Arabidopsis DET1 degrades HFR1 but stabilizes PIF1 to precisely regulate seed germination

Abstract

Seed is an essential propagation organ and a critical strategy adopted by terrestrial flowering plants to colonize the land. The ability of seeds to accurately respond to light is vital for plant survival. However, the underlying mechanism is largely unknown. In this study, we reveal a circuit of triple feed-forward loops adopted by Arabidopsis seeds to exclusively repress germination in dark conditions and precisely initiate germination under diverse light conditions. We identify that de-etiolated 1 (DET1), an evolutionarily conserved protein, is a central repressor of light-induced seed germination. Genetic analysis demonstrates that DET1 functions upstream of long hypocotyl in far-red 1 (HFR1) and phytochrome interacting factor 1 (PIF1), the key positive and negative transcription regulators in seed germination. We further find that DET1 and constitutive photomorphogenic 10 (COP10) target HFR1 for protein degradation by assembling a COP10-DET1-damaged DNA binding protein 1-cullin4 E3 ligase complex. Moreover, DET1 and COP10 directly interact with and promote the protein stability of PIF1. Computational modeling reveals that phytochrome B (phyB)-DET1-HFR1-PIF1 and phyB-DET1-Protease-PIF1 are new signaling pathways, independent of the previously identified phyB-PIF1 pathway, respectively 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, this study provides a comprehensive molecular framework for light-regulated seed germination, improving our understanding of how plants respond to changeable environments.S eed germination is controlled by a wide range of environmental factors to ensure that plants start a new lifecycle in favorable conditions. Among them, light plays a major role in initiating seed germination (1-4). Plants perceive light signals through distinct families of photoreceptors, in which the red light photoreceptor phytochrome B (phyB) mediates the initial phase of light-induced seed germination (3,(5)(6)(7)(8). Previous studies showed that in seeds, phyB modulates downstream regulatory networks through one of its interacting factors, phytochrome interacting factor 1 (PIF1) (9-11). PIF1 is a basic helix-loop-helix (bHLH) transcription factor that plays a primary role in repressing seed germination, and PIF1 proteins are highly accumulated in dark-incubated seeds (9, 10, 12). Under light irradiation, the light-activated phyB interacts with PIF1 to induce PIF1 phosphorylation and degradation via the 26S proteasome (12-16). Our recent study identified long hypocotyl in far-red 1 (HFR1) as a core transcription regulator in seed germination (17). HFR1 positively regulates seed germination by forming heterodimers with PIF1 to sequester PIF1 from binding to its target genes (17). The HFR1-PIF1 pair governs the transcriptional networks of light-initiated seed germination (17). However, how...

Salt Stress and Ethylene Antagonistically Regulate Nucleocytoplasmic Partitioning of COP1 to Control Seed Germination

“…It is important to improve seed germination to maintain the sustainable development of agriculture (Bewley, 1997;FinchSavage and Leubner-Metzger, 2006;Holdsworth et al, 2008;Weitbrecht et al, 2011). Moreover, photomorphogenic regulators are involved in light-initiated seed germination in Arabidopsis (Shi et al, 2013(Shi et al, , 2015 and participate in phytohormone-controlled seedling growth Seo et al, 2009;Yu et al, 2013). In addition, increasing numbers of studies have revealed that ethylene suppresses SSG (Negm and Smith, 1978;Chang et al, 2010;Lin et al, 2012); however, it remains unclear whether the light signaling factor COP1 participates in SSG.…”

“…For instance, light is a major environmental factor that affects seed germination (Borthwick et al, 1952;Seo et al, 2009). DE-ETIOLATED1 regulates the stabilization of LONG HYPOCOTYL IN FAR-RED1 (HFR1) and PHYTOCHROME INTERACTING FACTOR1 (PIF1), and the HFR1-PIF1 complex inversely modulates the entire genomic transcriptional network in phytochrome B-dependent seed germination (Shi et al, 2013(Shi et al, , 2015. CONSTITUTIVE PHOTOMOR-PHOGENESIS1 (COP1), a central repressor of light signaling, is a ring finger E3 ligase Torii et al, 1998;Jang et al, 2010;Osterlund et al, 2000;Yi and Deng, 2005), which itself is regulated by multiple factors (Zhong et al, 2009;Yu et al, 2013).…”

A Negative Feedback Loop between PHYTOCHROME INTERACTING FACTORs and HECATE Proteins Fine-Tunes Photomorphogenesis in Arabidopsis

“…Strikingly, PIF1 functions as a cofactor of the COP1 E3 Ubiquitin ligase and promotes substrate recruitment and auto-and transubiquitylation of HY5, thereby synergistically represses photomorphogenesis in the dark . In contrast, DET1 interacts with PIFs and stabilize them in the dark (Dong et al, 2014;Shi et al, 2015). Overall, PIFs interact with multiple unrelated proteins to modulate various signaling pathways.…”

Two B-Box Proteins Regulate Photomorphogenesis by Oppositely Modulating HY5 through their Diverse C-Terminal Domains

“…In Arabidopsis, of HFR1-PIF heterodimers that inhibit the promoter binding of the PIFs to their target genes (Hornitschek 427 et al, 2009;Lorrain et al, 2009;Shi et al, 2013;Shi et al, 2015). In addition, PIF4 and PIF5 directly 428 promote the expression of HFR1, thus forming a negative feedback loop ).…”