NuA4 and H2A.Z control environmental responses and autotrophic growth in Arabidopsis

Tomasz Bieluszewski,Anna Bieluszewska,Nancy De Winne,Piotr A Ziolkowski,Michał Kabza,Wojciech Dziegielewski,Geert De Jaeger,Weronika Sura,Jacques Côté,Mateusz Abram,Jan Sadowski,Piotr Wlodzimierz,Catherine Lachance,Maja Szymanska-Lejman

doi:10.1038/s41467-021-27882-5

Abstract

Nucleosomal acetyltransferase of H4 (NuA4) is an essential transcriptional coactivator in eukaryotes, but remains poorly characterized in plants. Here, we describe Arabidopsis homologs of the NuA4 scaffold proteins Enhancer of Polycomb-Like 1 (AtEPL1) and Esa1-Associated Factor 1 (AtEAF1). Loss of AtEAF1 results in inhibition of growth and chloroplast development. These effects are stronger in the Atepl1 mutant and are further enhanced by loss of Golden2-Like (GLK) transcription factors, suggesting that NuA4 activates nuclear plastid genes alongside GLK. We demonstrate that AtEPL1 is necessary for nucleosomal acetylation of histones H4 and H2A.Z by NuA4 in vitro. These chromatin marks are diminished genome-wide in Atepl1, while another active chromatin mark, H3K9 acetylation (H3K9ac), is locally enhanced. Expression of many chloroplast-related genes depends on NuA4, as they are downregulated with loss of H4ac and H2A.Zac. Finally, we demonstrate that NuA4 promotes H2A.Z deposition and by doing so prevents spurious activation of stress response genes.

Highlights

Nucleosomal acetyltransferase of H4 (NuA4) is an essential transcriptional coactivator in eukaryotes, but remains poorly characterized in plants
We show that the expression of the photosynthetic apparatus of the model plant A. thaliana depends on histone acetylation by a highly conserved transcriptional coactivator, the nucleosomal acetyltransferase of H4 (NuA4) complex
The yeast NuA4 complex consists of the catalytic module piccolo NuA4 and a regulatory module attached to picNuA4 through the platform subunit EAF131 (Fig. 1a)

Summary

Introduction

Nucleosomal acetyltransferase of H4 (NuA4) is an essential transcriptional coactivator in eukaryotes, but remains poorly characterized in plants. Loss of AtEAF1 results in inhibition of growth and chloroplast development These effects are stronger in the Atepl[1] mutant and are further enhanced by loss of Golden2-Like (GLK) transcription factors, suggesting that NuA4 activates nuclear plastid genes alongside GLK. Our results suggest a direct link between NuA4 activity and the expression of nuclear-encoded plastid genes, which depends on high levels of H2A.Z in the +1 nucleosome. Based on these findings, we propose that NuA4, by controlling both the acetylation and deposition of H2A.Z, contributes to the switch between the stress response and autotrophic growth

Methods

Results

Conclusion