{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,10,29]],"date-time":"2025-10-29T05:08:33Z","timestamp":1761714513381,"version":"build-2065373602"},"reference-count":49,"publisher":"CSIRO Publishing","issue":"11","license":[{"start":{"date-parts":[[2025,5,27]],"date-time":"2025-05-27T00:00:00Z","timestamp":1748304000000},"content-version":"vor","delay-in-days":2569,"URL":"https:\/\/doi.org\/10.1071\/journalslicense"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2018,10,3]]},"abstract":"<jats:p>Mitochondria are vital cellular organelles that have the ability to change their shape under different conditions, such as in response to stress, disease, changes in metabolic rate, energy requirements and apoptosis. In the present study, we observed remodelling of mitochondria during spermiogenesis and its relationship with mitochondria-associated granules (MAG). At the beginning of spermiogenesis, mitochondria are characterised by their round shape. As spermiogenesis progresses, the round-shaped mitochondria change into elongated and then swollen mitochondria, subsequently forming a crescent-like shape and finally developing into onion-like shaped mitochondria. We also noted changes in mitochondrial size, location and patterns of cristae at different stages of spermiogenesis. Significant differences (P &amp;lt; 0.0001) were found in the size of the different-shaped mitochondria. In early spermatids transitioning to the granular nucleus stage, the size of the mitochondria decreased, but increased subsequently during spermiogenesis. Changes in size and morphological variations were achieved through marked mitochondrial fusion. We also observed a non-membranous structure (MAG) closely associated with mitochondria that may stimulate or control fusion during mitochondrial remodelling. The end product of this sophisticated remodelling process in turtle spermatozoa is an onion-like mitochondrion. The acquisition of this kind of mitochondrial configuration is one strategy for long-term sperm storage in turtles.<\/jats:p>","DOI":"10.1071\/rd18010","type":"journal-article","created":{"date-parts":[[2018,5,14]],"date-time":"2018-05-14T21:15:24Z","timestamp":1526332524000},"page":"1514-1521","source":"Crossref","is-referenced-by-count":10,"title":["Remodelling of mitochondria during spermiogenesis of Chinese soft-shelled turtle (Pelodiscus sinensis)"],"prefix":"10.1071","volume":"30","author":[{"given":"Abdul","family":"Haseeb","sequence":"first","affiliation":[{"name":"ALaboratory of Animal Cell Biology and Embryology, College of Veterinary Medicine, Nanjing Agricultural University, 1 Weigang, Nanjing, Jiangsu Province 210095, China."},{"name":"BFaculty of Veterinary and Animal Sciences, University of Poonch Rawalakot, 12350, Azad Kashmir, Pakistan."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Hong","family":"Chen","sequence":"additional","affiliation":[{"name":"ALaboratory of Animal Cell Biology and Embryology, College of Veterinary Medicine, Nanjing Agricultural University, 1 Weigang, Nanjing, Jiangsu Province 210095, China."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yufei","family":"Huang","sequence":"additional","affiliation":[{"name":"ALaboratory of Animal Cell Biology and Embryology, College of Veterinary Medicine, Nanjing Agricultural University, 1 Weigang, Nanjing, Jiangsu Province 210095, China."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Ping","family":"Yang","sequence":"additional","affiliation":[{"name":"ALaboratory of Animal Cell Biology and Embryology, College of Veterinary Medicine, Nanjing Agricultural University, 1 Weigang, Nanjing, Jiangsu Province 210095, China."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Xuejing","family":"Sun","sequence":"additional","affiliation":[{"name":"ALaboratory of Animal Cell Biology and Embryology, College of Veterinary Medicine, Nanjing Agricultural University, 1 Weigang, Nanjing, Jiangsu Province 210095, China."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Adeela","family":"Iqbal","sequence":"additional","affiliation":[{"name":"ALaboratory of Animal Cell Biology and Embryology, College of Veterinary Medicine, Nanjing Agricultural University, 1 Weigang, Nanjing, Jiangsu Province 210095, China."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Nisar","family":"Ahmed","sequence":"additional","affiliation":[{"name":"ALaboratory of Animal Cell Biology and Embryology, College of Veterinary Medicine, Nanjing Agricultural University, 1 Weigang, Nanjing, Jiangsu Province 210095, China."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Taozhi","family":"Wang","sequence":"additional","affiliation":[{"name":"ALaboratory of Animal Cell Biology and Embryology, College of Veterinary Medicine, Nanjing Agricultural University, 1 Weigang, Nanjing, Jiangsu Province 210095, China."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Noor","family":"Samad Gandahi","sequence":"additional","affiliation":[{"name":"ALaboratory of Animal Cell Biology and Embryology, College of Veterinary Medicine, Nanjing Agricultural University, 1 Weigang, Nanjing, Jiangsu Province 210095, China."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Xuebing","family":"Bai","sequence":"additional","affiliation":[{"name":"ALaboratory of Animal Cell Biology and Embryology, College of Veterinary Medicine, Nanjing Agricultural University, 1 Weigang, Nanjing, Jiangsu Province 210095, China."}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Qiusheng","family":"Chen","sequence":"additional","affiliation":[{"name":"ALaboratory of Animal Cell Biology and Embryology, College of Veterinary Medicine, Nanjing Agricultural University, 1 Weigang, Nanjing, Jiangsu Province 210095, China."},{"name":"CCorresponding author. Email: chenqsh305@njau.edu.cn"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"67","published-online":{"date-parts":[[2018,5,15]]},"reference":[{"key":"2025102819485410500_R1","doi-asserted-by":"publisher","first-page":"ra47","DOI":"10.1126\/SCISIGNAL.2002712","article-title":"Perinuclear mitochondrial clustering creates an oxidant-rich nuclear domain required for hypoxia-induced transcription.","volume":"5","author":"Al-Mehdi","year":"2012","journal-title":"Sci. Signal."},{"key":"2025102819485410500_R2","doi-asserted-by":"publisher","first-page":"R163","DOI":"10.1530\/REP-13-0178","article-title":"Mitochondria functionality and sperm quality.","volume":"146","author":"Amaral","year":"2013","journal-title":"Reproduction"},{"key":"2025102819485410500_R3"},{"key":"2025102819485410500_R4","doi-asserted-by":"publisher","first-page":"287","DOI":"10.1016\/J.DEVCEL.2011.03.003","article-title":"piRNAs meet mitochondria.","volume":"20","author":"Aravin","year":"2011","journal-title":"Dev. Cell"},{"key":"2025102819485410500_R5","doi-asserted-by":"publisher","first-page":"202","DOI":"10.1016\/J.MICRON.2012.06.010","article-title":"The ultrastructural characteristics of the spermatozoa stored in the cauda epididymidis in Chinese soft-shelled turtle Pelodiscus sinensis during the breeding season.","volume":"44","author":"Bian","year":"2013","journal-title":"Micron"},{"key":"2025102819485410500_R6","doi-asserted-by":"publisher","first-page":"1396","DOI":"10.1038\/SJ.CDD.4401963","article-title":"Mitochondrial outer membrane permeabilization during apoptosis: the innocent bystander scenario.","volume":"13","author":"Chipuk","year":"2006","journal-title":"Cell Death Differ."},{"key":"2025102819485410500_R7","doi-asserted-by":"publisher","first-page":"179","DOI":"10.3109\/19396368.2012.691943","article-title":"Spermatogenesis in mammals: proteomic insights.","volume":"58","author":"Chocu","year":"2012","journal-title":"Syst Biol Reprod Med"},{"key":"2025102819485410500_R8","doi-asserted-by":"publisher","first-page":"1616","DOI":"10.1093\/EMBOJ\/21.7.1616","article-title":"Mitochondria are morphologically and functionally heterogeneous within cells.","volume":"21","author":"Collins","year":"2002","journal-title":"EMBO J."},{"key":"2025102819485410500_R9","doi-asserted-by":"publisher","first-page":"6373","DOI":"10.1021\/CR3002033","article-title":"Mitochondrial outer membrane channels.","volume":"112","author":"Colombini","year":"2012","journal-title":"Chem. Rev."},{"key":"2025102819485410500_R10","doi-asserted-by":"publisher","first-page":"23911","DOI":"10.1074\/JBC.M111.252056","article-title":"Atypical cristae morphology of human syncytiotrophoblast mitochondria role for complex V.","volume":"286","author":"De los Rios Castillo","year":"2011","journal-title":"J. Biol. Chem."},{"key":"2025102819485410500_R11","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1007\/BF00236345","article-title":"Morphological, histochemical and biochemical studies on germ cell mitochondria of normal rats.","volume":"196","author":"De Martino","year":"1979","journal-title":"Cell Tissue Res."},{"key":"2025102819485410500_R12","doi-asserted-by":"publisher","first-page":"684","DOI":"10.1111\/JNC.13090","article-title":"Changes in mitochondrial morphology induced by calcium or rotenone in primary astrocytes occur predominantly through ROS-mediated remodeling.","volume":"133","author":"Deheshi","year":"2015","journal-title":"J. Neurochem."},{"key":"2025102819485410500_R13","doi-asserted-by":"publisher","first-page":"42373","DOI":"10.1074\/JBC.M112.413674","article-title":"Electron microscopic analysis of a spherical mitochondrial structure.","volume":"287","author":"Ding","year":"2012","journal-title":"J. Biol. Chem."},{"key":"2025102819485410500_R14","doi-asserted-by":"publisher","first-page":"197","DOI":"10.4161\/SPMG.21798","article-title":"Drosophila spermiogenesis: big things come from little packages.","volume":"2","author":"Fabian","year":"2012","journal-title":"Spermatogenesis"},{"key":"2025102819485410500_R15"},{"key":"2025102819485410500_R16","doi-asserted-by":"publisher","first-page":"250","DOI":"10.4161\/SPMG.1.3.18092","article-title":"Reptilian spermatogenesis: a histological and ultrastructural perspective.","volume":"1","author":"Gribbins","year":"2011","journal-title":"Spermatogenesis"},{"key":"2025102819485410500_R17","doi-asserted-by":"publisher","first-page":"337","DOI":"10.1002\/JMOR.10069","article-title":"Cytological evaluation of spermatogenesis and organization of the germinal epithelium in the male slider turtle, Trachemys scripta.","volume":"255","author":"Gribbins","year":"2003","journal-title":"J. Morphol."},{"key":"2025102819485410500_R18","doi-asserted-by":"publisher","first-page":"14157","DOI":"10.1074\/JBC.274.20.14157","article-title":"Mitochondria suppress local feedback activation of inositol 1,4,5-trisphosphate receptors by Ca2+.","volume":"274","author":"Hajn\u00f3czky","year":"1999","journal-title":"J. Biol. Chem."},{"key":"2025102819485410500_R19","doi-asserted-by":"publisher","first-page":"473","DOI":"10.1002\/AR.1092290406","article-title":"Ultrastructure of the turtle spermatozoon.","volume":"229","author":"Hess","year":"1991","journal-title":"Anat. Rec."},{"key":"2025102819485410500_R20","doi-asserted-by":"publisher","first-page":"376","DOI":"10.1016\/J.DEVCEL.2011.01.004","article-title":"piRNA-associated germline nuage formation and spermatogenesis require MitoPLD profusogenic mitochondrial-surface lipid signaling.","volume":"20","author":"Huang","year":"2011","journal-title":"Dev. Cell"},{"issue":"Suppl. 1","key":"2025102819485410500_R21","doi-asserted-by":"publisher","first-page":"S8","DOI":"10.1023\/A:1013842820458","article-title":"Germ plasm and germ-line cell determination: the role of mitochondria.","volume":"27","author":"Isaeva","year":"2001","journal-title":"Russ. J. Mar. Biol."},{"key":"2025102819485410500_R22","doi-asserted-by":"publisher","first-page":"1543","DOI":"10.1091\/MBC.E04-08-0697","article-title":"The mitochondrial inner membrane protein mitofilin controls cristae morphology.","volume":"16","author":"John","year":"2005","journal-title":"Mol. Biol. Cell"},{"key":"2025102819485410500_R23","first-page":"455","article-title":"Technological study on sperm storage.","volume":"33","author":"Li","year":"2005","journal-title":"J Anhui Agric Sci"},{"key":"2025102819485410500_R24","doi-asserted-by":"publisher","first-page":"357","DOI":"10.1159\/000353883","article-title":"From structure to function: mitochondrial morphology, motion and shaping in vascular smooth muscle.","volume":"50","author":"McCarron","year":"2013","journal-title":"J. Vasc. Res."},{"key":"2025102819485410500_R25","doi-asserted-by":"publisher","first-page":"108","DOI":"10.1093\/HUMUPD\/5.2.108","article-title":"Mini symposium. New aspects of spermatogenesis. Expression of mitochondrial marker proteins during spermatogenesis.","volume":"5","author":"Meinhardt","year":"1999","journal-title":"Hum. Reprod. Update"},{"key":"2025102819485410500_R26","doi-asserted-by":"publisher","first-page":"779","DOI":"10.1643\/0045-8511(2002)002[0779:SCOTFS]2.0.CO;2","article-title":"Spermatogenic cycle of the Florida softshell turtle, Apalone ferox.","author":"Meylan","year":"2002","journal-title":"Copeia"},{"key":"2025102819485410500_R27","doi-asserted-by":"publisher","DOI":"10.1016\/J.JKSUS.2017.02.002","article-title":"Spermiogenesis in the African sideneck turtle (Pelusios castaneus): acrosomal vesicle formation and nuclear morphogenesis.","author":"Olukole","year":"2017","journal-title":"Journal of King Saud University-Science"},{"key":"2025102819485410500_R28","doi-asserted-by":"publisher","first-page":"37","DOI":"10.1007\/S00418-011-0875-2","article-title":"Expression of DDX25 in nuage components of mammalian spermatogenic cells: immunofluorescence and immunoelectron microscopic study.","volume":"137","author":"Onohara","year":"2012","journal-title":"Histochem. Cell Biol."},{"key":"2025102819485410500_R29"},{"key":"2025102819485410500_R30","doi-asserted-by":"publisher","first-page":"1863","DOI":"10.1093\/EMBOJ\/20.8.1863","article-title":"Perinuclear, perigranular and sub-plasmalemmal mitochondria have distinct functions in the regulation of cellular calcium transport.","volume":"20","author":"Park","year":"2001","journal-title":"EMBO J."},{"key":"2025102819485410500_R31","doi-asserted-by":"publisher","first-page":"505","DOI":"10.1146\/ANNUREV-PHYSIOL-021115-105011","article-title":"Mito-morphosis: mitochondrial fusion, fission, and cristae remodeling as key mediators of cellular function.","volume":"78","author":"Pernas","year":"2016","journal-title":"Annu. Rev. Physiol."},{"key":"2025102819485410500_R32","doi-asserted-by":"publisher","first-page":"419","DOI":"10.1016\/J.MITO.2010.05.015","article-title":"Mitochondria, spermatogenesis and male infertility.","volume":"10","author":"Rajender","year":"2010","journal-title":"Mitochondrion"},{"key":"2025102819485410500_R33","doi-asserted-by":"publisher","first-page":"74","DOI":"10.1016\/J.MCE.2013.06.005","article-title":"Mitochondria and mammalian reproduction.","volume":"379","author":"Ramalho-Santos","year":"2013","journal-title":"Mol. Cell. Endocrinol."},{"key":"2025102819485410500_R34","doi-asserted-by":"publisher","first-page":"139","DOI":"10.1046\/J.1440-169X.2000.00492.X","article-title":"Nuage constituents arising from mitochondria: is it possible?","volume":"42","author":"Reunov","year":"2000","journal-title":"Dev. Growth Differ."},{"key":"2025102819485410500_R35","doi-asserted-by":"publisher","first-page":"79","DOI":"10.1002\/AR.1091900108","article-title":"Ultrastructural characterization of nuage in spermatocytes of the rat testis.","volume":"190","author":"Russell","year":"1978","journal-title":"Anat. Rec."},{"key":"2025102819485410500_R36"},{"key":"2025102819485410500_R37","doi-asserted-by":"publisher","first-page":"1255","DOI":"10.1038\/NCB1487","article-title":"A common lipid links Mfn-mediated mitochondrial fusion and SNARE-regulated exocytosis.","volume":"8","author":"Choi","year":"2006","journal-title":"Nat. Cell Biol."},{"key":"2025102819485410500_R38","doi-asserted-by":"publisher","first-page":"97","DOI":"10.4236\/ABB.2010.12014","article-title":"Mitochondria: transportation, distribution and function during spermiogenesis.","volume":"1","author":"Sun","year":"2010","journal-title":"Adv. Biosci. Biotechnol."},{"key":"2025102819485410500_R39","doi-asserted-by":"publisher","first-page":"59","DOI":"10.1016\/J.MOLCEL.2004.09.026","article-title":"Drp-1-dependent division of the mitochondrial network blocks intraorganellar Ca2+ waves and protects against Ca2+-mediated apoptosis.","volume":"16","author":"Szabadkai","year":"2004","journal-title":"Mol. Cell"},{"key":"2025102819485410500_R40","doi-asserted-by":"publisher","first-page":"169","DOI":"10.1007\/S00418-012-1067-4","article-title":"Expression of MAEL in nuage and non-nuage compartments of rat spermatogenic cells and colocalization with DDX4, DDX25 and MIWI.","volume":"140","author":"Takebe","year":"2013","journal-title":"Histochem. Cell Biol."},{"key":"2025102819485410500_R41","doi-asserted-by":"publisher","first-page":"241","DOI":"10.1161\/01.HYP.0000254415.31362.A7","article-title":"Role of oxidative stress in cardiac hypertrophy and remodeling.","volume":"49","author":"Takimoto","year":"2007","journal-title":"Hypertension"},{"key":"2025102819485410500_R42","first-page":"389","article-title":"Spermiogenesis in scorpion mud turtle, Kinosternon scorpioides.","volume":"4","author":"Viana","year":"2015","journal-title":"Rev. Bras. Med. Vet."},{"key":"2025102819485410500_R43","doi-asserted-by":"publisher","first-page":"30610","DOI":"10.1038\/SREP30610","article-title":"The spectrum of mitochondrial ultrastructural defects in mitochondrial myopathy.","volume":"6","author":"Vincent","year":"2016","journal-title":"Sci. Rep."},{"key":"2025102819485410500_R44","doi-asserted-by":"publisher","first-page":"364","DOI":"10.1016\/J.DEVCEL.2011.01.005","article-title":"MITOPLD is a mitochondrial protein essential for nuage formation and piRNA biogenesis in the mouse germline.","volume":"20","author":"Watanabe","year":"2011","journal-title":"Dev. Cell"},{"key":"2025102819485410500_R45","doi-asserted-by":"publisher","first-page":"435","DOI":"10.1016\/J.ANIREPROSCI.2007.09.011","article-title":"Seasonal changes of sperm storage and correlative structures in male and female soft-shelled turtles, Trionyx sinensis.","volume":"108","author":"Xiangkun","year":"2008","journal-title":"Anim. Reprod. Sci."},{"key":"2025102819485410500_R46","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1007\/S00418-012-0962-Z","article-title":"Nuage proteins: their localization in subcellular structures of spermatogenic cells as revealed by immunoelectron microscopy.","volume":"138","author":"Yokota","year":"2012","journal-title":"Histochem. Cell Biol."},{"key":"2025102819485410500_R47","doi-asserted-by":"publisher","first-page":"1213","DOI":"10.1002\/AR.20587","article-title":"Spermiogenesis in soft-shelled turtle, Pelodiscus sinensis.","volume":"290","author":"Zhang","year":"2007","journal-title":"Anat. Rec."},{"key":"2025102819485410500_R48","doi-asserted-by":"crossref","first-page":"16096","DOI":"10.1038\/srep16096","article-title":"Modification of sperm morphology during long-term sperm storage in the reproductive tract of the Chinese soft-shelled turtle, Pelodiscus sinensis.","volume":"5","author":"Zhang","year":"2015","journal-title":"Sci. Rep."},{"key":"2025102819485410500_R49","doi-asserted-by":"crossref","first-page":"5","DOI":"10.1016\/j.bbamcr.2008.06.013","article-title":"Cristae formation \u2013 linking ultrastructure and function of mitochondria.","volume":"1793","author":"Zick","year":"2009","journal-title":"Biochim. Biophys. Acta"}],"container-title":["Reproduction, Fertility and Development"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/connectsci.au\/rd\/article-pdf\/30\/11\/1514\/312221\/rd18010.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/connectsci.au\/rd\/article-pdf\/30\/11\/1514\/312221\/rd18010.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,28]],"date-time":"2025-10-28T23:48:56Z","timestamp":1761695336000},"score":1,"resource":{"primary":{"URL":"https:\/\/connectsci.au\/rd\/article\/30\/11\/1514\/50160\/Remodelling-of-mitochondria-during-spermiogenesis"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2018,5,15]]},"references-count":49,"journal-issue":{"issue":"11","published-print":{"date-parts":[[2018,10,3]]}},"URL":"https:\/\/doi.org\/10.1071\/rd18010","relation":{},"ISSN":["1031-3613","1448-5990"],"issn-type":[{"type":"print","value":"1031-3613"},{"type":"electronic","value":"1448-5990"}],"subject":[],"published":{"date-parts":[[2018,5,15]]}}}