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Correlated expression of retrocopies and parental genes in zebrafish

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Abstract

Previous studies of the function and evolution of retrocopies in plants, Drosophila and non-mammalian chordates provided new insights into the origin of novel genes. However, little is known about retrocopies and their parental genes in teleosts, and it remains obscure whether there is any correlation between them. The present study aimed to characterize the spatial and temporal expression profiles of retrogenes and their parental genes based on RNA-Seq data from Danio rerio embryos and tissues from adult. Using a modified pipeline, 306 retrocopies were identified in the zebrafish genome, most of which exhibited ancient retroposition, and 76 of these showed a Ks < 2.0. Expression of a retrocopy is generally expected to present no correlation with its parental gene, as regulatory regions are not part of the retroposition event. Here, this assumption was tested based on RNA-Seq data from eight stages and thirteen tissue types of zebrafish. However, the result suggested that retrocopies displayed correlated expression with their parental genes. The level of correlation was found to decrease during embryogenesis, but to increase slightly within a tissue using Ks as the proxy for the divergence time. Tissue specificity was also observed: retrocopies were found to be expressed at a more specific level compared with their parental genes. Unlike Drosophila, which has sex chromosomes, zebrafish do not show testis-biased expression. Our study elaborated temporal and spatial patterns of expression of retrocopies in zebrafish, examined the correlation between retrocopies and parental genes and analyzed potential source of regulated elements of retrocopies, which lay a foundation for further functional study of retrocopies.

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Acknowledgments

We are thankful to Beide Fu and Ming Zou for their critical comments and suggestions.

Author information

Authors and Affiliations

  1. The Key Laboratory of Aquatic Biodiversity and Conservation of Chinese Academy of Sciences, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, 430072, Hubei, People’s Republic of China

    Zaixuan Zhong, Liandong Yang & Shunping He

  2. Key Laboratory of the Zoological Systematic and Evolution & State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Beijing, 100000, People’s Republic of China

    Yong E. Zhang

  3. University of Chinese Academy of Sciences, Beijing, 100039, People’s Republic of China

    Zaixuan Zhong, Liandong Yang & Yong E. Zhang

  4. Department of Biomedical Engineering, College of Life Science and Technology, Huazhong University of Science and Technology, Wuhan, 430074, Hubei, People’s Republic of China

    Yu Xue

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  1. Zaixuan Zhong
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  2. Liandong Yang
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  3. Yong E. Zhang
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  4. Yu Xue
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  5. Shunping He
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Corresponding author

Correspondence to Shunping He.

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Funding

This study was funded by the grants from Chinese Academy of Sciences (XDB13020100) and National Natural Science Foundation of China (91131014).

Conflict of interest

The authors declare that they have no competing interests.

Ethical approval

The methods involving animals in this study were conducted in accordance with the Laboratory Animal Management Principles of China. All experimental protocols were approved by the Ethics Committee of the Institute of Hydrobiology, Chinese Academy of Sciences.

Data access

The RNA-Seq data have been submitted to the NCBI Sequence Read Archive (SRA) with accession number SRR16957302. The retrocopies sequences have been submitted to Genbank (http://www.ncbi.nlm.nih.gov/genbank/) with accession number from KP324775 to KP324787.

Authors’ contributions

ZZ developed the algorithm, performed the analyses, and drafted the manuscript. LY participated in algorithm development. YZ participated in the design of the study and data analysis. SH conceived of the study, participated in its design and coordination, and helped to analyze the data. All authors read and approved the final manuscript.

Additional information

Communicated by J. Cerdá.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Results of RT-PCR. (TIFF 4176 kb)

Read quality and coverage of heart and brain (TIFF 3043 kb)

Frequency count of FPKM of intergenic region. (TIFF 2543 kb)

Four sources of regulatory elements for retrocopies (TIFF 704 kb)

FPKM values for zebrafish head, body and gonad of two sexes (TIFF 2127 kb)

The biological replicates analysis (DOCX 16 kb)

Retrocopies and their distributions of Ka, Ks, and ω. (XLS 55 kb)

Structures of the retrocopies. (XLS 61 kb)

Mean FPKM of intact retrocopies and retropseudogenes. (XLS 49 kb)

Primers used for RT-PCR. (XLS 25 kb)

List of Pearson coefficients. (XLS 51 kb)

Results of PAML. (XLS 80 kb)

Shannon entropy of retrocopies and parental genes (XLSX 19 kb)

Pearson coefficients of parental genes and promoter regions. (XLSX 18 kb)

A list of the 35 retrocopies which showed divergent expression with parental genes. (XLSX 11 kb)

11 pairs retrocopies with flcDNAs (XLSX 11 kb)

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Zhong, Z., Yang, L., Zhang, Y.E. et al. Correlated expression of retrocopies and parental genes in zebrafish. Mol Genet Genomics 291, 723–737 (2016). https://doi.org/10.1007/s00438-015-1140-5

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