The TOP-2/condensin II axis silences transcription during germline specification in C. elegans.

IF 2.1 3区 生物学 Q3 GENETICS & HEREDITY G3: Genes|Genomes|Genetics Pub Date : 2024-10-03 DOI:10.1093/g3journal/jkae236
Mezmur D Belew, Emilie Chien, Matthew Wong, W Matthew Michael
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Abstract

In C. elegans, the germline is specified via a preformation mechanism that relies on the PIE-1 protein's ability to globally silence mRNA transcription in germline precursor cells, also known as the P lineage. Recent work from our group has identified additional genome silencing events in C. elegans during oogenesis and in starved L1 larvae, and these require the condensin II complex, topoisomerase II (TOP-2), and components of the H3K9me/heterochromatin pathway. Interestingly, silencing in oocytes also requires PIE-1, but this is not the case in starved L1s. Here, we ask if additional genome silencing components besides PIE-1 are required to repress gene expression in the P lineage of early embryos, and we find that condensin II and TOP-2 are required and the H3K9me/heterochromatin pathway is not. We show that depletion of TOP-2/condensin II activates the normally suppressed RNA polymerase II to inappropriately transcribe somatic genes in the P lineage. We also present evidence that while both PIE-1 and TOP-2/condensin II are required for genome silencing in the P lineage, PIE-1 can silence transcription independently of TOP-2/condensin II when misexpressed in somatic cells. Thus, in oocytes, all three genome silencing systems (TOP-2/condensin II, H3K9me, and PIE-1) are operational while in both early embryos and starved L1s two of the three are active. Our data show that multiple, redundantly acting genome silencing mechanisms act in a mix and match manner to repress transcription at different developmental stages in the C. elegans germline.

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TOP-2/condensin II轴在秀丽隐杆线虫种系规格化过程中抑制转录。
在秀丽隐杆线虫中,种系是通过一种形成前机制指定的,这种机制依赖于 PIE-1 蛋白在种系前体细胞(也称为 P 系)中全面沉默 mRNA 转录的能力。我们研究小组最近的研究发现,在卵母细胞发生过程中和饥饿的 L1 幼虫体内,还存在其他基因组沉默事件,这些事件需要冷凝素 II 复合物、拓扑异构酶 II(TOP-2)和 H3K9me/异染色质通路的成分。有趣的是,卵母细胞中的沉默也需要 PIE-1,但饥饿的 L1 却不需要。在这里,我们询问除了 PIE-1 之外是否还需要其他基因组沉默元件来抑制早期胚胎 P 系中的基因表达,结果发现冷凝素 II 和 TOP-2 是必需的,而 H3K9me/异染色质通路则不是。我们发现,TOP-2/凝集素 II 的耗竭会激活正常受抑制的 RNA 聚合酶 II,从而不适当地转录 P 系中的体细胞基因。我们还提出证据表明,虽然 PIE-1 和 TOP-2/condensin II 都是 P 系基因组沉默所必需的,但在体细胞中错误表达时,PIE-1 可独立于 TOP-2/condensin II 而沉默转录。因此,在卵母细胞中,所有三个基因组沉默系统(TOP-2/condensin II、H3K9me 和 PIE-1)都能发挥作用,而在早期胚胎和饥饿的 L1s 中,三个系统中的两个都是活跃的。我们的数据表明,在秀丽隐杆线虫种系的不同发育阶段,多种冗余的基因组沉默机制以混合和匹配的方式抑制转录。
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来源期刊
G3: Genes|Genomes|Genetics
G3: Genes|Genomes|Genetics GENETICS & HEREDITY-
CiteScore
5.10
自引率
3.80%
发文量
305
审稿时长
3-8 weeks
期刊介绍: G3: Genes, Genomes, Genetics provides a forum for the publication of high‐quality foundational research, particularly research that generates useful genetic and genomic information such as genome maps, single gene studies, genome‐wide association and QTL studies, as well as genome reports, mutant screens, and advances in methods and technology. The Editorial Board of G3 believes that rapid dissemination of these data is the necessary foundation for analysis that leads to mechanistic insights. G3, published by the Genetics Society of America, meets the critical and growing need of the genetics community for rapid review and publication of important results in all areas of genetics. G3 offers the opportunity to publish the puzzling finding or to present unpublished results that may not have been submitted for review and publication due to a perceived lack of a potential high-impact finding. G3 has earned the DOAJ Seal, which is a mark of certification for open access journals, awarded by DOAJ to journals that achieve a high level of openness, adhere to Best Practice and high publishing standards.
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