between growth and survival under dark and carbon-limited conditions.