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.
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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
Bannister AJ, Kouzarides T (2011) Regulation of chromatin by histone modifrications. Cell Res 21:381–395
Bean CJ, Schaner CE, Kelly WG (2004) Meiotic pairing and imprinted X chromatin assembly in Caenorhabditis elegans. Nat Genet 36:100–105
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
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
Callan HG (1986) Lampbrush chromosomes. Springer Verlag, Berlin
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
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
Cruickshank WJ (1971) Follicle cell protein synthesis in moth oocytes. J Insect Physiol 17:217–232
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
Ennis TJ (1976) Sex chromatin and chromosome numbers in Lepidoptera. Can J Genet Cytol 18:119–130
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
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
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
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
Henderson SA (1964) RNA synthesis during male meiosis and spermiogenesis. Chromosoma 15:345–366
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
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
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
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
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
Kunz W (1967) Lampenbürstenchromosomen und multiple Nucleolen bei Orthopteren. Chromosoma 21:446–462
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
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
Lukhtanov VA (2000) Sex chromatin and sex chromosome systems in non-ditrysian Lepidoptera (Insecta). J Zool Syst Evol Res 38:73–79
Macgregor HC (1980) Recent developments in the study of lampbrush chromosomes. Heredity 44:3–35
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
Marec F, Traut W (1993) Synaptonemal complexes in female and male meiotic prophase of Ephestia kuehniella (Lepidoptera). Heredity 71:394–404
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
McKee BD, Handel MA (1993) Sex chromosomes, recombination, and chromatin formation. Chromosoma 102:71–80
Messthaler H, Traut W (1975) Phases of sex chromosome inactivation in Oncopeltus fasciatus and Pyrrhocoris apterus (Insecta Heteroptera). Caryologia 28:501–510
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
Mitter C, Davis DR, Cummings MP (2017) Phylogeny and evolution of Lepidoptera. Annu Rev Entomol 62:265–283
Pigozzi MI (2001) Distribution of MLH1 foci on the synaptonemal complexes of chicken oocytes. Cytogenet Genome Res 95:129–133
Pigozzi MI (2016) The chromosomes of birds during meiosis. Cytogenet Genome Res 150:128–138
Rasch EM (1974) The DNA content of sperm and hemocyte nuclei of the silkworm, Bombyx mori L. Chromosoma 45:1–26
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
Sahara K, Yoshido A, Traut W (2012) Sex chromosome evolution in moths and butterflies. Chromosom Res 20:83–94
Schimenti J (2005) Synapsis or silence. Nat Genet 37:11–13
Schoenmakers S, Wassenaar E, Hoogerbrugge JW, Laven JSE, Grootegoed JA, Baarends WM (2009) Female meiotic sex chromosome inactivation in chicken. PLoS Genet 5:e1000466
Schubert V, Weisshart K (2015) Abundance and distribution of RNA polymerase II in Arabidopsis interphase nuclei. J Exp Bot 66:1687–1698
Solari AJ (1992) Equalization of Z and W axes in chicken and quail oocytes. Cytogenet Cell Genet 59:52–56
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
Tanaka Y (1922) Sex-linkage in the silkworm. J Genet 12:163–172
Tazima Y (1964) The genetics of the silkworm. Academic Press, London
Traut W (1976) Pachytene mapping in the female silkworm, Bombyx mori L. (Lepidoptera). Chromosoma 58:275–284
Traut W (1977) The sequence of transcriptional activity of the oocyte chromosomes in a moth. Chromosomes Today 6:265–271
Traut W, Marec F (1996) Sex chromatin in Lepidoptera. Q Rev Biol 71:239–256
Traut W, Mosbacher C (1968) Geschlechtschromatin bei Lepidopteren. Chromosoma 25:343–356
Traut W, Sahara K, Otto TD, Marec F (1999) Molecular differentiation of sex chromosomes probed by comparative genomic hybridization. Chromosoma 108:173–180
Traut W, Scholz D (1978) Structure, replication and transcriptional activity of the sex-specific heterochromatin in a moth. Exp Cell Res 113:85–94
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
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
Turner JM (2015) Meiotic silencing in mammals. Annu Rev Genet 49:395–412
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
Vítková M, Fuková I, Kubičková S, Marec F (2007) Molecular divergence of the W chromosomes in pyralid moths (Lepidoptera). Chromosom Res 15:917–930
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
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
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
Yoshido A, Bando H, Yasukochi Y, Sahara K (2005) The Bombyx mori karyotype and the assignment of linkage groups. Genetics 170:675–685
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
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
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).
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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
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DOI: https://doi.org/10.1007/s00412-019-00722-8