Identification of candidate piRNAs in the gonads of Paralichthys olivaceus (Japanese flounder)

Chun-Lei WANG; Zhi-Peng WANG; Jia-Qi WANG; Ming-You Li; Xiao-Wu CHEN

doi:10.13918/j.issn.2095-8137.2016.5.301

Volume 37 Issue 5

Sep. 2016

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Article Navigation > Zoological Research > 2016 > 37(5): 301-306

Chun-Lei WANG, Zhi-Peng WANG, Jia-Qi WANG, Ming-You Li, Xiao-Wu CHEN. Identification of candidate piRNAs in the gonads of Paralichthys olivaceus (Japanese flounder). Zoological Research, 2016, 37(5): 301-306. doi: 10.13918/j.issn.2095-8137.2016.5.301

Citation:

Chun-Lei WANG, Zhi-Peng WANG, Jia-Qi WANG, Ming-You Li, Xiao-Wu CHEN. Identification of candidate piRNAs in the gonads of Paralichthys olivaceus (Japanese flounder). Zoological Research, 2016, 37(5): 301-306. doi: 10.13918/j.issn.2095-8137.2016.5.301

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Identification of candidate piRNAs in the gonads of Paralichthys olivaceus (Japanese flounder)

doi: 10.13918/j.issn.2095-8137.2016.5.301

Key Laboratory of Exploration and Utilization of Aquatic Genetic Resources, Ministry of Education, Shanghai Ocean University, Shanghai 201306, China

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Corresponding author: Xiao-Wu CHEN
Received Date: 2016-04-08
Rev Recd Date: 2016-09-05
Publish Date: 2016-09-18

Abstract

Abstract

Piwi-interacting RNA (piRNA) plays an important role in the gonadal development and maintenance of Teleostei. In this study, piRNA libraries derived from the adult gonads of Japanese flounder (Paralichthys olivaceus) were generated using next-generation sequencing technology. Using zebrafish piRNAs as a reference, 5 865 unique candidate piRNAs were identified; 289 candidate piRNA clusters (PRCs) were generated from the above piRNAs. Among the isolated candidate PRCs, a total of 38 ovary-specific, 45 ovary-bias, 24 testis-specific, and 131 testis-bias PRCs were found. The relative expression levels of seven PRCs were validated through quantitative reverse transcription-polymerase chain reaction. The results of this study will help facilitate exploration of the development and maintenance of the phenotypic sex mechanism in P. olivaceus.
- Paralichthys olivaceus,
- Ovary,
- Testis,
- piRNA

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References(38)

References

[1]	Anders S, McCarthy DJ, Chen YS, Okoniewski M, Smyth GK, Huber W, Robinson MD. 2013. Count-based differential expression analysis of RNA sequencing data using R and bioconductor. Nature Protocols, 8(9): 1765-1786.
[2]	Aquila S, Montanaro D, Guido C, Santoro M, Perrotta I, Gervasi S, De Amicis F, Lanzino M. 2015. Human sperm molecular anatomy: The enzyme 5α-reductase (SRD5A) is present in the sperm and may be involved in the varicocele-related infertility. Histochemistry and Cell Biology, 144(1): 67-76.
[3]	Aravin AA, Hannon GJ, Brennecke J. 2007. The Piwi-piRNA pathway provides an adaptive defense in the transposon arms race. Science, 318(5851): 761-764.
[4]	Aravin A, Gaidatzis D, Pfeffer S, Lagos-Quintana M, Landgraf P, Iovino N, Morris P, Brownstein MJ, Kuramochi-Miyagawa S, Nakano T, Chien M, Russo JJ, Ju JY, Sheridan R, Sander C, Zavolan M, Tuschl T. 2006. A novel class of small RNAs bind to MILI protein in mouse testes. Nature, 442(7099): 203-207.
[5]	Cora E, Pandey RR, Xiol J, Taylor J, Sachidanandam R, McCarthy AA, Pillai RS. 2014. The MID-PIWI module of Piwi proteins specifies nucleotide- and strand-biases of piRNAs. RNA, 20(6): 773-781.
[6]	Freedberg S, Taylor DR. 2007. Sex ratio variance and the maintenance of environmental sex determination. Journal of Evolutionary Biology, 20(1): 213-220.
[7]	Girard A, Sachidanandam R, Hannon GJ, Carmell MA. 2006. A germline-specific class of small RNAs binds mammalian Piwi proteins. Nature, 442(7099): 199-202.
[8]	Godwin J. 2010. Neuroendocrinology of sexual plasticity in teleost fishes. Front in Neuroendocrinology, 31(2): 203-216.
[9]	Gu YF, Zhang L, Chen XW. 2014. Differential expression analysis of Paralichthys olivaceus microRNAs in adult ovary and testis by deep sequencing. General and Comparative Endocrinology, 204: 181-184.
[10]	Hayes TB. 1998. Sex determination and primary sex differentiation in amphibians: Genetic and developmental mechanisms. The Journal of Experimental Zoology, 281(5): 373-399.
[11]	Heule C, Salzburger W, Bohne A. 2014. Genetics of sexual development: an evolutionary playground for fish. Genetics, 196(3): 579-591.
[12]	Houwing S, Kamminga LM, Berezikov E, Cronembold D, Girard A, van den Elst H, Filippov DV, Blaser H, Raz E, Moens CB, Plasterk RHA, Hannon GJ, Draper BW, Ketting RF. 2007. A role for Piwi and piRNAs in germ cell maintenance and transposon silencing in zebrafish. Cell, 129(1): 69-82.
[13]	Huang HY, Houwing S, Kaaij LJT, Meppelink A, Redl S, Gauci S, Vos H, Draper BW, Moens CB, Burgering BM, Ladurner P, Krijgsveld J, Berezikov E, Ketting RF. 2011. Tdrd1 acts as a molecular scaffold for Piwi proteins and piRNA targets in zebrafish. The EMBO Journal, 30(16): 3298-3308.
[14]	Jing J, Wu JJ, Liu W, Xiong ST, Ma WG, Zhang J, Wang WM, Gui JF, Mei J. 2014. Sex-biased miRNAs in gonad and their potential roles for testis development in yellow catfish. PLoS One, 9(9): e107946.
[15]	Kitano T, Takamune K, Kobayashi T, Nagahama Y, Abe SI. 1999. Suppression of P450 aromatase gene expression in sex-reversed males produced by rearing genetically female larvae at a high water temperature during a period of sex differentiation in the Japanese flounder (Paralichthys olivaceus). Journal of Molecular Endocrinology, 23(2): 167-176.
[16]	Lakshmi SS, Agrawal S. 2008. PiRNABank: a web resource on classified and clustered Piwi-interacting RNAs. Nucleic Acids Research, 36(S1): D173-D177.
[17]	Li CJ, Vagin VV, Lee S, Xu J, Ma SM, Xi HL, Seitz H, Horwich MD, Syrzycka M, Honda BM, Kittler ELW, Zapp ML, Klattenhoff C, Schulz N, Theurkauf WE, Weng ZP, Zamore PD. 2009. Collapse of germline piRNAs in the absence of argonaute3 reveals somatic piRNAs in flies. Cell, 137(3): 509-521.
[18]	Li Q, Zhou X, Guo YQ, Shang X, Chen H, Lu H, Cheng HH, Zhou RJ. 2008. Nuclear localization, DNA binding and restricted expression in neural and germ cells of zebrafish Dmrt3. Biology of the Cell, 100(8): 453-463.
[19]	Ma RQ, He F, Wen HS, Li JF, Mu WJ, Liu M, Zhang YQ, Hu J, Qun L. 2012. Polymorphysims of CYP17-I gene in the exons were associated with the reproductive endocrine of Japanese flounder (Paralichthys olivaceus). Asian-Australasian Journal of Animal Sciences, 25(6): 794-799.
[20]	Malone CD, Brennecke J, Dus M, Stark A, McCombie WR, Sachidanandam R, Hannon GJ. 2009. Specialized piRNA pathways act in germline and somatic tissues of the Drosophila ovary. Cell, 137(3): 522-535.
[21]	Matsuda M, Nagahama Y, Shinomiya A, Sato T, Matsuda C, Kobayashi T, Morrey CE, Shibata N, Asakawa S, Shimizu N, Hori H, Hamaguchi S, Sakaizumi M. 2002. DMY is a Y-specific DM-domain gene required for male development in the medaka fish. Nature, 417(6888): 559-563.
[22]	Mishima T, Takizawa T, Luo SS, Ishibashi O, Kawahigashi Y, Mizuguchi Y, Ishikawa T, Mori M, Kanda T, Goto T, Takizawa T. 2008. MicroRNA (miRNA) cloning analysis reveals sex differences in miRNA Expression profiles between adult mouse testis and ovary. Reproduction, 136(6): 811-822.
[23]	Palakodeti D, Smielewska M, Lu YC, Yeo GW, Graveley BR. 2008. The PIWI proteins SMEDWI-2 and SMEDWI-3 are required for stem cell function and piRNA expression in planarians. RNA, 14(6): 1174-1186.
[24]	Pfaffl MW. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Research, 29(9): e45.
[25]	Schiffer L, Anderko S, Hannemann F, Eiden-Plach A, Bernhardt R. 2015. The CYP11B subfamily. The Journal of Steroid Biochemistry and Molecular Biology, 151: 38-51.
[26]	Shibata Y, Paul-Prasanth B, Suzuki A, Usami T, Nakamoto M, Matsuda M, Nagahama Y. 2010. Expression of gonadal soma derived factor (GSDF) is spatially and temporally correlated with early testicular differentiation in medaka. Gene Expression Patterns, 10(6): 283-289.
[27]	Sigurdsson MI, Smith AV, Bjornsson HT, Jonsson JJ. 2012. The distribution of a germline methylation marker suggests a regional mechanism of LINE-1 silencing by the piRNA-PIWI system. BMC Genetics, 13: 31.
[28]	Spencer RJ, Janzen FJ. 2014. A novel hypothesis for the adaptive maintenance of environmental sex determination in a turtle. Proceedings of the Royal Society B: Biological Sciences, 281(1789): 20140831.
[29]	Storey JD. 2003. The positive false discovery rate: a Bayesian interpretation and the q-Value. The Annals of Statistics, 31(6): 2013-2035.
[30]	Weick EM, Miska EA. 2014. piRNAs: from biogenesis to function. Development, 141(18): 3458-3471.
[31]	Wen AY, You F, Sun P, Li J, Xu DD, Wu ZH, Ma DY, Zhang PJ. 2014. CpG methylation of dmrt1 and cyp19a promoters in relation to their sexual dimorphic expression in the Japanese flounder Paralichthys olivaceus. Journal of Fish Biology, 84(1): 193-205.
[32]	Wen AY, You F, Tan XG, Sun P, Ni J, Zhang YQ, Xu DD, Wu ZH, Xu YL, Zhang PJ. 2009. Expression pattern of dmrt4 from olive flounder (Paralichthys olivaceus) in adult gonads and during embryogenesis. Fish Physiology and Biochemistry, 35(3): 421-433.
[33]	Xiao J, Zhong H, Zhou Y, Yu F, Gao Y, Luo YJ, Tang ZY, Guo ZB, Guo EY, Gan X, Zhang M, Zhang YP. 2014. Identification and characterization of microRNAs in ovary and testis of Nile tilapia (Oreochromis Niloticus) by using solexa sequencing technology. PLoS One, 9(1): e86821.
[34]	Yamaguchi T, Yamaguchi S, Hirai T, Kitano T. 2007. Follicle-stimulating hormone signaling and Foxl2 are involved in transcriptional regulation of aromatase gene during gonadal sex differentiation in Japanese Flounder, Paralichthys olivaceus. Biochemical and Biophysical Research Communications, 359(4): 935-940.
[35]	Zhang DP, Duarte-Guterman P, Langlois VS, Trudeau VL. 2010. Temporal expression and steroidal regulation of piRNA pathway genes (mael, piwi, vasa) during Silurana (Xenopus) tropicalis embryogenesis and early larval development. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 152(2): 202-206.
[36]	Zhang T, Murphy MW, Gearhart MD, Bardwell VJ, Zarkower D. 2014. The mammalian Doublesex homolog DMRT6 coordinates the transition between mitotic and meiotic developmental programs during spermatogenesis. Development, 141(19): 3662-3671.
[37]	Zheng K, Xiol J, Reuter M, Eckardt S, Leu NA, McLaughlin KJ, Stark A, Sachidanandam R, Pillai RS, Wang PJ. 2010. Mouse MOV10L1 associates with Piwi proteins and is an essential component of the Piwi-interacting RNA (piRNA) pathway. Proceedings of the National Academy of Sciences of the United States of America, 107(26): 11841-11846.
[38]	Zhu XP, You F, Zhang PJ, Xu YL, Xu JH. 2006. Effects of cold shock on microtubule organization and cell cycle in gynogenetically activated eggs of olive flounder (Paralichthys olivaceus). Marine Biotechnology, 8(3): 312-318.