{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,27]],"date-time":"2026-09-27T20:18:15Z","timestamp":1790540295937,"version":"4.1.0"},"reference-count":43,"publisher":"Oxford University Press (OUP)","issue":"4","license":[{"start":{"date-parts":[[2022,10,18]],"date-time":"2022-10-18T00:00:00Z","timestamp":1666051200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100000275","name":"Leverhulme Trust","doi-asserted-by":"publisher","award":["RPG-2019-329"],"award-info":[{"award-number":["RPG-2019-329"]}],"id":[{"id":"10.13039\/501100000275","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000001","name":"National Science Foundation","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100000001","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2022,11,30]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>The unequal partitioning of molecules and organelles during cell division results in daughter cells with different fates. An extreme example is female meiosis, in which consecutive asymmetric cell divisions give rise to 1 large oocyte and 2 small polar bodies with DNA and minimal cytoplasm. Here, we test the hypothesis that during an asymmetric cell division during spermatogenesis of the nematode Auanema rhodensis, the late segregating X chromatids orient the asymmetric partitioning of cytoplasmic components. In previous studies, the secondary spermatocytes of wild-type XO males were found to divide asymmetrically to generate functional spermatids that inherit components necessary for sperm viability and DNA-containing residual bodies that inherit components to be discarded. Here we extend that analysis to 2 novel contexts. First, the isolation and analysis of a strain of mutant XX pseudomales revealed that such animals have highly variable patterns of X-chromatid segregation. The pattern of late segregating X chromatids nevertheless predicted the orientation of organelle partitioning. Second, while wild-type XX hermaphrodites were known to produce both 1X and 2X sperm, here, we show that spermatocytes within specific spermatogonial clusters exhibit 2 different patterns of X-chromatid segregation that correlate with distinct patterns of organelle partitioning. Together this analysis suggests that A. rhodensis has coopted lagging X chromosomes during anaphase II as a mechanism for determining the orientation of organelle partitioning.<\/jats:p>","DOI":"10.1093\/genetics\/iyac159","type":"journal-article","created":{"date-parts":[[2022,10,18]],"date-time":"2022-10-18T09:38:05Z","timestamp":1666085885000},"source":"Crossref","is-referenced-by-count":6,"title":["Lagging X chromatids specify the orientation of asymmetric organelle partitioning in XX spermatocytes of\n                    <i>Auanema rhodensis<\/i>"],"prefix":"10.1093","volume":"222","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-0835-958X","authenticated-orcid":false,"given":"Talal","family":"Al-Yazeedi","sequence":"first","affiliation":[{"name":"School of Life Sciences, University of Warwick , Coventry CV4 7AL, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9895-9716","authenticated-orcid":false,"given":"Emily L","family":"Xu","sequence":"additional","affiliation":[{"name":"Department of Biology, William & Mary , Williamsburg, VA 23187, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7740-5602","authenticated-orcid":false,"given":"Jasmin","family":"Kaur","sequence":"additional","affiliation":[{"name":"School of Life Sciences, University of Warwick , Coventry CV4 7AL, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9677-5577","authenticated-orcid":false,"given":"Diane C","family":"Shakes","sequence":"additional","affiliation":[{"name":"Department of Biology, William & Mary , Williamsburg, VA 23187, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0741-7197","authenticated-orcid":false,"given":"Andre","family":"Pires-daSilva","sequence":"additional","affiliation":[{"name":"School of Life Sciences, University of Warwick , Coventry CV4 7AL, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2022,10,18]]},"reference":[{"issue":"1","key":"2022120108054866100_iyac159-B1","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1007\/BF00710603","article-title":"Segregation of holocentric chromosomes at meiosis in the nematode, Caenorhabditis elegans","volume":"1","author":"Albertson","year":"1993","journal-title":"Chromosome Res"},{"issue":"2","key":"2022120108054866100_iyac159-B2","doi-asserted-by":"crossref","first-page":"303","DOI":"10.1007\/BF00222339","article-title":"Morphogenesis and fate of the residual body in human spermiogenesis","volume":"240","author":"Breucker","year":"1985","journal-title":"Cell Tissue Res"},{"key":"2022120108054866100_iyac159-B3","doi-asserted-by":"crossref","first-page":"17676","DOI":"10.1038\/srep17676","article-title":"Mating dynamics in a nematode with three sexes and its evolutionary implications","volume":"5","author":"Chaudhuri","year":"2015","journal-title":"Sci Rep"},{"key":"2022120108054866100_iyac159-B4","doi-asserted-by":"publisher","DOI":"10.3791\/2293","article-title":"An introduction to worm lab: from culturing worms to mutagenesis","volume":"47","author":"Chaudhuri","year":"2011","journal-title":"J Vis Exp"},{"key":"2022120108054866100_iyac159-B5","doi-asserted-by":"crossref","first-page":"171","DOI":"10.1007\/978-1-4614-4015-4_7","article-title":"Spermatogenesis","volume":"757","author":"Chu","year":"2013","journal-title":"Adv Exp Med Biol"},{"issue":"Pt 13","key":"2022120108054866100_iyac159-B6","first-page":"2955","article-title":"Biased inheritance of mitochondria during asymmetric cell division in the mouse oocyte","volume":"126","author":"Dalton","year":"2013","journal-title":"J Cell Sci"},{"issue":"suppl 1","key":"2022120108054866100_iyac159-B7","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1093\/humrep\/13.suppl_1.1","article-title":"Spermatogenesis","volume":"13","author":"de Kretser","year":"1998","journal-title":"Hum Reprod"},{"key":"2022120108054866100_iyac159-B8","doi-asserted-by":"crossref","first-page":"303","DOI":"10.1016\/S0091-679X(08)61393-X","article-title":"Blastomere culture and analysis","volume":"48","author":"Edgar","year":"1995","journal-title":"Methods Cell Biol"},{"issue":"796","key":"2022120108054866100_iyac159-B9","doi-asserted-by":"crossref","first-page":"514","DOI":"10.1126\/science.31.796.514","article-title":"The sex-determining chromosomes in Ascaris","volume":"31","author":"Edwards","year":"1910","journal-title":"Science"},{"issue":"20","key":"2022120108054866100_iyac159-B10","doi-asserted-by":"crossref","first-page":"e3785","DOI":"10.21769\/BioProtoc.3785","article-title":"Live-cell imaging and quantitative analysis of meiotic divisions in Caenorhabditis elegans males","volume":"10","author":"Fabig","year":"2020","journal-title":"Bio Protoc"},{"key":"2022120108054866100_iyac159-B11","doi-asserted-by":"crossref","first-page":"55","DOI":"10.1007\/s00427-003-0376-y","article-title":"Alternative morphs and plasticity of vulval development in a rhabditid nematode species","volume":"214","author":"F\u00e9lix","year":"2004","journal-title":"Dev Genes Evol"},{"issue":"4","key":"2022120108054866100_iyac159-B12","doi-asserted-by":"crossref","first-page":"e10161","DOI":"10.1371\/journal.pone.0010161","article-title":"A monoclonal antibody toolkit for C. elegans","volume":"5","author":"Hadwiger","year":"2010","journal-title":"PLoS One"},{"issue":"1","key":"2022120108054866100_iyac159-B13","doi-asserted-by":"crossref","first-page":"67","DOI":"10.1093\/genetics\/91.1.67","article-title":"Nondisjuncion mutants of the nematode Caenorhabditis elegans","volume":"91","author":"Hodgkin","year":"1979","journal-title":"Genetics"},{"issue":"2 Pt. 1","key":"2022120108054866100_iyac159-B14","doi-asserted-by":"crossref","first-page":"275","DOI":"10.1093\/genetics\/86.2.275","article-title":"Mutations causing transformation of sexual phenotype in the nematode Caenorhabditis elegans","volume":"86","author":"Hodgkin","year":"1977","journal-title":"Genetics"},{"issue":"4","key":"2022120108054866100_iyac159-B15","doi-asserted-by":"crossref","first-page":"e3000211","DOI":"10.1371\/journal.pbio.3000211","article-title":"Distinct roles of two myosins in C. elegans spermatid differentiation","volume":"17","author":"Hu","year":"2019","journal-title":"PLoS Biol"},{"issue":"24","key":"2022120108054866100_iyac159-B16","doi-asserted-by":"crossref","first-page":"4613","DOI":"10.1242\/dev.086769","article-title":"Residual body removal during spermatogenesis in C. elegans requires genes that mediate cell corpse clearance","volume":"139","author":"Huang","year":"2012","journal-title":"Development"},{"issue":"1","key":"2022120108054866100_iyac159-B17","doi-asserted-by":"crossref","first-page":"25","DOI":"10.1146\/annurev.ecolsys.32.081501.113958","article-title":"Sex chromosome meiotic drive","volume":"32","author":"Jaenike","year":"2001","journal-title":"Annu Rev Ecol Syst"},{"issue":"1","key":"2022120108054866100_iyac159-B18","doi-asserted-by":"crossref","first-page":"11135","DOI":"10.1038\/s41598-017-09871-1","article-title":"Description of two three-gendered nematode species in the new genus Auanema (Rhabditina) that are models for reproductive mode evolution","volume":"7","author":"Kanzaki","year":"2017","journal-title":"Sci Rep"},{"issue":"3","key":"2022120108054866100_iyac159-B19","doi-asserted-by":"crossref","first-page":"1415","DOI":"10.1534\/genetics.107.073668","article-title":"Comparative genetics of sex determination: masculinizing mutations in Caenorhabditis briggsae","volume":"178","author":"Kelleher","year":"2008","journal-title":"Genetics"},{"issue":"23","key":"2022120108054866100_iyac159-B20","doi-asserted-by":"crossref","first-page":"1489","DOI":"10.1016\/S0960-9822(00)00828-9","article-title":"Myosin VI is required for asymmetric segregation of cellular components during C. elegans spermatogenesis","volume":"10","author":"Kelleher","year":"2000","journal-title":"Curr Biol"},{"issue":"15","key":"2022120108054866100_iyac159-B21","doi-asserted-by":"crossref","first-page":"3357","DOI":"10.1242\/dev.01916","article-title":"C. elegans sperm bud vesicles to deliver a meiotic maturation signal to distant oocytes","volume":"132","author":"Kosinski","year":"2005","journal-title":"Development"},{"issue":"7","key":"2022120108054866100_iyac159-B22","doi-asserted-by":"crossref","first-page":"3205","DOI":"10.1007\/s00018-020-03735-0","article-title":"Mechanisms of meiotic drive in symmetric and asymmetric meiosis","volume":"78","author":"Kruger","year":"2021","journal-title":"Cell Mol Life Sci"},{"issue":"2","key":"2022120108054866100_iyac159-B23","doi-asserted-by":"crossref","first-page":"362","DOI":"10.1016\/j.ydbio.2017.08.010","article-title":"Germ cell cysts and simultaneous sperm and oocyte production in a hermaphroditic nematode","volume":"430","author":"McCaig","year":"2017","journal-title":"Dev Biol"},{"issue":"6","key":"2022120108054866100_iyac159-B24","doi-asserted-by":"crossref","first-page":"2559","DOI":"10.1091\/mbc.e06-01-0031","article-title":"Myosin VI stabilizes an actin network during Drosophila spermatid individualization","volume":"17","author":"Noguchi","year":"2006","journal-title":"Mol Biol Cell"},{"issue":"9","key":"2022120108054866100_iyac159-B25","doi-asserted-by":"crossref","first-page":"1338","DOI":"10.3390\/genes12091338","article-title":"Flavors of non-random meiotic segregation of autosomes and sex chromosomes","volume":"12","author":"Pajpach","year":"2021","journal-title":"Genes (Basel)"},{"issue":"5","key":"2022120108054866100_iyac159-B26","doi-asserted-by":"crossref","first-page":"331","DOI":"10.1007\/s003350040003","article-title":"Nonrandom segregation during meiosis: the unfairness of females","volume":"12","author":"Pardo-Manuel de Villena","year":"2001","journal-title":"Mamm Genome"},{"key":"2022120108054866100_iyac159-B27","doi-asserted-by":"crossref","first-page":"5485","DOI":"10.1038\/ncomms6485","article-title":"Dynamic SUMO modification regulates mitotic chromosome assembly and cell cycle progression in Caenorhabditis elegans","volume":"5","author":"Pelisch","year":"2014","journal-title":"Nat Commun"},{"issue":"10","key":"2022120108054866100_iyac159-B28","doi-asserted-by":"crossref","first-page":"1198","DOI":"10.1101\/gad.293504","article-title":"Conservation of the global sex determination gene tra-1 in distantly related nematodes","volume":"18","author":"Pires-daSilva","year":"2004","journal-title":"Genes Dev"},{"key":"2022120108054866100_iyac159-B29","doi-asserted-by":"crossref","first-page":"157","DOI":"10.1038\/ncomms1160","article-title":"Asymmetric spermatocyte division as a mechanism for controlling sex ratios","volume":"2","author":"Shakes","year":"2011","journal-title":"Nat Commun"},{"issue":"8","key":"2022120108054866100_iyac159-B30","doi-asserted-by":"crossref","first-page":"e1000611","DOI":"10.1371\/journal.pgen.1000611","article-title":"Spermatogenesis-specific features of the meiotic program in Caenorhabditis elegans","volume":"5","author":"Shakes","year":"2009","journal-title":"PLoS Genet"},{"key":"2022120108054866100_iyac159-B31","first-page":"1","author":"Smith","year":"2014"},{"issue":"2","key":"2022120108054866100_iyac159-B32","doi-asserted-by":"crossref","first-page":"e1041345","DOI":"10.1080\/21565562.2015.1041345","article-title":"Separating from the pack: molecular mechanisms of Drosophila spermatid individualization","volume":"5","author":"Steinhauer","year":"2015","journal-title":"Spermatogenesis"},{"key":"2022120108054866100_iyac159-B33","doi-asserted-by":"crossref","first-page":"179275","DOI":"10.1242\/dev.179275","article-title":"Combover interacts with the axonemal component Rsp3 and is required for Drosophila sperm individualization","volume":"146","author":"Steinhauer","year":"2019","journal-title":"Development"},{"key":"2022120108054866100_iyac159-B34","first-page":"1","author":"Stiernagle","year":"2006"},{"issue":"1","key":"2022120108054866100_iyac159-B35","doi-asserted-by":"crossref","first-page":"93","DOI":"10.1016\/j.cub.2017.11.037","article-title":"Sex- and gamete-specific patterns of X chromosome segregation in a trioecious nematode","volume":"28","author":"Tandonnet","year":"2018","journal-title":"Curr Biol"},{"issue":"4","key":"2022120108054866100_iyac159-B36","doi-asserted-by":"crossref","first-page":"1211","DOI":"10.1534\/g3.119.0011","article-title":"Chromosome-wide evolution and sex determination in the three-sexed nematode Auanema rhodensis","volume":"9","author":"Tandonnet","year":"2019","journal-title":"G3 (Bethesda)"},{"key":"2022120108054866100_iyac159-B37","first-page":"20211572","author":"Van Goor","year":"2022"},{"issue":"7","key":"2022120108054866100_iyac159-B38","doi-asserted-by":"crossref","first-page":"1793","DOI":"10.3390\/cells10071793","article-title":"Fisher vs. the worms: extraordinary sex ratios in nematodes and the mechanisms that produce them","volume":"10","author":"Van Goor","year":"2021","journal-title":"Cells"},{"issue":"3","key":"2022120108054866100_iyac159-B39","doi-asserted-by":"crossref","first-page":"911","DOI":"10.1534\/genetics.117.300259","article-title":"Autosomal trisomy and triploidy are corrected during female meiosis in Caenorhabditis elegans","volume":"207","author":"Vargas","year":"2017","journal-title":"Genetics"},{"issue":"1","key":"2022120108054866100_iyac159-B40","doi-asserted-by":"crossref","first-page":"26","DOI":"10.1083\/jcb.91.1.26","article-title":"Sperm morphogenesis in wild-type and fertilization-defective mutants of Caenorhabditis elegans","volume":"91","author":"Ward","year":"1981","journal-title":"J Cell Biol"},{"issue":"18","key":"2022120108054866100_iyac159-B41","doi-asserted-by":"crossref","first-page":"3253","DOI":"10.1242\/dev.153841","article-title":"Cytoskeletal variations in an asymmetric cell division support diversity in nematode sperm size and sex ratios","volume":"144","author":"Winter","year":"2017","journal-title":"Development"},{"key":"2022120108054866100_iyac159-B42","first-page":"70","volume-title":"Biology","author":"Xu","year":"2020"},{"issue":"3","key":"2022120108054866100_iyac159-B43","doi-asserted-by":"crossref","first-page":"323","DOI":"10.1007\/s00418-020-01954-x","article-title":"Diverse functions of myosin VI in spermiogenesis","volume":"155","author":"Zakrzewski","year":"2021","journal-title":"Histochem Cell Biol"}],"container-title":["Genetics"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/academic.oup.com\/genetics\/advance-article-pdf\/doi\/10.1093\/genetics\/iyac159\/46694964\/iyac159.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/genetics\/article-pdf\/222\/4\/iyac159\/47467233\/iyac159.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/genetics\/article-pdf\/222\/4\/iyac159\/47467233\/iyac159.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,10,5]],"date-time":"2024-10-05T20:43:10Z","timestamp":1728160990000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/genetics\/article\/doi\/10.1093\/genetics\/iyac159\/6762860"}},"subtitle":[],"editor":[{"given":"J","family":"Engebrecht","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2022,10,18]]},"references-count":43,"journal-issue":{"issue":"4","published-online":{"date-parts":[[2022,10,18]]},"published-print":{"date-parts":[[2022,11,30]]}},"URL":"https:\/\/doi.org\/10.1093\/genetics\/iyac159","relation":{"has-preprint":[{"id-type":"doi","id":"10.1101\/2022.03.15.484444","asserted-by":"object"}]},"ISSN":["1943-2631"],"issn-type":[{"value":"1943-2631","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2022,12,1]]},"published":{"date-parts":[[2022,10,18]]},"article-number":"iyac159"}}