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Back to the roots: segregation of univalent sex chromosomes in meiosis

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Abstract

In males of many taxa, univalent sex chromosomes normally segregate during the first meiotic division, and analysis of sex chromosome segregation was foundational for the chromosome theory of inheritance. Correct segregation of single or multiple univalent sex chromosomes occurs in a cellular environment where every other chromosome is a bivalent that is being partitioned into homologous chromosomes at anaphase I. The mechanics of univalent chromosome segregation vary among animal taxa. In some, univalents establish syntelic attachment of sister kinetochores to the spindle. In others, amphitelic attachment is established. Here, we review how this problem of segregation of unpaired chromosomes is solved in different animal systems. In addition, we give a short outlook of how mechanistic insights into this process could be gained by explicitly studying model organisms, such as Caenorhabditis elegans.

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References

  • Albertson DG, Thomson JN (1993) Segregation of holocentric chromosomes at meiosis in the nematode Caenorhabditis elegans. Chromosome Res 1:15–26

    Article  CAS  PubMed  Google Scholar 

  • Ault JG (1984) Unipolar orientation stability of the sex univalent in the grasshopper (Melanoplus sanguinipes). Chromosoma 89:201–205

    Article  Google Scholar 

  • Ault JG (1986) Stable versus unstable orientations of sex chromosomes in two grasshopper species. Chromosoma 93:298–304

    Article  CAS  PubMed  Google Scholar 

  • Bean CJ, Schaner CE, Kelly WG (2004) Meiotic pairing and imprinted X chromatin assembly in Caenorhabditis elegans. Nat Genet 36:100–105

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Benavente R, Wettstein R (1977) An ultrastructural cytogenetic study on the evolution of sex chromosomes during the spermatogenesis of Lycosa malitosa (Arachnida). Chromosoma 64:255–277

    Article  Google Scholar 

  • Boring AM (1909) A small chromosome in Ascaris megalocephala. Arch f Zellf 4:120–131

    Google Scholar 

  • Boveri T (1899) Die Entwicklung von Ascaris megalocephala mit besonderer Rücksicht auf die Kernverhältnisse. In: Festschrift zum siebzigsten Geburtstag von Carl v. Kupffer, Jena., pp 383–429

    Google Scholar 

  • Boveri T (1909) Über Geschlechtschromosomen bei Nematoden. Arch f Zellf 4:132–141

    Google Scholar 

  • Brady M, Paliulis LV (2015) Chromosome interaction over a distance in meiosis. R Soc open sci 2:150029

    Article  PubMed  PubMed Central  Google Scholar 

  • Cattanach BM (1962) X0 mice. Genet Res 3:487–490

    Article  Google Scholar 

  • Church K (1979a) The grasshopper X chromosome. I. States of condensation and the nuclear envelope at G1, S and G2 of premeiotic interphase and at early meiotic prophase. Chromosoma 71:347–358

    Article  CAS  PubMed  Google Scholar 

  • Church K (1979b) The grasshopper X chromosome. II. Negative heteropycnosis, transcription activities and compartmentation during spermatogonial stages. Chromosoma 71:359–370

    Article  CAS  PubMed  Google Scholar 

  • Chaudhuri J, Kache V, Pires da Silva A (2011) Regulation of sexual plasticity in a nematode that produces males, females, and hermaphrodites. Current Biol 21:1548–1551

    Article  CAS  Google Scholar 

  • Cochran JC, Sindelar CV, Mulko NK, Collins KA, Kong SE, Hawley RS, Kull FJ (2009) ATPase cycle of the nonmotile kinesin NOD allows microtubule end tracking and drives chromosome movement. Cell 136:110–122

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dietz R (1954) Multiple Geschlechtschromosomen bei dem Ostracoden Notodromas monacha. Chromosoma 6:397–418

    Article  CAS  PubMed  Google Scholar 

  • Edwards CL (1910) The sex determining chromosomes in Ascaris. Science 31:514–515

    Article  CAS  PubMed  Google Scholar 

  • Flaquer A, Rappold GA, Wienker TF, Fischer C (2008) The human pseudoautosomal regions: a review for genetic epidemiologists. E J Hum Genet 16:771–779

    Article  CAS  Google Scholar 

  • Forer A, Ferraro-Gideon J, Berns M (2013) Distance segregation of sex chromosomes in crane-fly spermatocytes studied using laser microbeam irradiations. Protoplasma 250:1045–1055

    Article  CAS  PubMed  Google Scholar 

  • Geinitz B (1915) Über Abweichungen bei der Eireifung von Ascaris. Arch f Zellf 18:588–633

    Google Scholar 

  • Gillies SC, Lane FM, Paik W, Pyrtel K, Wallace NT, Gilliland WD (2013) Nondisjunctional segregations in Drosophila female meiosis I are preceded by homolog malorientation at metaphase arrest. Genetics 193:443–451

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goldstein P (1977) Spermatogenesis and spermiogenesis in Ascaris lumbricoides var. suum. J Morphol 154:317–338

    Article  CAS  PubMed  Google Scholar 

  • Goldstein P (1978) Ultrastructural analysis of sex determination in Ascaris lumbricoides var. suum. Chromosoma 66:59–69

    Article  Google Scholar 

  • Honda T, Suzuki H, Itoh M (1977) An unusual sex chromosome constitution found in the amami spinous country-rat, Tokudaia osmensis osmensis. Jpn J Genet 52:247–249

    Article  Google Scholar 

  • Hughes SE, Gililand WD, Cotitta JL, Takeo S, Collins KA, Hawley RS (2009) Heterochromatic threads connect oscillating chromosomes during prometaphase I in Drosophila oocytes. PLoS Genet. E1000348

  • Hughes-Schrader S (1943) Polarization, kinetochore movements, and bivalent structure in the meiosis of male mantids. Biol Bull 85:265–300

    Article  Google Scholar 

  • Hughes-Schrader S (1948) Cytology of coccids (Coccoidea-Homoptera). Adv Genet 35:127–203

    Article  CAS  PubMed  Google Scholar 

  • Hunt P, LeMaire R, Embury P, Sheean L, Mroz K (1995) Analysis of chromosome behavior in intake mammalian oocytes: monitoring the segregation of a univalent chromosome during female meiosis. Hum Mol Gen 4:2007–2012

    Article  CAS  PubMed  Google Scholar 

  • Jaramillo-Lambert A, Engebrecht J (2010) A single unpaired and transcriptionally silenced X chromosome locally precludes checkpoint signaling in the Caenorhabditis elegans germ line. Genetics 184:613–628

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • John B, Claridge MF (1974) Chromosome variation in British populations of Oncopsis (Hemiptera-Cicadellidae). Chromosoma 46:77–89

    Article  CAS  PubMed  Google Scholar 

  • Jorgensen EM, Mango SE (2002) The art and design of genetic screens: Caenorhabditis elegans. Nat Rev Genet 3:356–369

    Article  CAS  PubMed  Google Scholar 

  • Just W, Baumstark A, Süss A, Graphodatsky A, Rens W, Schäfer N, Bakloushinskaya I, Hameister H, Vogel W (2007) Ellobius lutescens: sex determination and sex chromosome. Sexual Dev 1:211–221

    Article  CAS  Google Scholar 

  • Kautzsch G (1913) Studien über Entwicklungsanomalien bei Ascaris II. Arch f Entwicklungsmech d Organismen 35:642–691

    Article  Google Scholar 

  • Kolomiets OL, Vorontsov NN, Lyapunova EA, Mazurova TF (1991) Ultrastructure, meiotic behavior, and evolution of sex chromosomes of the genus Ellobius. Genetica 84:179–189

    Article  Google Scholar 

  • Král J, Musilová J, Št'áhlavský F, Rezác M, Akan Z, Edwards RL, Coyle FA, Almerje CR (2006) Evolution of the karyotype and sex chromosome systems in basal clades of araneomorph spiders (Araneae: Araneomorphae). Chromosome Res 14:859–880

    Article  PubMed  Google Scholar 

  • LaFountain JR, Cohan CS, Oldenbourg R (2012) Pac-man motility of kinetochores unleashed by laser microsurgery. Mol Biol Cell 23:3133–3142

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • LeMaire-Adkins R, Hunt PA (2000) Nonrandom segregation of the mouse univalent X chromosome: evidence of spindle-mediated meiotic drive. Genetics 156:775–783

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lukinavičius G, Umezawa K, Olivier N, Honigmann A, Yang G, Plass T, Mueller V, Reymond L, Corrêa IR Jr, Luo ZG, Schultz C, Lemke EA, Heppenstall P, Eggeling C, Manley S, Johnsson K (2013) A near-infrared fluorophore for live-cell super-resolution microscopy of cellular proteins. Nat Chem 5:132–139

    Article  PubMed  Google Scholar 

  • McClung CE (1902) The accessory chromosome—sex determinant? Biol Bull 3:43–84

    Article  Google Scholar 

  • Melters DP, Paliulis LV, Korf IF, Chan SWL (2012) Holocentric chromosomes: convergent evolution, meiotic adaptations, and genomic analysis. Chromosome Res 20:579–593

    Article  CAS  PubMed  Google Scholar 

  • Montgomery TH (1910) Are particular chromosomes sex determinants? Biol Bull 19:1–17

    Article  Google Scholar 

  • Morris T (1968) The XO and OY chromosome constitutions in the mouse. Genet Res 12:125–137

    Article  CAS  PubMed  Google Scholar 

  • Nagaoka SI, Hodges CA, Albertini DF, Hunt PA (2011) Oocyte-specific differences in cell cycle control create an innate susceptibility to meiotic errors. Curr Biol 21:651–657

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nicklas RB (1961) Recurrent pole-to-pole movements of the sex chromosome during prometaphase I in Melanoplus differentials spermatocytes. Chromosoma 12:97–115

    Article  CAS  PubMed  Google Scholar 

  • Nicklas RB, Campbell MS, Ward SC, Gorbsky GJ (1998) Tension-sensitive kinetochore phosphorylation in vitro. J Cell Sci 111:3189–3196

    CAS  PubMed  Google Scholar 

  • Nicklas RB, Waters JC, Salmon ED, Ward SC (2001) Checkpoint signals in grasshopper meiosis are sensitive to microtubule attachment, but tension is still essential. J Cell Sci 114:4173–4183

    CAS  PubMed  Google Scholar 

  • Page J, Viera A, Parra MT, de la Fuente R, Suja JA, Prieto I, Barbero JL, Rufas JS, Berríos S, Fernández-Donoso R (2006) Involvement of synaptonemal complex proteins in sex chromosome segregation during marsupial male meiosis. PLoS Genet 2(8):e136

    Article  PubMed  PubMed Central  Google Scholar 

  • Pardo-Manuel de Villena F, Sapienza C (2001) Nonrandom segregation during meiosis: the unfairness of females. Mamm Genome 12:331–339

    Article  CAS  PubMed  Google Scholar 

  • Pelletier L, O’Toole E, Schwager A, Hyman AA, Müller-Reichert T (2006) Centriole assembly in Caenorhabditis elegans. Nature 444:619–623

    Article  CAS  PubMed  Google Scholar 

  • Peters N, Perez DE, Song MH, Liu Y, Müller-Reichert T, Caron C, Kemphues KJ, O’Connell K (2010) Control of mitotic and meiotic centriole duplication by the PLK4-related kinase ZYG-1. J Cell Sci 123:795–805

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Revell SH (1947) Controlled X-segregation at meiosis in Tegenaria. Heredity 1:337–347

    Article  Google Scholar 

  • Schrader F (1935) Notes on the mitotic behavior of long chromosomes. Cytologia 6:422–430

    Article  Google Scholar 

  • Shakes DC, Wu JC, Sadler PL, LaPrade K, Moore LL, Noritake A, Chu DS (2009) Spermatogenesis-specific features of the meiotic program in Caenorhabditis elegans. PLoS Genet 5:e1000611

    Article  PubMed  PubMed Central  Google Scholar 

  • Shakes DC, Neva BJ, Huynh H, Chaudhuri J, Pires da Silva A (2011) Asymmetric spermatocyte division as a mechanism for controlling sex ratios. Nat Commun 2:157

    Article  PubMed  Google Scholar 

  • Soullier S, Hanni C, Catzeflis F, Berta F, Laudet V (1998) Male sex determination in the spiny rat Tokudaia osimensis (Rodentia: Muridae) is not Sry dependent. Mamm Genome 9:590–592

    Article  CAS  PubMed  Google Scholar 

  • Srayko M, O’Toole ET, Hyman AA, Müller-Reichert T (2006) Katanin disrupts the microtubule lattice and increases polymer number in C. elegans meiosis. Curr Biol 16:1944–1949

    Article  CAS  PubMed  Google Scholar 

  • Sutou S, Mitsui Y, Tsuchiya K (2001) Sex determination without the Y chromosome in two Japanese rodents Tokudaia osimensis osimensis and Tokudaia osimensis spp. Mamm Genome 12:17–21

    Article  CAS  PubMed  Google Scholar 

  • Sutton WS (1902) On the morphology of the chromosome group in Brachystola magna. Biol Bull 4:24–39

    Article  Google Scholar 

  • Sutton WS (1903) The chromosomes in heredity. Biol Bull 4:231–241

    Article  Google Scholar 

  • Theurkauf WE, Hawley RS (1992) Meiotic spindle assembly in Drosophila females—behavior of nonexchange chromosomes and the effects of mutations in the Nod kinesin-like protein. J Cell Sci 115:1541–1549

    Google Scholar 

  • Turner JM (2007) Meiotic sex chromosome inactivation. Development 134:1823–1831

    Article  CAS  PubMed  Google Scholar 

  • Welshons WJ, Russell LB (1959) The Y-chromosome as the bearer of male determining factors in the mouse. Proc Natl Acad Sci U S A 45:560–566

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • White MJD (1977), Animal Cytology and Evolution. Cambridge University Press

  • White MJD (1940) The heteropycnosis of sex chromosomes and its interpretation in terms of spiral structure. J Genet 40:67–82

    Article  Google Scholar 

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Acknowledgments

The authors thank Drs. Mary Howe and Andre Pires da Silva for critically reading the manuscript, as well as Dr. Kai Johnsson (EPFL, Switzerland) for sharing unpublished reagents. C. remanei, C. brenneri, and Pristionchus pacificus were obtained from the Caenorhabditis Genetics Center (CGC), which is funded by an NIH Research Infrastructure Program (P40 OD010440). The authors would also like to thank Franziska Friedrich (MPI-CBG, Dresden, Germany) for help in scientific drawing. Research on meiosis in the Müller-Reichert lab is funded by the Deutsche Forschungsgemeinschaft (DFG SPP1384 “Mechansims of Genome Haploidization,” grant MU1423/3-1 and 3-2 to TMR).

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Authors and Affiliations

  1. Experimental Center, Faculty of Medicine Carl Gustav Carus, Technische Universität Dresden, Fiedlerstraße 42, 01307, Dresden, Germany

    Gunar Fabig & Thomas Müller-Reichert

  2. Biology Department, Bucknell University, Lewisburg, PA, 17837, USA

    Leocadia V. Paliulis

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  1. Gunar Fabig
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  2. Thomas Müller-Reichert
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Correspondence to Leocadia V. Paliulis.

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The authors declare that they have no conflict of interest. This article does not contain any studies with human participants performed by any of the authors. All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

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This article is part of a Special Issue on “Recent advances in meiotic chromosome structure, recombination and segregation” edited by Marco Barchi, Paula Cohen and Scott Keeney.

Thomas Müller-Reichert and Leocadia V. Paliulis are joint last authors.

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Fabig, G., Müller-Reichert, T. & Paliulis, L.V. Back to the roots: segregation of univalent sex chromosomes in meiosis. Chromosoma 125, 277–286 (2016). https://doi.org/10.1007/s00412-015-0550-9

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