Epigenetic regulation of anthocyanin biosynthesis by an antagonistic interaction between H2A.Z and H3K4me3

Abstract

The accumulation of anthocyanins in response to specific developmental cues or environmental conditions plays a vital role in plant development and protection against stresses. Extensive research has examined the regulation of anthocyanin biosynthetic genes at the transcriptional and post-transcriptional levels, but the role of chromatin in this regulation remains unknown. Chromatin immunoprecipitation and quantitative reverse transcription-polymerase chain reaction (qRT-PCR) analyses were performed. Genetic interactions between trimethylation of lysine 4 on histone H3 (H3K4me3) and the chromatin remodeling complex SWR1 in the control of anthocyanin biosynthesis were further studied. In this study, we provide evidence that a conserved histone H2 variant, H2A.Z, negatively regulates anthocyanin accumulation through deposition at a set of anthocyanin biosynthetic genes and consequently represses their expression in Arabidopsis thaliana. Our data indicate that the accumulation of anthocyanin in H2A.Z deposition-deficient mutants is associated with increased H3K4me3, which is required for promotion of the expression of anthocyanin biosynthetic genes. We further provide evidence that H3K4me3 in anthocyanin biosynthetic genes is negatively associated with the presence of H2A.Z. Our results reveal an antagonistic relationship between H2A.Z and H3K4me3 in the regulation of the expression of anthocyanin biosynthesis genes, adding another layer of regulation to anthocyanin biosynthesis genes and highlighting the role of chromatin in gene regulation.

Genome-wide investigation of calcium-dependent protein kinase gene family in pineapple: evolution and expression profiles during development and stress

“…Real-time PCR was performed to analysis the relative transcript levels of selected genes according to the Bio-Rad Real-time PCR system (Foster City, CA, USA) and the SYBR Premix Ex Taq II system (TaKaRa Perfect Real Time), and the primers used has been listed in Additional file 15: Table S12. The qRT-PCR program was: 95°C for 30 s; 40 cycles of 95°C for 5 s and 60°C for 34 s; 95°C for 15 s [61,62]. The relative transcript levels of the analyzed pineapple genes were normalized to the transcript levels of AcoActin.…”

Arabidopsis YAF9 histone readers modulate flowering time through NuA4‐complex‐dependent H4 and H2A.Z histone acetylation at FLC chromatin

“…However, mutations affecting the same SWR1-C subunits result in the activation of a number of abiotic/biotic plant response genes involved in drought, heat, phosphate starvation and disease resistance responses, as well as in the floral integrator gene FT, indicating a repressive role for H2A.Z in these loci (March-Diaz et al, 2008;Kumar & Wigge, 2010;Smith et al, 2010;Berriri et al, 2016;Cortijo et al, 2017;Sura et al, 2017;G omez-Zambrano et al, 2018;Zahraeifard et al, 2018). This dual transcriptional regulatory role of H2A.Z may be enlightened by the interplay of the SWR1-C with other chromatin modifiers that affect DNA methylation or posttranslational modifications of histones and histone variants, and end up in different degrees of nucleosome stability (Deal & Henikoff, 2011;Billon & Cote, 2012;Coleman-Derr & Zilberman, 2012b;Gerhold & Gasser, 2014;Subramanian et al, 2015;Dai et al, 2017;Cai et al, 2018;Carter et al, 2018;Xu et al, 2018). For example, differential stability of H2A.Z-containing nucleosomes by the acetylation of H2A.Z variant has been reported in yeast, vertebrates and humans (Millar et al, 2006;Ishibashi et al, 2009;Valdes-Mora et al, 2017) but, in plants, the consequences of H2A.Z acetylation on transcription remain to be explored.…”

SWR1 Chromatin Remodeling Complex: A Key Transcriptional Regulator in Plants

“…Additionally, a recent report in rice also supported preferential deposition of H2A.Z at the gene locus to negatively regulate nutrient-responsive genes, whereas the positive regulation was found for the expression of housekeeping genes during nutrient starvation [25]. In a different study, SWR1-C negatively regulated the expression of anthocyanin biosynthetic genes through enrichment of H2A.Z, which ultimately reduced the anthocyanin accumulation in Arabidopsis [34]. Moreover, another study suggests that the dual role of H2A.Z in gene expression depends on the post-translational modification of H2A.Z, whereas the H2A.Z level within the gene depends on the transcriptional activity [87].…”