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Genomic identification, rapid evolution, and expression of Argonaute genes in the tilapia, Oreochromis niloticus

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Abstract

Argonaute proteins are key components of the small RNA-induced silencing complex and have multiple roles in RNA-directed regulatory pathways. Argonaute genes can be divided into two subfamilies: the Ago (interacting with microRNA/small interfering RNA) and Piwi subfamilies (interacting with piwi-interacting RNAs (piRNAs)). In the present study, genome-wide analyses firstly yielded the identification of different members of Agos and Piwis in the tilapia, coelacanth, spotted gar, and elephant shark. The additional teleost Ago3b was generated following the fish-specific genome duplication event. Selective pressure analysis on Agos and Piwis between cichlids and other teleosts showed an accelerated evolution of Piwil1 in the cichlid lineages, and the positive selected sites were located in the region of PIWI domain, suggesting that these amino acid substitutions are adapt to targeted cleavage of messenger RNA (mRNA) in cichlids. Ago1 and Ago4 were detected at higher levels at 5 days after hatching (dah) in both ovaries and testes compared with other stages, supporting the previously reported requirement of Ago-mediated pathways to clear the maternal mRNAs during the early embryogenesis. The Piwis were abundantly expressed in tilapia testes, indicating their essential roles in male germline, especially in spermatogenesis. Notable expression of Piwis was also detected in skeletal muscle, indicating that piRNA pathway may not only be confined to development and maintenance of the germline but may also play important roles in somatic tissues. The expression of Piwil1 and Piwil2 was examined by quantitative PCR (qPCR) and in situ hybridization (ISH) to validate the spatial and temporal expression profiles. Taken together, these results present a thorough overview of tilapia Argonaute family and provide a new perspective on the evolution and function of this family in teleosts.

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Acknowledgments

This work was supported by grants 31502147, 91331119, 31030063, and 31572609 from the National Natural Science Foundation of China; grant 2012CB723205 from the National Basic Research Program of China; grant 20130182130003 from the Specialized Research Fund for the Doctoral Program of Higher Education of China; grants cstc2013kjrc-tdjs80003 and cstc2014jcyjA80001 from the Natural Science Foundation Project of Chongqing, Chongqing Science and Technology Commission; and grants XDJK2016A003, XDJK2016B011, and XDJK2014B040 from the Fundamental Research Funds for the Central Universities.

Authors’ contributions

This study was designed by DSW and WJT and organized by DSW. JLC managed the experimental fish, HJS and LNS dissected the fish gonads, and WJT and JLC carried out RNA extractions. WJT, JLC, and LNS carried out the bioinformatics analyses. WJT, DSW, and HJS wrote the manuscript, and all authors critiqued the manuscript for important intellectual content. All authors read and approved the final manuscript.

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  1. Key Laboratory of Freshwater Fish Reproduction and Development (Ministry of Education), Key Laboratory of Aquatic Science of Chongqing, School of Life Science, Southwest University, 400715, Chongqing, People’s Republic of China

    Wenjing Tao, Lina Sun, Jinlin Chen, Hongjuan Shi & Deshou Wang

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  1. Wenjing Tao
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  2. Lina Sun
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  3. Jinlin Chen
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  4. Hongjuan Shi
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Correspondence to Deshou Wang.

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Communicated by Matthias Hammerschmidt

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Table S1

Accession numbers and genomic locations of vertebrate Argonaute genes. (XLS 38 kb)

Table S2

Accession numbers and genomic locations of cichlid Argonaute genes. (XLSX 11 kb)

Fig. S1

Synteny map comparing the orthologs of the Piwil1 gene locus and the genes flanking it in human, Coelacanth, chicken, clawed frog, spotted gar, fugu, tilapia and zebrafish. This map has been obtained by using the genome browser Genomicus. The genes (indicated by arrows) on the first line are from the reference species tilapia. The direction of arrows indicates the gene orientation only in this species. Orthologs of each gene in other species are shown in the same column. (GIF 49 kb)

High resolution image (TIFF 398 kb)

Fig. S2

Full amino acid sequences of Piwil. Solid lines indicate PIWI and PAZ domains. (GIF 457 kb)

High resolution image (TIFF 2.39 mb)

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Tao, W., Sun, L., Chen, J. et al. Genomic identification, rapid evolution, and expression of Argonaute genes in the tilapia, Oreochromis niloticus . Dev Genes Evol 226, 339–348 (2016). https://doi.org/10.1007/s00427-016-0554-3

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