Institute of Biotechnology, National Taiwan University, No.1, Sec. 4, Roosevelt Rd., Taipei 106319, Taiwan, ROC.
Graduate Institute of Translational Medicine, College of Medical Science and Technology, Taipei Medical University, No. 250 Wu-Xing St., Taipei 11031, Taiwan, ROC.
Plant Cell Physiol. 2024 Oct 3;65(9):1414-1433. doi: 10.1093/pcp/pcae080.
As a model plant for bryophytes, Marchantia polymorpha offers insights into the role of RNA silencing in aiding early land plants navigate the challenges posed by high-temperature environments. Genomic analysis revealed unique ARGONAUTE1 ortholog gene (MpAGO1) in M. polymorpha, which is regulated by two species-specific microRNAs (miRNAs), miR11707.1 and miR11707.2. Comparative studies of small RNA profiles from M. polymorpha cellular and MpAGO1 immunoprecipitation (MpAGO1-IP) profiles at various temperatures, along with analyses of Arabidopsis AGO1 (AtAGO1), revealed that MpAGO1 has a low selectivity for a diverse range of small RNA species than AtAGO1. Protein structural comparisons revealed no discernible differences in the guide strand small RNA recognition middle domain, MID domain, of MpAGO1 and AtAGO1, suggesting the complexity of miRNA species specificity and necessitating further exploration. Small RNA profiling and size exclusion chromatography have pinpointed a subset of M. polymorpha miRNAs, notably miR11707, that remain in free form within the cell at 22°C but are loaded into MpAGO1 at 28°C to engage in RNA silencing. Investigations into the mir11707 gene editing (mir11707ge) mutants provided evidence of the regulation of miR11707 in MpAGO1. Notably, while MpAGO1 mRNA expression decreases at 28°C, the stability of the MpAGO1 protein and its associated miRNAs is essential for enhancing the RNA-inducing silencing complex (RISC) activity, revealing the importance of RNA silencing in enabling M. polymorpha to survive thermal stress. This study advances our understanding of RNA silencing in bryophytes and provides groundbreaking insights into the evolutionary resilience of land plants to climatic adversities.
作为苔藓植物的模式植物，地钱为我们深入了解 RNA 沉默在帮助早期陆生植物应对高温环境带来的挑战方面所起的作用提供了线索。基因组分析揭示了地钱中独特的 ARGONAUTE1 直系同源基因（MpAGO1），该基因受两种物种特异性 microRNA（miRNA）miR11707.1 和 miR11707.2 的调控。在不同温度下对地钱小 RNA 谱和 MpAGO1 免疫沉淀（MpAGO1-IP）谱的小 RNA 谱进行比较研究，以及对拟南芥 AGO1（AtAGO1）的分析表明，MpAGO1 对各种小 RNA 种类的选择性低于 AtAGO1。蛋白质结构比较显示，MpAGO1 和 AtAGO1 的引导链小 RNA 识别中间结构域（MID 结构域）没有明显差异，这表明 miRNA 物种特异性的复杂性，需要进一步探索。小 RNA 谱分析和排阻色谱法确定了地钱的一小部分 miRNAs，特别是 miR11707，在 22°C 时仍以游离形式存在于细胞内，但在 28°C 时被加载到 MpAGO1 中以参与 RNA 沉默。对地钱 mir11707 基因编辑（mir11707ge）突变体的研究提供了证据表明 miR11707 在 MpAGO1 中的调控。值得注意的是，虽然 MpAGO1 mRNA 的表达在 28°C 时降低，但 MpAGO1 蛋白及其相关 miRNAs 的稳定性对于增强 RNA 诱导沉默复合物（RISC）的活性是必不可少的，这揭示了 RNA 沉默在地钱应对热应激中的重要性。本研究增进了我们对苔藓植物中 RNA 沉默的理解，并为陆地植物对气候逆境的进化弹性提供了开创性的见解。
