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Transcription of Satellite DNAs in Insects

Chapter
Part of the Progress in Molecular and Subcellular Biology book series (PMSB, volume 51)

Abstract

The very complex life cycle and extreme diversity of insect life forms require a carefully regulated network of biological processes to switch on and off the right genes at the right time. Chromatin condensation is an important regulatory mechanism of gene silencing as well as gene activation for the hundreds of functional protein genes harbored in heterochromatic regions of different insect species. Being the major heterochromatin constituents, satellite DNAs (satDNAs) serve important roles in heterochromatin regulation in insects in general. Their expression occurs in all developmental stages, being the highest during embryogenesis. satDNA transcripts range from small RNAs, corresponding in size to siRNAs, and piwiRNAs, to large, a few kb long RNAs. The long transcripts are preferentially nonpolyadenylated and remain in the nucleus. The actively regulated expression of satDNAs by cis or trans elements as well as by environmental stress, rather than constitutive transcription, speaks in favor of their involvement in differentiation, development, and environmental response.

Keywords

Satellite DNAs Satellite Repeat Heterochromatin Formation Satellite Sequence Hammerhead Ribozyme 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

This work was supported by EU FP6 Marie Curie Transfer of Knowledge Grant MTKD-CT-2006-042248 and grant 00982604 from the Croatian Ministry of Science. Isidoro Feliciello is Marie Curie Fellow at Ruder Boskovic Institute.

References

  1. Amaral PP, Mattick JS (2008) Noncoding RNA in development. Mamm Genome 19:454–492PubMedCrossRefGoogle Scholar
  2. Aravin AA, Lagos-Quintana M, Yalcin A, Zavolan M, Marks D, Snyder B et al (2003) The small RNA profile during Drosophila melanogaster development. Dev Cell 5:337–350PubMedCrossRefGoogle Scholar
  3. Arnason U, Höglund M, Widegren B (1984) Conservation of highly repetitive DNA in cetaceans. Chromosoma 89:238–242PubMedCrossRefGoogle Scholar
  4. Bonaccorsi S, Gatti M, Pisano C, Lohe A (1990) Transcription of a satellite DNA on two Y chromosome loops of Drosophila melanogaster. Chromosoma 99(4):260–266PubMedCrossRefGoogle Scholar
  5. Borstnik B, Pumpernik D, Lukman D, Ugarković Đ, Plohl M (1994) Tandemly repeated pentanucleotides in DNA sequences of eukaryotes. Nucleic Acids Res 22(16):3412–3417PubMedCrossRefGoogle Scholar
  6. Brennecke J, Aravin AA, Stark A, Dus M, Kellis M, Sachidanandam R, Hannon GJ (2007) Discrete small RNA generating loci as master regulators of transposon activity in Drosophila. Cell 128:1089–1103PubMedCrossRefGoogle Scholar
  7. Bruvo-Mađarić B, Plohl M, Ugarković Đ (2007) Wide distribution of related satellite DNA families within the genus Pimelia (Tenebrionidae). Genetica 130:35–42PubMedCrossRefGoogle Scholar
  8. Charlesworth B, Sniegowski P, Stephan W (1994) The evolutionary dynamics of repetitive DNA in eukaryotes. Nature 371:215–220PubMedCrossRefGoogle Scholar
  9. Coats SR, Zhang Y, Epstein LM (1994) Transcription of satellite 2 DNA from the newt is driven by a snRNA type of promoter. Nucleic Acids Res 22:4697–4704PubMedCrossRefGoogle Scholar
  10. Croisetiere S, Bernatchez L, Belhumeur P (2010) Temperature and length-dependent modulation of the MH class IIβ gene expression in brook charr (Salvelinus fontinalis) by a cis-acting minisatellite. Mol Immun 47:1817–1829CrossRefGoogle Scholar
  11. Davis CA, Wyatt GR (1989) Distribution and sequence homogeneity of an abundant satellite DNA in the beetle, Tenebrio molitor. Nucleic Acids Res 17(14):5579–5586PubMedCrossRefGoogle Scholar
  12. De la Herrán R, Fontana F, Lanfredi M, Congiu L, Leis M, Rossi R, Ruiz Rejón C, Ruiz Rejón M, Garrido-Ramos MA (2001) Slow rates of evolution and sequence homogenization in an ancient satellite DNA family of sturgeons. Mol Biol Evol 18:432–436CrossRefGoogle Scholar
  13. Diaz MO, Barsacchi-Pilone G, Mahon KA, Gall JG (1981) Transcripts from both DNA strands of a satellite DNA occur on lampbrush chromosome loops of the newt Notophthalmus. Cell 24:649–659PubMedCrossRefGoogle Scholar
  14. Dimitri P, Caizzi R, Giordano E, Carmela Accardo M, Lattanzi G, Biamonti G (2009) Constitutive heterochromatin: a surprising variety of expressed sequences. Chromosoma 118:419–435PubMedCrossRefGoogle Scholar
  15. Djupedal I, Kos-Braun IC, Mosher RA, Söderholm N, Simmer F, Hardcastle TJ, Fender A, Heidrich N, Kagansky A, Bayne E, Wagner EG, Baulcombe DC, Allshire RC, Ekwall K (2009) Analysis of small RNA in fission yeast; centromeric siRNAs are potentially generated through a structured RNA. EMBO J 28(24):3832–3844PubMedCrossRefGoogle Scholar
  16. Dover G (2002) Molecular drive. Trends Genet 18:587–589PubMedCrossRefGoogle Scholar
  17. Durajlija Žinić S, Ugarković Đ, Cornudella L, Plohl M (2000) A novel interspersed type of organization of satellite DNAs in Tribolium madens heterochromatin. Chromosome Res 8:201–212CrossRefGoogle Scholar
  18. Ebert A, Lein S, Schotta G, Reuter G (2006) Histone modification and the control of heterochromatin gene silencing in Drosophila. Chromosome Res 14:377–392PubMedCrossRefGoogle Scholar
  19. Epstein LM, Mahon KA, Gall JG (1986) Transcription of a satellite DNA in the newt. J Cell Biol 103:1137–1144PubMedCrossRefGoogle Scholar
  20. Epstein LM, Gall JG (1987) Self-cleaving transcripts of a satellite DNA in a newt. Cell 48:535–543PubMedCrossRefGoogle Scholar
  21. Fagegaltier D, Bougé AL, Berry B, Poisot E, Sismeiro O, Coppée JY, Théodore L, Voinnet O, Antoniewski C (2009) The endogenous siRNA pathway is involved in heterochromatin formation in Drosophila. Proc Natl Acad Sci USA 106:21258–21263PubMedCrossRefGoogle Scholar
  22. Ferbeyre G, Smith JM, Cedergren R (1998) Schistosome satellite DNA encodes active hammerhead-ribozymes. Mol Cell Biol 18:3880–3888PubMedGoogle Scholar
  23. Ferree PM, Barbash DA (2009) Species-specific heterochromatin prevents mitotic chromosome segregation to cause hybrid lethality in Drosophila. PLoS Biol 7:e1000234PubMedCrossRefGoogle Scholar
  24. Fitzgerald DJ, Dryden GL, Bronson EC, Williams JS, Anderson JN (1994) Conserved pattern of bending in satellite and nucleosome positioning DNA. J Biol Chem 269:21303–21314PubMedGoogle Scholar
  25. Fry K, Salser W (1977) Nucleotide sequences of HS-α satellite DNA from kangaroo rat Dipodomys ordii and characterisation of similar sequences in other rodents. Cell 12:1069–1084PubMedCrossRefGoogle Scholar
  26. Gaubatz JW, Cutler RG (1990) Mouse satellite DNA is transcribed in senescent cardiac muscle. J Biol Chem 265:17753–17758PubMedGoogle Scholar
  27. Green B, Pabon-Pena LM, Graham TA, Peach SE, Coats SR, Epstein LM (1993) Conserved sequence and functional domains in satellite 2 from three families of salamanders. Mol Biol Evol 10:732–750PubMedGoogle Scholar
  28. Hamilton A, Voinnet O, Chappell L, Baulcombe D (2002) Two classes of short interfering RNA in RNA silencing. EMBO J 21:4671PubMedCrossRefGoogle Scholar
  29. Kipling D, Warburton PE (1997) Centromeres, CENP-B and Tigger too. Trends Genet 13:141–145PubMedCrossRefGoogle Scholar
  30. Klattenhoff C, Xi H, Li C, Lee S, Xu J, Khurana JS, Zhang F, Schultz N, Koppetsch BS, Nowosielska A, Seitz H, Zamore PD, Weng Z, Theurkauf WE (2009) The Drosophila HP1 homolog Rhino is required for transposon silencing and piRNA production by dual-strand clusters. Cell 138(6):1137–1149PubMedCrossRefGoogle Scholar
  31. Li YX, Kirby ML (2003) Coordinated and conserved expression of alphoid repeat and alphoid repeat-tagged coding sequences. Dev Dyn 228:72–81PubMedCrossRefGoogle Scholar
  32. Lohe A, Roberts P (1988) Evolution of satellite DNA sequences in Drosophila. In: Verma RS (ed) Heterochromatin: molecular and structural aspects. Cambridge University Press, Cambridge, pp 148–186Google Scholar
  33. Lorite P, Carrillo JA, Tinaut A, Palomeque T (2002a) Comparative study of satellite DNA in ants of the Messor genus. Gene 297(1–2):113–122PubMedCrossRefGoogle Scholar
  34. Lorite P, Renault S, Rouleux-Bonnin F, Bigot S, Periquet G, Palomeque T (2002b) Genomic organization and transcription of satellite DNA in the ant Aphaenogaster subterranea (Hymenoptera, Formicidae). Genome 45:609–616PubMedCrossRefGoogle Scholar
  35. Lu BY, Ma J, Eissenberg JC (1998) Developmental regulation of heterochromatin-mediated silencing in Drosophila. Development 125:2223–2234PubMedGoogle Scholar
  36. Lucchesi JC, Kelly WG, Panning B (2005) Chromatin remodeling in dosage compensation. Annu Rev Genet 39:615–651PubMedCrossRefGoogle Scholar
  37. Martínez-Guitarte JL, Díez JL, Morcillo G (2008) Transcription and activation under environmental stress of the complex telomeric repeats of Chironomus thummi. Chromosome Res 16(8):1085–1096PubMedCrossRefGoogle Scholar
  38. Masumoto H, Masukata H, Muro Y, Nozaki N, Okazaki T (1989) A human centromere antigen (CENP-B) interacts with a short specific sequence in alphoid DNA, a human centromeric satellite. J Cell Biol 109:1963–1973PubMedCrossRefGoogle Scholar
  39. Meštrović N, Plohl M, Mravinac B, Ugarković Ð (1998) Evolution of satellite DNAs from the genus Palorus – experimental evidence for the ‘library’ hypothesis. Mol Biol Evol 15:1062–1068PubMedCrossRefGoogle Scholar
  40. Metz A, Soret J, Vourc’h C, Tazi J, Jolly C (2004) A key role for stress-induced satellite III transcripts in the relocalization of splicing factors into nuclear stress granules. J Cell Sci 117:4551–4558PubMedCrossRefGoogle Scholar
  41. Mravinac B, Plohl M, Meštrović N, Ugarković Đ (2002) Sequence of PRAT satellite DNA “frozen” in some coleopteran species. J Mol Evol 54:774–783PubMedCrossRefGoogle Scholar
  42. Mravinac B, Plohl M, Ugarković Đ (2004) Conserved patterns in the evolution of Tribolium satellite DNAs. Gene 332:169–177PubMedCrossRefGoogle Scholar
  43. Mravinac B, Plohl M, Ugarković Đ (2005) Preservation and high sequence conservation of satellite DNAs suggest functional constraints. J Mol Evol 61:542–550PubMedCrossRefGoogle Scholar
  44. Ohzeki J, Nakano M, Okada T, Masumoto H (2002) CENP-B box is required for de novo centromere chromatin assembly on human alphoid DNA. J Cell Biol 159:765–775PubMedCrossRefGoogle Scholar
  45. Palomeque T, Lorite P (2008) Satellite DNA in insects: a review. Heredity 100:564–573PubMedCrossRefGoogle Scholar
  46. Pezer Z, Ugarković Đ (2008) RNA Pol II promotes transcription of centromeric satellite DNA in beetles. PLoS One 3:e1594PubMedCrossRefGoogle Scholar
  47. Pezer Z, Ugarković Đ (2009) Transcription of pericentromeric heterochromatin in beetles – satellite DNAs as active regulatory elements. Cytogenet Genome Res 124:268–276PubMedCrossRefGoogle Scholar
  48. Pimpinelli S, Sullivan W, Prout M, Sandler L (1985) On biological functions mapping to the heterochromatin of Drosophila melanogaster. Genetics 109:701–724PubMedGoogle Scholar
  49. Plohl M, Meštrović N, Bruvo B, Ugarković Đ (1998) Similarity of structural features and evolution of satellite DNAs from Palorus subdepressus (Coleoptera) and related species. J Mol Evol 46:234–249PubMedCrossRefGoogle Scholar
  50. Pons J (2004) Cloning and characterization of a transponsable-like repeat in the heterochromatin of the darkling beetle Misolampus goudoti. Genome 47:769–774PubMedCrossRefGoogle Scholar
  51. Pons J, Bruvo B, Juan C, Petitpierre E, Plohl M, Ugarković Ð (1997) Conservation of satellite DNA in species of the genus Pimelia (Tenebrionidae, Coleoptera). Gene 205:183–190PubMedCrossRefGoogle Scholar
  52. Raff JW, Kellum R, Alberts B (1994) The Drosophila GAGA transcription factor is associated with specific regions of heterochromatin throughout the cell cycle. EMBO J 13:5977–5983PubMedGoogle Scholar
  53. Renault S, Rouleux-Bonnin F, Periquet G, Bigot Y (1999) Satellite DNA transcription in Diadromus pulchellus (Hymenoptera). Insect Biochem Mol Biol 29:103–111PubMedCrossRefGoogle Scholar
  54. Rojas AA, Vázquez-Tello A, Ferbeyre G, Venanzetti F, Bachmann L, Paquin B et al (2000) Hammerhead-mediated processing of satellite pDo500 family transcripts from Dolichopoda cave crickets. Nucleic Acids Res 28:4037–4043PubMedCrossRefGoogle Scholar
  55. Romanova LY, Deriagin GV, Mashkova TD, Tumeneva IG, Mushegian AR, Kisselev LL, Alexandrov IA (1996) Evidence for selection in evolution of alpha satellite DNA: the central role of CENP-B/pJ alpha binding region. J Mol Biol 261(3):334–340PubMedCrossRefGoogle Scholar
  56. 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 238:752–759PubMedCrossRefGoogle Scholar
  57. 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 47:877–888PubMedCrossRefGoogle Scholar
  58. Rudert F, Bronner S, Garnier J-M, Dollé P (1995) Transcripts from opposite strands of gamma satellite DNA are differentially expressed during mouse development. Mamm Genome 6:76–83PubMedCrossRefGoogle Scholar
  59. Schueler MG, Higgins AW, Rudd MK, Gustashaw K, Willard HF (2001) Genomic and genetic definition of a functional human centromere. Science 294:109–115PubMedCrossRefGoogle Scholar
  60. Shestakova EA, Mansuroglu Z, Mokrani H, Ghinea N, Bonnefoy E (2004) Transcription factor YY1 associates with pericentromeric y-satellite DNA in cycling but not in quiescent (G0) cells. Nucleic Acids Res 32:4390–4399PubMedCrossRefGoogle Scholar
  61. Spradling AC, de Cicco DV, Wakimoto BT, Levine JF, Katfayan LJ, Cooley L (1987) Amplification of the X-linked Drosophila chorion gene cluster requires a region upstream from the s38 chorion gene. EMBO J 6:1045–1053PubMedGoogle Scholar
  62. Sun X, Wahlstrom J, Karpen GH (1997) Molecular structure of a functional Drosophila centromere. Cell 91:1007–1019PubMedCrossRefGoogle Scholar
  63. Tartof KD, Hobbs C, Jones M (1984) A structural basis for variegating position effects. Cell 37:869–878PubMedCrossRefGoogle Scholar
  64. Tomoyasu Y, Miller SC, Tomita S, Schoppmeier M, Grossman D, Bucher G (2008) Exploring systemic RNA interference in insects: a genome-wide survey for RNAi genes in Tribolium. Genome Biol 9:R10PubMedCrossRefGoogle Scholar
  65. Trapitz P, Wlaschek M, Bunemann H (1988) Structure and function of Y chromosomal DNA II. Analysis of lampbrush loop associated transcripts in nuclei of primary spermatocytes of Drosophila hydei by in situ hybridization using asymmetric RNA probes of four different families of repetitive DNA. Chromosoma 96:159–170PubMedCrossRefGoogle Scholar
  66. Ugarković Đ (2005) Functional elements residing within satellite DNAs. EMBO Rep 6:1035–1039PubMedCrossRefGoogle Scholar
  67. Ugarković Đ (2008) Satellite DNA libraries and centromere evolution. Open Evol J 2:1–6CrossRefGoogle Scholar
  68. Ugarković Đ (2009a) Centromere: structure and evolution. Springer, BerlinCrossRefGoogle Scholar
  69. Ugarković Đ (2009b) Centromere-competent DNA: structure and evolution. Prog Mol Subcell Biol 48:53–76PubMedCrossRefGoogle Scholar
  70. Ugarković Đ, Plohl M, Lucijanić-Justić V, Borštnik B (1992) Detection of satellite DNA in Palorus ratzeburgii: analysis of curvature profiles and comparison with Tenebrio molitor satellite DNA. Biochimie 74:1075–1082PubMedCrossRefGoogle Scholar
  71. Ugarković Đ, Podnar M, Plohl M (1996) Satellite DNA of the red flour beetle Tribolium castaneum – comparative study of satellites from the genus Tribolium. Mol Biol Evol 13:1059–1066PubMedCrossRefGoogle Scholar
  72. Ugarković Đ, Plohl M (2002) Variation in satellite DNA profiles – causes and effects. EMBO J 21(22):5955–5959PubMedCrossRefGoogle Scholar
  73. Usakin L, Abad J, Vagin VV, de Pablos B, Villasante A et al (2007) Transcription of the 1.688 Satellite DNA family is under the control of RNA interference machinery in Drosophila melanogaster ovaries. Genetics 176:1343–1349PubMedCrossRefGoogle Scholar
  74. Valgardsdottir R, Chiodi I, Giordano M, Cobianchi F, Riva S, Biamonti G (2005) Structural and functional characterization of noncoding repetitive RNAs transcribed in stressed human cells. Mol Biol Cell 16:2597–2604PubMedCrossRefGoogle Scholar
  75. Varadaraj K, Skinner DM (1994) Cytoplasmic localization of transcripts of a complex G + C-rich crab satellite DNA. Chromosoma 103:423–431PubMedCrossRefGoogle Scholar
  76. Volpe TA, Kidner C, Hall IM, Teng G, Grewal SIS, Martienssen RA (2002) Regulation of heterochromatic silencing and histone H3 lysine-9 methylation by RNAi. Science 297:1833–1837PubMedCrossRefGoogle Scholar
  77. Waye JS, Willard HF (1986) Structure, organization, and sequence of alpha satellite DNA from human chromosome 17: evidence for evolution by unequal crossing-over and an ancestral pentamer repeat shared with the human X chromosome. Moll Cell Biol 6:3156–3165Google Scholar
  78. Wu ZG, Murphy C, Gall JG (1986) A transcribed satellite DNA from the bullfrog Rana catesbeiana. Chromosoma 93(4):291–297PubMedCrossRefGoogle Scholar
  79. Zheng B, Wang Z, Li S, Yu B, Liu JY, Chen X (2009) Intergenic transcription by RNA polymerase II coordinates Pol IV and Pol V in siRNA-directed transcriptional gene silencing in Arabidopsis. Genes Dev 23:2850–2860PubMedCrossRefGoogle Scholar

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© Springer-Verlag Berlin Heidelberg 2011

Authors and Affiliations

  1. 1.Ruđer Bošković InstituteZagrebCroatia
  2. 2.Dipartimento di Medicina Clinica e SperimentaleUniversità degli Studi di Napoli Federico IINapoliItaly

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