The survival of seed plants in natural environments requires the successful emergence from the soil. Our study first showed that the ethylene signaling pathway is utilized by plants to sense and respond to the mechanical resistance of the soil. Then, we further found that CONSTITUTIVE PHOTOMORPHOGENESIS 1 (COP1) , a central repressor of light signaling, is a key component required for seedlings to sense the depth of soil overlay. Mutation in COP1 causes severe defects in penetrating soil, due to decreased level of EIN3, a master transcription factor in ethylene pathway that mediates seedling emergence. We show that COP1 directly targets the F-box proteins EBF1 and EBF2 for ubiquitination and degradation, thus stabilizing EIN3. As seedlings grow towards the surface, the depth of soil overlay decreases, resulting in a gradual increase of light fluences. COP1 channels the light signals while ethylene transduces the information on soil mechanical conditions, which cooperatively control EIN3 protein levels to promote seedling emergence from the soil. The COP1-EBF1/2-EIN3 module reveals a mechanism by which plants sense the depth to surface and uncovers a novel regulatory paradigm of an ubiquitin E3 ligase cascade.

Seed is an essential propagation organ and a critical strategy adopted by terrestrial flowering plants to colonize the land. The ability of seeds accurately responding to light is vital for plant survival. However, the underlying mechanism is largely unknown. In this study, we reveal a circuit oftriple feed-forward loops adopted by Arabidopsis seeds to exclusively repress germination in dark and precisely initiate germination upon perse light conditions. We identify that DET1, an evolutionarily conserved protein, is a central repressor of light-induced seed germination. Genetic analysis demonstrates that DET1 functions upstream of HFR1 and PIF1, the key positive and negative transcription regulators in seed germination. We further find that DET1 and COP10 target HFR1 for protein degradation by assembling a COP10-DET1-DDB1-CUL4 E3 ligase complex. Moreover, DET1 and COP10 directly interact with and promote the protein stability of PIF1. Computational modeling reveals that phyB-DET1-HFR1-PIF1 and phyB-DET1-Protease-PIF1 are new signaling pathways, independent of the previously identified phyB-PIF1 pathway, respectively in mediating the rapid and time-lapse responses to light irradiation. The model-simulated results are highly consistent with their experimental validations, suggesting that our mathematical model captures the essence of Arabidopsis seed germination networks. Taken together, our study provides a novel molecular framework for light-regulated seed germination, improving our understanding of how plants respond to the changeable environments.

Xue Liu, Mohan Lyu, Honglei Wang, Jing Li, Yingjun Yu, Yan Zhao, Ningli Xu, Xiaoxia Kou, Huan Li, Sheng Xu, Yiyao Li, Mingming Zhao, Zhicong Feng, Yufeng Wu, Hongling Li, Yixuan Fan