Dataset Information

Transcriptome analysis to unravel the gene expression profile of ovarian follicular development in Magang goose.

ABSTRACT: Magang geese exhibit a unique characteristic of follicular development, with eight largest orderly arranged pre-ovulatory follicles in the abdominal cavity. However, little is known about the mechanisms underlying this follicular development. This study aimed to compare gene expression profiles of granulosa cells (GCs) at different stages of follicular development and provide comprehensive insights into follicle selection and the mechanisms underlying the well-defined follicle hierarchy in Magang geese. GCs of large white follicles (LWFs), small yellow follicles (SYFs), F8, F4, and F1 were used for RNA-seq analysis; 374, 1117, 791, and 593 genes were differentially expressed in stages LWFs to SYFs, SYFs to F8, F8 to F4, and F4 to F1, respectively, suggesting that these genes contribute to follicle selection and development. Reliability of sequencing data was verified through qPCR analysis of 24 genes. Gene Ontology and Kyoto Encyclopedia of Genes and Genomes pathways revealed a complex mechanism that remodels the extracellular matrix and turnover of extracellular matrix components in follicular development and ovulation and involves multiple pathway, such as focal adhesion, adherens junction, and extracellular matrix-receptor interaction. Some unique characteristics were observed during the different follicular development stages. For instance, some differentially expressed genes were enriched in progesterone-mediated oocyte maturation and steroid biosynthesis from stage SYFs to F8, whereas others were enriched in actin cytoskeleton regulation and vascular smooth muscle contraction from stage F4 to F1. These findings enhance our current understanding of GC function and ovarian follicles during the key stages of follicular development.

SUBMITTER: Lei M

PROVIDER: S-EPMC7470900 | biostudies-literature | 2020 Aug

REPOSITORIES: biostudies-literature

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Transcriptome analysis to unravel the gene expression profile of ovarian follicular development in Magang goose.

Lei Mingming M Chen Rong R Qin Qingming Q Zhu Huanxi H Shi Zhendan Z

The Journal of reproduction and development 20200411 4

Magang geese exhibit a unique characteristic of follicular development, with eight largest orderly arranged pre-ovulatory follicles in the abdominal cavity. However, little is known about the mechanisms underlying this follicular development. This study aimed to compare gene expression profiles of granulosa cells (GCs) at different stages of follicular development and provide comprehensive insights into follicle selection and the mechanisms underlying the well-defined follicle hierarchy in Magan ...[more]

PMID: 32281545

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Project description:In contrast to the situation in mammals, very little is known about the molecular mechanisms regulating early avian ovarian development. This study aimed to investigate the dynamic changes in the histomorphology as well as the genome-wide transcriptome and chromatin accessibility landscapes of the goose ovary during late embryonic and early post-hatching stages. Results from hematoxylin-eosin, periodic acid-Schiff, and anti-CVH immunohistochemical stainings demonstrated that programmed oocyte loss, oocyte nest breakdown and primordial follicle formation, and the primordial-to-secondary follicle transition occur during the periods from embryonic day 15 (E15) to post-hatching day 0 (P0), from P0 to P4, and from P4 to P28, respectively. RNA-seq and ATAC-seq analyses revealed dynamic changes in both the ovarian transcriptome and accessible chromatin landscapes during early ovarian development, exhibiting the most extensive changes during peri-hatching oocyte loss, and moreover, differences were also identified in the genomic distribution of the differential ATAC-seq peaks between different developmental stages, suggesting that chromatin-level regulation of gene expression is facilitated by modulating the accessibility of different functional genomic regions to transcription factors. Motif analysis of developmental stage-selective peak regions identified hundreds of potential cis-regulatory elements that contain binding sites for many transcription factors, including SF1, NR5A2, ESRRβ, NF1, and THRβ, as well as members of the GATA, SMAD, and LHX families, whose expression fluctuated throughout early goose ovarian development. Integrated ATAC-seq and RNA-seq analysis suggested that the number and genomic distribution of the newly appeared and disappeared peaks differed according to developmental stage, and in combination with qRT-PCR validation potentiated the critical actions of the DEGs enriched in cell cycle, MAPK signaling, and FoxO signaling pathways during peri-hatching oocyte loss and those in ligand-receptor interaction, tissue remodeling, lipid metabolism, and Wnt signaling during primordial follicle formation and development. In conclusion, our study provides a framework for understanding the transcriptome and accessible chromatin dynamics during early avian ovarian development and a new avenue to unravel the transcriptional regulatory mechanisms that facilitate the occurrence of relevant molecular events.

Project description:BACKGROUND: Egg laying in Magang geese is characterized by extended interruption between clutches and lowing laying rate. Both the ovarian follicular development and ovulation characteristics, and the associated endocrine and molecular regulatory mechanisms involved are poorly understood, but could be important for guiding development of molecule aided selection of egg laying performances in geese. This study, therefore, recorded egg-laying characteristics of Magang geese, and the endocrine and molecular regulatory mechanisms of ovarian follicular development, maturation, and ovulation in Magang geese. METHODS: Oviposition, ovarian follicle development, and reproductive hormone and gene expression profiles were observed in a small flock of Magang geese. RESULTS: Greater than 73% of eggs were laid during the day. The average oviposition interval was 46.8 h (36-55 h). It took approximately 18 days for large white follicles to develop into mature F1 follicles; follicular growth was exponential. LHR expression levels increased from the small to the large mature follicles, but FSHR expression decreased in the granulosa and thecal layers. As the follicles matured, inhibin alpha and inhibin betaA expression increased in the granulosa layer. Activin IR, activin IIRA, activin IIRB, and beta-glycan expressions also increased as the follicles increased in size, but were more abundantly expressed in the thecal than in the granulosa layers. During the oviposition cycle, plasma concentrations of gonadal hormones decreased rapidly, whereas the level of PGFM peaked around ovulation. The profiles of activin, inhibin, follistatin, estradiol, and progesterone leading to ovulation were characterized. CONCLUSIONS: The molecular and endocrine mechanisms that regulate follicular development in Magang geese are similar to those in chickens. Moreover, gonadotropin regulation and interaction between activin, inhibin, and follistatin secretion may govern 3-stage maturation in the final preovulatory follicles in Magang geese. The rapid rebound of post-ovulatory secretions of inhibin and follistatin may inhibit recruitment of new SYF recruitment once a sequence of eggs is started, and may limit the egg clutch size to no more than the number of LYFs present before the first sequence egg.

Project description:This study sought to understand the regulation mechanism of OPN5 through the TSH-DIO2/DIO3 pathway mediated photoperiod on the breeding activity of short-day breeding birds. In this study, the reproductive activity of Magang goose was regulated by artificial light, and the reproductive activity of the ganders were determined according to the daily laying rate of female geese. The testicular development and the serum reproductive hormone concentrations of ganders were measured during the reproductive period (d 0), the reproductive degeneration period (d 13 and 27) and the resting period (d 45). The mRNA and protein expression patterns of OPN5, the HPG axis reproductive genes, and TSH-DIO2/DIO3 pathway related genes were examined. Results showed that the laying rate of geese and the gonadal indices (GSI) decreased gradually after the photoperiod increased. Histological observation found that the spermatogenic function of the testis was normal on d 0 and 13, while degeneration occurred by d 27 and 45. Serum testosterone, FSH, and LH concentration showed a slight increase on d 13, followed by a sharp decrease on d 27 and 45 (P < 0.01), while PRL concentrations were low on d 0 and 13, and increased rapidly on d 27 and 45 (P < 0.01).The expression pattern of GnRH, FSH, LH, and THRβ mRNA were similar, with high levels on d 0 and 13 and a decreasing trend on d 27 and 45 (P < 0.05 or P < 0.01); and GnRHR mRNA levels were higher on d 13 (P < 0.05), but then had decreased by d 27 and 45 (P < 0.01). The expression pattern of GnIH and GnIHR was similar, which was opposite to that of GnRHR. VIP, PRL, and PRLR increased gradually and peaked on d 45 (P < 0.01). The expression trend of TRH, TSHβ, and DIO2 was similar to that of GnRHR, and the expression abundance increased on d 13, and then decreased on d 27 and 45. GnRH protein expression was significantly higher than during the other 3 periods (P < 0.01) while the GnIH protein levels were extremely low on d 0, had gradually increased by d 13, and significantly increased by d 27 and 45 (P < 0.01). The protein expression trends of THR and DIO2 were similar to that of GNIH. DIO3 protein expression was low on d 0 and 13, and increased by d 27 and 45. These results suggest that when the photoperiod increased, the hypothalamus OPN5 gene and protein were upregulated and the pituitary TSHβ, TSHR, and hypothalamus THRβ, TRH, and DIO2 were downregulated, and thus the reproductive activity of geese was inhibited.

Project description:In contrast to the later stages of follicle development, little is known about the characteristics and mechanisms associated with early folliculogenesis in avian species. The objectives of the present study were to examine and compare the histomorphological and molecular changes of primordial, primary, and secondary follicles from duck and goose ovaries during the first 6 post-hatching week. Morphological analysis showed that the length and width of both duck and goose ovaries increased steadily during weeks 1 to 5 but increased acutely at week 6, whereas a greater increment was observed in the ovarian length of ducks than that of geese during weeks 4 to 5. Furthermore, smaller diameters of the 3 categories of follicles were observed in ducks than those in geese at the first appearance, but they reached a similar size at week 6. More importantly, secondary follicles were found in the ovaries of ducks 1 wk earlier than in those of geese. These results indicated a more rapid growth rate for ovarian follicles in ducks than in geese during early post-hatching development. At the molecular level, it was found that the mRNAs encoding follicle stimulating hormone receptor (FSHR), anti-Müllerian hormone (AMH), B-cell leukemia/lymphoma 2, and cysteine-dependent aspartate specific protease 3 (CASPASE3) were ubiquitously expressed in all ovarian follicles of ducks and geese with different expression profiles in each follicular category during the first 6 post-hatching week. Notably, transcript levels of FSHR, AMH, and CASPASE3 changed differently between ducks and geese during weeks 5 to 6, which was postulated to be one of the mechanisms inducing more rapid growth of ovarian follicles in ducks rather than in geese. In conclusion, our results revealed, for the first time, differences in early folliculogenesis, including the rate of growth of each follicular category and the timing of transition of primary to secondary follicles, between ducks and geese, and these differences could result from different expression profiles of FSHR, AMH, and CASPASE3 during early post-hatching development.

Dataset Information

Transcriptome analysis to unravel the gene expression profile of ovarian follicular development in Magang goose.

Publications

Transcriptome analysis to unravel the gene expression profile of ovarian follicular development in Magang goose.

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