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Transcriptome Profiling and Analysis of Genes Associated with High Temperature–Induced Masculinization in Sex-Undifferentiated Nile Tilapia Gonad

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Abstract

Artificially high temperatures during critical thermosensitive periods (TSPs) can induce the sex reversal of Nile tilapia (Oreochromis niloticus) females into pseudomales; Nile tilapia is a GSD + TE (genotypic plus temperature effects) fish species. Previous studies have shown that water temperature affects the expression levels of many genes in the gonad or brain in various teleost species. However, few studies on the effect of temperature at the whole-gonad transcriptomic level in the early stage of sex differentiation have been reported in fish species exhibiting GSD + TE. In this study, RNA-Seq was performed to characterize the transcriptomic profile and identify genes exhibiting temperature- and sex-biased expressions in the Nile tilapia gonad at 21 dpf. A total of 42 genes were found to be associated with both high-temperature treatment and sex development, as the expression levels of these genes differed in both FC (female control) vs MC (male control) and FC vs FT (high temperature–treated females in the TSP). Among these genes, the transcriptional alterations of many male sex determination and differentiation genes, such as Dmrt1, Gsdf, and the DNA damage-inducible protein GADD45 alpha, suggested that the male pathway is initiated after high-temperature treatment and that its initiation may play a role in high temperature–induced masculinization in Nile tilapia. The qRT-PCR validation results for thirteen differentially expressed genes showed that the Pearson’s correlation of the log10 fold change values between the qPCR and RNA-Seq results was 0.70 (p < 0.001), indicating the accuracy and reliability of the RNA-Seq results. Our study provides insights into how high-temperature treatment induces the sex reversal of Nile tilapia females.

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Data Availability

All data accompanying these experiments have been deposited in Sequence Read Archive (SRA) (https://www.ncbi.nlm.nih.gov/sra); the accession number for our submission is SRP221530.

Abbreviations

dmrt1 :

Doublesex and mab-3-related transcription factor 1

Mb :

Myoglobin

Gadd45a :

Growth arrest and DNA damage-inducible protein GADD45 alpha isoform X1

Cbx7 :

Chromo domain-containing protein cec-1

gsdf :

Growth/differentiation factor 6-B-like

rtbdn :

Retbindin

ch25h :

Cholesterol 25-hydroxylase

htr1e :

5-Hydroxytryptamine receptor 1E

spp120 :

Seminal plasma glycoprotein 120

nr0b2 :

Nuclear receptor subfamily 0 group B member 2

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Acknowledgments

We thank Guangzhou Genedenovo Biotechnology Co., Ltd. for assisting in the sequencing and bioinformatics analysis.

Funding

This study was supported by grants from the National Natural Science Foundation of China (31902349; 31472270) and the Natural Science Foundation of Shandong Province (ZR2018MC030) and funds from the Shandong “Double Tops” Program.

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  1. Jan Teng and Yan Zhao contributed equally.

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  1. Shandong Provincial Key Laboratory of Animal Biotechnology and Disease Control and Prevention, Shandong Agricultural University, Daizong Street 61, Tai’an, Shandong, China

    Jian Teng, Yan Zhao, Hong Ju Chen, Hui Wang & **ang Shan Ji

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  1. Jian Teng
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Contributions

**ang Shan Ji conceived and designed the experiments. Jian Teng performed the experiments. Jian Teng, Yan Zhao, and Hong Ju Chen analyzed the data. Jian Teng and Yan Zhao wrote the paper.

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Correspondence to **ang Shan Ji.

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Animal experiments were approved by the Shandong Agricultural University Animal Care and Use Committee under approval number SDAUA-2015-017. Many efforts were made to reduce the suffering of Nile tilapia.

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Teng, J., Zhao, Y., Chen, H.J. et al. Transcriptome Profiling and Analysis of Genes Associated with High Temperature–Induced Masculinization in Sex-Undifferentiated Nile Tilapia Gonad. Mar Biotechnol 22, 367–379 (2020). https://doi.org/10.1007/s10126-020-09956-5

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