A domesticated Harbinger transposase forms a complex with HDA6 and promotes histone H3 deacetylation at genes but not TEs in Arabidopsis

• Published in: Journal of integrative plant biology 2021-08, Vol.63 (8), p.1462-1474
• Main Authors: Zhou, Xishi, He, Junna, Velanis, Christos N., Zhu, Yiwang, He, Yuhan, Tang, Kai, Zhu, Mingku, Graser, Lisa, Leau, Erica, Wang, Xingang, Zhang, Lingrui, Andy Tao, W., Goodrich, Justin, Zhu, Jian‐Kang, Zhang, Cui‐Jun
• Format: Article
• Language: English
• Subjects: Acetylation; Arabidopsis - genetics; Arabidopsis Proteins - metabolism; Deacetylation; DNA Transposable Elements - genetics; Domestication; Eukaryotes; Flowering; Flowers - physiology; Gene expression; Gene Expression Regulation, Plant; Gene regulation; Gene silencing; Genes; Genes, Plant; Harbinger; HDA6; histone acetylation; Histone deacetylase; Histone Deacetylases - metabolism; Histone H3; Histones; Histones - metabolism; Models, Biological; Mutants; Mutation; Phenotype; Phenotypes; Plants (botany); protein complex; Protein Interaction Maps; Proteins; Repressor Proteins - metabolism; Repressors; SANT; Transcription activation; Transcriptomes; Transposase; Transposases - metabolism; Transposons
• ISSN: 1672-9072; 1744-7909
• DOI: 10.1111/jipb.13108

ABSTRACT In eukaryotes, histone acetylation is a major modification on histone N‐terminal tails that is tightly connected to transcriptional activation. HDA6 is a histone deacetylase involved in the transcriptional regulation of genes and transposable elements (TEs) in Arabidopsis thaliana. HDA6 has been shown to participate in several complexes in plants, including a conserved SIN3 complex. Here, we uncover a novel protein complex containing HDA6, several Harbinger transposon‐derived proteins (HHP1, SANT1, SANT2, SANT3, and SANT4), and MBD domain‐containing proteins (MBD1, MBD2, and MBD4). We show that mutations of all four SANT genes in the sant‐null mutant cause increased expression of the flowering repressors FLC, MAF4, and MAF5, resulting in a late flowering phenotype. Transcriptome deep sequencing reveals that while the SANT proteins and HDA6 regulate the expression of largely overlapping sets of genes, TE silencing is unaffected in sant‐null mutants. Our global histone H3 acetylation profiling shows that SANT proteins and HDA6 modulate gene expression through deacetylation. Collectively, our findings suggest that Harbinger transposon‐derived SANT domain‐containing proteins are required for histone deacetylation and flowering time control in plants. Although usually considered as selfish or parasitic, transposable elements are important sources of emerging new genes. Harbinger transposon‐derived proteins form a complex with the histone deacetylase HDA6 and promote histone H3 deacetylation and flowering.