{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,10,23]],"date-time":"2025-10-23T04:40:04Z","timestamp":1761194404167,"version":"build-2065373602"},"reference-count":67,"publisher":"MDPI AG","issue":"10","license":[{"start":{"date-parts":[[2025,10,21]],"date-time":"2025-10-21T00:00:00Z","timestamp":1761004800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100007129","name":"Natural Science Foundation of Shandong Province","doi-asserted-by":"publisher","award":["ZR2022MC100"],"award-info":[{"award-number":["ZR2022MC100"]}],"id":[{"id":"10.13039\/501100007129","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["31702331"],"award-info":[{"award-number":["31702331"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Biology"],"abstract":"<jats:p>PIWI-interacting RNAs (piRNAs) are small non-coding RNAs that interact with PIWI proteins and play essential roles in genome stability, gonadal development, and gametogenesis in animals. The Japanese flounder (Paralichthys olivaceus) is an important marine culture teleost in North Asia, showing pronounced sexual size dimorphism, where gynogenetic induction of all-female cohorts can markedly enhance production. However, the PIWI\/piRNA pathway in gynogenetic diploid P. olivaceus, which often exhibit gonadal dysgenesis, poor gamete quality, and low fertilization rates, remains poorly understood. In this study, RNA-seq and small RNA-seq data from 11 tissues and 6 developmental stages of common P. olivaceus, as well as the gonads of gynogenetic P. olivaceus, were analyzed to characterize the PIWI\/piRNA pathway and its roles in transposon and gene regulation within the germline. The results showed that PIWI\/piRNA genes were predominantly expressed in gonads and early embryogenesis in common P. olivaceus, with the highest expression in testis. Clustered piRNAs were identified in the testis and early embryos of common P. olivaceus, which targeted multiple transposon and gene families. Intriguingly, gynogenetic P. olivaceus gonads harbored abundant clustered piRNAs not only in the testes but also in the ovaries, both targeting similar transposon families as that in common P. olivaceus. Notably, the DNA transposon Tc1\/Mariner family and pim genes were the most heavily targeted by piRNAs in gynogenetic P. olivaceus, with testis-biased expression. Expanded pim genes were identified in P. olivaceus, overlapping with piRNA clusters, and the in vitro test in P. olivaceus testes revealed that the expanded pim genes may be pseudogenes as a piRNA cluster reference to generate piRNAs regulating the conventional pim members. These unique features of the PIWI\/piRNA pathway in gynogenetic diploid P. olivaceus may underline their impaired reproductive ability, and have important theoretical and practical implications for teleost gynogenetic breeding.<\/jats:p>","DOI":"10.3390\/biology14101464","type":"journal-article","created":{"date-parts":[[2025,10,21]],"date-time":"2025-10-21T14:53:19Z","timestamp":1761058399000},"page":"1464","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Dynamic Regulation of Gonadal Transposons and Pseudogenes via PIWI\/piRNA Pathway in Gynogenetic Japanese Flounder (Paralichthys olivaceus)"],"prefix":"10.3390","volume":"14","author":[{"given":"Zeyu","family":"Liu","sequence":"first","affiliation":[{"name":"Key Laboratory of Marine Genetics and Breeding (Ministry of Education), College of Marine Life Sciences, Ocean University of China, Qingdao 266003, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Weigang","family":"Li","sequence":"additional","affiliation":[{"name":"Key Laboratory of Marine Genetics and Breeding (Ministry of Education), College of Marine Life Sciences, Ocean University of China, Qingdao 266003, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Fengchi","family":"Wang","sequence":"additional","affiliation":[{"name":"Key Laboratory of Marine Genetics and Breeding (Ministry of Education), College of Marine Life Sciences, Ocean University of China, Qingdao 266003, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Wei","family":"Lu","sequence":"additional","affiliation":[{"name":"Key Laboratory of Marine Genetics and Breeding (Ministry of Education), College of Marine Life Sciences, Ocean University of China, Qingdao 266003, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Fan","family":"Yang","sequence":"additional","affiliation":[{"name":"Key Laboratory of Marine Genetics and Breeding (Ministry of Education), College of Marine Life Sciences, Ocean University of China, Qingdao 266003, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Qingke","family":"Zhang","sequence":"additional","affiliation":[{"name":"Key Laboratory of Marine Genetics and Breeding (Ministry of Education), College of Marine Life Sciences, Ocean University of China, Qingdao 266003, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8835-3171","authenticated-orcid":false,"given":"Jie","family":"Cheng","sequence":"additional","affiliation":[{"name":"Key Laboratory of Marine Genetics and Breeding (Ministry of Education), College of Marine Life Sciences, Ocean University of China, Qingdao 266003, China"},{"name":"Key Laboratory of Tropical Aquatic Germplasm of Hainan Province, Sanya Oceanographic Institution, Ocean University of China, Sanya 572024, China"},{"name":"Shandong Key Laboratory of Marine Seed Industry, Ocean University of China, Qingdao 266003, China"},{"name":"Laboratory for Marine Fisheries Science and Food Production Processes, Qingdao Marine Science and Technology Center, Qingdao 266237, China"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2025,10,21]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"363","DOI":"10.1126\/science.1130164","article-title":"Characterization of the piRNA complex from rat testes","volume":"313","author":"Lau","year":"2006","journal-title":"Science"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"1089","DOI":"10.1016\/j.cell.2007.01.043","article-title":"Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila","volume":"128","author":"Brennecke","year":"2007","journal-title":"Cell"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"484","DOI":"10.1016\/j.cell.2016.09.002","article-title":"Crystal structure of silkworm PIWI-clade Argonaute Siwi bound to piRNA","volume":"167","author":"Matsumoto","year":"2016","journal-title":"Cell"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"812","DOI":"10.1126\/science.aaa1039","article-title":"piRNA-guided slicing specifies transcripts for Zucchini-dependent, phased piRNA biogenesis","volume":"348","author":"Mohn","year":"2015","journal-title":"Science"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"819","DOI":"10.1038\/s41467-017-00854-4","article-title":"PNLDC1 is essential for piRNA 3\u2032 end trimming and transposon silencing during spermatogenesis in mice","volume":"8","author":"Ding","year":"2017","journal-title":"Nat. Commun."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"962","DOI":"10.1016\/j.cell.2016.01.008","article-title":"Identification and functional analysis of the pre-piRNA 3\u2032 trimmer in silkworms","volume":"164","author":"Izumi","year":"2016","journal-title":"Cell"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"708","DOI":"10.1016\/j.molcel.2014.10.016","article-title":"The initial uridine of primary piRNAs does not create the tenth adenine that is the hallmark of secondary piRNAs","volume":"56","author":"Wang","year":"2014","journal-title":"Mol. Cell"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"775","DOI":"10.1016\/j.molcel.2018.08.007","article-title":"A single mechanism of biogenesis, initiated and directed by PIWI proteins, explains piRNA production in most animals","volume":"71","author":"Gainetdinov","year":"2018","journal-title":"Mol. Cell"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"R730","DOI":"10.1016\/j.cub.2014.07.037","article-title":"PiRNAs","volume":"24","author":"Han","year":"2014","journal-title":"Curr. Biol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"e27889","DOI":"10.4161\/spmg.27889","article-title":"Mammalian piRNAs: Biogenesis, function, and mysteries","volume":"4","author":"Fu","year":"2014","journal-title":"Spermatogenesis"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"803","DOI":"10.1261\/rna.038521.113","article-title":"GPAT2, a mitochondrial outer membrane protein, in piRNA biogenesis in germline stem cells","volume":"19","author":"Shiromoto","year":"2013","journal-title":"RNA"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"1698","DOI":"10.1016\/j.cell.2014.05.018","article-title":"RNA clamping by Vasa assembles a piRNA amplifier complex on transposon transcripts","volume":"157","author":"Xiol","year":"2014","journal-title":"Cell"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"199","DOI":"10.1038\/nature04917","article-title":"A germline-specific class of small RNAs binds mammalian Piwi proteins","volume":"442","author":"Girard","year":"2006","journal-title":"Nature"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"e1010868","DOI":"10.1371\/journal.pgen.1010868","article-title":"The piRNA protein Asz1 is essential for germ cell and gonad development in zebrafish and exhibits differential necessities in distinct types of germ granules","volume":"21","author":"Ahmad","year":"2025","journal-title":"PLoS Genet."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"14","DOI":"10.1186\/s13059-025-03475-z","article-title":"Dynamic co-evolution of transposable elements and the piRNA pathway in African cichlid fishes","volume":"26","author":"Almeida","year":"2025","journal-title":"Genome Biol."},{"key":"ref_16","doi-asserted-by":"crossref","unstructured":"Ji, Q., Xie, Z., Gan, W., Wang, L., and Song, W. (2022). Identification and Characterization of PIWI-Interacting RNAs in Spinyhead Croakers (Collichthys lucidus) by Small RNA Sequencing. Fishes, 7.","DOI":"10.3390\/fishes7050297"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"411","DOI":"10.1016\/j.molcel.2017.03.017","article-title":"Piwi is required during Drosophila embryogenesis to license dual-strand piRNA clusters for transposon repression in adult ovaries","volume":"66","author":"Akkouche","year":"2017","journal-title":"Mol. Cell"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"3384","DOI":"10.4161\/cc.8.20.9885","article-title":"Astrin regulates meiotic spindle organization, spindle pole tethering and cell cycle progression in mouse oocytes","volume":"8","author":"Yuan","year":"2009","journal-title":"Cell Cycle"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.mce.2013.11.019","article-title":"Elevated expression of Piwi and piRNAs in ovaries of triploid crucian carp","volume":"383","author":"Zhou","year":"2014","journal-title":"Mol. Cell. Endocrinol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"740899","DOI":"10.1016\/j.aquaculture.2024.740899","article-title":"Establishment of recombinant doubled haploid lines of Japanese flounder and evaluation of their reproductive capacity","volume":"587","author":"Zhang","year":"2024","journal-title":"Aquaculture"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"18","DOI":"10.1007\/s42995-021-00118-7","article-title":"Evolutionary dynamics and conserved function of the Tudor domain-containing (TDRD) proteins in teleost fish","volume":"4","author":"Liu","year":"2022","journal-title":"Mar. Life Sci. Technol."},{"key":"ref_22","doi-asserted-by":"crossref","unstructured":"Zong, W., Wang, Y., Zhang, L., Lu, W., Li, W., Wang, F., and Cheng, J. (2024). DNA methylation mediates sperm quality via piwil1 and piwil2 regulation in Japanese flounder (Paralichthys olivaceus). Int. J. Mol. Sci., 25.","DOI":"10.3390\/ijms25115935"},{"key":"ref_23","first-page":"100609","article-title":"Rapid evolution of piRNA pathway and its transposon targets in Japanese flounder (Paralichthys olivaceus)","volume":"31","author":"Song","year":"2019","journal-title":"Comp. Biochem. Physiol. Part D Genom. Proteom."},{"key":"ref_24","doi-asserted-by":"crossref","unstructured":"Yang, F., Wang, Y., Lu, W., Zong, W., Zhu, Q., and Cheng, J. (2022). The comparative survey of coordinated regulation of steroidogenic pathway in Japanese flounder (Paralichthys olivaceus) and Chinese tongue sole (Cynoglossus Semilaevis). Int. J. Mol. Sci., 23.","DOI":"10.3390\/ijms23105520"},{"key":"ref_25","doi-asserted-by":"crossref","unstructured":"Cheng, J., Yang, F., Liu, S., Zhao, H., Lu, W., and Zhang, Q. (2022). Transcriptomic analysis reveals functional interaction of mRNA\u2013lncRNA\u2013miRNA in steroidogenesis and spermatogenesis of gynogenetic Japanese flounder (Paralichthys olivaceus). Biology, 11.","DOI":"10.3390\/biology11020213"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"740975","DOI":"10.1016\/j.aquaculture.2024.740975","article-title":"Coordinated regulatory feedback between estradiol and miR-17-92 cluster in ovaries of Japanese flounder Paralichthys olivaceus","volume":"589","author":"Wang","year":"2024","journal-title":"Aquaculture"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"1441","DOI":"10.1007\/s11802-018-3656-x","article-title":"Weighted correlation network analysis (WGCNA) of Japanese flounder (Paralichthys olivaceus) embryo transcriptome provides crucial gene sets for understanding haploid syndrome and rescue by diploidization","volume":"17","author":"Zhao","year":"2018","journal-title":"J. Ocean Univ. China"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"1338","DOI":"10.12688\/f1000research.15931.1","article-title":"FastQ Screen: A tool for multi-genome mapping and quality control","volume":"7","author":"Wingett","year":"2018","journal-title":"F1000Research"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"2114","DOI":"10.1093\/bioinformatics\/btu170","article-title":"Trimmomatic: A flexible trimmer for Illumina sequence data","volume":"30","author":"Bolger","year":"2014","journal-title":"Bioinformatics"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"907","DOI":"10.1038\/s41587-019-0201-4","article-title":"Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype","volume":"37","author":"Kim","year":"2019","journal-title":"Nat. Biotechnol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"290","DOI":"10.1038\/nbt.3122","article-title":"StringTie enables improved reconstruction of a transcriptome from RNA-seq reads","volume":"33","author":"Pertea","year":"2015","journal-title":"Nat. Biotechnol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"309","DOI":"10.1016\/j.gdata.2015.06.026","article-title":"Piwi proteins and piRNAs in mammalian oocytes and early embryos: From sample to sequence","volume":"5","author":"Rosenkranz","year":"2015","journal-title":"Genom. Data"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"644","DOI":"10.1186\/s12864-017-4031-9","article-title":"unitas: The universal tool for annotation of small RNAs","volume":"18","author":"Gebert","year":"2017","journal-title":"BMC Genom."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"137","DOI":"10.1038\/s42003-018-0141-4","article-title":"PIWI genes and piRNAs are ubiquitously expressed in mollusks and show patterns of lineage-specific adaptation","volume":"1","author":"Jehn","year":"2018","journal-title":"Commun. Biol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"5","DOI":"10.1186\/1471-2105-13-5","article-title":"proTRAC-a software for probabilistic piRNA cluster detection, visualization and analysis","volume":"13","author":"Rosenkranz","year":"2012","journal-title":"BMC Bioinform."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"4","DOI":"10.1002\/0471250953.bi0410s05","article-title":"Using Repeat Masker to identify repetitive elements in genomic sequences","volume":"5","author":"Chen","year":"2004","journal-title":"Curr. Protoc. Bioinform."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"421","DOI":"10.1186\/1471-2105-10-421","article-title":"BLAST+: Architecture and applications","volume":"10","author":"Camacho","year":"2009","journal-title":"BMC Bioinform."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"e228","DOI":"10.1002\/imt2.228","article-title":"OmicShare tools: A zero-code interactive online platform for biological data analysis and visualization","volume":"3","author":"Mu","year":"2024","journal-title":"Imeta"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"357","DOI":"10.1038\/nmeth.1923","article-title":"Fast gapped-read alignment with Bowtie 2","volume":"9","author":"Langmead","year":"2012","journal-title":"Nat. Methods"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"418","DOI":"10.1016\/S0168-9525(00)02093-X","article-title":"Repbase Update: A database and an electronic journal of repetitive elements","volume":"16","author":"Jurka","year":"2000","journal-title":"Trends Genet."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"67","DOI":"10.1016\/j.margen.2017.05.003","article-title":"Characterization of autonomous families of Tc1\/mariner transposons in neoteleost genomes","volume":"34","author":"Gao","year":"2017","journal-title":"Mar. Genom."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"33","DOI":"10.1016\/S0378-1119(01)00819-8","article-title":"ORF-FINDER: A vector for high-throughput gene identification","volume":"282","author":"Rombel","year":"2002","journal-title":"Gene"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"1870","DOI":"10.1093\/molbev\/msw054","article-title":"MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets","volume":"33","author":"Kumar","year":"2016","journal-title":"Mol. Biol. Evol."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"D493","DOI":"10.1093\/nar\/gkx922","article-title":"20 years of the SMART protein domain annotation resource","volume":"46","author":"Letunic","year":"2017","journal-title":"Nucleic Acids Res."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"1101","DOI":"10.1038\/nprot.2008.73","article-title":"Analyzing real-time PCR data by the comparative CT method","volume":"3","author":"Schmittgen","year":"2008","journal-title":"Nat. Protoc."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"638","DOI":"10.1016\/j.fsi.2010.12.014","article-title":"Evaluation of housekeeping genes as references for quantitative real time RT-PCR analysis of gene expression in Japanese flounder (Paralichthys olivaceus)","volume":"30","author":"Zheng","year":"2011","journal-title":"Fish. Shellfish Immunol."},{"key":"ref_47","doi-asserted-by":"crossref","unstructured":"Liu, S., Song, H., Liu, Z., Lu, W., Zhang, Q., and Cheng, J. (2022). Selection of references for microRNA quantification in Japanese flounder (Paralichthys olivaceus) normal tissues and Edwardsiella tarda-infected livers. Genes, 13.","DOI":"10.3390\/genes13020175"},{"key":"ref_48","unstructured":"Chandler, M., Gellert, M., Lambowitz, A.M., Rice, P.A., and Sandmeyer, S.B. (2015). Sleeping beauty transposition. Mobile DNA III, John Wiley & Sons, Inc."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"503","DOI":"10.1016\/j.devcel.2007.03.001","article-title":"MIWI2 is essential for spermatogenesis and repression of transposons in the mouse male germline","volume":"12","author":"Carmell","year":"2007","journal-title":"Dev. Cell"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"136","DOI":"10.1095\/biolreprod.113.111211","article-title":"Conservation and expression of PIWI-interacting RNA pathway genes in male and female adult gonad of amniotes","volume":"89","author":"Lim","year":"2013","journal-title":"Biol. Reprod."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"44","DOI":"10.1016\/j.cbpb.2018.03.005","article-title":"Differential expression of two Piwil orthologs during embryonic and gonadal development in pufferfish, Takifugu fasciatus","volume":"219","author":"Wen","year":"2018","journal-title":"Comp. Biochem. Physiol. Part B Biochem. Mol. Biol."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"274","DOI":"10.1038\/s41586-020-2159-2","article-title":"A satellite repeat-derived piRNA controls embryonic development of Aedes","volume":"580","author":"Halbach","year":"2020","journal-title":"Nature"},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"302","DOI":"10.1186\/s12864-020-6660-7","article-title":"Identification and application of piwi-interacting RNAs from seminal plasma exosomes in Cynoglossus semilaevis","volume":"21","author":"Zhang","year":"2020","journal-title":"BMC Genom."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"1732","DOI":"10.1101\/gad.1425706","article-title":"Identification and characterization of two novel classes of small RNAs in the mouse germline: Retrotransposon-derived siRNAs in oocytes and germline small RNAs in testes","volume":"20","author":"Watanabe","year":"2006","journal-title":"Genes Dev."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"264","DOI":"10.1038\/nature10672","article-title":"Miwi catalysis is required for piRNA amplification-independent LINE1 transposon silencing","volume":"480","author":"Reuter","year":"2011","journal-title":"Nature"},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"459","DOI":"10.1007\/s10126-011-9426-z","article-title":"Identification and characterization of piRNA-like small RNAs in the gonad of sea urchin (Strongylocentrotus nudus)","volume":"14","author":"Wei","year":"2012","journal-title":"Mar. Biotechnol."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"357","DOI":"10.1186\/s12864-016-2697-z","article-title":"Germ cell and tumor associated piRNAs in the medaka and Xiphophorus melanoma models","volume":"17","author":"Kneitz","year":"2016","journal-title":"BMC Genom."},{"key":"ref_58","first-page":"43","article-title":"The Sleeping Beauty transposable element: Evolution, regulation and genetic applications","volume":"6","author":"Ivics","year":"2004","journal-title":"Curr. Issues Mol. Biol."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"929","DOI":"10.1093\/gbe\/evs069","article-title":"Horizontal transfers of Tc1 elements between teleost fishes and their vertebrate parasites, lampreys","volume":"4","author":"Kuraku","year":"2012","journal-title":"Genome Biol. Evol."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"727","DOI":"10.1186\/1471-2164-15-727","article-title":"Genomic landscape and evolutionary dynamics of mariner transposable elements within the Drosophila genus","volume":"15","author":"Wallau","year":"2014","journal-title":"BMC Genom."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"726","DOI":"10.1016\/j.biocel.2004.11.005","article-title":"The serine\/threonine kinase Pim-1","volume":"37","author":"Bachmann","year":"2005","journal-title":"Int. J. Biochem. Cell Biol."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"1841","DOI":"10.1101\/gad.1105003","article-title":"The serine\/threonine kinase Pim-2 is a transcriptionally regulated apoptotic inhibitor","volume":"17","author":"Fox","year":"2003","journal-title":"Genes Dev."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"1182","DOI":"10.1038\/leu.2011.60","article-title":"The serine\/threonine kinase Pim-2 is a novel anti-apoptotic mediator in myeloma cells","volume":"25","author":"Asano","year":"2011","journal-title":"Leukemia"},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"519","DOI":"10.1007\/s13258-016-0400-z","article-title":"Identification and comparative analysis of piRNAs in ovary and testis of Nile tilapia (Oreochromis niloticus)","volume":"38","author":"Zhou","year":"2016","journal-title":"Genes Genom."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"1045","DOI":"10.1007\/s00438-014-0889-2","article-title":"Whole-genome duplication in teleost fishes and its evolutionary consequences","volume":"289","author":"Glasauer","year":"2014","journal-title":"Mol. Genet. Genom."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"1085","DOI":"10.1261\/rna.046482.114","article-title":"The small RNA content of human sperm reveals pseudogene-derived piRNAs complementary to protein-coding genes","volume":"21","author":"Pantano","year":"2015","journal-title":"RNA"},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"1088","DOI":"10.1093\/gbe\/evz060","article-title":"Primate piRNA cluster evolution suggests limited relevance of pseudogenes in piRNA-mediated gene regulation","volume":"11","author":"Gebert","year":"2019","journal-title":"Genome Biol. Evol."}],"container-title":["Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2079-7737\/14\/10\/1464\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,23]],"date-time":"2025-10-23T04:38:26Z","timestamp":1761194306000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2079-7737\/14\/10\/1464"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,10,21]]},"references-count":67,"journal-issue":{"issue":"10","published-online":{"date-parts":[[2025,10]]}},"alternative-id":["biology14101464"],"URL":"https:\/\/doi.org\/10.3390\/biology14101464","relation":{},"ISSN":["2079-7737"],"issn-type":[{"type":"electronic","value":"2079-7737"}],"subject":[],"published":{"date-parts":[[2025,10,21]]}}}