Abstract:
Although there is increasing understanding of regulatory impacts from particular epigenetic marks, much less is known about how crosstalk occurring among multiple marks affects genetic regulation. Here, we show that Dwarf-related WD40 protein 1 (DRW1) mediates DNA 6mA demethylation, H3K27 trimethylation, and RNA m5 C methylation in rice, based on its respective recruitment of the DNA demethylase AlkB homolog 1 (OsALKBH1), the histone methyltransferase CURLY LEAF (OsCLF), and NOP2/Sun RNA methyltransferase family member 2 (OsNSUN2). DRW1 knockout significantly reduces the extent of chromatin occupancy by OsALKBH1, OsCLF, and OsNSUN2, augments chromatin accessibility, and promotes the expression of brassinosteroid biosynthesis and signaling biomolecules. Gene editing at a CAAT36 box (ATTGG→ATTGA) and a GATA motif (GATAGGG→GAT) in the DRW1 promoter leads to increased DRW1 transcription and to enhancement of both grain yield and salt tolerance. In field trials, DRW1-overexpressing rice lines display yield increases of ~30.2% (on both normal and saline soils), accompanied by decreases in DNA 6mA and increases of H3K27me3 and RNA m5 C levels for target genes. Overall, our study uncovers crosstalk among DNA 6mA, H3K27me3, and
RNA m5C mediated by DRW1, and shows how this crosstalk controls transcriptional and post transcriptional regulation affecting yield and salt toleranceKey Words:
DRW1, recruiter, epigenetic crosstalk, chromatin accessibility, grain yield


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