National Key Laboratory of Crop Genetic Improvement, Hubei Hongshan Laboratory, Huazhong Agricultural University, Wuhan, 430070, China.
Key Laboratory of Plant Functional Genomics of the Ministry of Education/Jiangsu Key Laboratory of Crop Genomics and Molecular Breeding, College of Agriculture, Yangzhou University, Yangzhou, 225009, China.
Genome Biol. 2024 Apr 2;25(1):84. doi: 10.1186/s13059-024-03222-w.
Epigenetic marks are reprogrammed during sexual reproduction. In flowering plants, DNA methylation is only partially remodeled in the gametes and the zygote. However, the timing and functional significance of the remodeling during plant gametogenesis remain obscure.
Here we show that DNA methylation remodeling starts after male meiosis in rice, with non-CG methylation, particularly at CHG sites, being first enhanced in the microspore and subsequently decreased in sperm. Functional analysis of rice CHG methyltransferase genes CMT3a and CMT3b indicates that CMT3a functions as the major CHG methyltransferase in rice meiocyte, while CMT3b is responsible for the increase of CHG methylation in microspore. The function of the two histone demethylases JMJ706 and JMJ707 that remove H3K9me2 may contribute to the decreased CHG methylation in sperm. During male gametogenesis CMT3a mainly silences TE and TE-related genes while CMT3b is required for repression of genes encoding factors involved in transcriptional and translational activities. In addition, CMT3b functions to repress zygotic gene expression in egg and participates in establishing the zygotic epigenome upon fertilization.
Collectively, the results indicate that DNA methylation is dynamically remodeled during male gametogenesis, distinguish the function of CMT3a and CMT3b in sex cells, and underpin the functional significance of DNA methylation remodeling during rice reproduction.
表观遗传标记在有性生殖过程中被重新编程。在开花植物中,配子和受精卵中 DNA 甲基化仅部分重塑。然而,植物配子发生过程中重塑的时间和功能意义仍不清楚。
本文显示,在水稻中,DNA 甲基化重塑始于雄性减数分裂后,非 CG 甲基化,特别是 CHG 位点,首先在小孢子中增强,随后在精子中减少。对水稻 CHG 甲基转移酶基因 CMT3a 和 CMT3b 的功能分析表明,CMT3a 作为水稻减数分裂细胞中的主要 CHG 甲基转移酶,而 CMT3b 负责增加小孢子中的 CHG 甲基化。两种组蛋白去甲基酶 JMJ706 和 JMJ707 的功能可能有助于精子中 CHG 甲基化的减少,它们去除 H3K9me2。在雄性配子发生过程中,CMT3a 主要沉默转座因子及其相关基因,而 CMT3b 则抑制参与转录和翻译活性的基因编码因子。此外,CMT3b 抑制卵中的合子基因表达,并在受精时参与建立合子的表观基因组。
总之,这些结果表明,DNA 甲基化在雄性配子发生过程中动态重塑,区分了 CMT3a 和 CMT3b 在性细胞中的功能,并为水稻生殖过程中 DNA 甲基化重塑的功能意义提供了依据。