Frontiers in Cell and Developmental Biology (Mar 2022)

Single-Cell Atlas of the Chinese Tongue Sole (Cynoglossus semilaevis) Ovary Reveals Transcriptional Programs of Oogenesis in Fish

  • Xiang Liu,
  • Xiang Liu,
  • Yingyi Huang,
  • Yingyi Huang,
  • Fujian Tan,
  • Fujian Tan,
  • Hong-Yan Wang,
  • Hong-Yan Wang,
  • Jian-Yang Chen,
  • Jian-Yang Chen,
  • Jian-Yang Chen,
  • Xianghui Zhang,
  • Xianghui Zhang,
  • Xiaona Zhao,
  • Xiaona Zhao,
  • Kaiqiang Liu,
  • Kaiqiang Liu,
  • Qian Wang,
  • Qian Wang,
  • Shanshan Liu,
  • Shanshan Liu,
  • Shanshan Liu,
  • Francesc Piferrer,
  • Guangyi Fan,
  • Guangyi Fan,
  • Changwei Shao,
  • Changwei Shao

DOI
https://doi.org/10.3389/fcell.2022.828124
Journal volume & issue
Vol. 10

Abstract

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Oogenesis is a highly orchestrated process that depends on regulation by autocrine/paracrine hormones and growth factors. However, many details of the molecular mechanisms that regulate fish oogenesis remain elusive. Here, we performed a single-cell RNA sequencing (scRNA-seq) analysis of the molecular signatures of distinct ovarian cell categories in adult Chinese tongue sole (Cynoglossus semilaevis). We characterized the successive stepwise development of three germ cell subtypes. Notably, we identified the cellular composition of fish follicle walls, including four granulosa cell types and one theca cell type, and we proposed important transcription factors (TFs) showing high activity in the regulation of cell identity. Moreover, we found that the extensive niche–germline bidirectional communications regulate fish oogenesis, whereas ovulation in fish is accompanied by the coordination of simultaneous and tightly sequential processes across different granulosa cells. Additionally, a systems biology analysis of the homologous genes shared by Chinese tongue sole and macaques revealed remarkably conserved biological processes in germ cells and granulosa cells across vertebrates. Our results provide key insights into the cell-type-specific mechanisms underlying fish oogenesis at a single-cell resolution, which offers important clues for exploring fish breeding mechanisms and the evolution of vertebrate reproductive systems.

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