Li Zhiwei, Jiang Guoxiang, Liu Xuncheng, Ding Xiaochun, Zhang Dandan, Wang Xiaowan, Zhou Yijie, Yan Huiling, Li Taotao, Wu Keqiang, Jiang Yueming, Duan Xuewu
Key Laboratory of Plant Resources Conservation and Sustainable Utilization, South China Botanical Garden, Chinese Academy of Sciences, Guangzhou, 510650, China.
University of Chinese Academy of Sciences, Beijing, 100049, China.
New Phytol. 2020 Aug;227(4):1138-1156. doi: 10.1111/nph.16590. Epub 2020 May 14.
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.
果实成熟受复杂的调控网络支配。可逆的组蛋白甲基化和去甲基化调节染色质结构和基因表达。然而，关于组蛋白去甲基化酶在调控果实成熟中的作用知之甚少。在此，我们发现番茄（Solanum lycopersicum）SlJMJ6编码一种组蛋白赖氨酸去甲基化酶，它特异性地去除H3K27甲基化。SlJMJ6的过表达加速番茄果实成熟，这与大量成熟相关基因的表达上调有关。RNA测序和染色质免疫沉淀测序的综合分析确定了32个被SlJMJ6直接靶向且在SlJMJ6过表达果实中随着H3K27m3减少而转录上调的基因。许多受SlJMJ6调控的基因参与转录调控、乙烯生物合成、细胞壁降解和激素信号传导。包括成熟抑制因子（RIN）、1-氨基环丙烷-1-羧酸合酶-4（ACS4）、1-氨基环丙烷-1-羧酸氧化酶1（ACO1）、果胶酸裂解酶（PL）和β-半乳糖苷酶4（TBG4）在内的11个成熟相关基因，以及一种DNA去甲基化酶DML2，被证实通过去除H3K27me3直接受SlJMJ6调控。我们的结果表明，SlJMJ6是一种促进成熟的H3K27me3去甲基化酶，通过调节H3K27me3激活成熟相关基因的表达，从而促进番茄果实成熟。我们的工作还揭示了在调控果实成熟过程中组蛋白去甲基化与DNA去甲基化之间的新联系。据我们所知，这是关于组蛋白赖氨酸去甲基化酶参与果实成熟调控的首次报道。
