Single-cell profiling reveals transcriptome dynamics during bovine oocyte growth

Latorraca, LB; Galvao, A; Rabaglino, MB; D'Augero, JM; Kelsey, G; Fair, T

Abstract

Background Mammalian follicle development is characterized by extensive changes in morphology, endocrine responsiveness, and function, providing the optimum environment for oocyte growth, development, and resumption of meiosis. In cattle, the first signs of transcription activation in the oocyte are observed in the secondary follicle, later than during mouse and human oogenesis. While many studies have generated extensive datasets characterizing gene expression in bovine oocytes, they are mostly limited to the analysis of fully grown and matured oocytes. The aim of the present study was to apply single-cell RNA sequencing to interrogate the transcriptome of the growing bovine oocyte from the secondary follicle stage through to the mid-antral follicle stage. Results Single-cell RNA-seq libraries were generated from oocytes of known diameters (< 60 to > 120 mu m), and datasets were binned into non-overlapping size groups for downstream analysis. Combining the results of weighted gene co-expression network and Trendy analyses, and differently expressed genes (DEGs) between size groups, we identified a decrease in oxidative phosphorylation and an increase in maternal -genes and transcription regulators across the bovine oocyte growth phase. In addition, around 5,000 genes did not change in expression, revealing a cohort of stable genes. An interesting switch in gene expression profile was noted in oocytes greater than 100 mu m in diameter, when the expression of genes related to cytoplasmic activities was replaced by genes related to nuclear activities (e.g., chromosome segregation). The highest number of DEGs were detected in the comparison of oocytes 100-109 versus 110-119 mu m in diameter, revealing a profound change in the molecular profile of oocytes at the end of their growth phase. Conclusions The current study provides a unique dataset of the key genes and pathways characteristic of each stage of oocyte development, contributing an important resource for a greater understanding of bovine oogenesis.

Citation

Latorraca, L., Galvao, A., Rabaglino, M., D'Augero, J., Kelsey, G., & Fair, T. (2024). Single-cell profiling reveals transcriptome dynamics during bovine oocyte growth. BMC Genomics, 25(1), https://doi.org/10.1186/s12864-024-10234-0

• Journal Article Type: Article
• Acceptance Date: Mar 18, 2024
• Online Publication Date: Apr 6, 2024
• Publication Date: 2024
• Deposit Date: Apr 16, 2024
• Publicly Available Date: Apr 16, 2024
• Print ISSN: 1471-2164
• Publisher: BioMed Central
• Peer Reviewed: Peer Reviewed
• Volume: 25
• Issue: 1
• DOI: https://doi.org/10.1186/s12864-024-10234-0
• Keywords: Oogenesis; RNA sequencing; Gene Expression; Cattle; RNA-SEQ; FOLLICLE; ULTRASTRUCTURE; COMPETENCE; METABOLISM; COMPLEX; GENES