H3K36 methylation stamps transcription resistive to preserve development in plants

Eukaryotic euchromatin is the less-compact chromatin and is modified by many histone modifications such as H3 lysine 36 methylation (H3K36me). Here we report a new chromatin state, 'transcription resistive', which is differentiated from activation and silencing. Transcription resistive is stamped by H3K36me with almost undetectable transcription activity but open-chromatin state, and occupies most documented plant essential genes. Mutating SDG8, previously known as the major H3K36 methyltransferase in Arabidopsis, surprisingly elevates 78.7% of H3K36me3-marked resistive loci, which accounts for 39.4% of the coding genome. Genetically, SDG8 prevents H3K36me activity of SDG4 at short and intronless genes to secure plant fertility, while it collaborates with other H3K36me methyltransferases on long and intron-rich genes. Together, our results reveal that SDG8 is the primary sensor that suppresses excessive H3K36me, and uncovered that 'transcription resistive' is a conserved H3K36me-stamped novel transcription state in plants, highlighting the regulatory diversities and biological significance of H3K36 methylation in eukaryotes.