Journal Article

Histone demethylase SlJMJ6 promotes fruit ripening by removing H3K27 methylation of ripening-related genes in tomato

Wang, Xiaowan, Jiang, Guoxiang, Li, Zhiwei, Jiang, Yueming, Zhang, Dandan, Zhou, Yijie, Liu, Xuncheng, Ding, Xiaochun, Yan, Huiling, Li, Taotao, Wu, Keqiang, Duan, Xuewu

2020

Overview

• Fruit ripening is governed by a complex regulatory network. Reversible histone methylation and demethylation regulate chromatin structure and gene expression. However, little is known about the involvement of histone demethylases in regulating fruit ripening. • Here, we found that the tomato (Solanum lycopersicum) SlJMJ6 encodes a histone lysine demethylase that specifically demethylates H3K27 methylation. Overexpression of SlJMJ6 accelerates tomato fruit ripening, which is associated with the upregulated expression of a large number of ripening-related genes. • Integrated analysis of RNA-seq and chromatin immunoprecipitation followed by sequencing identified 32 genes directly targeted by SlJMJ6 and transcriptionally upregulated with decreased H3K27m3 in SlJMJ6-overexpressed fruit. Numerous SlJMJ6-regulated genes are involved in transcription regulation, ethylene biosynthesis, cell wall degradation and hormone signaling. Eleven ripening-related genes including RIPENING INHIBITOR (RIN), 1-aminocyclopropane 1-carboxylate synthase-4 (ACS4), 1-aminocyclopropane-1-carboxylate oxidase 1 (ACO1), pectate lyase (PL) and beta-galactosidase 4 (TBG4), and a DNA demethylase DML2, were confirmed to be regulated directly by SlJMJ6 through removing H3K27me3. • Our results demonstrate that SlJMJ6 is a ripening-prompting H3K27me3 demethylase that activates the expression of the ripening-related genes by modulating H3K27me3, thereby facilitating tomato fruit ripening. Our work also reveals a novel link between histone demethylation and DNA demethylation in regulating fruit ripening. To our knowledge, this is the first report of the involvement of a histone lysine demethylase in the regulation of fruit ripening.

• Publisher: Wiley,Wiley Subscription Services, Inc
• Subject: ACO / aminocyclopropanecarboxylate oxidase / beta-galactosidase / Biosynthesis / Cell walls / Chromatin / chromatin immunoprecipitation / Demethylation / Deoxyribonucleic acid / DML2 / DNA / DNA demethylase / DNA demethylation / DNA methylation / ethylene production / Ethylenes / Fruit - genetics / Fruit - metabolism / fruit ripening / Fruits / Gene expression / Gene Expression Regulation, Plant / Gene regulation / Gene sequencing / Genes / H3K27 demethylase / histone demethylases / Histone Demethylases - genetics / histone demethylation / Histones / Hormones / Immunoprecipitation / JmjC‐domain protein / Lycopersicon esculentum - genetics / Lycopersicon esculentum - metabolism / Lysine / Methylation / Nucleic acids / Pectate lyase / Plant Proteins - genetics / Plant Proteins - metabolism / Ribonucleic acid / RIN / Ripening / RNA / sequence analysis / Solanum lycopersicum / Tomatoes / Transcription / transcription (genetics) / β-Galactosidase