Kumar Suresh, Seem Karishma, Kumar Santosh, Vinod K K, Chinnusamy Viswanathan, Mohapatra Trilochan
Division of Biochemistry, ICAR-Indian Agricultural Research Institute, New Delhi, India.
Decode Genomics Private Limited, New Delhi, India.
Front Plant Sci. 2022 May 31;13:871890. doi: 10.3389/fpls.2022.871890. eCollection 2022.
Cytosine methylation, epigenetic DNA modification, is well known to regulate gene expression. Among the epigenetic modifications, 5-methylcytosine (5-mC) has been one of the extensively studied epigenetic changes responsible for regulating gene expression in animals and plants. Though a dramatic change in 5-mC content is observed at the genome level, the variation in gene expression is generally less than that it is expected. Only less is understood about the significance of 5-mC in gene regulation under P-starvation stress in plants. Using whole-genome bisulfite sequencing of a pair of rice [Pusa-44 and its near-isogenic line (NIL)-23 harboring QTL] genotypes, we could decipher the role of on DNA (de)methylation-mediated regulation of gene expression under P-starvation stress. We observed 13-15% of total cytosines to be methylated in the rice genome, which increased significantly under the stress. The number of differentially methylated regions (DMRs) for hypomethylation (6,068) was higher than those (5,279) for hypermethylated DMRs under the stress, particularly in root of NIL-23. Hypomethylation in CHH context caused upregulated expression of 489 genes in shoot and 382 genes in root of NIL-23 under the stress, wherein 387 genes in shoot and 240 genes in root were upregulated exclusively in NIL-23. Many of the genes for DNA methylation, a few for DNA demethylation, and RNA-directed DNA methylation were upregulated in root of NIL-23 under the stress. Methylation or demethylation of DNA in genic regions differentially affected gene expression. Correlation analysis for the distribution of DMRs and gene expression indicated the regulation of gene mainly through (de)methylation of promoter. Many of the P-responsive genes were hypomethylated or upregulated in roots of NIL-23 under the stress. Hypermethylation of gene body in CG, CHG, and CHH contexts caused up- or downregulated expression of transcription factors (TFs), P transporters, phosphoesterases, retrotransposon proteins, and other proteins. Our integrated transcriptome and methylome analyses revealed an important role of the QTL in epigenetic regulation of the genes for transporters, TFs, phosphatases, carbohydrate metabolism, hormone-signaling, and chromatin architecture or epigenetic modifications in P-starvation tolerance. This provides insights into the molecular function of in modulating gene expression through DNA (de)methylation, which might be useful in improving P-use efficiency or productivity of rice in P-deficient soil.
胞嘧啶甲基化作为一种表观遗传DNA修饰，在调节基因表达方面广为人知。在各种表观遗传修饰中，5-甲基胞嘧啶（5-mC）一直是在动植物中负责调节基因表达的广泛研究的表观遗传变化之一。尽管在基因组水平上观察到5-mC含量有显著变化，但基因表达的变化通常小于预期。关于5-mC在植物磷饥饿胁迫下基因调控中的意义，人们了解得还很少。通过对一对水稻[Pusa-44及其携带QTL的近等基因系（NIL）-23]基因型进行全基因组亚硫酸氢盐测序，我们能够解读磷饥饿胁迫下DNA（去）甲基化介导的基因表达调控作用。我们观察到水稻基因组中13%-15%的总胞嘧啶发生了甲基化，在胁迫下这一比例显著增加。胁迫下，低甲基化的差异甲基化区域（DMRs）数量（6068个）高于高甲基化的DMRs数量（5279个），特别是在NIL-23的根中。在胁迫下，CHH背景下的低甲基化导致NIL-23地上部489个基因和根部382个基因的表达上调，其中地上部387个基因和根部240个基因仅在NIL-23中上调。许多DNA甲基化基因、少数DNA去甲基化基因以及RNA指导的DNA甲基化基因在胁迫下NIL-23的根中上调。基因区域中DNA的甲基化或去甲基化对基因表达有不同影响。DMRs分布与基因表达的相关性分析表明，基因调控主要通过启动子的（去）甲基化进行。许多磷响应基因在胁迫下NIL-23的根中发生低甲基化或上调。CG、CHG和CHH背景下基因体的高甲基化导致转录因子（TFs）、磷转运蛋白、磷酸酯酶、逆转座子蛋白和其他蛋白质的表达上调或下调。我们的转录组和甲基化组综合分析揭示了QTL在磷饥饿耐受性中对转运蛋白、TFs、磷酸酶、碳水化合物代谢、激素信号传导以及染色质结构或表观遗传修饰相关基因的表观遗传调控中起重要作用。这为通过DNA（去）甲基化调节基因表达的分子功能提供了见解，这可能有助于提高水稻在缺磷土壤中的磷利用效率或生产力。
