Unravelled new mechanistic insights into the role of histone acetylation in controlling the expression of floral repressor FLC in Arabidopsis

We have demonstrated the role of the Arabidopsis YAF9 proteins in the control of different developmental processes. Our data support that YAF9A and YAF9B are histone H3 readers with unequally redundant functions that control flowering by regulating FLC expression through the modulation of the acetylation levels of histone H4 and H2A.Z at this locus.


To optimize their reproductive success, plants have evolved a number of mechanisms to modulate flowering time in response to both environmental cues (daylength, temperature) and internal signals (nutrients, hormones) that reflect the developmental state.

Chromatin remodelling plays a crucial role in both the establishment and maintenance of specific gene expression patterns that are closely associated with plant developmental transitions. Post-translational histone modifications and the dynamics of histone variant H2A.Z are key mechanisms underlying the floral transition. In yeast, SWR1-C and NuA4-C chromatin remodelling complexes mediate the deposition of H2A.Z and the acetylation of histone H4, H2A and H2A.Z respectively. YAF9 homologues are widely conserved from yeast to human and are integral components of SWR1-C and NuA4-C. The Arabidopsis genome contains two YAF9 homologs, YAF9A and YAF9B, but their functional significance has remained largely unknown.

Researchers from the MOLECULAR BASIS OF PLANT DEVELOPMENTAL PHASE TRANSITIONS at CBGP have pursued physiological, genetic, genomic, epigenetic, proteomics and cell biology approaches to get an insight into the role of Arabidopsis YAF9 proteins in plant developmental responses. Their data reveal that YAF9A and YAF9B are histone H3 readers with unequally redundant functions. They show that double mutant yaf9a yaf9b plants display pleiotropic developmental phenotypic alterations, including an acceleration of flowering time, as well as the misregulation of a wide variety of genes. They also demonstrate that YAF9 proteins regulate flowering time by both FLC-dependent and independent mechanisms that work in parallel to SWR1-C. Interestingly, they show that YAF9A binds the chromatin of the floral repressor FLC, and that YAF9 proteins regulate FLC expression by modulating the acetylation levels of H2A.Z and H4, but do not affect the deposition of H2A.Z at FLC locus. In agreement with that, they found that YAF9A interacts with HAM1, a putative catalytic subunit of NuA4-C. Altogether, these data unveil an additional layer of complexity in the regulation of FLC expression and show a novel regulatory mechanism of gene expression exerted by the YAF9 proteins through Nu4A-C-dependent H4 and H2A.Z histone acetylation in Arabidopsis. Remarkably they reveal for the first time the occurrence of H2A.Z acetylation in plants, a hitherto unknown modification, demonstrating that its presence at FLC chromatin is required for the proper modulation of flowering time. In several eukaryotes, the hyperacetylated form of H2A.Z is augmented at active genes. Future studies will be necessary to conclude if the occurrence of H2A.Zac in plants also correlates widely with gene activation.

This work represents an important step forward in understanding the molecular function of plant YAF9 histone readers, contributing to unravel new mechanistic insights into the role of eukaryotic histone acetylation in controlling gene expression, and opening new venues for the study of posttranslational histone modifications in plants.


Original Paper:

Crevillén, P., Gómez‐Zambrano, Á., López, J.A., Vázquez, J., Piñeiro, M., Jarillo, J.A. 2019. Arabidopsis YAF9 histone readers modulate flowering time through NuA4-complex-dependent H4 and H2A.Z histone acetylation at FLC chromatin. New Phytologist. DOI: 10.1111/nph.15737