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Gonadal lipidomics profile of an ovoviviparity teleost, black rockfish, during gonadal development

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Abstract

In order to study the variation of gonad lipidomics during reproductive cycle, black rockfish was employed as the research model in the present study. Using histology, lipidomics, and qPCR, the profile of gonad lipidomics and the expression levels of related genes during different developmental stages were detected and analyzed to show the potential regulatory network of lipid metabolism. Based on Ultra High-Performance Liquid Tandem Chromatography Quadrupole Time of Flight Mass Spectrometry (UHPLC-QTOFMS), four significant differential glycerophospholipid metabolic pathways including phosphatidylcholine (PC), phosphatidylethanolamine (PE), phosphatidylserine (PS), and phosphatidic acid (PA) were enriched by KEGG. Pathway-related enzyme-coding genes, including phosphatidylserine decarboxylase (pisd), phosphatidylserine synthase (ptdss1, ptdss2), and phospholipase D (pld1, pld2) were identified from the whole genome data and confirmed by cloning. The expression profiles of these genes were tested by qPCR in the tissues and gonads in developmental stages, and we found that pisd, pld, and ptdss genes were all downregulated through the developmental process in the brain of male, and the latter two genes were upregulated in the liver and testis at stage IV, which were the opposite trend observed in the female. Thus, our findings would be helpful in further understanding the substance metabolism and regulation during gonad development in ovoviviparity teleosts.

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The authors confirm that the data supporting the findings of this study are available within the article and its supplementary materials.

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Funding

This study was supported by the National Natural Science Foundation of China (41676126, 41976089) and the National Key R&D Program of China (2018YFD0901204). Our funding agencies did not play a role in the study design, data collection, analysis, interpretation of the data, or preparation of the manuscript.

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Authors and Affiliations

  1. Key Laboratory of Mariculture, Ministry of Education, Ocean University of China, Qingdao, People’s Republic of China

    Jianshuang Li, Haishen Wen, Ying Zhang, Yun Li, Likang Lyu, Xiaojie Wang & Xin Qi

  2. College of Animal Science, Inner Mongolia Agricultural University, Hohhot, Inner Mongolia, People’s Republic of China

    Min Song

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  1. Jianshuang Li
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Contributions

WHS, LY, and QX designed the study. SM performed the metabolome and qRT-PCR experiment. LLK, WXJ, ZY, SM, and LJS performed in samples collection. LJS wrote the manuscript, and QX provided manuscript editing and feedback. All authors read and approved the final manuscript.

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Correspondence to Xin Qi.

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Ethical approval

All procedures involved in dealing of fish in this study were approved by the Animal Research and Ethics Committees of the Ocean University of China (Permit Number: 20141201) prior to the initiation of the study. The studies did not involve endangered or protected species. And all experiments were performed in accordance with the Guidelines for the Care and Use of Laboratory Animals in China.

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Supplementary information

Supplementary figure 1:

Lipidomics profile of male black rockfish gonads during different gonadal stages. a,b total ion current chromatograms (TIC) of QC samples in positive and negative ion mode, respectively. c,d Score scatter plot of total samples PCA model in positive and negative ion mode, respectively. (PDF 361 kb)

Supplementary figure 2:

The multivariate data analysis between stage IV and III of testis. a,b Score plot of PCA analysis in positive and negative ion mode, respectively. c,d Score plot of OPLS-DA model in positive and negative ion mode. e,f Permutation test of OPLS-DA model in positive and negative ion mode, respectively. (PDF 2525 kb)

Supplementary figure 3:

The multivariate data analysis between stage V and IV of testis. a,b Score plot of PCA analysis in positive and negative ion mode, respectively. c,d Score plot of OPLS-DA model in positive and negative ion mode, respectively. e,f Permutation test of OPLS-DA model in positive and negative ion mode, respectively. (PDF 2539 kb)

Supplementary figure 4:

Lipidomics profile of female black rockfish gonads during different gonadal stages. a,b TIC of QC samples in positive and negative ion mode, respectively. c,d Score scatter plot of total samples PCA model in positive and negative ion mode, respectively. (PDF 1865 kb)

Supplementary figure 5:

The multivariate data analysis between stage IV and II of ovaries. a,b Score plot of PCA analysis in positive and negative ion mode, respectively. c,d Score plot of OPLS-DA model in positive and negative ion mode. e,f Permutation test of OPLS-DA model in positive and negative ion mode, respectively. (PDF 2453 kb)

Supplementary figure 6:

The multivariate data analysis between stage V and IV of ovaries. a,b Score plot of PCA analysis in positive and negative ion mode, respectively. c,d Score plot of OPLS-DA model in positive and negative ion mode, respectively. e,f Permutation test of OPLS-DA model in positive and negative ion mode, respectively. (PDF 2470 kb)

Supplementary figure 7:

Phylogenetic tree of gene. a, pld. b, ptdss. c, pisd. (PDF 1338 kb)

Supplementary figure 8:

Gene expression levels in different tissue. a,b pld. c,d ptdss. e, pisd. (PDF 282 kb)

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Li, J., Song, M., Wen, H. et al. Gonadal lipidomics profile of an ovoviviparity teleost, black rockfish, during gonadal development. Fish Physiol Biochem 47, 811–828 (2021). https://doi.org/10.1007/s10695-021-00936-7

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