Histone chaperone ASF1 mediates H3.3-H4 deposition in Arabidopsis
Zhenhui Zhong, Yafei Wang, Ming Wang, Fan Yang, Quentin Angelo Thomas, Yan Xue, Yaxin Zhang, Wanlu Liu, Yasaman Jami-Alahmadi, Linhao Xu, Suhua Feng, Sebastian Marquardt, James A. Wohlschlegel, Israel Ausin and Steven E. Jacobsen
Nature Communications
DOI: 10.1038/s41467-022-34648-0
Abstract
Histone chaperones and chromatin remodelers control nucleosome dynamics, which are essential for transcription, replication, and DNA repair. The histone chaperone Anti-Silencing Factor 1 (ASF1) plays a central role in facilitating CAF-1-mediated replication-dependent H3.1 deposition and HIRA-mediated replication-independent H3.3 deposition in yeast and metazoans. Whether ASF1 function is evolutionarily conserved in plants is unknown. Here, we show that Arabidopsis ASF1 proteins display a preference for the HIRA complex. Simultaneous mutation of both Arabidopsis ASF1 genes caused a decrease in chromatin density and ectopic H3.1 occupancy at loci typically enriched with H3.3. Genetic, transcriptomic, and proteomic data indicate that ASF1 proteins strongly prefers the HIRA complex over CAF-1. asf1 mutants also displayed an increase in spurious Pol II transcriptional initiation and showed defects in the maintenance of gene body CG DNA methylation and in the distribution of histone modifications. Furthermore, ectopic targeting of ASF1 caused excessive histone deposition, less accessible chromatin, and gene silencing. These findings reveal the importance of ASF1-mediated histone deposition for proper epigenetic regulation of the genome. Histone chaperones and chromatin remodelers control nucleosome dynamics. Here the authors show that the Arabidopsis ASF1 chaperone primarily supplies histone variants to the HIRA complex to ensure proper epigenetic gene regulation.