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Genetica

, Volume 144, Issue 4, pp 385–395 | Cite as

CpSAT-1, a transcribed satellite sequence from the codling moth, Cydia pomonella

  • Pavlína Věchtová
  • Martina Dalíková
  • Miroslava Sýkorová
  • Martina Žurovcová
  • Zoltán Füssy
  • Magda ZrzaváEmail author
Article

Abstract

Satellite DNA (satDNA) is a non-coding component of eukaryotic genomes, located mainly in heterochromatic regions. Relevance of satDNA began to emerge with accumulating evidence of its potential yet hardly comprehensible role that it can play in the genome of many organisms. We isolated the first satDNA of the codling moth (Cydia pomonella, Tortricidae, Lepidoptera), a species with holokinetic chromosomes and a single large heterochromatic element, the W chromosome in females. The satDNA, called CpSAT-1, is located on all chromosomes of the complement, although in different amounts. Surprisingly, the satellite is almost missing in the heterochromatic W chromosome. Additionally, we isolated mRNA from all developmental stages (1st–5th instar larva, pupa, adult), both sexes (adult male and female) and several tissues (Malpighian tubules, gut, heart, testes, and ovaries) of the codling moth and showed the CpSAT-1 sequence was transcribed in all tested samples. Using CpSAT-1 specific primers we amplified, cloned and sequenced 40 monomers from cDNA and gDNA, respectively. The sequence analysis revealed a high mutation rate and the presence of potentially functional motifs, mainly in non-conserved regions of the monomers. Both the chromosomal distribution and the sequence analysis suggest that CPSAT-1 has no function in the C. pomonella genome.

Keywords

Cydia pomonella Satellite DNA Holokinetic chromosomes Sex chromosomes Lepidoptera 

Notes

Acknowledgments

We thank Marie Korchová for rearing of the codling moth and František Marec for critical reading of the manuscript. This research was funded by Grants KJB501410901 of the Grant Agency of the Academy of Sciences of the Czech Republic and 523/09/2106 of the Grant Agency of the Czech Republic (GACR). MD and MS were supported from GACR Grant 14-22765S. Additional support from grant 052/2013/P of the Grant Agency of the University of South Bohemia is also acknowledged. Finally, we wish to thank Juan Pedro M. Camacho, Francisco J. Ruiz-Ruano (both University of Granada, Spain), and two anonymous reviewers for valuable comments to the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

10709_2016_9907_MOESM1_ESM.pdf (61 kb)
Supplementary material 1 (PDF 60 kb)
10709_2016_9907_MOESM2_ESM.pdf (129 kb)
Supplementary material 2 (PDF 129 kb)
10709_2016_9907_MOESM3_ESM.pdf (87 kb)
Supplementary material 3 (PDF 86 kb)

References

  1. Abe H, Mita K, Yasukochi Y et al (2005) Retrotransposable elements on the W chromosome of the silkworm, Bombyx mori. Cytogenet Genome Res 110:144–151. doi: 10.1159/000084946 CrossRefPubMedGoogle Scholar
  2. Abe H, Fujii T, Shimada T, Mita K (2010) Novel non-autonomous transposable elements on W chromosome of the silkworm, Bombyx mori. J Genet 89:375–387CrossRefGoogle Scholar
  3. Alexandrov I, Kazakov A, Tumeneva I et al (2001) Alpha-satellite DNA of primates: old and new families. Chromosoma 110:253–266. doi: 10.1007/s004120100146 CrossRefPubMedGoogle Scholar
  4. Ausubel FM, Brent R, Kingston RE et al (2003) Current protocols in molecular biology. Wiley, New YorkGoogle Scholar
  5. Bardella VB, da Rosa JA, Vanzela ALL (2014) Origin and distribution of AT-rich repetitive DNA families in Triatoma infestans (Heteroptera). Infect Genet Evol 23:106–114. doi: 10.1016/j.meegid.2014.01.035 CrossRefPubMedGoogle Scholar
  6. Biessmann H, Donath J, Walter MF (1996) Molecular characterization of the Anopheles gambiae 2L telomeric region via an integrated transgene. Insect Mol Biol 5:11–20. doi: 10.1111/j.1365-2583.1996.tb00035.x CrossRefPubMedGoogle Scholar
  7. Bizzaro D, Manicardi GC, Bianchi U (1996) Chromosomal localization of a highly repeated EcoRI DNA fragment in Megoura viciae (Homoptera, Aphididae) by nick translation and fluorescence in situ hybridization. Chromosome Res 4:392–396. doi: 10.1007/BF02257275 CrossRefPubMedGoogle Scholar
  8. Charlesworth B, Charlesworth D (2000) The degeneration of Y chromosomes. Philos Trans R Soc Lond B Biol Sci 355:1563–1572. doi: 10.1098/rstb.2000.0717 CrossRefPubMedPubMedCentralGoogle Scholar
  9. Charlesworth B, Sniegowski P, Stephan W (1994) The evolutionary dynamics of repetitive DNA in eukaryotes. Nature 371:215–220. doi: 10.1038/371215a0 CrossRefPubMedGoogle Scholar
  10. Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Res 10:564–567. doi: 10.1111/j.1755-0998.2010.02847.x CrossRefGoogle Scholar
  11. Feliciello I, Akrap I, Ugarković Đ (2015) Satellite DNA modulates gene expression in the beetle Tribolium castaneum after heat stress. PLoS Genet 11:e1005466. doi: 10.1371/journal.pgen.1005466 CrossRefPubMedPubMedCentralGoogle Scholar
  12. Ferbeyre G, Smith J, Cedergren R (1998) Schistosome satellite DNA encodes active hammerhead ribozymes. Mol Cell Biol 18:3880–3888CrossRefPubMedPubMedCentralGoogle Scholar
  13. Fuková I, Nguyen P, Marec F (2005) Codling moth cytogenetics: karyotype, chromosomal location of rDNA, and molecular differentiation of sex chromosomes. Genome 1092:1083–1092. doi: 10.1139/G05-063 CrossRefGoogle Scholar
  14. Fuková I, Traut W, Vítková M et al (2007) Probing the W chromosome of the codling moth, Cydia pomonella, with sequences from microdissected sex chromatin. Chromosoma 116:135–145. doi: 10.1007/s00412-006-0086-0 CrossRefPubMedGoogle Scholar
  15. Gabrielian A, Vlahovicek K, Pongor S (1997) Distribution of sequence-dependent curvature in genomic DNA sequences. FEBS Lett 406:69–74. doi: 10.1016/S0014-5793(97)00236-6 CrossRefPubMedGoogle Scholar
  16. Heckmann S, MacAs J, Kumke K et al (2013) The holocentric species Luzula elegans shows interplay between centromere and large-scale genome organization. Plant J 73:555–565. doi: 10.1111/tpj.12054 CrossRefPubMedGoogle Scholar
  17. Kohany O, Gentles AJ, Hankus L, Jurka J (2006) Annotation, submission and screening of repetitive elements in Repbase: repbaseSubmitter and Censor. BMC Bioinform 7:474. doi: 10.1186/1471-2105-7-474 CrossRefGoogle Scholar
  18. Li Y-X, Kirby ML (2003) Coordinated and conserved expression of alphoid repeat and alphoid repeat-tagged coding sequences. Dev Dyn 228:72–81. doi: 10.1002/dvdy.10355 CrossRefPubMedGoogle Scholar
  19. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452. doi: 10.1093/bioinformatics/btp187 CrossRefPubMedGoogle Scholar
  20. Lorite P, Renault S, Bigot S et al (2002) Genomic organization and transcription of satellite DNA in the ant Aphaenogaster subterranea (Hymenoptera, Formicidae). Genome 616:609–616. doi: 10.1139/G02-022 CrossRefGoogle Scholar
  21. Lu YJ, Kochert GD, Isenhour DJ, Adang MJ (1994) Molecular characterization of a strain-specific repeated DNA sequence in the fall armyworm Spodoptera frugiperda (Lepidoptera: Noctuidae). Insect Mol Biol 3:123–130. doi: 10.1111/j.1365-2583.1994.tb00159.x CrossRefPubMedGoogle Scholar
  22. Mahendran B, Acharya C, Dash R et al (2006) Repetitive DNA in tropical tasar silkworm Antheraea mylitta. Gene 370:51–57. doi: 10.1016/j.gene.2005.11.010 CrossRefPubMedGoogle Scholar
  23. Mandrioli M, Bizzaro D, Manicardi GC et al (1999) Cytogenetic and molecular characterization of a highly repeated DNA sequence in the peach potato aphid Myzus persicae. Chromosoma 108:436–442. doi: 10.1007/s004120050395 CrossRefPubMedGoogle Scholar
  24. Mandrioli M, Manicardi GC, Marec F (2003) Cytogenetic and molecular characterization of the MBSAT1 satellite DNA in holokinetic chromosomes of the cabbage moth, Mamestra brassicae (Lepidoptera). Chromosome Res 11:51–56. doi: 10.1023/A:1022058032217 CrossRefPubMedGoogle Scholar
  25. Masumoto H, Masukata H, Muro Y et al (1989) A human centromere antigen (CENP-B) interacts with a short specific sequence in alphoid DNA, a human centromeric satellite. J Cell Biol 109:1963–1973. doi: 10.1083/jcb.109.5.1963 CrossRefPubMedGoogle Scholar
  26. Metz A, Soret J, Vourc’h C et al (2004) A key role for stress-induced satellite III transcripts in the relocalization of splicing factors into nuclear stress granules. J Cell Sci 117:4551–4558. doi: 10.1242/jcs.01329 CrossRefPubMedGoogle Scholar
  27. Mita K, Kasahara M, Sasaki S et al (2004) The genome sequence of silkworm, Bombyx mori. DNA Res 11:27–35. doi: 10.1093/dnares/11.1.27 CrossRefPubMedGoogle Scholar
  28. Mravinac B, Plohl M, Ugarković D (2004) Conserved patterns in the evolution of Tribolium satellite DNAs. Gene 332:169–177. doi: 10.1016/j.gene.2004.02.055 CrossRefPubMedGoogle Scholar
  29. Nguyen P, Sýkorová M, Šíchová J et al (2013) Neo-sex chromosomes and adaptive potential in tortricid pests. Proc Natl Acad Sci USA 110:6931–6936. doi: 10.1073/pnas.1220372110 CrossRefPubMedPubMedCentralGoogle Scholar
  30. Palomeque T, Lorite P (2008) Satellite DNA in insects: a review. Heredity (Edinb) 100:564–573. doi: 10.1038/hdy.2008.24 CrossRefGoogle Scholar
  31. Plohl M, Luchetti A, Mestrović N, Mantovani B (2008) Satellite DNAs between selfishness and functionality: structure, genomics and evolution of tandem repeats in centromeric (hetero)chromatin. Gene 409:72–82. doi: 10.1016/j.gene.2007.11.013 CrossRefPubMedGoogle Scholar
  32. Reese MG (2001) Application of a time-delay neural network to promoter annotation in the Drosophila melanogaster genome. Comput Chem 26:51–56. doi: 10.1016/S0097-8485(01)00099-7 CrossRefPubMedGoogle Scholar
  33. Renault S, Rouleux-Bonnin F, Periquet G, Bigot Y (1999) Satellite DNA transcription in Diadromus pulchellus (Hymenoptera). Insect Biochem Mol Biol 29:103–111. doi: 10.1016/S0965-1748(98)00113-1 CrossRefPubMedGoogle Scholar
  34. Rouleux-Bonnin F, Renault S, Bigot Y, Periquet G (1996) Transcription of four satellite DNA subfamilies in Diprion pini (Hymenoptera, Symphyta, Diprionidae). Eur J Biochem 238:752–759. doi: 10.1111/j.1432-1033.1996.0752w.x CrossRefPubMedGoogle Scholar
  35. Rouleux-Bonnin F, Bigot S, Bigot Y (2004) Structural and transcriptional features of Bombus terrestris satellite DNA and their potential involvement in the differentiation process. Genome 47:877–888. doi: 10.1139/g04-053 CrossRefPubMedGoogle Scholar
  36. Sahara K, Marec F, Traut W (1999) TTAGG telomeric repeats in chromosomes of some insects and other arthropods. Chromosome Res 7:449–460. doi: 10.1023/A:1009297729547 CrossRefPubMedGoogle Scholar
  37. Sahara K, Yoshido A, Traut W (2012) Sex chromosome evolution in moths and butterflies. Chromosome Res 20:83–94. doi: 10.1007/s10577-011-9262-z CrossRefPubMedGoogle Scholar
  38. Saiga H, Edström JE (1985) Long tandem arrays of complex repeat units in Chironomus telomeres. EMBO J 4:799–804PubMedPubMedCentralGoogle Scholar
  39. Šíchová J, Nguyen P, Dalíková M, Marec F (2013) Chromosomal evolution in tortricid moths: conserved karyotypes with diverged features. PLoS One 8:e64520. doi: 10.1371/journal.pone.0064520 CrossRefPubMedPubMedCentralGoogle Scholar
  40. Spence JM, Blackman RL, Testa JM, Ready PD (1998) A 169-base pair tandem repeat DNA marker for subtelomeric heterochromatin and chromosomal rearrangements in aphids of the Myzus persicae group. Chromosome Res 6:167–175. doi: 10.1023/A:1009251415941 CrossRefPubMedGoogle Scholar
  41. Tamura K, Peterson D, Peterson N et al (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739. doi: 10.1093/molbev/msr121 CrossRefPubMedPubMedCentralGoogle Scholar
  42. Teacher AGF, Griffiths DJ (2011) HapStar: automated haplotype network layout and visualization. Mol Ecol Resour 11:151–153. doi: 10.1111/j.1755-0998.2010.02890.x CrossRefPubMedGoogle Scholar
  43. The International Silkworm Genome Consortium (2008) The genome of a lepidopteran model insect, the silkworm Bombyx mori. Insect Biochem Mol Biol 38:1036–1045. doi: 10.1016/j.ibmb.2008.11.004 CrossRefGoogle Scholar
  44. Traut W, Szczepanowski M, Vítková M et al (2007) The telomere repeat motif of basal Metazoa. Chromosome Res 15:371–382. doi: 10.1007/s10577-007-1132-3 PubMedGoogle Scholar
  45. Traut W, Vogel H, Glöckner G et al (2013) High-throughput sequencing of a single chromosome: a moth W chromosome. Chromosome Res 21:491–505. doi: 10.1007/s10577-013-9376-6 CrossRefPubMedGoogle Scholar
  46. Van’t Hof A, Nguyen P, Dalíková M et al (2012) Linkage map of the peppered moth, Biston betularia (Lepidoptera, Geometridae): a model of industrial melanism. Heredity 110:283–295. doi: 10.1038/hdy.2012.84 CrossRefPubMedPubMedCentralGoogle Scholar
  47. Vítková M, Fuková I, Kubíčková S, Marec F (2007) Molecular divergence of the W chromosomes in pyralid moths (Lepidoptera). Chromosome Res 15:917–930. doi: 10.1007/s10577-007-1173-7 CrossRefPubMedGoogle Scholar
  48. Vlahoviček K, Kaján L, Pongor S (2003) DNA analysis servers: plot.it, bend.it, model.it and IS. Nucl Acids Res 31:3686–3687. doi: 10.1093/nar/gkg559 CrossRefPubMedPubMedCentralGoogle Scholar
  49. Volpe TA, Kidner C, Hall IM et al (2002) Regulation of heterochromatic silencing and histone H3 lysine-9 methylation by RNAi. Science 297:1833–1837. doi: 10.1126/science.1074973 CrossRefPubMedGoogle Scholar
  50. Xia Q, Zhou Z, Lu C et al (2004) A draft sequence for the genome of the domesticated silkworm (Bombyx mori). Science 306:1937–1940. doi: 10.1126/science.1102210 CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Pavlína Věchtová
    • 1
    • 2
    • 3
  • Martina Dalíková
    • 1
    • 2
  • Miroslava Sýkorová
    • 1
    • 2
  • Martina Žurovcová
    • 2
  • Zoltán Füssy
    • 1
    • 3
  • Magda Zrzavá
    • 1
    • 2
    Email author
  1. 1.Faculty of ScienceUniversity of South BohemiaCeske BudejoviceCzech Republic
  2. 2.Institute of EntomologyBiology Centre CASCeske BudejoviceCzech Republic
  3. 3.Institute of ParasitologyBiology Centre CASCeske BudejoviceCzech Republic

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