DET1-mediated COP1 regulation avoids HY5 activity over second-site gene targets to tune plant photomorphogenesis.

Abstract DE-ETIOLATED1 (DET1) and CONSTITUTIVE PHOTOMORPHOGENESIS 1 (COP1) are two essential repressors of Arabidopsis photomorphogenesis. These proteins were described to associate to CULLIN4 to form independent CRL4-based E3 ubiquitin ligases that mediate the degradation of several photomorphogenic transcription factors, including ELONGATED HYPOCOTYL5 (HY5), thereby controlling multiple gene regulatory networks. Despite extensive biochemical and genetic analyses of their multi-subunit complexes, the functional links between DET1 and COP1 have long remained elusive. Here, we report that DET1 associates with COP1 in vivo, enhances COP1-HY5 interaction, and promotes COP1 destabilization in a process that dampens HY5 protein abundance. By regulating its accumulation, DET1 avoids HY5 association to hundreds of second-site genomic loci, which are also frequently targeted by the skotomorphogenic transcription factor PHYTOCHROME-INTERACTING FACTOR 3 (PIF3). Accordingly, ectopic HY5 chromatin enrichment favours local gene repression and can trigger fusca-like phenotypes. This study therefore shows that DET1 mediated regulation of COP1 stability tunes down the HY5 cistrome, avoiding hyper-photomorphogenic responses that might compromise plant viability.