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Differential Gene Expression Profiles and Alternative Isoform Regulations in Gill of Nile Tilapia in Response to Acute Hypoxia

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Abstract

Fish often encounters exposures to acute environmental hypoxia either spatially or temporally. Gill organ plays important roles in response to hypoxic stress in fish. Few studies focus on the molecular regulation mechanisms of gills under hypoxic stress. In this study, we investigated the transcriptomic response to 12-h acute hypoxia in gill of a hypoxia tolerant fish, Nile tilapia Oreochromis niloticus through RNA sequencing (RNA-Seq). We sequenced messenger RNA from three control samples and three hypoxia-treated samples. Bioinformatics analysis identified 239 differentially expressed genes (DEG) and 34 genes (DUES) that had significant differential alternative isoform regulation events in at least one exonic region in gill in response to acute hypoxia. The spatiotemporal expression analysis in five tissues (heart, liver, brain, gill, and spleen) sampled at three time points (6, 12, and 24 h) under hypoxia treatment confirmed the significant association of differential exon usages in two DUES genes (TLDC2 and SSX2IPA) with hypoxia conditions. Further functional analysis suggested several energy and immune response-related pathways, e.g., metabolic pathway and antigen processing and presentation, contained the most abundant DEG genes. We found that some GO biological processes for DEG genes were significantly enriched under hypoxic stress, such as glycolysis, metabolic process, generation of precursor metabolites and energy, and cholesterol metabolic process. Our findings suggest abundant differential gene expression changes and alternative isoform regulation events in genes involved in the hypoxia response in gill. Our results provide a basis for exploring the gene regulation mechanism under hypoxic stress in fish.

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Acknowledgements

We thank two anonymous reviewers for comments on the manuscript. This work was supported by the National Natural Science Foundation of China (No. 31572612), Natural Science Foundation of Guangdong Province, China (No. 2015A030313150), Special Fund for Marine Fisheries-Scientific Research of Guangdong Province (A201501A04), and Modern Agriculture Talents Support Program (2016–2020).

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  1. State Key Laboratory of Biocontrol, Institute of Aquatic Economic Animals and Guangdong Provincial Key Laboratory for Aquatic Economic Animals, College of Life Sciences, Sun Yat-Sen University, Guangzhou, 510275, People’s Republic of China

    Hong Lian Li, Hao Ran Lin & Jun Hong Xia

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  1. Hong Lian Li
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  2. Hao Ran Lin
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  3. Jun Hong Xia
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Contributions

JHX and HRL contributed to project conception. Experiment and data analysis was conducted by HLL. The manuscript was prepared by JHX and HLL. All authors read and approved the final manuscript.

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Correspondence to Jun Hong Xia.

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The authors declare that they have no competing interests.

Availability of Data and Materials Section

All protein and cDNA sequence files used in this study can be found in Additional files.

Electronic supplementary material

Supplementary Table S1

The summary information for the DEG genes identified in the gill samples in response to hypoxia. (XLSX 33 kb)

Supplementary Table S2

The summary information for the DUES genes identified in the gill samples in response to hypoxia. (XLSX 226 kb)

Supplementary Table S3

The qRT-PCR primer list for evaluation of the gene expression profiles in the gill samples. (XLSX 13 kb)

Supplementary Table S4

KEGG pathway analysis of the DEG genes in the gill samples in response to hypoxic stress. (XLSX 15 kb)

Supplementary Table S5

KEGG pathway analysis of the DUES genes in the gill samples in response to hypoxic stress. (XLSX 29 kb)

Supplementary Table S6

GO slimmer functional annotation of the DEG and DUES genes that identified in the gill samples in response to hypoxic stress. (XLSX 12 kb)

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Li, H.L., Lin, H.R. & Xia, J.H. Differential Gene Expression Profiles and Alternative Isoform Regulations in Gill of Nile Tilapia in Response to Acute Hypoxia. Mar Biotechnol 19, 551–562 (2017). https://doi.org/10.1007/s10126-017-9774-4

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