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. 1999 Apr;151(4):1471–1478. doi: 10.1093/genetics/151.4.1471

The relationship between DNA methylation and chromosome imprinting in the coccid Planococcus citri.

S Bongiorni 1, O Cintio 1, G Prantera 1
PMCID: PMC1460555  PMID: 10101170

Abstract

The phenomenon of chromosome, or genomic, imprinting indicates the relevance of parental origin in determining functional differences between alleles, homologous chromosomes, or haploid sets. In mealybug males (Homoptera, Coccoidea), the haploid set of paternal origin undergoes heterochromatization at midcleavage and remains so in most of the tissues. This different behavior of the two haploid sets, which depends on their parental origin, represents one of the most striking examples of chromosome imprinting. In mammals, DNA methylation has been postulated as a possible molecular mechanism to differentially imprint DNA sequences during spermatogenesis or oogenesis. In the present article we addressed the role of DNA methylation in the imprinting of whole haploid sets as it occurs in Coccids. We investigated the DNA methylation patterns at both the molecular and chromosomal level in the mealybug Planococcus citri. We found that in both males and females the paternally derived haploid set is hypomethylated with respect to the maternally derived one. Therefore, in males, it is the paternally derived hypomethylated haploid set that is heterochromatized. Our data suggest that the two haploid sets are imprinted by parent-of-origin-specific DNA methylation with no correlation with the known gene-silencing properties of this base modification.

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Selected References

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  1. Achwal C. W., Iyer C. A., Chandra H. S. Immunochemical evidence for the presence of 5mC, 6mA and 7mG in human, Drosophila and mealybug DNA. FEBS Lett. 1983 Jul 25;158(2):353–358. doi: 10.1016/0014-5793(83)80612-7. [DOI] [PubMed] [Google Scholar]
  2. Adolph S., Hameister H. In situ nick translation of human metaphase chromosomes with the restriction enzymes MspI and HpaII reveals an R-band pattern. Cytogenet Cell Genet. 1990;54(3-4):132–136. doi: 10.1159/000132976. [DOI] [PubMed] [Google Scholar]
  3. BROWN S. W., NUR U. HETEROCHROMATIC CHROMOSOMES IN THE COCCIDS. Science. 1964 Jul 10;145(3628):130–136. doi: 10.1126/science.145.3628.130. [DOI] [PubMed] [Google Scholar]
  4. Brown S W, Nelson-Rees W A. Radiation Analysis of a Lecanoid Genetic System. Genetics. 1961 Aug;46(8):983–1007. doi: 10.1093/genetics/46.8.983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bullerdiek J., Dittmer J., Faehre A., Bartnitzke S., Kasche V., Schloot W. A new banding pattern of human chromosomes by in situ nick translation using ECO RI and biotin-dUTP. Clin Genet. 1985 Aug;28(2):173–176. doi: 10.1111/j.1399-0004.1985.tb00379.x. [DOI] [PubMed] [Google Scholar]
  6. Burkholder G. D. Morphological and biochemical effects of endonucleases on isolated mammalian chromosomes in vitro. Chromosoma. 1989 Mar;97(5):347–355. doi: 10.1007/BF00292761. [DOI] [PubMed] [Google Scholar]
  7. Crouse H V. The Controlling Element in Sex Chromosome Behavior in Sciara. Genetics. 1960 Oct;45(10):1429–1443. doi: 10.1093/genetics/45.10.1429. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Devajyothi C., Brahmachari V. Detection of a CpA methylase in an insect system: characterization and substrate specificity. Mol Cell Biochem. 1992 Mar 25;110(2):103–111. doi: 10.1007/BF02454187. [DOI] [PubMed] [Google Scholar]
  9. Epstein H., James T. C., Singh P. B. Cloning and expression of Drosophila HP1 homologs from a mealybug, Planococcus citri. J Cell Sci. 1992 Feb;101(Pt 2):463–474. doi: 10.1242/jcs.101.2.463. [DOI] [PubMed] [Google Scholar]
  10. Feil R., Walter J., Allen N. D., Reik W. Developmental control of allelic methylation in the imprinted mouse Igf2 and H19 genes. Development. 1994 Oct;120(10):2933–2943. doi: 10.1242/dev.120.10.2933. [DOI] [PubMed] [Google Scholar]
  11. Ferraro M., Prantera G. Human NORs show correlation between transcriptional activity, DNase I sensitivity, and hypomethylation. Cytogenet Cell Genet. 1988;47(1-2):58–61. doi: 10.1159/000132506. [DOI] [PubMed] [Google Scholar]
  12. Ferraro M., Predazzi V., Prantera G. In human chromosomes telomeric regions are enriched in CpGs relative to R-bands. Chromosoma. 1993 Dec;102(10):712–717. doi: 10.1007/BF00650897. [DOI] [PubMed] [Google Scholar]
  13. Gerbi S. A. Unusual chromosome movements in sciarid flies. Results Probl Cell Differ. 1986;13:71–104. doi: 10.1007/978-3-540-39838-7_2. [DOI] [PubMed] [Google Scholar]
  14. HUGHES-SCHRADER S. Cytology of coccids (Coccoïdea-Homoptera). Adv Genet. 1948;35(2):127–203. doi: 10.1016/s0065-2660(08)60468-x. [DOI] [PubMed] [Google Scholar]
  15. Khosla S., Kantheti P., Brahmachari V., Chandra H. S. A male-specific nuclease-resistant chromatin fraction in the mealybug Planococcus lilacinus. Chromosoma. 1996;104(5):386–392. doi: 10.1007/BF00337228. [DOI] [PubMed] [Google Scholar]
  16. Lalande M. Parental imprinting and human disease. Annu Rev Genet. 1996;30:173–195. doi: 10.1146/annurev.genet.30.1.173. [DOI] [PubMed] [Google Scholar]
  17. Manicardi G. C., Bizzaro D., Galli E., Bianchi U. Heterochromatin heterogeneity in the holocentric X chromatin of Megoura viciae (Homoptera, Aphididae). Genome. 1996 Apr;39(2):465–470. doi: 10.1139/g96-059. [DOI] [PubMed] [Google Scholar]
  18. Moore T., Haig D. Genomic imprinting in mammalian development: a parental tug-of-war. Trends Genet. 1991 Feb;7(2):45–49. doi: 10.1016/0168-9525(91)90230-N. [DOI] [PubMed] [Google Scholar]
  19. Nicholls R. D., Saitoh S., Horsthemke B. Imprinting in Prader-Willi and Angelman syndromes. Trends Genet. 1998 May;14(5):194–200. doi: 10.1016/s0168-9525(98)01432-2. [DOI] [PubMed] [Google Scholar]
  20. Nur U. Heterochromatization and euchromatization of whole genomes in scale insects (Coccoidea: Homoptera). Dev Suppl. 1990:29–34. [PubMed] [Google Scholar]
  21. Odierna G., Baldanza F., Aprea G., Olmo E. Occurrence of G-banding in metaphase chromosomes of Encarsia berlesei (Hymenoptera: Aphelinidae). Genome. 1993 Aug;36(4):662–667. doi: 10.1139/g93-088. [DOI] [PubMed] [Google Scholar]
  22. Peterson K., Sapienza C. Imprinting the genome: imprinted genes, imprinting genes, and a hypothesis for their interaction. Annu Rev Genet. 1993;27:7–31. doi: 10.1146/annurev.ge.27.120193.000255. [DOI] [PubMed] [Google Scholar]
  23. Prantera G., Ferraro M. Analysis of methylation and distribution of CpG sequences on human active and inactive X chromosomes by in situ nick translation. Chromosoma. 1990 Apr;99(1):18–23. doi: 10.1007/BF01737285. [DOI] [PubMed] [Google Scholar]
  24. Razin A., Cedar H. DNA methylation and genomic imprinting. Cell. 1994 May 20;77(4):473–476. doi: 10.1016/0092-8674(94)90208-9. [DOI] [PubMed] [Google Scholar]
  25. Stöger R., Kubicka P., Liu C. G., Kafri T., Razin A., Cedar H., Barlow D. P. Maternal-specific methylation of the imprinted mouse Igf2r locus identifies the expressed locus as carrying the imprinting signal. Cell. 1993 Apr 9;73(1):61–71. doi: 10.1016/0092-8674(93)90160-r. [DOI] [PubMed] [Google Scholar]
  26. Tweedie S., Charlton J., Clark V., Bird A. Methylation of genomes and genes at the invertebrate-vertebrate boundary. Mol Cell Biol. 1997 Mar;17(3):1469–1475. doi: 10.1128/mcb.17.3.1469. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Wutz A., Smrzka O. W., Schweifer N., Schellander K., Wagner E. F., Barlow D. P. Imprinted expression of the Igf2r gene depends on an intronic CpG island. Nature. 1997 Oct 16;389(6652):745–749. doi: 10.1038/39631. [DOI] [PubMed] [Google Scholar]
  28. de la Torre J., Mitchell A. R., Summer A. T. Restriction endonuclease/nick translation of fixed mouse chromosomes: a study of factors affecting digestion of chromosomal DNA in situ. Chromosoma. 1991 Mar;100(3):203–211. doi: 10.1007/BF00337249. [DOI] [PubMed] [Google Scholar]
  29. de la Torre J., Sumner A. T., Gosalvez J., Stuppia L. The distribution of genes on human chromosomes as studied by in situ nick translation. Genome. 1992 Oct;35(5):890–894. doi: 10.1139/g92-135. [DOI] [PubMed] [Google Scholar]
  30. del Mazo J., Prantera G., Torres M., Ferraro M. DNA methylation changes during mouse spermatogenesis. Chromosome Res. 1994 Mar;2(2):147–152. doi: 10.1007/BF01553493. [DOI] [PubMed] [Google Scholar]

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