Skip to main content
Log in

Activity and inactivity of moth sex chromosomes in somatic and meiotic cells

  • Original Article
  • Published:
Chromosoma Aims and scope Submit manuscript

Abstract

Moths and butterflies (Lepidoptera) are the most species-rich group of animals with female heterogamety, females mostly having a WZ, males a ZZ sex chromosome constitution. We studied chromatin conformation, activity, and inactivity of the sex chromosomes in the flour moth Ephestia kuehniella and the silkworm Bombyx mori, using immunostaining with anti-H3K9me2/3, anti-RNA polymerase II, and fluoro-uridine (FU) labelling of nascent transcripts, with conventional widefield fluorescence microscopy and ‘spatial structured illumination microscopy’ (3D-SIM). The Z chromosome is euchromatic in somatic cells and throughout meiosis. It is transcriptionally active in somatic cells and in the postpachaytene stage of meiosis. The W chromosome in contrast is heterochromatic in somatic cells as well as in meiotic cells at pachytene, but euchromatic and transcriptionally active like all other chromosomes at postpachytene. As the W chromosomes are apparently devoid of protein-coding genes, their transcripts must be non-coding. We found no indication of ‘meiotic sex chromosome inactivation’ (MSCI) in the two species.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12
Fig. 13
Fig. 14
Fig. 15
Fig. 16

Similar content being viewed by others

References

  • Abe H, Mita K, Yasukochi Y, Oshiki T, Shimada T (2005) Retrotransposable elements on the W chromosome of the silkworm, Bombyx mori. Cytogenet Genome Res 110:144–151

    CAS  PubMed  Google Scholar 

  • Bannister AJ, Kouzarides T (2011) Regulation of chromatin by histone modifrications. Cell Res 21:381–395

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Buntrock L, Marec F, Krueger S, Traut W (2012) Organ growth without cell division: somatic polyploidy in a moth, Ephestia kuehniella. Genome 55:755–763

    PubMed  Google Scholar 

  • Cabrero J, Teruel M, Carmona FD, Jiménez R, Camacho JPM (2007) Histone H3 lysine 9 acetylation pattern suggests that X and B chromosomes are silenced during entire male meiosis in a grasshopper. Cytogenet Genome Res 119:135–142

    CAS  PubMed  Google Scholar 

  • Callan HG (1986) Lampbrush chromosomes. Springer Verlag, Berlin

    Google Scholar 

  • Carrel L, Brown CJ (2017) When the Lyon(ized chromosome) roars: ongoing expression from an inactive X chromosome. Philos Trans R Soc B 372:20160355

    Google Scholar 

  • Caspari EW, Gottlieb FJ (1975) The Mediterranean meal moth, Ephestia kuehniella. In: King RC (ed) Handbook of genetics. Plenum Press, New York, pp 125–147

    Google Scholar 

  • Cruickshank WJ (1971) Follicle cell protein synthesis in moth oocytes. J Insect Physiol 17:217–232

    Google Scholar 

  • Dalíková M, Zrzavá M, Hladová I, Nguyen P, Šonský I, Flegrová M, Kubíčková S, Voleníková A, Kawahara AY, Peters RS, Marec F (2017) New insights into the evolution of the W chromosome in Lepidoptera. J Hered 108:709–719

    PubMed  Google Scholar 

  • Ennis TJ (1976) Sex chromatin and chromosome numbers in Lepidoptera. Can J Genet Cytol 18:119–130

    CAS  PubMed  Google Scholar 

  • Fraïsse C, Picard MAL, Vicoso B (2017) The deep conservation of the Lepidoptera Z chromosome suggests a non-canonical origin of the W. Nat Commun 8:1486

    PubMed  PubMed Central  Google Scholar 

  • Gaginskaya E, Kulikova T, Krasikova A (2009) Avian lampbrush chromosomes: a powerful tool for the exploration of genome expression. Cytogenet Genome Res 124:251–267

    CAS  PubMed  Google Scholar 

  • Guélin M (1994) Activité de l'hétérochromatine sexuelle-W et accumulation du nuage dans les cellules nouricières du Lépidoptère Ephestia kuehniella. C R Acd Sci Paris, Sciences de la vie 317:54–61

    Google Scholar 

  • Guioli S, Lovell-Badge R, Turner JM (2012) Error-prone ZW pairing and no evidence for meiotic sex chromosome inactivation in the chicken germ line. PLoS Genet 8:e1002560

    CAS  PubMed  PubMed Central  Google Scholar 

  • Henderson SA (1964) RNA synthesis during male meiosis and spermiogenesis. Chromosoma 15:345–366

    CAS  Google Scholar 

  • Hennig W (1987) The Y chromosomal lampbrush loops of Drosophila. In: Hennig W (ed) Results and problems in cell differentiation, 14th edn. Springer, Berlin, Heidelberg, pp 133–146

    Google Scholar 

  • Hess O (1974) Local structural variations of the Y chromosome of Drosophila hydei and their correlation to genetic activity. Cold Spring Harb Symp Quant Biol 38:663–671

    CAS  PubMed  Google Scholar 

  • Hore TA, Wakefield MJ, Graves JAM (2008) X-chromosome inactivation. eLS. John Wiley & Sons Ltd., Chichester

  • Kawamura N (1979) Cytological studies on the mosaic silkworms induced by low temperature treatment. Chromosoma 74:179–188

    Google Scholar 

  • Kawaoka S, Kadota K, Arai Y, Suzuki Y, Fujii T, Abe H, Yasukochi Y, Mita K, Sugano S, Shimizu K, Tomari Y, Shimada T, Katsuma S (2011) The silkworm W chromosome is a source of female-enriched piRNAs. RNA 17:2144–2151

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kiuchi T, Koga H, Kawamoto M, Shoji K, Sakai H, Arai Y, Ishihara G, Kawaoka S, Sugano S, Shimada T, Suzuki Y, Suzuki MG, Katsuma S (2014) A single female-specific piRNA is the primary determiner of sex in the silkworm. Nature 509:633–636

    CAS  PubMed  Google Scholar 

  • Kunz W (1967) Lampenbürstenchromosomen und multiple Nucleolen bei Orthopteren. Chromosoma 21:446–462

    CAS  PubMed  Google Scholar 

  • Lee J, Kiuchi T, Kawamoto M, Shimada T, Katsuma S (2015) Identification and functional analysis of a Masculinizer orthologue in Trilocha varians (Lepidoptera: Bombycidae). Insect Mol Biol 24:561–569

    CAS  PubMed  Google Scholar 

  • Li Y, Wang G, Tian J, Liu H, Yang H, Yi Y, Wang J, Shi X, Jiang F, Yao B, Zhang Z (2012) Transcriptome analysis of the silkworm (Bombyx mori) by high-throughput RNA sequencing. PLoS One 7:e43713. https://doi.org/10.1371/journal.pone.0043713

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lukhtanov VA (2000) Sex chromatin and sex chromosome systems in non-ditrysian Lepidoptera (Insecta). J Zool Syst Evol Res 38:73–79

    Google Scholar 

  • Macgregor HC (1980) Recent developments in the study of lampbrush chromosomes. Heredity 44:3–35

    Google Scholar 

  • Marec F, Sahara K, Traut W (2010) Rise and fall of the W chromosome in Lepidoptera. In: Goldsmith MR, Marec F (eds) Molecular biology and genetics of the Lepidoptera. CRC Press, Boca Raton, pp 49–63

    Google Scholar 

  • Marec F, Traut W (1993) Synaptonemal complexes in female and male meiotic prophase of Ephestia kuehniella (Lepidoptera). Heredity 71:394–404

    Google Scholar 

  • Marec F, Traut W (1994) Sex chromosome pairing and sex chromatin bodies in W-Z translocation strains of Ephestia kuehniella (Lepidoptera). Genome 37:426–435

    CAS  PubMed  Google Scholar 

  • McKee BD, Handel MA (1993) Sex chromosomes, recombination, and chromatin formation. Chromosoma 102:71–80

    CAS  PubMed  Google Scholar 

  • Messthaler H, Traut W (1975) Phases of sex chromosome inactivation in Oncopeltus fasciatus and Pyrrhocoris apterus (Insecta Heteroptera). Caryologia 28:501–510

    Google Scholar 

  • Ni Z, Schwartz BE, Werner J, Suarez JR, Lis JT (2004) Coordination of transcription, RNA processing, and surveillance by P-TEFb kinase on heat shock genes. Mol Cell 13:55–65

    CAS  PubMed  Google Scholar 

  • Mitter C, Davis DR, Cummings MP (2017) Phylogeny and evolution of Lepidoptera. Annu Rev Entomol 62:265–283

    CAS  PubMed  Google Scholar 

  • Pigozzi MI (2001) Distribution of MLH1 foci on the synaptonemal complexes of chicken oocytes. Cytogenet Genome Res 95:129–133

    CAS  Google Scholar 

  • Pigozzi MI (2016) The chromosomes of birds during meiosis. Cytogenet Genome Res 150:128–138

    PubMed  Google Scholar 

  • Rasch EM (1974) The DNA content of sperm and hemocyte nuclei of the silkworm, Bombyx mori L. Chromosoma 45:1–26

    CAS  PubMed  Google Scholar 

  • Sahara K, Yoshido A, Kawamura N, Ohnuma A, Abe H, Mita K, Oshiki T, Shimada T, Asano S, Bando H, Yasukochi Y (2003) W-derived BAC probes as a new tool for identification of the W chromosome and its aberrations in Bombyx mori. Chromosoma 112:48–55

    CAS  PubMed  Google Scholar 

  • Sahara K, Yoshido A, Traut W (2012) Sex chromosome evolution in moths and butterflies. Chromosom Res 20:83–94

    CAS  Google Scholar 

  • Schimenti J (2005) Synapsis or silence. Nat Genet 37:11–13

    CAS  PubMed  Google Scholar 

  • Schoenmakers S, Wassenaar E, Hoogerbrugge JW, Laven JSE, Grootegoed JA, Baarends WM (2009) Female meiotic sex chromosome inactivation in chicken. PLoS Genet 5:e1000466

    PubMed  PubMed Central  Google Scholar 

  • Schubert V, Weisshart K (2015) Abundance and distribution of RNA polymerase II in Arabidopsis interphase nuclei. J Exp Bot 66:1687–1698

    CAS  PubMed  PubMed Central  Google Scholar 

  • Solari AJ (1992) Equalization of Z and W axes in chicken and quail oocytes. Cytogenet Cell Genet 59:52–56

    CAS  PubMed  Google Scholar 

  • Solovei I, Gaginskaya E, Hutchison N, Macgregor H (1993) Avian sex chromosomes in the lampbrush form: the ZW lampbrush bivalents from six species of bird. Chromosom Res 1:153–166

    CAS  Google Scholar 

  • Tanaka Y (1922) Sex-linkage in the silkworm. J Genet 12:163–172

    Google Scholar 

  • Tazima Y (1964) The genetics of the silkworm. Academic Press, London

    Google Scholar 

  • Traut W (1976) Pachytene mapping in the female silkworm, Bombyx mori L. (Lepidoptera). Chromosoma 58:275–284

    CAS  PubMed  Google Scholar 

  • Traut W (1977) The sequence of transcriptional activity of the oocyte chromosomes in a moth. Chromosomes Today 6:265–271

    Google Scholar 

  • Traut W, Marec F (1996) Sex chromatin in Lepidoptera. Q Rev Biol 71:239–256

    CAS  PubMed  Google Scholar 

  • Traut W, Mosbacher C (1968) Geschlechtschromatin bei Lepidopteren. Chromosoma 25:343–356

    CAS  PubMed  Google Scholar 

  • Traut W, Sahara K, Otto TD, Marec F (1999) Molecular differentiation of sex chromosomes probed by comparative genomic hybridization. Chromosoma 108:173–180

    CAS  PubMed  Google Scholar 

  • Traut W, Scholz D (1978) Structure, replication and transcriptional activity of the sex-specific heterochromatin in a moth. Exp Cell Res 113:85–94

    CAS  PubMed  Google Scholar 

  • Traut W, Vogel H, Glöckner G, Hartmann E, Heckel DG (2013) High-throughput sequencing of a single chromosome: a moth W chromosome. Chromosom Res 21:491–505

    CAS  Google Scholar 

  • Traut W, Weith A, Traut G (1986) Synaptic adjustment, non-homologous pairing, and non-pairing of homologous segments in sex chromosome mutants of Ephestia kuehniella (Insecta, Lepidoptera). Chromosoma 94:125–131

    Google Scholar 

  • Turner JM (2015) Meiotic silencing in mammals. Annu Rev Genet 49:395–412

    CAS  PubMed  Google Scholar 

  • Turner JM, Mahadevaiah SK, Fernandez-Capetillo O, Nussenzweig A, Xu X, Deng CX, Burgoyne PS (2005) Silencing of unsynapsed meiotic chromosomes in the mouse. Nat Genet 37:41–47

    CAS  PubMed  Google Scholar 

  • Vítková M, Fuková I, Kubičková S, Marec F (2007) Molecular divergence of the W chromosomes in pyralid moths (Lepidoptera). Chromosom Res 15:917–930

    Google Scholar 

  • Walters J, Hardcastle T (2011) Getting a full dose? Reconsidering sex chromosome dosage compensation in the silkworm, Bombyx mori. Genome Biol Evol 3:491–504

    CAS  PubMed  PubMed Central  Google Scholar 

  • Weisshart K, Fuchs J, Schubert V (2016) Structured illumination microscopy (SIM) and photoactivated localization microscopy (PALM) to analyze the abundance and distribution of RNA polymerase II molecules on flow-sorted Arabidopsis nuclei. Bio-protocol 6:e1725

    Google Scholar 

  • Weith A, Traut W (1980) Synaptonemal complexes with associated chromatin in a moth, Ephestia kuehniella Z. The fine structure of the W chromosomal heterochromatin. Chromosoma 78:275–291

    Google Scholar 

  • Yoshido A, Bando H, Yasukochi Y, Sahara K (2005) The Bombyx mori karyotype and the assignment of linkage groups. Genetics 170:675–685

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yoshido A, Marec F, Sahara K (2016) The fate of W chromosomes in hybrids between wild silkmoths, Samia cynthia ssp.: no role in sex determination and reproduction. Heredity 116:424–433

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang Z, Niu B, Ji D, Li M, Li K, James AA, Tan A, Huanga Y (2018) Silkworm genetic sexing through W chromosome-linked, targeted gene integration. PNAS 115:8752–8756

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The skilled help of Conni Reuter (Lübeck, Germany) is gratefully acknowledged. We thank the National BioResource Project of Japan and the Laboratory of Applied Molecular Entomology in Hokkaido University for providing p50 and a hybrid B. mori, respectively.

Funding

M.D. and F.M. were supported by grants 17-17211S and 17-1713713S respectively of the Czech Science Foundation. K.S. received support from Kaken No. 16H05050 of the Japan Society for the Promotion of Science (JSPS).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to W. Traut.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Traut, W., Schubert, V., Daliková, M. et al. Activity and inactivity of moth sex chromosomes in somatic and meiotic cells. Chromosoma 128, 533–545 (2019). https://doi.org/10.1007/s00412-019-00722-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00412-019-00722-8

Keywords

Navigation