Transcription factor interaction with COMPASS-like complex regulates histone H3K4 trimethylation for specific gene expression in plants

Abstract

Accumulation of unfolded or misfolded proteins causes endoplasmic reticulum (ER) stress, which activates a set of ER membraneassociated transcription factors for protein homeostasis regulation. Previous genome-wide chromatin immunoprecipitation analysis shows a strong correlation between histone H3K4 trimethylation (H3K4me3) and active gene expression. However, how the histone modification complex is specifically and timely recruited to the active promoters remains unknown. Using ER stress responsive gene expression as a model system, we demonstrate that sequencespecific transcription factors interact with COMPASS-like components and affect H3K4me3 formation at specific target sites in Arabidopsis. Gene profiling analysis reveals that membrane-associated basic leucine zipper (bZIP) transcription factors bZIP28 and bZIP60 regulate most of the ER stress responsive genes. Loss-offunctions of bZIP28 and bZIP60 impair the occupancy of H3K4me3 on promoter regions of ER stress responsive genes. Further, in vitro pull-down assays and in vivo bimolecular fluorescence complementation (BiFC) experiments show that bZIP28 and bZIP60 interact with Ash2 and WDR5a, both of which are core COMPASS-like components. Knockdown expression of either Ash2 or WDR5a decreased the expression of several ER stress responsive genes. The COMPASSlike complex is known to interact with histone methyltransferase to facilitate preinitiation complex (PIC) assembly and generate H3K4me3 during transcription elongation. Thus, our data shows that the ER stress stimulus causes the formation of PIC and deposition of H3K4me3 mark at specific promoters through the interaction between transcription factor and COMPASS-like components.COMPASS-like | ER stress | H3K4 trimethylation | transcription factor | unfolded protein response

HY5, a positive regulator of light signaling, negatively controls the unfolded protein response in Arabidopsis

“…Previously, it has been reported that bZIP28 forms a transcriptional complex with NF-Y TFs, which is important for full induction of the BIP3 gene (18). Recently, bZIP28 has been shown to be involved in formation of a transcriptional complex with COMPASS-like components, which are involved in histone H3K4 trimethylation (H3K4me3), which correlates with active gene expression (33). Moreover, it is also known that histone modification plays an important role in HY5-mediated gene expression (4,34).…”

ATX3, ATX4, and ATX5 Encode Putative H3K4 Methyltransferases and Are Critical for Plant Development

“…Prior to this study, nearly all H3K4 methyl transferases characterized in Arabidopsis were those controlling H3K4me3 (Berr et al, 2015;Song et al, 2015). The only enzyme described to catalyze H3K4me2 was E, Boxplot of ChIP-seq peak height of ATX3/4/5-and SDG2-affected H3K4me3 sites.…”

“…The next intriguing question raised is how such association of is fulfilled. Recently, Song et al (2015) have shown that the H3K4 methyltransferase complex can directly interact with specific transcription factor to regulate gene expression in Arabidopsis. Therefore, we speculate that ATX3/4/5 and SDG2 may interact with different transcription factors to facilitate the gene expression and generate the deposition of H3K4me3 mark at specific loci.…”

Unique COPII component AtSar1a/AtSec23a pair is required for the distinct function of protein ER export in Arabidopsis thaliana

“…Interestingly, the unique AtSar1a/AtSec23a pair, but not the other Sar1 and Sec23 homologs, were recently shown to be bZIP28-dependent ER stress-responsive genes in a microarray analysis (30). bZIP28, an ER resident stress sensor/transducer related to the mammalian ATF6, is exported from the ER to the Fig.…”