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 A light-induced switch of plant development, called photomorphogenesis, involves huge transcriptional reprogramming. It requires fine control of specific transcription activators and chromatin marks that facilitate Polymerase II (Pol II) progression, as well as intense protein turnover via the ubiquitin-proteasome system. DE-ETIOLATED1 (DET1) is an atypical DDB1-CULLIN4 Associated Factor (DCAF) that, together with DDB1, COP10 and DDA1, constitutes a substrate adaptor module of CUL4 E3 ubiquitin ligases. The evolutionarily conserved complexes control the stability of cell proliferation factors in animals or circadian and photomorphogenesis regulators in plants. However, the exact mechanism by which DET1 affects the stability of these regulators and controls transcription remains largely unknown. Previous work showed that Arabidopsis DET1 displays high binding affinity for histone H2B, but the molecular and physiological consequences of that binding remained elusive. We found that det1-1 plants display defects in H2B monoubiquitination (H2Bub) and dramatic alterations in gene expression. The DET1-associated protein DDA1 directly interacts with SGF11, a member of an H2Bub deubiquitination module (DUBm). Besides SGF11, this atypical DUBm comprises UBP22 and ENY2 proteins, putative orthologues of yeast Sgf11, Ubp8 and Sus1, respectively, and appears to act independently from SAGA in the absence of a plant Sgf73-like subunit. In part through light-dependent degradation of a H2Bub deubiquitination module, DET1 controls H2Bub homeostasis and transcriptional outputs. Consistent with this, sgf11 and ubp22 mutations ameliorate the det1-1 defects in H2Bub, gene expression and photomorphogenesis. Our findings support a model in which H2B ubiquitination and deubiquitination dynamics impact photomorphogenesis by regulating transcription through progression of Pol II. Collectively, our studies gain insight into the mechanisms by which the evolutionarily conserved protein complexes controlling global H2Bub levels mediate developmental responses to external cues in plants. Park J et al, (2018) Proc Natl Acad Sci USA 115: E5400-E5409. doi: 10.1073/pnas.1721241115. Cardona-Lopez et al, (2015) Plant Cell 27: 2560-2581. doi: 10.1105/tpc.15.00393. Irigoyen et al, (2014) Plant Cell 26: 712-728. doi: 10.1105/tpc.113.122234.