Euchromatic Subdomains in Rice Centromeres Are Associated with Genes and Transcription

Abstract

The presence of the centromere-specific histone H3 variant, CENH3, defines centromeric (CEN) chromatin, but poorly understood epigenetic mechanisms determine its establishment and maintenance. CEN chromatin is embedded within pericentromeric heterochromatin in most higher eukaryotes, but, interestingly, it can show euchromatic characteristics; for example, the euchromatic histone modification mark dimethylated H3 Lys 4 (H3K4me2) is uniquely associated with animal centromeres. To examine the histone marks and chromatin properties of plant centromeres, we developed a genomic tiling array for four fully sequenced rice (Oryza sativa) centromeres and used chromatin immunoprecipitation-chip to study the patterns of four euchromatic histone modification marks: H3K4me2, trimethylated H3 Lys 4, trimethylated H3 Lys 36, and acetylated H3 Lys 4, 9. The vast majority of the four histone marks were associated with genes located in the H3 subdomains within the centromere cores. We demonstrate that H3K4me2 is not a ubiquitous component of rice CEN chromatin, and the euchromatic characteristics of rice CEN chromatin are hallmarks of the transcribed sequences embedded in the centromeric H3 subdomains. We propose that the transcribed sequences located in rice centromeres may provide a barrier preventing loading of CENH3 into the H3 subdomains. The separation of CENH3 and H3 subdomains in the centromere core may be favorable for the formation of three-dimensional centromere structure and for rice centromere function.

Repeatless and Repeat-Based Centromeres in Potato: Implications for Centromere Evolution

“…Each centromere contained several CENH3-enriched subdomains, which were interspersed with subdomains that were not enriched with CENH3. The CENH3-lacking subdomains likely consist of nucleosomes containing H3 (hereafter named as H3 subdomains) (Wu et al, 2011). The structure of intermingled CENH3 and H3 subdomains of potato centromeres is similar to that observed in rice (Oryza sativa) centromeres (Yan et al, 2008).…”

“…However, these genes are all located within the H3 subdomains embedded in the centromeric cores (Yan et al, 2008). Thus, the genes in rice centromeres are associated with H3 nucleosomes and show similar histone H3 modification patterns to those located outside of the centromeres (Wu et al, 2011). Most active genes (based on RNAseq annotation) in potato centromeres were mapped within H3 subdomains.…”

Formation of a Functional Maize Centromere after Loss of Centromeric Sequences and Gain of Ectopic Sequences

“…The 723-kb region has an abundance of transposable elements compared with other genomic sequences. Genes from the centromeric region of both human neocentromeres and plant centromeres can be actively transcribed (Saffery et al, 2003;Nagaki et al, 2004;May et al, 2005;Wong et al, 2006;Alonso et al, 2010;Wu et al, 2011;Gong et al, 2012). Most of the transcripts are associated with epigenetic modifications to maintain centromere identity.…”

Pericentric and centromeric transcription: a perfect balance required

“…1a, b). However, maize and rice appear unique as the centromeres of these species do not contain enrichment for H3K4me2 (Wu et al 2011;Gent et al 2012). Instead, the specific type of centromere sequence present dictates the class of corresponding histone modifications.…”

“…Instead, the specific type of centromere sequence present dictates the class of corresponding histone modifications. For instance, genes present at rice centromeres have the same histone modifications as genes present in euchromatin (Yan et al 2005;Wu et al 2011). Thus, the lack of enrichment for H3K4me2 could be due to the presence of actively transcribed genes embedded in between clusters of centC centromeric satellite and centromeric retroelements of maize (CRM) retrotransposon sequences (Gent et al 2012).…”