Multipathway synergy promotes testicular transition from growth to spermatogenesis in early-puberty goats

Abstract

Background The microscopic process of postnatal testicular development in early-puberty animals is poorly understood. Therefore, in this study, 21 male Yiling goats with average ages of 0, 30, 60, 90, 120, 150 and 180 days old (each age group comprised three goats) were used to study the changes in organs, tissues and transcriptomes during postnatal testicle development to obtain a broad and deep insight into the dynamic process of testicular transition from growth to spermatogenesis in early-puberty animals. Results The inflection point of testicular weight was at 119 days postpartum (dpp), and the testicular weight increased rapidly from 119 dpp to 150 dpp. Spermatozoa were observed in the testis at 90 dpp by using haematoxylin–eosin staining. We found from the transcriptome analysis of testes that the testicular development of Yiling goat from birth to 180 dpp experienced three stages, namely, growth, transition and spermatogenesis stages. The goats in the testicular growth stage (0–60 dpp) showed a high expression of growth-related genes in neurogenesis, angiogenesis and cell junction, and a low expression of spermatogenesis-related genes. The goats aged 60–120 dpp were in the transitional stage which had a gradually decreased growth-related gene transcription levels and increased spermatogenesis-related gene transcription levels. The goats aged 120–180 dpp were in the spermatogenesis stage. At this stage, highly expressed spermatogenesis-related genes, downregulated testicular growth- and immune-related genes and a shift in the focus of testicular development into spermatogenesis were observed. Additionally, we found several novel hub genes, which may play key roles in spermatogenesis, androgen synthesis and secretion, angiogenesis, cell junction and neurogenesis. Moreover, the results of this study were compared with previous studies on goat or other species, and some gene expression patterns shared in early-puberty mammals were discovered. Conclusions The postnatal development of the testis undergoes a process of transition from organ growth to spermatogenesis. During this process, spermatogenesis-related genes are upregulated, whereas neurogenesis-, angiogenesis-, cell junction-, muscle- and immune-related genes are downregulated. In conclusion, the multipathway synergy promotes testicular transition from growth to spermatogenesis in early-puberty goats and may be a common rule shared by mammals.

Expression of Cell Proliferation Regulatory Factors Bricd5, Tnfrsf21, Cdk1 Correlates With Expression of Clock Gene Cry1 in Testis of Hu Rams During Puberty

“…The rapid development of spermatogenic cells in testis during the first estrus has also been observed in other animals. At the onset of puberty (90 days old), large cross-sectional seminiferous tubules, thick spermatogenic epithe lial cells and obvious sperm were observed [19], which was consistent with our observation in Hu sheep. The results showed that there were differences in the estrus stage among different breeds.…”

“…Go enrichment analysis by Panther website(http://geneontology.org/). Cattle (Bos taurus) gene bank with high homology with sheep was selected as the template, and the results of enrichment retained the genes with FDR value less than 0.05 significant enrichment [19]. Ggplot2 package of R language is used to draw go enrichment analysis results for visualization.…”

Accelerating Onset of Puberty Through Modification of Early Life Nutrition Induces Modest but Persistent Changes in Bull Sperm DNA Methylation Profiles Post-puberty

“…Together with our results, these reports indicate that ATP10A and SRGAP3, as putative candidate genes for sexual precocity, are regulated not only by genetic factors but also by environmental and epigenetic factors. The second compelling piece of evidence for the involvement of the differentially methylated genes in sexual maturity of HM bulls is provided by a study using Yiling goats, a native Chinese breed exhibiting precocious puberty, as a model to investigate the changes in the testis transcriptome that parallel the post-natal development of testis (Bo et al, 2020). In that study, 120 days of age was identified as the transition point at which testis weight dramatically increases and spermatogenesis becomes functional in Yiling goats; two genes targeted by differential methylation in our study, ALDOB and PIGR, are listed as "hub genes" whose expression is modified during this transition.…”

“…In that study, 120 days of age was identified as the transition point at which testis weight dramatically increases and spermatogenesis becomes functional in Yiling goats; two genes targeted by differential methylation in our study, ALDOB and PIGR , are listed as “hub genes” whose expression is modified during this transition. Although not listed as “hub genes” by Bo et al (2020) , we identified several genes involved in spermatid differentiation or highly expressed post-meiotically, such as RARB , ADCY8 , and OSBP2 (relevant references are provided in Supplementary Table 9 ). We also identified many differentially methylated genes involved in cytoskeleton remodeling, cilium growth and cell junction, such as ACTN1 , GSN , MTMR7 , PACRG , TUBB2B , and ARC .…”

Identification of Genes Targeted in South African Merino and Afrino Sheep Populations Under Long-Term Selection for Reproduction and Body Weight

“…Apart from being classi ed under the GO "Development processes" in the Afrino gene DAVID analysis, "Sperm capacitation" is another GO biological process of the BSPH1 gene [25] (https://david.ncifcrf.gov/). The HDAC9 gene was downregulated in 90-day old male goat kids and this was conducive to the vigorous development of spermatogenesis in this period [55] (Bo et al, 2020). TRPM8 is a testosterone receptor [56,57] (Asuthkar et al, 2015a; Asuthkar et al, 2015b) and TRPM8 channels may be implicated in various physiological processes regulated by androgens [58] (Sutton et al, 2018).…”