AtINO80 represses photomorphogenesis by modulating nucleosome density and H2A.Z incorporation in light-related genes

Abstract

Photomorphogenesis is a critical developmental process bridging light-regulated transcriptional reprogramming with morphological changes in organisms. Strikingly, the chromatin-based transcriptional control of photomorphogenesis remains poorly understood. Here, we show that the Arabidopsis (Arabidopsis thaliana) ortholog of ATP-dependent chromatin-remodeling factor AtINO80 represses plant photomorphogenesis. Loss of AtINO80 inhibited hypocotyl cell elongation and caused anthocyanin accumulation. Both light-induced genes and dark-induced genes were affected in the atino80 mutant. Genome-wide occupancy of the H2A.Z histone variant and levels of histone H3 were reduced in atino80. In particular, AtINO80 bound the gene body of ELONGATED HYPOCOTYL 5 (HY5), resulting in lower chromatin incorporations of H2A.Z and H3 at HY5 in atino80. Genetic analysis revealed that AtINO80 acts in a phytochrome B- and HY5-dependent manner in the regulation of photomorphogenesis. Together, our study elucidates a mechanism wherein AtINO80 modulates nucleosome density and H2A.Z incorporation and represses the transcription of light-related genes, such as HY5, to fine tune plant photomorphogenesis.

HY5: A Pivotal Regulator of Light-Dependent Development in Higher Plants

“…TEOSINTE BRANCHED1/CYCLOIDEA/PROLIFERATING CELL FACTOR (TCP2) and SHI-RELATED SEQUENCE 5 (SRS5) positively control the transcription of HY5 to promote photomorphogenesis ( He et al, 2016 ; Yuan et al, 2018 ). INOSITOL REQUIRING 80 (INO80) affects the chromatin modifications of HY5 and represses its transcription to inhibit photomorphogenic development ( Yang C. et al, 2020 ). COLD REGULATED 27 (COR27) and COR28 directly interact with HY5 to enhance its transcriptional activation activity toward downstream target genes, consequently leading to the promotion of photomorphogenic development ( Li X. et al, 2020 ; Zhu et al, 2020 ).…”

Chromatin‐remodeling complexes: Conserved and plant‐specific subunits in Arabidopsis

“…Compared to the function of the SWR1 complex in H2A.Z deposition, the functions of INO80 in H2A.Z‐H2B dimer replacement seem more complex. A global reduction of H2A.Z was detected in ino80‐5 seedlings grown under long‐day (16 h light, 8 h dark) conditions (Yang et al, 2020a), whereas no significant changes in H2A.Z enrichment at the genome‐wide level were found in etiolated ino80‐1 seedlings (Zander et al, 2019) or in ino80‐5 seedlings grown under short‐day (8 h light, 16 h dark) conditions (Xue et al, 2021). INO80 was reported to positively regulate H2A.Z deposition at the flowering repressor genes FLOWERING LOCUS C ( FLC ) and MADS AFFECTING FLOWERING 4/5 ( MAF4/5 ) and at the photomorphogenesis‐related gene HY5 (Zhang et al, 2015; Yang et al, 2020a).…”

“…A global reduction of H2A.Z was detected in ino80‐5 seedlings grown under long‐day (16 h light, 8 h dark) conditions (Yang et al, 2020a), whereas no significant changes in H2A.Z enrichment at the genome‐wide level were found in etiolated ino80‐1 seedlings (Zander et al, 2019) or in ino80‐5 seedlings grown under short‐day (8 h light, 16 h dark) conditions (Xue et al, 2021). INO80 was reported to positively regulate H2A.Z deposition at the flowering repressor genes FLOWERING LOCUS C ( FLC ) and MADS AFFECTING FLOWERING 4/5 ( MAF4/5 ) and at the photomorphogenesis‐related gene HY5 (Zhang et al, 2015; Yang et al, 2020a). In contrast, INO80 has been shown to negatively regulate H2A.Z deposition at ETHYLENE INSENSITIVE 2 ( EIN2 ), which encodes the master regulator of ethylene signaling, and to promote the transcription of EIN2 by coordinating the activation effect of the histone H3K27me3 demethylase REF6 on transcription (Zander et al, 2019).…”

Two bHLH transcription factors, bHLH48 and bHLH60, associate with phytochrome interacting factor 7 to regulate hypocotyl elongation in Arabidopsis

“…Eight-day-old white light grown 35S::PIF7-Flash and 35S::bHLH60-Flag #3 seedlings treated with 1 h shade were quickly plucked from plates to perform chromatin immunoprecipitation (ChIP) assays, as described previously (Yang et al, 2020). Briefly, approximately 4 g fresh seedlings were collected and treated with Fix Buffer [0.4 M sucrose, 10 mM Tris-HCl (pH 8.0), 1 mM EDTA, 1 mM PMSF, 1% formaldehyde, 1 3 protease inhibitor cocktail tablet (Roche)] under vacuum for 15 min.…”