OsAGO2 controls ROS production and the initiation of tapetal PCD by epigenetically regulating OsHXK1 expression in rice anthers
OsAGO2 controls ROS production and the initiation of tapetal PCD by epigenetically regulating OsHXK1 expression in rice anthers
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DOI：
10.1073/pnas.1817675116
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发表时间：
2019-03
影响因子：
11.1
通讯作者：
Shaoyan Zheng;Jing Li;Lu Ma;Hailong Wang;Hai Zhou;Erdong Ni;Dagang Jiang;Zhenlan Liu;C. Zhuan
中科院分区：
文献类型：
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作者：
Shaoyan Zheng;Jing Li;Lu Ma;Hailong Wang;Hai Zhou;Erdong Ni;Dagang Jiang;Zhenlan Liu;C. Zhuan
意义了解植物雄性生殖器官花药的发育对作物产量具有重要意义。表观遗传机制通过改变DNA或组蛋白的修饰以及通过非编码RNA来调节基因表达。许多研究已经研究了花药发育，但表观遗传机制的参与仍有待探讨。在这里，我们研究了ARGONAUTE（AGO）家族蛋白OsAGO 2的作用。我们发现OsAGO2通过调节己糖激酶（OsHXK）启动子区域的DNA甲基化修饰来表观遗传地调节花药发育。OsHXK1通过调节活性氧的产生和关键花药结构中细胞死亡的启动来影响花药发育。鉴定这种表观遗传调控机制对杂交作物品种的生产具有重要意义。Argonaute（AGO）家族的蛋白质在基因表达的表观遗传调节中起作用。虽然水稻（Oryza sativa）基因组编码19个预测的AGO蛋白，但迄今为止很少有其功能被表征。在这里，我们表明，AGO蛋白OsAGO2调节水稻花药发育。OsAGO 2在花药中高度表达。OsAGO2基因的敲除导致活性氧（ROS）的过度积累和花药发育异常，导致绒毡层细胞程序性死亡（PCD）的提前启动和花粉败育。在OsAGO2基因敲低的植株中，己糖激酶1（OsHXK1）的表达量显著增加，其启动子甲基化水平降低。OsHXK1的过表达还导致ROS的过度积累、PCD的过早启动和花粉败育。此外，OsHXKl的敲除恢复了OsAGO2敲除植物中的花粉育性。染色质免疫沉淀实验表明OsAGO2与OsHXK1的启动子直接结合，表明OsHXK1是OsAGO2的靶基因。这些结果表明，OsHXK1控制着ROS的适当产生和绒毡层PCD的适当时间，并通过表观遗传调控直接受OsAGO2的调控。
Significance Understanding the development of anthers, the male reproductive organs of plants, has key implications for crop yield. Epigenetic mechanisms modulate gene expression by altering modifications of DNA or histones and via noncoding RNAs. Many studies have examined anther development, but the involvement of epigenetic mechanisms remains to be explored. Here, we investigated the role of an ARGONAUTE (AGO) family protein, OsAGO2. We find that OsAGO2 epigenetically regulates anther development by modulating DNA methylation modifications in the Hexokinase (OsHXK) promoter region. OsHXK1, in turn, affects anther development by regulating the production of reactive oxygen and the initiation of cell death in key anther structures. Identification of this epigenetic regulatory mechanism has implications for the production of hybrid crop varieties. Proteins of the ARGONAUTE (AGO) family function in the epigenetic regulation of gene expression. Although the rice (Oryza sativa) genome encodes 19 predicted AGO proteins, few of their functions have thus far been characterized. Here, we show that the AGO protein OsAGO2 regulates anther development in rice. OsAGO2 was highly expressed in anthers. Knockdown of OsAGO2 led to the overaccumulation of reactive oxygen species (ROS) and abnormal anther development, causing premature initiation of tapetal programmed cell death (PCD) and pollen abortion. The expression level of Hexokinase 1 (OsHXK1) increased significantly, and the methylation levels of its promoter decreased, in plants with knocked-down OsAGO2 expression. Overexpression of OsHXK1 also resulted in the overaccumulation of ROS, premature initiation of PCD, and pollen abortion. Moreover, knockdown of OsHXK1 restored pollen fertility in OsAGO2 knockdown plants. Chromatin immunoprecipitation assays demonstrated that OsAGO2 binds directly to the OsHXK1 promoter region, suggesting that OsHXK1 is a target gene of OsAGO2. These results indicate that OsHXK1 controls the appropriate production of ROS and the proper timing of tapetal PCD and is directly regulated by OsAGO2 through epigenetic regulation.