pp 1–13 | Cite as

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

  • W. TrautEmail author
  • V. Schubert
  • M. Daliková
  • F. Marec
  • K. Sahara
Original Article


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.


Heterochromatin Sex chromatin Germline-limited activity MSCI Bombyx Ephestia 



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 information

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).


  1. 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 110:144–151CrossRefGoogle Scholar
  2. Bannister AJ, Kouzarides T (2011) Regulation of chromatin by histone modifrications. Cell Res 21:381–395CrossRefGoogle Scholar
  3. Bean CJ, Schaner CE, Kelly WG (2004) Meiotic pairing and imprinted X chromatin assembly in Caenorhabditis elegans. Nat Genet 36:100–105CrossRefGoogle Scholar
  4. Buntrock L, Marec F, Krueger S, Traut W (2012) Organ growth without cell division: somatic polyploidy in a moth, Ephestia kuehniella. Genome 55:755–763CrossRefGoogle Scholar
  5. 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 119:135–142CrossRefGoogle Scholar
  6. Callan HG (1986) Lampbrush chromosomes. Springer Verlag, BerlinCrossRefGoogle Scholar
  7. Carrel L, Brown CJ (2017) When the Lyon(ized chromosome) roars: ongoing expression from an inactive X chromosome. Philos Trans R Soc B 372:20160355CrossRefGoogle Scholar
  8. Caspari EW, Gottlieb FJ (1975) The Mediterranean meal moth, Ephestia kuehniella. In: King RC (ed) Handbook of genetics. Plenum Press, New York, pp 125–147Google Scholar
  9. Cruickshank WJ (1971) Follicle cell protein synthesis in moth oocytes. J Insect Physiol 17:217–232CrossRefGoogle Scholar
  10. 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 108:709–719CrossRefGoogle Scholar
  11. Ennis TJ (1976) Sex chromatin and chromosome numbers in Lepidoptera. Can J Genet Cytol 18:119–130CrossRefGoogle Scholar
  12. 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 8:1486CrossRefGoogle Scholar
  13. Gaginskaya E, Kulikova T, Krasikova A (2009) Avian lampbrush chromosomes: a powerful tool for the exploration of genome expression. Cytogenet Genome Res 124:251–267CrossRefGoogle Scholar
  14. 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 317:54–61Google Scholar
  15. 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:e1002560CrossRefGoogle Scholar
  16. Henderson SA (1964) RNA synthesis during male meiosis and spermiogenesis. Chromosoma 15:345–366CrossRefGoogle Scholar
  17. 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 133–146Google Scholar
  18. 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 38:663–671CrossRefGoogle Scholar
  19. Hore TA, Wakefield MJ, Graves JAM (2008) X-chromosome inactivation. eLS. John Wiley & Sons Ltd., ChichesterGoogle Scholar
  20. Kawamura N (1979) Cytological studies on the mosaic silkworms induced by low temperature treatment. Chromosoma 74:179–188CrossRefGoogle Scholar
  21. 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 17:2144–2151CrossRefGoogle Scholar
  22. 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 509:633–636CrossRefGoogle Scholar
  23. Kunz W (1967) Lampenbürstenchromosomen und multiple Nucleolen bei Orthopteren. Chromosoma 21:446–462CrossRefGoogle Scholar
  24. 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 24:561–569CrossRefGoogle Scholar
  25. 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. CrossRefGoogle Scholar
  26. Lukhtanov VA (2000) Sex chromatin and sex chromosome systems in non-ditrysian Lepidoptera (Insecta). J Zool Syst Evol Res 38:73–79CrossRefGoogle Scholar
  27. Macgregor HC (1980) Recent developments in the study of lampbrush chromosomes. Heredity 44:3–35CrossRefGoogle Scholar
  28. 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 49–63Google Scholar
  29. Marec F, Traut W (1993) Synaptonemal complexes in female and male meiotic prophase of Ephestia kuehniella (Lepidoptera). Heredity 71:394–404CrossRefGoogle Scholar
  30. Marec F, Traut W (1994) Sex chromosome pairing and sex chromatin bodies in W-Z translocation strains of Ephestia kuehniella (Lepidoptera). Genome 37:426–435CrossRefGoogle Scholar
  31. McKee BD, Handel MA (1993) Sex chromosomes, recombination, and chromatin formation. Chromosoma 102:71–80CrossRefGoogle Scholar
  32. Messthaler H, Traut W (1975) Phases of sex chromosome inactivation in Oncopeltus fasciatus and Pyrrhocoris apterus (Insecta Heteroptera). Caryologia 28:501–510CrossRefGoogle Scholar
  33. 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 13:55–65CrossRefGoogle Scholar
  34. Mitter C, Davis DR, Cummings MP (2017) Phylogeny and evolution of Lepidoptera. Annu Rev Entomol 62:265–283CrossRefGoogle Scholar
  35. Pigozzi MI (2001) Distribution of MLH1 foci on the synaptonemal complexes of chicken oocytes. Cytogenet Genome Res 95:129–133CrossRefGoogle Scholar
  36. Pigozzi MI (2016) The chromosomes of birds during meiosis. Cytogenet Genome Res 150:128–138CrossRefGoogle Scholar
  37. Rasch EM (1974) The DNA content of sperm and hemocyte nuclei of the silkworm, Bombyx mori L. Chromosoma 45:1–26CrossRefGoogle Scholar
  38. 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 112:48–55CrossRefGoogle Scholar
  39. Sahara K, Yoshido A, Traut W (2012) Sex chromosome evolution in moths and butterflies. Chromosom Res 20:83–94CrossRefGoogle Scholar
  40. Schimenti J (2005) Synapsis or silence. Nat Genet 37:11–13CrossRefGoogle Scholar
  41. Schoenmakers S, Wassenaar E, Hoogerbrugge JW, Laven JSE, Grootegoed JA, Baarends WM (2009) Female meiotic sex chromosome inactivation in chicken. PLoS Genet 5:e1000466CrossRefGoogle Scholar
  42. Schubert V, Weisshart K (2015) Abundance and distribution of RNA polymerase II in Arabidopsis interphase nuclei. J Exp Bot 66:1687–1698CrossRefGoogle Scholar
  43. Solari AJ (1992) Equalization of Z and W axes in chicken and quail oocytes. Cytogenet Cell Genet 59:52–56CrossRefGoogle Scholar
  44. 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 1:153–166CrossRefGoogle Scholar
  45. Tanaka Y (1922) Sex-linkage in the silkworm. J Genet 12:163–172CrossRefGoogle Scholar
  46. Tazima Y (1964) The genetics of the silkworm. Academic Press, LondonGoogle Scholar
  47. Traut W (1976) Pachytene mapping in the female silkworm, Bombyx mori L. (Lepidoptera). Chromosoma 58:275–284CrossRefGoogle Scholar
  48. Traut W (1977) The sequence of transcriptional activity of the oocyte chromosomes in a moth. Chromosomes Today 6:265–271Google Scholar
  49. Traut W, Marec F (1996) Sex chromatin in Lepidoptera. Q Rev Biol 71:239–256CrossRefGoogle Scholar
  50. Traut W, Mosbacher C (1968) Geschlechtschromatin bei Lepidopteren. Chromosoma 25:343–356CrossRefGoogle Scholar
  51. Traut W, Sahara K, Otto TD, Marec F (1999) Molecular differentiation of sex chromosomes probed by comparative genomic hybridization. Chromosoma 108:173–180CrossRefGoogle Scholar
  52. Traut W, Scholz D (1978) Structure, replication and transcriptional activity of the sex-specific heterochromatin in a moth. Exp Cell Res 113:85–94CrossRefGoogle Scholar
  53. Traut W, Vogel H, Glöckner G, Hartmann E, Heckel DG (2013) High-throughput sequencing of a single chromosome: a moth W chromosome. Chromosom Res 21:491–505CrossRefGoogle Scholar
  54. 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 94:125–131CrossRefGoogle Scholar
  55. Turner JM (2015) Meiotic silencing in mammals. Annu Rev Genet 49:395–412CrossRefGoogle Scholar
  56. 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 37:41–47CrossRefGoogle Scholar
  57. Vítková M, Fuková I, Kubičková S, Marec F (2007) Molecular divergence of the W chromosomes in pyralid moths (Lepidoptera). Chromosom Res 15:917–930CrossRefGoogle Scholar
  58. Walters J, Hardcastle T (2011) Getting a full dose? Reconsidering sex chromosome dosage compensation in the silkworm, Bombyx mori. Genome Biol Evol 3:491–504CrossRefGoogle Scholar
  59. 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:e1725CrossRefGoogle Scholar
  60. 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 78:275–291CrossRefGoogle Scholar
  61. Yoshido A, Bando H, Yasukochi Y, Sahara K (2005) The Bombyx mori karyotype and the assignment of linkage groups. Genetics 170:675–685CrossRefGoogle Scholar
  62. 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 116:424–433CrossRefGoogle Scholar
  63. 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 115:8752–8756CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Institut für Biologie, Zentrum für medizinische Struktur- und ZellbiologieUniversität zu LübeckLübeckGermany
  2. 2.Leibniz Institute of Plant Genetics and Crop Plant Research (IPK) GaterslebenSeelandGermany
  3. 3.Biology Centre of the Czech Academy of Sciences, Institute of EntomologyČeské BudĕjoviceCzech Republic
  4. 4.Laboratory of Applied Entomology, Faculty of AgricultureIwate UniversityMoriokaJapan

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