Skip to main content
Download PDF

Volume 23 Supplement 1

The 20th International Conference on Bioinformatics (InCoB 2021): genomics

A time-course transcriptome analysis of gonads from yellow catfish (Pelteobagrus fulvidraco) reveals genes associated with gonad development

BMC Genomics volume 23, Article number: 409 (2022) Cite this article

Abstract

Background

The yellow catfish, Pelteobagrus fulvidraco, is a commercially important fish species. It is widely distributed in the fresh water areas of China, including rivers, lakes, and reservoirs. Like many other aquaculture fish species, people have observed significant size dimorphism between male and female yellow catfish and it shows a growth advantage in males.

Results

Here, at the first time, the time-course transcriptome was used to explore the various expression profiles of genes in different gonad developmental stages and genders. A total of 2696 different expression genes (DEGs) were identified from different stages. Based on these DEGs, 13 gonad development related genes were identified which showed time-specific or sex biased expression patterns.

Conclusion

This study will provide the crucial information on the molecular mechanism of gonad development of female and male yellow catfish. Especially, during the different gonad development stages, these 13 gonad development related genes exhibit various expression patterns in female and male individual respectively. These results could inspire and facilitate us to understanding the various roles of these genes play in different gonad development stages and genders.

Background

Yellow catfish, Pelteobagrus fulvidraco, has become an important freshwater variety in Chinese aquaculture (cite China Fishery Statistical Yearbook 2018). Because of its tender flesh, few inter-muscular spines, and delicious flavor, this fish becomes much more popular in China. Meanwhile, yellow catfish also has been regarded as an ideal model to research the sexual dimorphism, considering the significant different growth rates and maximum body sizes between female and male yellow catfish [1]. So, the studies of genetic mechanisms of sex dimorphism are crucial to yellow catfish. It is also benefited for yellow catfish aquaculture.

Gonad is the primary organ presenting morphological signs of sexual dimorphism. Thus, the studies of gonad development genes could provide valuable insights in studying sexual dimorphism [2]. To date, many gonad development genes have been identified for several fish species, including dmrt1 (double-sex and mab-3 related transcription factor 1) in half-tongue sole (Cynoglossus semilaevis), sdy (sexually dimorphic on the Y chromosome) in rainbow trout (Oncorhynchus mykiss), and amhr2 (anti-Muellerian hormone receptor type II) in tiger pufferfish (Takifugu rubripes) [3].

For yellow catfish, although several gonad development genes have been detected by previous studies, such as amhr2, gdf9 (growth and differentiation factor 9), cyp1a1 (cytochrome P450 1A1), cyp19a (cytochrome P450 19A), piwi (P-element induced wimpy testis like) and vasa [4,5,6]. The performance of different gonad development genes in various gonad development stages is still ambiguous for yellow catfish.

In order to obtain the various expression patterns of gonad development genes during the entire gonad development stages of yellow catfish. A time-course gonadal transcriptome of yellow catfish was generated with high-through sequencing. The DEGs were identified among different comparison groups. The further annotation of gonad development DEGs may help us to illuminate the mechanism involved in gonad development and sexual dimorphism.

Results

Overview of RNA-Seq results

In order to identify gonad development related genes in yellow catfish, the RNA-Seq was performed in all of sample groups. The data sets yielded from 8.54 Gbp to 16.38 Gbp and the average mapping rate for P. fulvidraco reference genome was 84.24%. The flowchart of processing steps in our pipeline is shown in Fig. 1. The sequencing results were listed in Table 1.

Fig. 1
figure 1

Flowchart of the pipeline used to a time-course transcriptome analysis of gonads from yellow catfish

Full size image
Table 1 Summary of the RNA-Seq data sets and the mapping ratios for all sample groups. Note: The sample names represent the different gonad development stages when the samples were collected. BG: before gonad differentiation; MG: male gonad differentiation; MGC: male gonad differentiation control; FG: female gonad differentiation; FGC: female gonad differentiation control; MAG: male after gonad differentiation; FAG: female after gonad differentiation
Full size table

Transcriptome assembly, annotation and Avaluation

Based on mapped reads, the time-coure transcriptome of P. fulvidraco was generated by Cufflinks. A total size of draft transcriptome was 271.25 Mbp including over 85,880 raw transcripts. In order to obtain a final assembly, two filter metrics were set, including the minor length is 150 bp and this transcript must express (FPKM > 0) at least in a group. The final assembly consisted of 41,329 transcripts. These transcripts were annotated via searching against the Nr, GO and KEGG database respectively. There were 34,273 transcripts corresponding to 16,861 genes, with an E-value cutoff less than 1e-5. A total number of 29,303 transcripts were assigned at least one GO term, corresponding to 14,637 genes. 14,223 transcripts were annotated into 344 KEGG pathways (Additional file 1). The Benchmarking Universal Single-Copy Orthologs (BUSCO) was used to estimate transcriptome completeness using the actinopterygii_odb9 BUSCO set [7]. Among all of (4584) BUSCO core genes, 3694 (80.6%) BUSCO core genes were identified in the yellow catfish transcriptome which suggested that this assembly was good enough to subsequent analysis.

Identification of gonad development related DEGs

According to the method, 2696 DEGs were identified from all of these comparison groups. For the different ovary development stages, several gonad development related DEGs were detected in Fig. 2A-C and Table 2. For example, for BG vs. FG, 447 DEGs were up-regulated including Aurka (aurora kinase A), cyp1a1, piwi, plk1 (polo-like kinase 1) and vasa. For FG vs. FGC, Aurka, cyp1a1, org (oogenesis-related isoform A), piwi, plk1 and vasa were significantly highly expressed in female individual (FG). Cyp1a1 was down-regulated in FG vs. FAG comparison group.

Fig. 2
figure 2

These volcano plots displayed the number of differentially expressed genes between the comparison libraries. A BG vs. FG comparison group; (B) FG vs. FGC comparison group; (C) FG vs. FAG comparison group; (D) BG vs. MG comparison group; (E) MG vs. MGC comparison group; (F) MG vs. MAG comparison group; (G) FAG vs. MAG comparison group; (H) a Venn diagram of all comparison groups

Full size image
Table 2 Gonad development related DEGs in yellow catfish
Full size table

For the different testis development stages, cyp1a1 was up-regulated in BG vs. MG. In the MG vs. MAG comparison group, amhr2, piwi and vasa showed higher expressed level in MAG. On the contrary, cyp1a1 showed higher expressed level in MG (Table 2).

Additionally, in the after gonad differentiation comparison group (FAG vs. MAG), bmp15, gdf9 and org were activated in ovary and sox9a was activated in testis. In sum up, there are 13 gonad development related DEGs were found from these comparison among different groups (Table 2).

GO and KEGG enrichment analysis of sex-related DEGs

To better understand the possible functions involved in gonad development of yellow catfish, the DEGs from each comparison group were enriched with the GO database. As a result, several gonad development related genes were enriched into go terms. For example, piwi and vasa were enriched in germ plasm cellular part for MG vs. MAG comparison group (Additional files 2 and 3).

Correspondingly, the KEGG pathway enrichment analysis was performed. In BG vs. FG comparison group, cyp1a1 was enriched in ovarian steroidogenesis pathway and plk1 was enriched in cell cycle pathway. For FG vs. FGC group, cyp1a1 was enriched in steroid hormone biosynthesis, plk1 and aurka were enriched in oocyte meiosis. Cyp1a1 was enriched in steroid hormone biosynthesis and ovarian steroidogenesis pathway for FG vs. FAG comparison group (Additional file 4).

Moreover, cyp1a1 was enriched in steroid hormone biosynthesis pathway for BG vs. MG comparison group. Aurka was enriched in oocyte meiosis pathway for MG vs. MGC. Cyp1a1 was also enriched in steroid hormone biosynthesis pathway for MG vs. MAG. Bmp15, gdf9 and org were enriched in cytokine-cytokine receptor interaction pathway for FAG vs. MAG (Additional file 4).

Time-course analysis of expression profiles of genes

We further clustered genes which exhibited the similar expression profiles in the entire gonad development stages of female and male respectively. Then, these clustered genes were annotated and enriched by GO and KEGG database (Additional files 5 and 6).

For female, BG, FG, MGC and FAG were considered as four different ovary development stages. Seven clusters were obtained from these results (Fig. 3A). In profile 15, aurka was enriched in nuclear part (Additional files 5 and 7). In profile 17, piwi and org were enriched in intracellular; vasa was enriched in organelle and intracellular organelle (Additional files 5 and 7).

Fig. 3
figure 3

Gene clustering in different gonad development stages. Each box corresponds to a model expression profile. For each box, the left top number represents the profile number, the right bottom number represents the contained genes number. Colored profiles have a statistically significant number of gene assigned. A Expression pattern of female gonad development stages. B Expression pattern of male gonad development stages

Full size image

For male, BG, FGC, MG and MAG were considered as four different gonad development stages. Six clusters were obtained from these time-course transcriptome analysis results (Fig. 3B). In profile 7, spata22 (spermatogenesis-associated protein 22), tex11 (testis-expressed sequence 11 protein) and tex15 (testis-expressed sequence 15 protein) were enriched in meiotic cell cycle and reproduction biological process (Additional files 5 and 8).

Verification of DEGs by RT-qPCR

Seven DEGs were randomly selected for RT-qPCR validation to verify the RNA-Seq results of time-course gonadal transcriptome. The primers used for these genes are listed in Table 3.

Table 3 PCR primers used in this study
Full size table

The expression profiles of these selected genes obtained from RT-qPCR corresponded to the RNA-Seq results (Fig. 4).

Fig. 4
figure 4

Validation of the expression patterns both in RNA-Seq (red) and RT-qPCR (blue). A BG vs. FG, (B) FG vs. FGC, (C) FG vs. FAG, (D) BG vs. MG, (E) MG vs. MGC, (F) MG vs. MAG, (G) FAG vs. MAG. Gene relative expression: log2(fold change). RT-qPCR fold changes is normalized by changes in beta-actin values. The averages of three relative quantities of biological replications were used in a two-tailed student’s t test with a 95% confidence level (P < 0.05) to determine the gene expression significance

Full size image

Discussion

In this work, a time-course gonadal transcriptome of yellow catfish was constructed with Illumina HiSeq 2000 sequencing technology. These results provided the valuable genetic resources to understand the mechanisms of gonad development and sexual dimorphism. A total of 2696 DEGs were obtained. Then, these DEGs were annotated and enriched by GO and KEGG databases. Time-course analysis were employed to detect the genes with similar expression profiles in female and male entire gonad development stages. Finally, 13 gonad development related genes were obtained from different gonad development stages of female and male yellow catfish (Table 2).

Cyp1a1 gene

Cyp1a1, a cytochrome P450 monooxygenase, involved in the metabolism of various endogenous substrates, including fatty acids, steroid hormones and vitamins [8,9,10,11]. Exhibits high catalytic activity for the formation of hydroxyestrogens from estrone (E1) and 17β-estradiol (E2) (Additional file 9). In this study, compare with BG, cyp1a1 was up-regulated in early gonad differentiation stage (Additional file 9). Then, this gene was enriched in ovarian steroidogenesis (for female) and steroid hormone biosynthesis pathway (for male). These results suggested that cyp1a1 may play a role in early gonad development through metabolizes steroid sex hormones (E1 and E2) in the gonad, and finally induces spermatogenesis and oogenesis.

Piwi and vasa genes

Additionally, the time-specific expression patterns of piwi and vasa were detected in BG vs. FG and MG vs. MAG comparison group. In details, the two gonad development related genes showed highly expression levels in the period of ovary differentiation (in FG) and testis after differentiation (in MAG) respectively. Piwi controls the number of primordial germ cells (PGCs) via protecting maternal mRNA from decay and adult germ stem cell division in Drosophila [12]. In zebrafish, piwi is required for maintaining germ cells, because loss of piwi leads to germ cell loss by apoptosis [13]. For medaka, piwi is required not only for determining the PGC number but also for controlling PGC migration [14]. Vasa (ATP-dependent RNA helicase DDX4) gene is a RNA helicase of the DEAD-box helicase family, which plays a crucial role in germ cell formation. Vasa is localized specifically in germline cells, indicating a particular function in gonads [15]. Differential expression of a vasa homolog in the gonads of tilapia (Oreochromis niloticus) during gametogenesis suggests a possible role for vasa in regulating the meiotic progression of male and female germ cells [16]. So, time-specific expression patterns of piwi and vasa might be suggested that these two genes played more important roles in both ovary differentiation and testis maintain.

Female-biased genes

According to our results, aurka was activated in early stage of ovary differentiation (Fig. 5A). Aurka, which is a centrosome-localized serine/threonine kinase crucial for cell cycle control, plays an important role in mitosis [17] and also regulates the meiotic cell cycle of Xenopus oocytes [18]. Meanwhile, plk1, which could be activated by aukra, was also up-regulated in FG (Fig. 5E). It has multiple regulatory roles in the cell cycle, including the control of cell cycle progression into mitosis [19]. These two genes were enriched in oocyte meiosis suggesting that aurka and plk1 may play roles in proliferation and differentiation during the early stage of ovary development.

Fig. 5
figure 5

Sexual biased genes and clustered sex-related genes were identified from this study. A-E These histograms showed the female-biased sex-related genes. F-G These two male-biased sex-related genes were displayed by histograms. H spata22, tex11 and tex15 show increasing expression from FGC to MAG

Full size image

In FAG vs. MAG comparison group, bmp15 and gdf9 displayed the significant highly expression only in FAG (Fig. 5B and C). Bmp15 and gdf9 are two closely related members of the TGF-β superfamily who can regulate granulosa cell development [20,21,22,23,24]. Specifically, zebrafish bmp15 mutants can initially develop as females. But during the juvenile stage, their sex revert to fertile males [21]. In our results, bmp15 and gdf9 had significantly higher expression levels in female after gonad differentiation. It is suggested that bmp15 and gdf9 may perform functions in maintaining the sexual phenotype of female yellow catfish.

Male-biased genes

Amhr2 and sox9a displayed the significant male-biased expression in male yellow catfish testis and they were up-regulated in MAG (Fig. 5F-G). Amh (anti-Muellerian hormone) is the gonadal hormone responsible for the regression of Mullerian ducts in male fetuses during mammalian embryogenesis [25, 26]. Amh signals through the amhr2 to regulate the differentiation and growth of target cells in mammals [27]. In fish, an amhr2 mutation results in a male-to-female sex change in XY medaka suggested that amhr2 is involved in sex determination [28]. Our laboratory have observed highly expression of sox9a in 1-year-old and 2-year-old yellow catfish testis. The present results consist with our previous studies which indicated that these two genes are not only important to testis differentiation but also are crucial to the maintenance and development of testis.

The clustered genes

Additionally, from the results of STEM, we found that spata22, tex11 and tex15 showed increased expressions from FGC to MAG (Fig. 5H). Spata22 is required early in meiotic prophase in both male and female germ cells [29]. Tex11 and tex15 display testis-specific expression which is required for meiotic recombination [30, 31].

Conclusions

Thanks for published high quality chromosome-level yellow catfish reference genome, a time-course gonadal transcriptome analysis was performed with cufflinks for yellow catfish to explore the mechanisms of gonad development and sexual dimorphism. A final assembly which consists of 41,329 transcripts was generated and annotated. GO and KEGG enrichment analysis and STEM cluster analysis revealed that all of 13 gonad development related genes were enriched in multiple go terms and pathways including meiotic cell cycle, reproduction biological process, ovarian steroidogenesis, steroid hormone biosynthesis, and oocyte meiosis pathway. These gonad development related genes showed various expression patterns. For example, cyp1a1 was up-regulated in gonad differentiation stages and enriched in ovarian steroidogenesis (in FG) or steroid hormone biosynthesis pathway (in MG). These results indicated that cyp1a1 may play a role in early gonad development through metabolizes steroid sex hormones (E1 and E2) in the gonad, and finally induces spermatogenesis and oogenesis. Moreover, piwi and vasa showed highly expression levels in ovary differentiation stage (FG) and after testis differentiation stage (MAG) respectively. It is suggested that these two genes may play an important role in ovary differentiation and testis maintaining. These results provided a reference for subsequent research on the mechanism of sexual dimorphism and sex control of yellow catfish.

Materials and methods

Samples and RNA extraction

Depended on previous studies, in yellow catfish, the gonad differentiation was observed at 13dph (day post-hatch) and 54 dph in females and males respectively [32, 33]. To compare the gene expression patterns of different gonad stages, a total of 42 full-sibling offsprings were sampled at before gonad differentiation (3dph), gonad differentiation (13dph for female and 54dph for male), and after gonad differentiation (90dph) respectively. Additionally, at female gonad differentiation stage, male individuals were collected into a control group (FGC). Similarly, at male gonad differentiation stage, female individuals were collected into a control group (MGC). All details of sampled groups were listed in Table 4.

Table 4 Summary of sampling and grouping from different gonad development stages
Full size table

The sex of each individual was confirmed by sex-linked marker as described previously [34]. Then, for each group, gonad tissues were sampled and pooled from 6 individuals to obtain enough total RNA and avoid individual variations. Total RNAs were extracted by Trizol method with manufacturer’s protocol (Ambion). The concentration and quality of each RNA sample were examined using a NanoDrop-2000 spectrophotometer (Thermo Scientific, Waltham, MA, USA). The RNA integrity was checked by ethidium bromide staining of 28S and 18S ribosomal bands on a 1% agarose gel.

Libraries construction and sequencing

Equal amounts of high-quality RNA samples were used to synthesize cDNA libraries. Briefly, mRNAs were purified from total RNAs and used as templates to synthesize the first-strand and the second-strand of cDNAs, according to the protocol of Super Script Double-Stranded cDNA Synthesis kit (Thermo Fisher Scientific, MA, USA). cDNAs were cut into short fragments following the TruSeq RNA sample preparation guide. After end repair and the addition of poly (A), the short fragments were ligated with sequencing adapters and enriched by PCR amplification to construct the cDNA library templates. Finally, transcriptome sequencing was performed using the Illumina HiSeq 2000 platform, which generated about 100-bp paired-end (PE) raw reads.

Sequence assembly and annotation

Raw reads were cleaned by removing the adaptor-containing sequences and low-quality reads. All clean reads were aligned and mapped using Tophat [35] to the published yellow catfish reference genome [36]. These mapped reads were subsequently used by Cufflinks [37] to generate non-redundant set of transcript contigs representing the transcriptome of yellow catfish. Cuffnorm was run on each group reads separately to estimate transcript abundance (read counts). Cuffdiff was then performed to differential expression analysis of 1) BG vs. FG; 2) BG vs. MG; 3) FG vs. FGC; 4) MG vs. MGC; 5) FG vs. FAG; 6) MG vs. MAG; and 7) FAG vs. MAG respectively. The considered thresholds of DEGs including p-value ≦ 0.05 and |log2 (fold change)| ≥ 1.

All assembled transcripts were annotated using several popular publicly available databases, including NCBI non-redundant protein sequences (Nr), Gene Ontology (GO) database [38] and Kyoto Encyclopedia of Genes and Genomes (KEGG) database [39] by using BLASTX [40] with a cut-off of E ≤ 1e-5, OmicsX, and KOBAS respectively. Combined with the results of annotation and enrichment of DEGs, two criteria were used to identify the gonad development related DEGs in yellow catfish: 1) the DEGs were enriched (p-value ≤0.05) in gonad related GO terms or KEGG pathways, such as ovarian steroidogenesis, reproduction biological process; 2) the DEGs were enriched in GO terms or KEGG pathways and reported by previous gonad development studies, such as gdf9 and vasa.

Gene expression during the developmental stages of gonad

Depended on the transcript abundance results produced by Cuffnorm, Short Time-series Expression Miner (STEM) [41] were employed to cluster these genes which exhibited the similar expression profiles in entire gonad development stages (from before gonad differentiation to after gonad differentiation stage) in female and male respectively. Genes were considered as having similar expression patterns which were clustered into a same cluster. The clustered profile with FDR value ≤0.05 were regarded as a valid cluster.

Real-time PCR verification

Seven randomly selected DEGs were validated by real-time quantitative PCR (RT-qPCR) to prove the reliability of RNA-seq results. The PrimerScript TM RT regent Kit with gDNA Eraser was used to cDNA synthesis following the manufacturer’s instructions. The primer information for these genes are available in Table 3. β-actin was employed as the endogenous reference gene. The qPCR mixture consisted of 10 μl of 2 × Master Mix, 1 μl of cDNA, 0.5 μl of each primer and 8 μl of ddH2O under the following conditions to collect fluorescence: denaturation at 95 °C for 30 min, followed by 40 cycles of amplification at 95 °C for 5 s and 60 °C for 40s. To establish the melting curve of the PCR product, the reaction was performed at 95 °C for 10s, 60 °C for 60s, and 95 °C for 15 s, after which it was slowly heated from 60 °C to 99 °C. The relative expression levels of target genes in each sample were individually determined using the 2-∆∆CT method [42].

Availability of data and materials

All datasets from the Illumina sequencing platform can be found in the Short Read Archive (SRA) database of the National Center for Biotechnology Information (NCBI) under accession number (PRJNA668564).

Abbreviations

BG:

Before gonad differentiation

BUSCO:

Benchmarking Universal Single-Copy Orthologs

DEG:

Different expression genes

FAG:

Female after gonad differentiation

FDR:

False discovery rate

FG:

Female gonad differentiation

FGC:

Female gonad differentiation control

GO:

Gene ontology

KEGG:

Kyoto Encyclopedia of Genes and Genomes

MAG:

Male after gonad differentiation

MG:

Male gonad differentiation

MGC:

Male gonad differentiation control

Nr:

Non-redundant protein sequences

PCR:

Polymerase chain reaction

RT-qPCR:

Real-time quantitative PCR

STEM:

Short time-series expression miner

References

  1. Mei J, Gui J-F. Sexual size dimorphism, sex determination, and sex control in yellow catfish. Sex Control Aquacult. 2018. Chapter 24:495–507.

  2. Siegfried KR. In search of determinants: gene expression during gonadal sex differentiation. J Fish Biol. 2010;76(8):1879–902.

    Article  CAS  Google Scholar 

  3. Kamiya T, Kai W, Tasumi S, Oka A, Matsunaga T, Mizuno N, et al. A trans-species missense SNP in Amhr2 is associated with sex determination in the tiger pufferfish, Takifugu rubripes (fugu). PLoS Genet. 2012;8(7):e1002798.

    Article  CAS  Google Scholar 

  4. Chen X, Mei J, Wu J, Jing J, Ma W, Zhang J, et al. A comprehensive transcriptome provides candidate genes for sex determination/differentiation and SSR/SNP markers in yellow catfish. Mar Biotechnol (NY). 2015;17(2):190–8.

    Article  CAS  Google Scholar 

  5. Lu J, Luan P, Zhang X, Xue S, Peng L, Sun X. Gonadal Transcriptomic Analysis of Yellow Catfish (Pelteobagrus fulvidraco): Identification of Sex-related Genes and Genetic Markers. Physiol Genomics. 2014;46:798–807.

    Article  Google Scholar 

  6. Lu J, Zheng M, Zheng J, Liu J, Liu Y, Peng L, et al. Transcriptomic analyses reveal novel genes with sexually dimorphic expression in yellow catfish (Pelteobagrus fulvidraco) brain. Marine Biotechnol (New York, NY). 2015;17(5):613–23.

    Article  CAS  Google Scholar 

  7. Simão FA, Waterhouse RM, Ioannidis P, Kriventseva EV, Zdobnov EM. BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics. 2015;31(19):3210–2.

    Article  Google Scholar 

  8. Kisselev P, Schunck W-H, Roots I, Schwarz D. Association of CYP1A1 polymorphisms with differential metabolic activation of 17beta-estradiol and estrone. Cancer Res. 2005;65(7):2972–8.

    Article  CAS  Google Scholar 

  9. Li D, Wang M, Cheng S, Zhang C, Wang Y, Zhang W, et al. CYP1A1 based on metabolism of xenobiotics by cytochrome P450 regulates chicken male germ cell differentiation. In Vitro Cell Dev Biol Anim. 2017;53(4):293–303.

    Article  CAS  Google Scholar 

  10. Sowers MR, Wilson AL, Kardia SR, Chu J, McConnell DS. CYP1A1 and CYP1B1 polymorphisms and their association with estradiol and estrogen metabolites in women who are premenopausal and Perimenopausal. Am J Med. 2006;119(9, Supplement 1):S44–51.

    Article  CAS  Google Scholar 

  11. Xu H, Zhang X, Ye Y, Li X. Bisphenol a affects estradiol metabolism by targeting CYP1A1 and CYP19A1 in human placental JEG-3 cells. Toxicol Vitro. 2019;61:104615.

    Article  CAS  Google Scholar 

  12. Lin H, Spradling AC. A novel group of pumilio mutations affects the asymmetric division of germline stem cells in the drosophila ovary. Development. 1997;124(12):2463.

    Article  CAS  Google Scholar 

  13. Houwing S, Kamminga LM, Berezikov E, Cronembold D, Girard A, van den Elst H, et al. A role for Piwi and piRNAs in germ cell maintenance and transposon silencing in zebrafish. Cell. 2007;129(1):69–82.

    Article  CAS  Google Scholar 

  14. Li M, Hong N, Gui J, Hong Y. Medaka piwi is essential for primordial germ cell migration. Curr Mol Med. 2012;12(8):1040–9.

    Article  Google Scholar 

  15. Hartung O, Forbes MM, Marlow FL. Zebrafish vasa is required for germ-cell differentiation and maintenance. Mol Reprod Dev. 2014;81(10):946–61.

    Article  CAS  Google Scholar 

  16. Kobayashi T, Kajiura-Kobayashi H, Nagahama Y. Differential expression of vasa homologue gene in the germ cells during oogenesis and spermatogenesis in a teleost fish, tilapia, Oreochromis niloticus. Mech Dev. 2000;99(1):139–42.

    Article  CAS  Google Scholar 

  17. Jeon H-Y, Lee H. Depletion of Aurora-A in zebrafish causes growth retardation due to mitotic delay and p53-dependent cell death. FEBS J. 2013;280(6):1518–30.

    Article  CAS  Google Scholar 

  18. Sarkissian M, Mendez R, Richter JD. Progesterone and insulin stimulation of CPEB-dependent polyadenylation is regulated by Aurora a and glycogen synthase kinase-3. Genes Dev. 2004;18(1):48–61.

    Article  CAS  Google Scholar 

  19. Medema RH, Lin C-C. Yang JC-H: polo-like kinase 1 inhibitors and their potential role in anticancer therapy, with a focus on NSCLC. Clin Cancer Res. 2011;17(20):6459.

    Article  CAS  Google Scholar 

  20. Clelland E, Kohli G, Campbell RK, Sharma S, Shimasaki S, Peng C. Bone morphogenetic Protein-15 in the zebrafish ovary: complementary deoxyribonucleic acid cloning, genomic organization, tissue distribution, and role in oocyte maturation. Endocrinology. 2006;147(1):201–9.

    Article  CAS  Google Scholar 

  21. Dranow DB, Hu K, Bird AM, Lawry ST, Adams MT, Sanchez A, et al. Bmp15 is an oocyte-produced signal required for maintenance of the adult female sexual phenotype in zebrafish. PLoS Genet. 2016;12(9):e1006323.

    Article  Google Scholar 

  22. Liu L, Ge W. Growth differentiation factor 9 and its spatiotemporal expression and regulation in the zebrafish Ovary1. Biol Reprod. 2007;76(2):294–302.

    Article  Google Scholar 

  23. McGrath-Morrow S, Esquela-Kerscher A, Lee S. Oocyte specific expression of growth differentiation factor-9. Mol Endocrinol (Baltimore, Md). 1995;9:131–6.

    Google Scholar 

  24. Dube JL, Wang P, Elvin J, Lyons KM, Celeste AJ, Matzuk MM. The bone morphogenetic protein 15 gene is X-linked and expressed in oocytes. Mol Endocrinol. 1998;12(12):1809–17.

    Article  CAS  Google Scholar 

  25. Behringer RR, Cate RL, Froelick GJ, Palmiter RD, Brinster RL. Abnormal sexual development in transgenic mice chronically expressing Müllerian inhibiting substance. Nature. 1990;345(6271):167–70.

    Article  CAS  Google Scholar 

  26. Pfennig F, Standke A, Gutzeit H. The role of Amh signaling in teleost fish - Multiple functions not restricted to the gonads. Gen Comp Endocrinol. 2015;223:87–107.

    Article  CAS  Google Scholar 

  27. Behringer RR, Finegold MJ, Cate RL. Müllerian-inhibiting substance function during mammalian sexual development. Cell. 1994;79(3):415–25.

    Article  CAS  Google Scholar 

  28. Morinaga C, Saito D, Nakamura S, Sasaki T, Asakawa S, Shimizu N, et al. The hotei mutation of medaka in the anti-Mullerian hormone receptor causes the dysregulation of germ cell and sexual development. Proc Natl Acad Sci U S A. 2007;104(23):9691–6.

    Article  CAS  Google Scholar 

  29. La Salle S, Palmer K, O'Brien M, Schimenti JC, Eppig J, Handel MA. Spata22, a novel vertebrate-specific gene, is required for meiotic progress in mouse germ cells. Biol Reprod. 2012;86(2):45.

    Article  Google Scholar 

  30. Boroujeni PB, Sabbaghian M, Totonchi M, Sodeifi N, Sarkardeh H, Samadian A, et al. Expression analysis of genes encoding TEX11, TEX12, TEX14 and TEX15 in testis tissues of men with non-obstructive azoospermia. JBRA Assist Reprod. 2018;22(3):185–92.

    Google Scholar 

  31. Yang F, Eckardt S, Leu NA, McLaughlin KJ, Wang PJ. Mouse TEX15 is essential for DNA double-strand break repair and chromosomal synapsis during male meiosis. J Cell Biol. 2008;180(4):673–9.

    Article  CAS  Google Scholar 

  32. YJCJoZ H. Sex differentiation in Pelteobagrus fulvidraco. Chin J Zool. 2008;43:103–8.

    Google Scholar 

  33. Li-Na P, Jian-Guo LU, Pei-Xian L, Yan-Long GE, Shu-Qun X, Xiao-Feng Z, et al. Observation on Gonadal Differentiation in Yellow Catfish Pelteobagrus fulvidraco. Chin J Fisheries. 2014;27(3):48–51.

    Google Scholar 

  34. Dan C, Mei J, Wang D, Gui J-F. Genetic differentiation and efficient sex-specific marker development of a pair of Y- and X-linked markers in yellow catfish. Int J Biol Sci. 2013;9(10):1043–9.

    Article  CAS  Google Scholar 

  35. Trapnell C, Pachter L, Salzberg SL. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics. 2009;25(9):1105–11.

    Article  CAS  Google Scholar 

  36. Gong G, Dan C, Xiao S, Guo W, Huang P, Xiong Y, et al. Chromosomal-level assembly of yellow catfish genome using third-generation DNA sequencing and Hi-C analysis. Giga Sci. 2018;7(11):giy120.

    Google Scholar 

  37. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, et al. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol. 2010;28(5):511–5.

    Article  CAS  Google Scholar 

  38. Young MD, Wakefield MJ, Smyth GK, Oshlack A. Gene ontology analysis for RNA-seq: accounting for selection bias. Genome Biol. 2010;11(2):R14.

    Article  Google Scholar 

  39. Kanehisa M, Araki M, Goto S, Hattori M, Hirakawa M, Itoh M, et al. KEGG for linking genomes to life and the environment. Nucleic Acids Res. 2008;36(suppl_1):D480–4.

    CAS  Google Scholar 

  40. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990;215(3):403–10.

    Article  CAS  Google Scholar 

  41. Ernst, Jason, and Ziv Bar-Joseph. "STEM: a tool for the analysis of short time series gene expression data". BMC bioinformatics. 2006;7(1):1-11.

  42. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods. 2001;25(4):402–8.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

Not applicable.

About this supplement

This article has been published as part of BMC Genomics Volume 23 Supplement 1, 2022: The 20th International Conference on Bioinformatics (InCoB 2021): genomics. The full contents of the supplement are available online at https://bmcgenomics.biomedcentral.com/articles/supplements/volume-23-supplement-1.

Funding

This work was supported by Guangzhou Science and Technology Project [No. 201803020017], National Natural Science Foundation of China [No. 31902427], Innovation Group Project of Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai) [No. 311020005] and Yellowfin Seabream Breeding System Construction [No. K20–42000-018].

The design of this study was supported by Guangzhou Science and Technology Project [No. 201803020017]. The collection, analysis, and interpretation of our data were supported by National Natural Science Foundation of China [No. 31902427] and Innovation Group Project of Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai) [No. 311020005]. And the writing of the manuscript was supported by Yellowfin Seabream Breeding System Construction [No. K20–42000-018]. Publication costs are funded by Innovation Group Project of Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai) [No. 311020005].

Author information

Authors and Affiliations

  1. School of Marine Sciences, Sun Yat-Sen University, Zhuhai, 519082, China

    Dong Gao, Junrou Huang, Genmei Lin & Jianguo Lu

  2. Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), Zhuhai, 519080, China

    Jianguo Lu

  3. Guangdong Provincial Key Laboratory of Marine Resources and Coastal Engineering, Guangzhou, 510275, Guangdong, China

    Jianguo Lu

  4. Pearl River Estuary Marine Ecosystem Research Station, Ministry of Education, Zhuhai, 519000, China

    Jianguo Lu

Authors
  1. Dong Gao
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Junrou Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Genmei Lin
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jianguo Lu
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

J. L. conceived the study. D. G., G. L., and J. H. collected the samples. D. G., G. L. and J. H. extracted the genomic DNA. D. G. performed bioinformatics analysis. D. G. and J. L. wrote, reviewed and edited the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Jianguo Lu.

Ethics declarations

Ethics approval and consent to participate

All procedures in our study including the handling and treatment of fish were approved by the Ethic Committee on the Care and Use of Laboratory Animals of Sun Yat-Sen University, Guangzhou, China.

Consent for publication

Not applicable.

Competing interests

The authors declare that we don’t have any commercial or associative interest that represents a conflict of interests in connection with the work submitted.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Additional file 1: Table S1.

Nr, GO and KEGG annotation results of the transcriptome.

Additional file 2: Fig. S1.

Bubble plot for the GO enrichment results of DEGs.

Additional file 3: Table S2.

GO enrichment results of the DEGs.

Additional file 4: Table S3.

KEGG enrichment results of the DEGs.

Additional file 5: Table S4.

GO enrichment results of the clustered genes which exhibit the similar expression profiles in female or male entire gonad development stages.

Additional file 6: Table S5.

KEGG enrichment results of the clustered genes which exhibit the similar expression profiles in female or male entire gonad development stages.

Additional file 7: Table S6.

Bubble plot for the GO enrichment results of gene clusters in female gonad development stages.

Additional file 8: Fig. S2.

Bubble plot for the GO enrichment results of gene clusters in male gonad development stages.

Additional file 9: Fig. S3.

Steroid hormone biosynthesis pathway. The heat map shows the expression of cyp1a1 (log2 (FPKM)) in different gonad development stages.

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Gao, D., Huang, J., Lin, G. et al. A time-course transcriptome analysis of gonads from yellow catfish (Pelteobagrus fulvidraco) reveals genes associated with gonad development. BMC Genomics 23 (Suppl 1), 409 (2022). https://doi.org/10.1186/s12864-022-08651-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1186/s12864-022-08651-0

Keywords

  • Time-course transcriptome
  • Sexual dimorphism
  • Gonad development

BMC Genomics

ISSN: 1471-2164

Contact us