Photomorphogenesis is a critical plant developmental process that involves light-mediated transcriptome and histone modification changes. The transcription factor ELONGATED HYPOCOTYL5 (HY5) acts downstream of multiple families of photoreceptors to promote photomorphogenesis by regulating the expression of light-responsive genes. However, the molecular mechanism for HY5-mediated transcriptional regulation remains largely unclear. Here, we demonstrated that HY5 directly interacts with a Reduced Potassium Dependence3/Histone Deacetylase1 (HDA1)-type histone deacetylase, HDA15, both in vitro and in vivo. Phenotypic analysis revealed that HDA15 is a negative regulator of hypocotyl cell elongation under both red and far-red light conditions in Arabidopsis (Arabidopsis thaliana) seedlings. The enzymatic activity of HDA15 is required for inhibition of hypocotyl elongation. Furthermore, HDA15 and HY5 act interdependently in the repression of hypocotyl cell elongation in photomorphogenesis. Genome-wide transcriptome analysis revealed that HDA15 and HY5 corepress the transcription of a subset of cell wall organization and auxin signaling-related genes. In addition, HDA15 is required for the function of HY5 in the repression of genes related to hypocotyl cell elongation in Arabidopsis seedlings. Moreover, HY5 recruits HDA15 to the promoters of target genes and represses gene expression by decreasing the levels of histone H4 acetylation in a light-dependent manner. Our study revealed a key transcription regulatory node in which HY5 interacts with HDA15 involved in repressing hypocotyl cell elongation to promote photomorphogenesis.
Mammalian histone deacetylases (HDACs) undergo phosphorylation to regulate their localization, activity and function. However, little is known about the regulation of plant HDAC function and activity by phosphorylation. Here, we report the crystal structure of the Reduced Potassium Dependency3/Histone Deacetylase1 (RPD3/HDA1) type class II histone deacetylase HDA15 in Arabidopsis (Arabidopsis thaliana). The histone deacetylase domain of HDA15 (HDA15HD) assembles as tetrameric forms with each monomer composed of 12 α-helices and 9 β-sheets. The L1 loop and β2 sheet of HDA15HD are the essential interfaces for the tetramer formation. The N-terminal zinc finger domain enhances HDA15HD dimerization and increases its enzymatic activity. Furthermore, HDA15 can also be phosphorylated at Ser448 and Ser452 in etiolated seedlings. The HDA15 phosphorylation status determines its sub-nuclear localization and oligomerization. Phosphomimetics of HDA15 partially disrupt its oligomerization and cause loss of enzymatic activity and translocation from the nucleolus into nucleoplasm. Together, these data indicate that phosphorylation plays a critical role in regulating the structure and function of HDA15.
Histone deacetylases (HDAs) play an important role in transcriptional regulation of multiple biological processes. In this study, we investigated the function of HDA15 in abscisic acid (ABA) responses. We used immunopurification coupled with mass spectrometry-based proteomics to identify proteins interacting with HDA15 in Arabidopsis (Arabidopsis thaliana). HDA15 interacted with the core subunits of the MOS4-Associated Complex (MAC), MAC3A and MAC3B, with interaction between HDA15 and MAC3B enhanced by ABA. hda15 and mac3a/mac3b mutants were ABA-insensitive during seed germination and hyposensitive to salinity. RNA sequencing (RNA-seq) analysis demonstrated that HDA15 and MAC3A/MAC3B co-regulate ABA-responsive intron retention (IR). Furthermore, HDA15 reduced the histone acetylation level of genomic regions near ABA-responsive IR sites, and the association of MAC3B with ABA-responsive pre-mRNA was dependent on HDA15. Our results indicate that HDA15 is involved in ABA responses by interacting with MAC3A/MAC3B to mediate splicing of introns.
SUMMARY Histone deacetylases (HDAs) regulate many aspects of plant development and responses to environmental changes. Previous studies have demonstrated that the Arabidopsis histone deacetylase HDA15 is a positive regulator in far‐red (FR) light‐mediated inhibition of hypocotyl elongation. Furthermore, HDA15 can be phosphorylated and its enzymatic activity is negatively regulated by phosphorylation. However, the kinases that can phosphorylate HDA15 are still unknown. Cyclin‐dependent kinases (CDKs) are a large family of serine/threonine protein kinases and have been identified as major regulators of the cell cycle and transcription. In this study, we show that the cyclin‐dependent kinase CDKC2 interacts with HDA15 both in vitro and in vivo. In vitro kinase assays show that CDKC2 phosphorylates HDA15. Genetic evidence suggests that HDA15 acts downstream of CDKC2 in hypocotyl elongation under FR light. Furthermore, HDA15 and CDKC2 function synergistically in the regulation of FR‐mediated cell elongation. The expression of cell wall organization‐ and auxin signaling‐related genes under FR light is increased in hda15 and cdkc2/hda15 mutants. Taken together, our study indicates that CDKC2 can phosphorylate HDA15 and plays an important role in FR light‐regulated hypocotyl elongation.
Histone deacetylases (HDAs) play an important role in transcriptional regulation involved in multiple biological processes. In this study, we investigate the function of HDA15 in abscisic acid (ABA) responses. Immunopurification coupled with mass spectrometry-based proteomics was used to identify the HDA15 interacting proteins. We found that HDA15 can interact with the core subunits of MOS4-Associated Complex (MAC), MAC3A and MAC3B. In addition, ABA enhances the interaction of HDA15 with MAC3B. hda15 and mac3a/mac3b mutants are ABA-insensitive in seed germination and hyposensitive to salinity. RNA sequencing (RNA-seq) analysis demonstrate that HDA15 and MAC3A/MAC3B not only affect the expression of ABA-related genes, but also regulate ABA-responsive intron retention (IR). Furthermore, HDA15 and MAC3A/MAC3B reduce the histone acetylation level of the genomic regions near ABA-responsive IRs. Our studies uncovered the role of histone deacetylation in ABA-mediated splicing regulation and identified that HDA15-MAC3A/MAC3B acts as an important regulation module to mediate splicing of introns in ABA responses.One Sentence SummaryHDA15 and MAC3A/MAC3B coregulate intron retention and reduce the histone acetylation level of the genomic regions near ABA-responsive retained introns.
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