Nonsense-Mediated RNA Decay Factor UPF1 Is Critical for Posttranscriptional and Translational Gene Regulation in Arabidopsis
Nonsense-Mediated RNA Decay Factor UPF1 Is Critical for Posttranscriptional and Translational Gene Regulation in Arabidopsis
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DOI：
10.1105/tpc.20.00244
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发表时间：
2020-09-01
期刊：
影响因子：
11.6
通讯作者：
Riha, Karel
中科院分区：
文献类型：
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作者：
Raxwal, Vivek K.;Simpson, Craig G.;Riha, Karel
无义介导的 RNA 衰减 (NMD) 是一种 RNA 控制机制，也与更广泛的基因表达调控有关。然而，NMD 在基因组调控中的作用尚未得到充分评估，部分原因是 NMD 失活对许多生物体来说是致命的。在这里，我们对缺乏 NMD 相关蛋白 UPF3、UPF1 和 SMG7 的拟南芥 (Arabidopsis thaliana) 突变体进行了深入的比较分析。我们发现这些蛋白质对 NMD 和拟南芥转录组有不同的影响，其中 UPF1 的影响最大。 UPF1缺失植物中的转录组组装揭示了选择性剪接的全基因组变化，表明UPF1在剪接中发挥作用。 UPF1 失活导致翻译抑制，表现为 mRNA 从多核糖体整体转变为单体，以及参与翻译和核糖体生物合成的基因下调。尽管存在这些全球性变化，但低水平表达、半衰期短的 NMD 靶标和 mRNA 在 upf1 突变体的多核糖体中富集，表明 UPF1/NMD 抑制异常 RNA 的翻译。特别引人注目的是含有 TIR 结构域、核苷酸结合、富含亮氨酸重复序列 (TNL) 免疫受体的翻译增加。通过 UPF1/NMD 介导的 mRNA 稳定性和翻译去抑制来调节 TNL，为响应病原体攻击而快速激活 TNL 提供了动态机制。在拟南芥中，RNA 解旋酶和 ATP 酶 UPF1 通过无义介导的 RNA 衰减、剪接和翻译来影响转录组稳态和基因表达。
Nonsense-mediated RNA decay (NMD) is an RNA control mechanism that has also been implicated in the broader regulation of gene expression. Nevertheless, a role for NMD in genome regulation has not yet been fully assessed, partially because NMD inactivation is lethal in many organisms. Here, we performed an in-depth comparative analysis of Arabidopsis (Arabidopsis thaliana) mutants lacking the NMD-related proteins UPF3, UPF1, and SMG7. We found different impacts of these proteins on NMD and the Arabidopsis transcriptome, with UPF1 having the biggest effect. Transcriptome assembly in UPF1-null plants revealed genome-wide changes in alternative splicing, suggesting that UPF1 functions in splicing. The inactivation of UPF1 led to translational repression, as manifested by a global shift in mRNAs from polysomes to monosomes and the downregulation of genes involved in translation and ribosome biogenesis. Despite these global changes, NMD targets and mRNAs expressed at low levels with short half-lives were enriched in the polysomes ofupf1mutants, indicating that UPF1/NMD suppresses the translation of aberrant RNAs. Particularly striking was an increase in the translation of TIR domain-containing, nucleotide binding, leucine-rich repeat (TNL) immune receptors. The regulation of TNLs via UPF1/NMD-mediated mRNA stability and translational derepression offers a dynamic mechanism for the rapid activation of TNLs in response to pathogen attack.The RNA helicase and ATPase UPF1 affects transcriptome homeostasis and gene expression through nonsense-mediated RNA decay, splicing, and translation in Arabidopsis.