Gene expression dynamics during the gonocyte to spermatogonia transition and spermatogenesis in the domestic yak

Guowen Wang; Yongchang Li; Qilin Yang; Shangrong Xu; Shike Ma; Rongge Yan; Ruina Zhang; Gongxue Jia; Deqiang Ai; Qi'en Yang

doi:10.1186/s40104-019-0360-7

Gene expression dynamics during the gonocyte to spermatogonia transition and spermatogenesis in the domestic yak

J Anim Sci Biotechnol. 2019 Jul 12:10:64. doi: 10.1186/s40104-019-0360-7. eCollection 2019.

Authors

Guowen Wang^#^{1

2}, Yongchang Li^#^{1

2}, Qilin Yang³, Shangrong Xu⁴, Shike Ma⁴, Rongge Yan^{1

2}, Ruina Zhang¹, Gongxue Jia¹, Deqiang Ai⁵, Qi'en Yang^{1

6

7}

Affiliations

¹ 1Key Laboratory of Adaptation and Evolution of Plateau Biota, Northwest Institute of Plateau Biology, Chinese Academy of Sciences, Xining, 810000 Qinghai China.
² 2University of Chinese Academy of Sciences, Beijing, 100049 China.
³ 3Department of Veterinary Sciences, Qinghai Vocational and Technical Institute of Animal Husbandry and Veterinary, Qinghai University, Xining, 810016 China.
⁴ 4Qinghai Academy of Animal Science and Veterinary Medicine, Qinghai University, Xining, 810016 China.
⁵ Animal Husbandry Technology Extension Station of Qinghai Province, Xining, 810001 Qinghai China.
⁶ 6Qinghai Key Laboratory of Animal Ecological Genomics, Northwest Institute of Plateau Biology, Chinese Academy of Sciences, Xining, 810001 Qinghai China.
⁷ 7CAS Center for Excellence in Tibetan Plateau Earth Sciences, Chinese Academy of Sciences, Beijing, 100101 China.

^# Contributed equally.

Abstract

Background: Spermatogenesis is a cellular differentiation process that includes three major events: mitosis of spermatogonia, meiosis of spermatocytes and spermiogenesis. Steady-state spermatogenesis relies on functions of spermatogonial stem cells (SSCs). Establishing and maintaining a foundational SSC pool is essential for continued spermatogenesis in mammals. Currently, our knowledge about SSC and spermatogenesis is severely limited in domestic animals.

Results: In the present study, we examined transcriptomes of testes from domestic yaks at four different stages (3, 5, 8 and 24 months of age) and attempted to identify genes that are associated with key developmental events of spermatogenesis. Histological analyses showed that the most advanced germ cells within seminiferous tubules of testes from 3, 5, 8 and 24 months old yaks were gonocytes, spermatogonia, spermatocytes and elongated spermatids, respectively. RNA-sequencing (RNA-seq) analyses revealed that 11904, 4381 and 2459 genes were differentially expressed during the gonocyte to spermatogonia transition, the mitosis to meiosis transition and the meiosis to post-meiosis transition. Further analyses identified a list of candidate genes than may regulate these important cellular processes. CXCR4, a previously identified SSC niche factor in mouse, was one of the up-regulated genes in the 5 months old yak testis. Results of immunohistochemical staining confirmed that CXCR4 was exclusively expressed in gonocytes and a subpopulation of spermatogonia in the yak testis.

Conclusions: Together, these findings demonstrated histological changes of postnatal testis development in the domestic yak. During development of spermatogonial lineage, meiotic and haploid germ cells are supported by dynamic transcriptional regulation of gene expression. Our transcriptomic analyses provided a list of candidate genes that potentially play crucial roles in directing the establishment of SSC and spermatogenesis in yak.

Keywords: Gonocyte; Meiosis; Spermatogenesis; Spermatogonia; Transcriptome.