DNA methylation remodeling and the functional implication during male gametogenesis in rice

• Published in: Genome Biology Vol. 25; no. 1; pp. 84 - 19
• Main Authors: Li, Xue, Zhu, Bo, Lu, Yue, Zhao, Feng, Liu, Qian, Wang, Jiahao, Ye, Miaomiao, Chen, Siyuan, Nie, Junwei, Xiong, Lizhong, Zhao, Yu, Wu, Changyin, Zhou, Dao-Xiu
• Format: Journal Article
• Language: English
• Published: England BioMed Central 02.04.2024; BMC
• Subjects: Cell division; CMT3; CRISPR; DNA Methylation; Egg; Embryos; Epigenetics; Fertilization; Flowering; Gametes; Gametogenesis; Gene expression; Gene Expression Regulation, Plant; Gene silencing; Genes; Histones; JMJ706; Life Sciences; Meiosis; Methyltransferase; Methyltransferases - metabolism; Mutation; Oryza - genetics; Oryza - metabolism; Pollen; Rice; Rice male gametogenesis; Seeds - metabolism; Sexual reproduction; Sperm; Transcription factors; Zygote; Zygotes; JMJ706; JMJ707; Egg; Zygote; CMT3; DNA methylation; Rice male gametogenesis
• ISSN: 1474-760X; 1474-7596; 1465-6906; 1474-760X
• 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.