{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,5,15]],"date-time":"2026-05-15T14:49:33Z","timestamp":1778856573837,"version":"3.51.4"},"reference-count":60,"publisher":"MDPI AG","issue":"24","license":[{"start":{"date-parts":[[2022,12,8]],"date-time":"2022-12-08T00:00:00Z","timestamp":1670457600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"National Key R&amp;D Program of China","award":["2018YFD0900301"],"award-info":[{"award-number":["2018YFD0900301"]}]},{"name":"National Key R&amp;D Program of China","award":["2019QY01"],"award-info":[{"award-number":["2019QY01"]}]},{"name":"National Key R&amp;D Program of China","award":["2020TD19"],"award-info":[{"award-number":["2020TD19"]}]},{"name":"National Key R&amp;D Program of China","award":["2017ASTCP-ES06"],"award-info":[{"award-number":["2017ASTCP-ES06"]}]},{"name":"Central Public-interest Scientific Institution Basal Research Fund","award":["2018YFD0900301"],"award-info":[{"award-number":["2018YFD0900301"]}]},{"name":"Central Public-interest Scientific Institution Basal Research Fund","award":["2019QY01"],"award-info":[{"award-number":["2019QY01"]}]},{"name":"Central Public-interest Scientific Institution Basal Research Fund","award":["2020TD19"],"award-info":[{"award-number":["2020TD19"]}]},{"name":"Central Public-interest Scientific Institution Basal Research Fund","award":["2017ASTCP-ES06"],"award-info":[{"award-number":["2017ASTCP-ES06"]}]},{"name":"Qingdao National Laboratory for Marine Science and Technology","award":["2018YFD0900301"],"award-info":[{"award-number":["2018YFD0900301"]}]},{"name":"Qingdao National Laboratory for Marine Science and Technology","award":["2019QY01"],"award-info":[{"award-number":["2019QY01"]}]},{"name":"Qingdao National Laboratory for Marine Science and Technology","award":["2020TD19"],"award-info":[{"award-number":["2020TD19"]}]},{"name":"Qingdao National Laboratory for Marine Science and Technology","award":["2017ASTCP-ES06"],"award-info":[{"award-number":["2017ASTCP-ES06"]}]},{"name":"Taishan Scholar Program Fund of Shandong of China","award":["2018YFD0900301"],"award-info":[{"award-number":["2018YFD0900301"]}]},{"name":"Taishan Scholar Program Fund of Shandong of China","award":["2019QY01"],"award-info":[{"award-number":["2019QY01"]}]},{"name":"Taishan Scholar Program Fund of Shandong of China","award":["2020TD19"],"award-info":[{"award-number":["2020TD19"]}]},{"name":"Taishan Scholar Program Fund of Shandong of China","award":["2017ASTCP-ES06"],"award-info":[{"award-number":["2017ASTCP-ES06"]}]},{"name":"National Ten-Thousands Talents Special Support Program","award":["2018YFD0900301"],"award-info":[{"award-number":["2018YFD0900301"]}]},{"name":"National Ten-Thousands Talents Special Support Program","award":["2019QY01"],"award-info":[{"award-number":["2019QY01"]}]},{"name":"National Ten-Thousands Talents Special Support Program","award":["2020TD19"],"award-info":[{"award-number":["2020TD19"]}]},{"name":"National Ten-Thousands Talents Special Support Program","award":["2017ASTCP-ES06"],"award-info":[{"award-number":["2017ASTCP-ES06"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Cells"],"abstract":"<jats:p>Spermatogenesis is a complex and continuous process of germ-cell differentiation. This complex process is regulated by many factors, of which gene regulation in spermatogenic cells plays a decisive role. Spermatogenesis has been widely studied in vertebrates, but little is known about spermatogenesis in protochordates. Here, for the first time, we performed single-cell RNA sequencing (scRNA-seq) on 6832 germ cells from the testis of adult Ciona intestinalis. We identified six germ cell populations and revealed dynamic gene expression as well as transcriptional regulation during spermatogenesis. In particular, we identified four spermatocyte subtypes and key genes involved in meiosis in C. intestinalis. There were remarkable similarities and differences in gene expression during spermatogenesis between C. intestinalis and two other vertebrates (Chinese tongue sole and human). We identified many spermatogenic-cell-specific genes with functions that need to be verified. These findings will help to further improve research on spermatogenesis in chordates.<\/jats:p>","DOI":"10.3390\/cells11243978","type":"journal-article","created":{"date-parts":[[2022,12,9]],"date-time":"2022-12-09T02:50:51Z","timestamp":1670554251000},"page":"3978","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":5,"title":["Single-Cell RNA Sequencing of the Testis of Ciona intestinalis Reveals the Dynamic Transcriptional Profile of Spermatogenesis in Protochordates"],"prefix":"10.3390","volume":"11","author":[{"given":"Yanan","family":"Li","sequence":"first","affiliation":[{"name":"College of Fisheries and Life Science, Shanghai Ocean University, Shanghai 201306, China"},{"name":"Key Lab of Sustainable Development of Marine Fisheries, Ministry of Agriculture and Rural Affairs, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao 266072, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Xiang","family":"Liu","sequence":"additional","affiliation":[{"name":"College of Fisheries and Life Science, Shanghai Ocean University, Shanghai 201306, China"},{"name":"Key Lab of Sustainable Development of Marine Fisheries, Ministry of Agriculture and Rural Affairs, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao 266072, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7970-8743","authenticated-orcid":false,"given":"Xianghui","family":"Zhang","sequence":"additional","affiliation":[{"name":"Key Lab of Sustainable Development of Marine Fisheries, Ministry of Agriculture and Rural Affairs, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao 266072, China"},{"name":"College of Marine Technology and Environment, Dalian Ocean University, Dalian 116023, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1754-4018","authenticated-orcid":false,"given":"Hongyan","family":"Wang","sequence":"additional","affiliation":[{"name":"Key Lab of Sustainable Development of Marine Fisheries, Ministry of Agriculture and Rural Affairs, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao 266072, China"},{"name":"Laboratory for Marine Fisheries Science and Food Production Processes, Qingdao National Laboratory for Marine Science and Technology, Qingdao 266071, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jianyang","family":"Chen","sequence":"additional","affiliation":[{"name":"BGI Research-Qingdao, BGI, Qingdao 266555, China"},{"name":"Qingdao-Europe Advanced Institute for Life Sciences, BGI-Qingdao, Qingdao 266555, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jiankai","family":"Wei","sequence":"additional","affiliation":[{"name":"Sars-Fang Centre, MoE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of China, Qingdao 266003, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yubang","family":"Li","sequence":"additional","affiliation":[{"name":"Key Lab of Sustainable Development of Marine Fisheries, Ministry of Agriculture and Rural Affairs, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao 266072, China"},{"name":"College of Life Sciences, Shandong Normal University, Jinan 250014, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Hongxi","family":"Chen","sequence":"additional","affiliation":[{"name":"BGI Research-Qingdao, BGI, Qingdao 266555, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0326-4410","authenticated-orcid":false,"given":"Qian","family":"Wang","sequence":"additional","affiliation":[{"name":"Key Lab of Sustainable Development of Marine Fisheries, Ministry of Agriculture and Rural Affairs, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao 266072, China"},{"name":"Laboratory for Marine Fisheries Science and Food Production Processes, Qingdao National Laboratory for Marine Science and Technology, Qingdao 266071, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Kaiqiang","family":"Liu","sequence":"additional","affiliation":[{"name":"Key Lab of Sustainable Development of Marine Fisheries, Ministry of Agriculture and Rural Affairs, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao 266072, China"},{"name":"Laboratory for Marine Fisheries Science and Food Production Processes, Qingdao National Laboratory for Marine Science and Technology, Qingdao 266071, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yuyan","family":"Liu","sequence":"additional","affiliation":[{"name":"Key Lab of Sustainable Development of Marine Fisheries, Ministry of Agriculture and Rural Affairs, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao 266072, China"},{"name":"Laboratory for Marine Fisheries Science and Food Production Processes, Qingdao National Laboratory for Marine Science and Technology, Qingdao 266071, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6953-2203","authenticated-orcid":false,"given":"Changwei","family":"Shao","sequence":"additional","affiliation":[{"name":"Key Lab of Sustainable Development of Marine Fisheries, Ministry of Agriculture and Rural Affairs, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao 266072, China"},{"name":"Laboratory for Marine Fisheries Science and Food Production Processes, Qingdao National Laboratory for Marine Science and Technology, Qingdao 266071, China"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2022,12,8]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"390","DOI":"10.1016\/j.ygcen.2009.02.013","article-title":"Spermatogenesis in fish","volume":"165","author":"Schulz","year":"2010","journal-title":"Gen. Comp. Endocrinol."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"3","DOI":"10.3724\/SP.J.1005.2008.00003","article-title":"Genes involved in spermatogenesis","volume":"30","author":"Ge","year":"2008","journal-title":"Yi Chuan Hered."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"459","DOI":"10.1002\/jemt.1070320602","article-title":"Spermatogenesis in nonmammalian vertebrates","volume":"32","author":"Pudney","year":"1995","journal-title":"Microsc. Res. Tech."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"445","DOI":"10.1006\/scdb.1998.0202","article-title":"Dynamics of meiotic prophase I during spermatogenesis: From pairing to division","volume":"9","author":"Cobb","year":"1998","journal-title":"Semin. Cell Dev. Biol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"579","DOI":"10.1007\/s10577-007-1142-1","article-title":"Dissecting the mammalian synaptonemal complex using targeted mutations","volume":"15","author":"Costa","year":"2007","journal-title":"Chromosome Res."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"337","DOI":"10.1023\/B:RUDO.0000049605.43877.0d","article-title":"Similarity of domain organization of proteins in phylogenetically distant organisms as a basis of meiosis conservatism","volume":"35","author":"Bogdanov","year":"2004","journal-title":"Russ. J. Dev. Biol."},{"key":"ref_7","first-page":"173","article-title":"In silico search for functionally similar proteins involved in meiosis and recombination in evolutionarily distant organisms","volume":"3","author":"Bogdanov","year":"2003","journal-title":"Biology"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"365","DOI":"10.1016\/0092-8674(93)90114-6","article-title":"ZIP1 is a synaptonemal complex protein required for meiotic chromosome synapsis","volume":"72","author":"Sym","year":"1993","journal-title":"Cell"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"3130","DOI":"10.1101\/gad.935001","article-title":"c (3) G encodes a Drosophila synaptonemal complex protein","volume":"15","author":"Page","year":"2001","journal-title":"Genes Dev."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"2157","DOI":"10.1126\/science.1080049","article-title":"The draft genome of Ciona intestinalis: Insights into chordate and vertebrate origins","volume":"298","author":"Dehal","year":"2002","journal-title":"Science"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"376","DOI":"10.1016\/S0168-9525(03)00144-6","article-title":"Ciona intestinalis: An emerging model for whole-genome analyses","volume":"19","author":"Satoh","year":"2003","journal-title":"Trends Genet."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"R152","DOI":"10.1186\/gb-2008-9-10-r152","article-title":"Improved genome assembly and evidence-based global gene model set for the chordate Ciona intestinalis: New insight into intron and operon populations","volume":"9","author":"Satou","year":"2008","journal-title":"Genome Biol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"431","DOI":"10.1002\/mrd.10131","article-title":"EST analysis of gene expression in testis of the ascidian Ciona intestinalis","volume":"62","author":"Inaba","year":"2002","journal-title":"Mol. Reprod. Dev."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"64","DOI":"10.1007\/s004270050012","article-title":"Characterization of an ascidian DEAD-box gene, Ci-DEAD1: Specific expression in the germ cells and its mRNA localization in the posterior-most blastomeres in early embryos","volume":"210","author":"Fujimura","year":"2000","journal-title":"Dev. Genes Evol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"381","DOI":"10.1038\/nbt.2859","article-title":"The dynamics and regulators of cell fate decisions are revealed by pseudotemporal ordering of single cells","volume":"32","author":"Trapnell","year":"2014","journal-title":"Nat. Biotechnol."},{"key":"ref_16","doi-asserted-by":"crossref","unstructured":"Langfelder, P., and Horvath, S. (2008). WGCNA: An R package for weighted correlation network analysis. BMC Bioinform., 9.","DOI":"10.1186\/1471-2105-9-559"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"2498","DOI":"10.1101\/gr.1239303","article-title":"Cytoscape: A software environment for integrated models of biomolecular interaction networks","volume":"13","author":"Shannon","year":"2003","journal-title":"Genome Res"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"884","DOI":"10.1038\/s41467-018-03282-0","article-title":"Characterizing the replicability of cell types defined by single cell RNA-sequencing data using MetaNeighbor","volume":"9","author":"Crow","year":"2018","journal-title":"Nat. Commun."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"e66747","DOI":"10.7554\/eLife.66747","article-title":"Mapping single-cell atlases throughout Metazoa unravels cell type evolution","volume":"10","author":"Tarashansky","year":"2021","journal-title":"Elife"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"2973","DOI":"10.1016\/j.cell.2021.04.005","article-title":"A stony coral cell atlas illuminates the molecular and cellular basis of coral symbiosis, calcification, and immunity","volume":"184","author":"Levy","year":"2021","journal-title":"Cell"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"e02963","DOI":"10.7554\/eLife.02963","article-title":"A molecular model for the role of SYCP3 in meiotic chromosome organisation","volume":"3","author":"Pellegrini","year":"2014","journal-title":"Elife"},{"key":"ref_22","doi-asserted-by":"crossref","unstructured":"Ye, D., Liu, T., Li, Y., and Sun, Y. (2022). Assessment of fish spermatogenesis through high-quality immunofluorescence against fish testicular samples with an antibody set. bioRxiv.","DOI":"10.1101\/2022.08.23.504910"},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Wu, X., Yang, Y., Zhong, C., Wang, T., Deng, Y., Huang, H., Lin, H., Meng, Z., and Liu, X. (2021). Single-Cell Atlas of Adult Testis in Protogynous Hermaphroditic Orange-Spotted Grouper, Epinephelus coioides. Int. J. Mol. Sci., 22.","DOI":"10.3390\/ijms222212607"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"14882","DOI":"10.1074\/jbc.M609116200","article-title":"Human TopBP1 participates in cyclin E\/CDK2 activation and preinitiation complex assembly during G1\/S transition","volume":"282","author":"Jeon","year":"2007","journal-title":"J. Biol. Chem."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"672191","DOI":"10.3389\/fcell.2021.672191","article-title":"High Resolution View on the Regulation of Recombinase Accumulation in Mammalian Meiosis","volume":"9","author":"Mhaskar","year":"2021","journal-title":"Front. Cell Dev. Biol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"591","DOI":"10.1093\/biolre\/ioz070","article-title":"Functions of cyclins and CDKs in mammalian gametogenesis","volume":"101","author":"Chotiner","year":"2019","journal-title":"Biol. Reprod."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"1077","DOI":"10.1046\/j.1365-2443.2001.00484.x","article-title":"Sptrx-2, a fusion protein composed of one thioredoxin and three tandemly repeated NDP-kinase domains is expressed in human testis germ cells","volume":"6","author":"Sadek","year":"2001","journal-title":"Genes Cells"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"718","DOI":"10.1078\/0171-9335-00097","article-title":"The spatial and temporal expression of Tekt1, a mouse tektin C homologue, during spermatogenesis suggest that it is involved in the development of the sperm tail basal body and axoneme","volume":"79","author":"Larsson","year":"2000","journal-title":"Eur. J. Cell Biol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"759","DOI":"10.1046\/j.1440-169x.1999.00471.x","article-title":"Differentiation of the gonad rudiment into ovary and testis in the solitary ascidian, Ciona intestinalis","volume":"41","author":"Okada","year":"1999","journal-title":"Dev. Growth Differ."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"10459","DOI":"10.1073\/pnas.89.21.10459","article-title":"CDC46\/MCM5, a yeast protein whose subcellular localization is cell cycle-regulated, is involved in DNA replication at autonomously replicating sequences","volume":"89","author":"Chen","year":"1992","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"237","DOI":"10.1093\/carcin\/bgm268","article-title":"CDC6: From DNA replication to cell cycle checkpoints and oncogenesis","volume":"29","author":"Borlado","year":"2008","journal-title":"Carcinogenesis"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"18291","DOI":"10.1074\/jbc.M110.106575","article-title":"Regulation of cyclin B2 expression and cell cycle G2\/m transition by menin","volume":"285","author":"Wu","year":"2010","journal-title":"J. Biol. Chem."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"159","DOI":"10.1016\/j.molmed.2009.02.002","article-title":"Mitogen-activated protein kinases in male reproductive function","volume":"15","author":"Li","year":"2009","journal-title":"Trends Mol. Med."},{"key":"ref_34","doi-asserted-by":"crossref","unstructured":"Holt, J.E., Stanger, S.J., Nixon, B., and McLaughlin, E.A. (2016). Non-coding RNA in spermatogenesis and epididymal maturation. Non-Coding RNA Reprod. Syst., 95\u2013120.","DOI":"10.1007\/978-94-017-7417-8_6"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"51","DOI":"10.1095\/biolreprod.114.124008","article-title":"Telomerase activity and telomere length in male germ cells","volume":"92","author":"Ozturk","year":"2015","journal-title":"Biol. Reprod."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"7657","DOI":"10.1128\/MCB.25.17.7657-7664.2005","article-title":"Reduction of spermatogenesis but not fertility in Creb3l4-deficient mice","volume":"25","author":"Adham","year":"2005","journal-title":"Mol. Cell. Biol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"433","DOI":"10.1038\/s41467-018-08182-x","article-title":"Loss-of-function mutations in QRICH2 cause male infertility with multiple morphological abnormalities of the sperm flagella","volume":"10","author":"Shen","year":"2019","journal-title":"Nat. Commun."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"181","DOI":"10.1530\/REP-18-0522","article-title":"The sperm-associated antigen 6 interactome and its role in spermatogenesis","volume":"158","author":"Liu","year":"2019","journal-title":"Reproduction"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"18278","DOI":"10.1038\/srep18278","article-title":"Dissecting the structural basis of MEIG1 interaction with PACRG","volume":"6","author":"Li","year":"2016","journal-title":"Sci. Rep."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"261","DOI":"10.1007\/s10815-021-02363-2","article-title":"A novel homozygous missense mutation in AK7 causes multiple morphological anomalies of the flagella and oligoasthenoteratozoospermia","volume":"39","author":"Xiang","year":"2022","journal-title":"J. Assist. Reprod. Genet."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"1141","DOI":"10.1038\/s41422-018-0099-2","article-title":"The adult human testis transcriptional cell atlas","volume":"28","author":"Guo","year":"2018","journal-title":"Cell Res."},{"key":"ref_42","doi-asserted-by":"crossref","unstructured":"Wang, H.-Y., Liu, X., Chen, J.-Y., Huang, Y., Lu, Y., Tan, F., Liu, Q., Yang, M., Li, S., and Zhang, X. (2022). Single-cell-resolution transcriptome map revealed novel genes involved in testicular germ cell progression and somatic cells specification in Chinese tongue sole with sex reversal. Sci. China Life Sci., 1674\u20137305.","DOI":"10.1007\/s11427-021-2236-4"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"122","DOI":"10.1186\/s40104-021-00638-3","article-title":"Single-cell RNA-sequencing reveals the dynamic process and novel markers in porcine spermatogenesis","volume":"12","author":"Zhang","year":"2021","journal-title":"J. Anim. Sci. Biotechnol."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"548","DOI":"10.1016\/j.devcel.2020.07.018","article-title":"Single-cell RNA sequencing of the cynomolgus macaque testis reveals conserved transcriptional profiles during mammalian spermatogenesis","volume":"54","author":"Lau","year":"2020","journal-title":"Dev. Cell"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"851719","DOI":"10.3389\/fgene.2022.851719","article-title":"Single Cell Transcriptome Sequencing of Zebrafish Testis Revealed Novel Spermatogenesis Marker Genes and Stronger Leydig-Germ Cell Paracrine Interactions","volume":"13","author":"Qian","year":"2022","journal-title":"Front. Genet."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"197","DOI":"10.1007\/s10695-008-9252-z","article-title":"An overview of functional and stereological evaluation of spermatogenesis and germ cell transplantation in fish","volume":"35","author":"Batlouni","year":"2009","journal-title":"Fish Physiol. Biochem."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"603","DOI":"10.1111\/j.1440-169X.2010.01196.x","article-title":"Piwi-expressing hemoblasts serve as germline stem cells during postembryonic germ cell specification in colonial ascidian, Botryllus primigenus","volume":"52","author":"Sunanaga","year":"2010","journal-title":"Dev. Growth Differ."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"457","DOI":"10.1016\/j.mod.2011.09.001","article-title":"Role of Vasa, Piwi, and Myc-expressing coelomic cells in gonad regeneration of the colonial tunicate, Botryllus primigenus","volume":"128","author":"Kawamura","year":"2011","journal-title":"Mech. Dev."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"20497","DOI":"10.1073\/pnas.1217018109","article-title":"Calaxin drives sperm chemotaxis by Ca2+-mediated direct modulation of a dynein motor","volume":"109","author":"Mizuno","year":"2012","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"2514","DOI":"10.1038\/s41598-020-59147-4","article-title":"Three multi-allelic gene pairs are responsible for self-sterility in the ascidian Ciona intestinalis","volume":"10","author":"Sawada","year":"2020","journal-title":"Sci. Rep."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"13508","DOI":"10.1073\/pnas.0806590105","article-title":"Gamete plasticity in a broadcast spawning marine invertebrate","volume":"105","author":"Crean","year":"2008","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"447","DOI":"10.1146\/annurev-genet-110410-132541","article-title":"Uniting germline and stem cells: The function of Piwi proteins and the piRNA pathway in diverse organisms","volume":"45","author":"Juliano","year":"2011","journal-title":"Annu. Rev. Genet."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"484","DOI":"10.5534\/wjmh.190038","article-title":"The role of endoplasmic reticulum stress response in male reproductive physiology and pathology: A review","volume":"38","author":"Karna","year":"2020","journal-title":"World J. Men\u2019s Health"},{"key":"ref_54","doi-asserted-by":"crossref","unstructured":"Da Cruz, I., Rodr\u00edguez-Casuriaga, R., Santi\u00f1aque, F.F., Far\u00edas, J., Curti, G., Capoano, C.A., Folle, G.A., Benavente, R., Sotelo-Silveira, J.R., and Geisinger, A. (2016). Transcriptome analysis of highly purified mouse spermatogenic cell populations: Gene expression signatures switch from meiotic-to postmeiotic-related processes at pachytene stage. BMC Genom., 17.","DOI":"10.1186\/s12864-016-2618-1"},{"key":"ref_55","doi-asserted-by":"crossref","unstructured":"Pieplow, C., and Wessel, G.M. (2022). Sex-Specific Genes Identified in Sea Urchin Gonads are Expressed Prior to Metamorphosis. bioRxiv.","DOI":"10.1101\/2022.01.26.477926"},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"794","DOI":"10.1038\/nrg3573","article-title":"Meiotic recombination in mammals: Localization and regulation","volume":"14","author":"Baudat","year":"2013","journal-title":"Nat. Rev. Genet."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"E125","DOI":"10.1038\/12956","article-title":"Meiosis: Rec8 is the reason for cohesion","volume":"1","author":"Amon","year":"1999","journal-title":"Nat. Cell Biol."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"e49273","DOI":"10.15252\/embr.201949273","article-title":"PDS 5 proteins regulate the length of axial elements and telomere integrity during male mouse meiosis","volume":"21","author":"Viera","year":"2020","journal-title":"EMBO Rep."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"761","DOI":"10.3389\/fpls.2019.00761","article-title":"The dmc1 mutant allows an insight into the DNA double-strand break repair during meiosis in barley (Hordeum vulgare L.)","volume":"10","author":"Baran","year":"2019","journal-title":"Front. Plant Sci."},{"key":"ref_60","doi-asserted-by":"crossref","unstructured":"Zhou, J., Yang, F., Leu, N.A., and Wang, P.J. (2012). MNS1 is essential for spermiogenesis and motile ciliary functions in mice. PLoS Genet., 8.","DOI":"10.1371\/journal.pgen.1002516"}],"container-title":["Cells"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2073-4409\/11\/24\/3978\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T01:36:50Z","timestamp":1760146610000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2073-4409\/11\/24\/3978"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,12,8]]},"references-count":60,"journal-issue":{"issue":"24","published-online":{"date-parts":[[2022,12]]}},"alternative-id":["cells11243978"],"URL":"https:\/\/doi.org\/10.3390\/cells11243978","relation":{},"ISSN":["2073-4409"],"issn-type":[{"value":"2073-4409","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,12,8]]}}}