Arabidopsis ORC1 is a PHD-containing H3K4me3 effector that regulates transcription

Abstract

Control of gene expression depends on a complex and delicate balance of various posttranslational modifications of histones. However, the relevance of specific combinations of histone modifications is not fully defined. Downstream effector proteins recognize particular histone modifications and transduce this information into gene expression patterns. Methylation of histone H3 at lysine 4 (H3K4me) is a landmark of gene expression control in eukaryotes. Its recognition depends on the presence in the effector protein of a motif termed plant homeodomain (PHD) that specifically binds to H3K4me3. Here, we establish that Arabidopsis ORC1, the large subunit of the origin recognition complex involved in defining origins of DNA replication, functions as a transcriptional activator of a subset of genes, the promoters of which are preferentially bound by ORC1. Arabidopsis ORC1 contains a PHD and binds to H3K4me3. In addition to H4 acetylation, ORC1 binding correlates with increased H4K20me3 in the proximal promoter region of ORC1 targets. This suggests that H4K20me3, unlike in animal cells, is associated with transcriptional activation in Arabidopsis. Thus, our data provide a molecular basis for the opposite role of ORC1 in transcriptional activation in plants and repression in animals. Since only ORC1 proteins of plant species contain a PHD, we propose that plant ORC1 constitutes a novel class of H3K4me3 effector proteins characteristic of the plant kingdom.cell cycle transcription ͉ histone H3 lysine 4 methylation ͉ ORC1 DNA replication ͉ plant homeodomain

Structural Basis for the Unique Multivalent Readout of Unmodified H3 Tail by Arabidopsis ORC1b BAH-PHD Cassette

“…To investigate the molecular basis underlying the linkage of plant DNA replication to histone mark recognition, we focused on the Arabidopsis ORC1, since it has a fused BAH-PHD cassette at its N-terminus, containing two known structural modules that recognize histone marks (Figure 1A and S1). Although it was reported previously that the isolated Arabidopsis ORC1b PHD finger alone can recognize the H3K4me3 mark by in vitro pulldown assay (de la Paz Sanchez and Gutierrez, 2009), our ITC data revealed that both Arabidopsis ORC1a and ORC1b PHD fingers exhibit a strong preference for unmodified H3 peptide over its methylated H3K4 peptide counterparts (Figure 1B and 1C). …”

“…Plant ORC1 proteins possess a BAH domain, but unlike yeast and metazoans, there is a PHD finger embedded within the primary sequence of the BAH domain, thereby generating a plant-specific fused BAH-PHD cassette arrangement (Figure 1A and S1). The PHD finger of Arabidopsis ORC1 was reported to bind H3K4me3 peptides by an in vitro pull-down assay (de la Paz Sanchez and Gutierrez, 2009). At the genome level, Arabidopsis DNA replication origin sites exhibit correlation with G+C enriched regions, and histone H2A.Z, H3K4me2, H3K4me3 and H4K5ac marks, as well as anti-correlation with H3K4me1 and H3K9me2 marks (Costas et al, 2011).…”

Reconsidering the nature and mode of action of metabolite retrograde signals from the chloroplast

“…The plant homeodomain (PHD) specifically binds methylated histones (H3K4me3) to promote transcription of downstream genes (De La Paz Sanchez and Gutierrez, 2009). Under normal conditions, PTM resides in the outer membrane of the chloroplast.…”

The florigen interactor BdES43 represses flowering in the model temperate grass Brachypodium distachyon

“…Interestingly, among the newly isolated partners of BdFTL2, BdES43 contains bromo‐adjacent homology (BAH) and plant homeodomain Zn finger (PHD) domains (Figure S6a). The PHD domain is thought to mediate protein−protein interactions, and usually appears in transcriptional regulators involved in chromatin remodeling (Wysocka et al , ; de la Paz Sanchez and Gutierrez, ; López‐González et al , ; Qian et al , ). Alignment and homology analyses showed that BdES43 was highly similar to AtEBS and AtSHL, especially in functionally important amino acid residues of the BAH and PHD domains, recognizing H3K27me3 and H3K4me3, respectively (Figure S6a–c; Qian et al , ).…”