Abstract
Oocyte maturation is the foundation for developing healthy individuals of mammals. Upon germinal vesicle breakdown, oocyte meiosis resumes and the synthesis of new transcripts ceases. To quantitatively profile the transcriptomic dynamics after meiotic resumption throughout the oocyte maturation, we generated transcriptome sequencing data with individual mouse oocytes at three main developmental stages: germinal vesicle (GV), metaphase I (MI), and metaphase II (MII). When clustering the sequenced oocytes, results showed that isoform-level expression analysis outperformed gene-level analysis, indicating isoform expression provided extra information that was useful in distinguishing oocyte stages. Comparing transcriptomes of the oocytes at the GV stage and the MII stage, in addition to identification of differentially expressed genes (DEGs), we detected many differentially expressed transcripts (DETs), some of which came from genes that were not identified as DEGs. When breaking down the isoform-level changes into alternative RNA processing events, we found the main source of isoform composition changes was the alternative usage of polyadenylation sites. With detailed analysis focusing on the alternative usage of 3′-UTR isoforms, we identified, out of 3,810 tested genes, 512 (13.7%) exhibiting significant switches of 3′-UTR isoforms during the process of moues oocyte maturation. Altogether, our data and analyses suggest the importance of examining isoform abundance changes during oocyte maturation, and further investigation of the pervasive 3′-UTR isoform switches in the transition may deepen our understanding on the molecular mechanisms underlying mammalian early development.
Highlights
The proper development of mammalian oocytes is crucial for females to provide high-quality eggs for the generation of new individuals, and improper oocyte maturation usually contributes to female infertility or unhealthy early embryos (Jose-Miller et al, 2007)
Oocyte maturation is the last stages of oocyte development, which typically refers to the dynamic process since the first meiotic resumption starting at oocyte germinal-vesicle breakdown (GVBD) (Pan and Li, 2019)
We conclude that rather than aggregating isoforms into gene loci, there is extra transcriptomic information contained in individual isoforms, useful for better understanding the dynamics in the transition from meiotic arrest to resumption during mouse oocyte maturation
Summary
The proper development of mammalian oocytes is crucial for females to provide high-quality eggs for the generation of new individuals, and improper oocyte maturation usually contributes to female infertility or unhealthy early embryos (Jose-Miller et al, 2007). Oocyte maturation is the last stages of oocyte development, which typically refers to the dynamic process since the first meiotic resumption starting at oocyte germinal-vesicle breakdown (GVBD) (Pan and Li, 2019). It has been shown in literature that the chromatin modification and remodeling in oocytes at the germinal vesicle (GV) stage are largely related to global transcriptional silence before entering meiotic resumption (De La Fuente, 2006). Genes related to meiosis I cell cycle process and mitochondrion organization degraded at the top speed during the GV to MII transition in mice (Zhao et al, 2020). With the degradation of such no-longer-needed transcripts, oocytes progressively get ready for fertilization and the sequential early embryonic development (Wu and Dean, 2020)
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