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Global Functional Targets of the Histone Methyltransferase SDG8 Uncover a Role for Histone Modification in Energy Metabolism

ABSTRACT: Histone methylation modulates gene expression in response to external and internal cues. We uncovered a non-redundant role for the Arabidopsis histone methyltransferase, SDG8, which provides a unique opportunity to study the global function of a specific histone methyltransferase within in a multicellular organism. We previously used a promoter responsive to light and carbon in a positive genetic screen to identify an Arabidopsis carbon and light insensitive mutant cli186. In this study, we characterize the mutant cli186 as a complete deletion of a histone methyltransferase gene SDG8 (now renamed sdg8-5). To assess the global role of SDG8, we compared the global histone methylation patterns and the transcriptome of sdg8-5 to wild type (WT) in the context of a transient carbon and light treatment. We showed that the complete deletion of SDG8 in sdg8-5 is associated with a dramatic reduction of H3K36me3 towards the 3’ of the gene body, which correlates with significant reduction in gene expression. We uncovered 1,084 “high confidence” functional targets of SDG8 – affected in both H3K36me3 marks and gene expression – that are associated with specific biological processes including defense, photosynthesis, nutrient metabolism and energy metabolism. Importantly, 71% of these functional targets are responsive to carbon and/or light. Our model suggests that SDG8 functions to mark specific sets of genes with H3K36me3 in the gene body for active transcription, to tune genes involved in primary metabolism that are responsive to the energy level in the environment.

ORGANISM(S): Arabidopsis thaliana

PROVIDER: GSE62435 | GEO | 2015/03/01

SECONDARY ACCESSION(S): PRJNA264092

REPOSITORIES: GEO

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Project description:The seed maturation program occurs only during late phase of embryo development and repression of the maturation genes is pivotal for seedling development. However, mechanisms that repress the expression of this program in vegetative tissues are not well understood. A genetic screen was performed for mutants that express maturation genes in leaves. Here, it is shown that mutations affecting SDG8 (SET DOMAIN GROUP 8), a putative histone methyltransferase, cause ectopic expression of a subset of maturation genes in leaves. Further, to investigate the relationship between SDG8 and the Polycomb Group (PcG) proteins, which are known to repress many developmentally important genes including seed maturation genes, double mutants was made and formation of somatic embryos was observed on mutant seedlings with mutations in both SDG8 and EMF2 (EMBRYONIC FLOWER 2). Interestingly, double mutant of sdg8 and mutations in VRN2 (VERNALIZATION 2), a paralog of EMF2, grow and develop normally to maturity. Analysis of histone methylation status at chromatins of a number of maturation loci revealed synergistic effect of emf2 and sdg8 on the deposition of the active histone mark, trimethylation of lysine 4 on histone 3 (H3K4me3), which is consistent with high expression of these genes (formation of somatic embryos) in emf2 sdg8 double mutants. These observations demonstrate a functional cooperative interplay between SDG8 and an EMF2-containing PcG complex in maintaining vegetative cell identity by repressing seed genes to promote seedling development. The work also indicates the functional specificities of PcG complexes in Arabidopsis. Total RNA was isolated from three independent biological replicates of Wild type (ProM-NM-2CG:GUS) and two independent biological replicates of sdg8-2 and essp4/sdg8-5, respectively. Four ATH1 chips were used for the two mutants and three for the wild type. Matrices comprising the signal intensity value of each gene per replicate hybridization and the averaged data of each gene generated from three replicate hybridizations of the wild type and two replicate hybridizations of mutant samples, respectively, are linked below as supplementary files.

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Global Functional Targets of the Histone Methyltransferase SDG8 Uncover a Role for Histone Modification in Energy Metabolism

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