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

Xishi Zhou,Yuhan He,Yiwang Zhu,Kai Tang,Lisa Graser,Mingku Zhu,W Andy Tao,Junna He,Lingrui Zhang,Xingang Wang,Christos N Velanis,Cui‐Jun Zhang,Erica De Leau,Justin Goodrich,Jian‐Kang Zhu

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.

Highlights

In eukaryotic cells, histones and DNA are packed and ordered into highly structured units called nucleosomes
Mutation of alp1 partially suppressed the early flowering and leaf curling phenotypes observed in the Polycomb group (PcG) mutant lhp1, whereas hhp1‐1 lhp1‐3 double mutant plants were phenotypically similar to the lhp1‐3 single mutant (Figure S1B, C)
We show that five co‐ domesticated proteins derived from the Harbinger transposon, HDA6‐associated Harbinger transposon‐derived protein 1 (HHP1) and SANT1–SANT4, form one or more novel histone deacetylase complexes with HDA6

Summary

Introduction

Histones and DNA are packed and ordered into highly structured units called nucleosomes. HDA6 is involved in various biological processes such as transcriptional gene silencing (Probst et al, 2004; Earley et al, 2010; To et al, 2011; Liu et al, 2012; Yu et al, 2017; Yang et al, 2020), responses to drought and salt stress (Chen et al, 2010; Kim et al, 2017), expression of circadian clock genes (Hung et al, 2018), mRNA polyadenylation (Lin et al, 2020), and flowering (Wu et al, 2008; Yu et al, 2011; Ning et al, 2019). Relatively little is known about how HDA6 regulates gene transcription

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Conclusion