Widespread regulation of the maternal transcriptome by Nanos in Drosophila.

IF 9.8 1区 生物学 Q1 Agricultural and Biological Sciences PLoS Biology Pub Date : 2024-10-14 eCollection Date: 2024-10-01 DOI:10.1371/journal.pbio.3002840
Mohammad Marhabaie, Tammy H Wharton, Sung Yun Kim, Robin P Wharton
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Abstract

The translational repressor Nanos (Nos) regulates a single target, maternal hunchback (hb) mRNA, to govern abdominal segmentation in the early Drosophila embryo. Nos is recruited to sites in the 3' UTR of hb mRNA in collaboration with the sequence-specific RNA-binding protein Pumilio (Pum); on its own, Nos has no binding specificity. Nos is expressed at other stages of development, but very few mRNA targets that might mediate its action at these stages have been described. Nor has it been clear whether Nos is targeted to other mRNAs in concert with Pum or via other mechanisms. In this report, we identify mRNAs targeted by Nos via 2 approaches. First, we identify mRNAs depleted upon expression of a chimera bearing Nos fused to the nonsense mediated decay (NMD) factor Upf1. We find that, in addition to hb, Upf1-Nos depletes approximately 2,600 mRNAs from the maternal transcriptome in early embryos. Virtually all of these appear to be targeted in a canonical, hb-like manner in concert with Pum. In a second, more conventional approach, we identify mRNAs that are stabilized during the maternal zygotic transition (MZT) in embryos from nos- females. Most (86%) of the 1,185 mRNAs regulated by Nos are also targeted by Upf1-Nos, validating use of the chimera. Previous work has shown that 60% of the maternal transcriptome is degraded in early embryos. We find that maternal mRNAs targeted by Upf1-Nos are hypoadenylated and inefficiently translated at the ovary-embryo transition; they are subsequently degraded in the early embryo, accounting for 59% of all destabilized maternal mRNAs. We suggest that the late ovarian burst of Nos represses a large fraction of the maternal transcriptome, priming it for later degradation by other factors in the embryo.

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果蝇的母体转录组受到 Nanos 的广泛调控。
翻译抑制因子Nanos(Nos)只调节一个目标,即母体驼背(hb)mRNA,从而控制果蝇早期胚胎的腹部分割。Nos 与序列特异性 RNA 结合蛋白 Pumilio(Pum)合作,被招募到 hb mRNA 的 3' UTR 位点;Nos 本身没有结合特异性。Nos 在发育的其他阶段也有表达,但在这些阶段可能介导其作用的 mRNA 靶点却很少被描述。也不清楚 Nos 是与 Pum 协同作用还是通过其他机制靶向其他 mRNA。在本报告中,我们通过两种方法确定了 Nos 靶向的 mRNA。首先,我们确定了表达 Nos 与无义介导衰变(NMD)因子 Upf1 融合的嵌合体时耗竭的 mRNA。我们发现,除 hb 外,Upf1-Nos 还会从早期胚胎的母体转录组中删除约 2,600 个 mRNA。几乎所有这些mRNA似乎都以类似于hb的典型方式与Pum协同作用。在第二种更传统的方法中,我们识别了在母系子代转换(MZT)过程中,nos-雌性胚胎中稳定的 mRNA。在受 Nos 调控的 1,185 个 mRNA 中,大部分(86%)也是 Upf1-Nos 的靶标,从而验证了嵌合体的有效性。以前的研究表明,60%的母体转录组在早期胚胎中降解。我们发现,Upf1-Nos 靶向的母体 mRNA 在卵巢-胚胎过渡阶段腺苷酸过低,翻译效率低下;随后在早期胚胎中降解,占所有不稳定母体 mRNA 的 59%。我们认为,卵巢晚期的 Nos 爆发抑制了母体转录组的很大一部分,使其在胚胎中被其他因子降解。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
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来源期刊
PLoS Biology
PLoS Biology BIOCHEMISTRY & MOLECULAR BIOLOGY-BIOLOGY
CiteScore
15.40
自引率
2.00%
发文量
359
审稿时长
3-8 weeks
期刊介绍: PLOS Biology is the flagship journal of the Public Library of Science (PLOS) and focuses on publishing groundbreaking and relevant research in all areas of biological science. The journal features works at various scales, ranging from molecules to ecosystems, and also encourages interdisciplinary studies. PLOS Biology publishes articles that demonstrate exceptional significance, originality, and relevance, with a high standard of scientific rigor in methodology, reporting, and conclusions. The journal aims to advance science and serve the research community by transforming research communication to align with the research process. It offers evolving article types and policies that empower authors to share the complete story behind their scientific findings with a diverse global audience of researchers, educators, policymakers, patient advocacy groups, and the general public. PLOS Biology, along with other PLOS journals, is widely indexed by major services such as Crossref, Dimensions, DOAJ, Google Scholar, PubMed, PubMed Central, Scopus, and Web of Science. Additionally, PLOS Biology is indexed by various other services including AGRICOLA, Biological Abstracts, BIOSYS Previews, CABI CAB Abstracts, CABI Global Health, CAPES, CAS, CNKI, Embase, Journal Guide, MEDLINE, and Zoological Record, ensuring that the research content is easily accessible and discoverable by a wide range of audiences.
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