, Volume 113, Issue 6, pp 284–294

Germline cyst development and imprinting in male mealybug Planococcus citri

Research Article


In the epigenetic modifications involved in the phenomenon of imprinting, which is thought to take place during gametogenesis, one of the primary roles is exerted by histone tail modifications acting on chromatin structure. What is more, in insects like mealybugs, with a lecanoid chromosome system, imprinting is strictly related to sex determination. In many diverse species gametes originate in specific, highly evolutionarily conserved structures called germline cysts. The use of staining techniques specific for fusomal components like F-actin has allowed us to describe for the first time the morphogenesis of male germline cysts in the mealybug Planococcus citri. Antibodies to anti-methylated lysine 9 of histone H3 (MeLy9-H3) and anti-heterochromatin protein 1 (HP1) were used during cyst formation to investigate the involvement of these epigenetic modifications in the phenomenon of imprinting and their possible concerted action in sex determination in P. citri. These observations indicate: (i) a specific role for F-actin in the segregation, typical of the lecanoid chromosome system, of genomes of paternal origin; (ii) that the two vital gametes originating from a given meiosis, although carrying the same genome, differ in the levels of both MeLy9-H3 and HP1, one of them being more heavily labelled by both antibodies.


  1. Bannister AJ, Zegerman P, Partridge JF, Miska EA, Thomas JO, Allshire RC, Kouzarides T (2001) Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain. Nature 410:120–124CrossRefPubMedGoogle Scholar
  2. Braun RE, Behringer RR, Peschon JJ, Brinster RL, Palmiter RD (1989) Genetically haploid spermatids are phenotypically diploid. Nature 337:373–376CrossRefPubMedGoogle Scholar
  3. Brown SW (1969) Developmental control of heterochromatization in coccids. Genetics Suppl 61:191–198Google Scholar
  4. Brown SW, Chandra S (1977) Imprinting and differential regulation of homologous chromosomes. In: Goldstein L, Prescott DM (eds) Cell biology: a comprehensive treatise, vol 1, Genetic mechanisms of cells. Academic, London, pp 110–181Google Scholar
  5. Brown SW, Nelson-Rees A (1961) Radiation analysis of a lecanoid genetic system. Genetics 46:983–1007Google Scholar
  6. Brown SW, Nur U (1964) Heterochromatic chromosomes in the coccids. Science 154:130–136Google Scholar
  7. Buning J (1994) The insect ovary: ultrastructure, previtellogenic growth and evolution. Chapman & Hall, LondonGoogle Scholar
  8. Byers TJ, Dubreuil R, Branton D, Kiehart DP, Goldstein LSB (1987) Drosophila spectrin. II. Conserved features of the alpha-subunit are revealed by analysis of cDNA clones and fusion proteins. J Cell Biol 105:2103–2110CrossRefPubMedGoogle Scholar
  9. Cowell IG, Aucott R, Mahadevaiah SK, Burgoyne PS, Huskisson N, Buongiorni S, Prantera G, Fanti L, Pimpinelli S, Wu R, Gilbert DM, Shi W, Fundele R, Morrison H, Jeppesen P, Singh P (2002) Heterochromatin, HP1 and methylation at lysine 9 of histone H3 in animals. Chromosoma 111:22–36CrossRefPubMedGoogle Scholar
  10. de Cuevas M, Lilly MA, Spradling AC (1997) Germline cyst formation in Drosophila. Annu Rev Genet 31:405–428CrossRefPubMedGoogle Scholar
  11. Epstein H, James TC, Singh PB (1992) Cloning and expression of Drosophila HP1 homologs from a mealybug, Planococcus citri. J Cell Sci 101:463–474PubMedGoogle Scholar
  12. Ferraro M, Epifani C, Bongiorni S, Nardone AM, Parodi-Delfino S, Pantera G (1998) Cytogenetic characterization of the genome of mealybug Planococcus citri (Homoptera, Coccoidea). Caryologia 51:37–49Google Scholar
  13. Ferraro M, Buglia GL, Romano F (2001) Involvement of histone H4 acetylation in the epigenetic inheritance of different activity states of maternally and paternally derived genomes in the mealybug Planococcus citri. Chromosoma 110:93–101PubMedGoogle Scholar
  14. Fischle W, Wang Y, Jacobs SA, Kim Y, Allis CD, Khorasanizadeh S (2003) Molecular basis for the discrimination of repressive methyl-lysine marks in histone H3 by Polycomb and HP1 chromodomains. Genes Dev 17:1870–1881CrossRefPubMedGoogle Scholar
  15. Grewal SIS, Elgin SCR (2002) Heterochromatin: new possibilities for the inheritance of structure. Curr Opin Genet Dev 12:178–187CrossRefPubMedGoogle Scholar
  16. Gunsalus KC, Bonaccorsi S, Williams E, Vernì F, Gatti M, Goldberg M (1995) Mutations in twinstar, a Drosophila gene encoding a cofilin/ADF homolog, result in defects in centrosome migration and cytokinesis. J Cell Biol 131:1243–1259CrossRefPubMedGoogle Scholar
  17. Hime GR, Brill JA, Fuller MT (1996) Assembly of ring canals in the male germ line from structural components of the contractile ring. J Cell Sci 109:2779–2788PubMedGoogle Scholar
  18. Hughes-Schrader S (1948) Cytology of coccids (Coccoidea–Homoptera). Adv Genet 2:127–203Google Scholar
  19. James TC, Elgin SCR (1986) Identification of a nonhistone chromosomal protein associated with heterochromatin in Drosophila melanogaster and its gene. Mol Cell Biol 6:3862–3872PubMedGoogle Scholar
  20. Jenuwein T, Allis CD (2001) Translating the histone code. Science 293:1074–1080CrossRefPubMedGoogle Scholar
  21. Lachner M, O’Carrol D, Rea S, Mechtler K, Jenuwein T (2001) Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature 410:116–120CrossRefPubMedGoogle Scholar
  22. Li Y, Kirschmann DA, Wallrath LL (2002) Does heterochromatin protein 1 always follow code? Proc Natl Acad Sci USA 99:16462–16469CrossRefPubMedGoogle Scholar
  23. Li Y, Danze, JR, Alvarez P, Belmont AS, Wallrath LL (2003) Effects of tethering HP1 to euchromatic regions of the Drosophila genome. Development 130:1817–1824CrossRefPubMedGoogle Scholar
  24. Nelson-Rees W (1960) A study of sex predetermination in the mealy bug Planococcus citri (Risso). J Exp Zool 144:111–137PubMedGoogle Scholar
  25. Noguchi T, Miller KG (2003) A role for actin dynamics in individualization during spermatogenesis in Drosophila melanogaster. Development 130:1805–1816CrossRefPubMedGoogle Scholar
  26. Nur U (1967) Reversal of heterochromatization and the activity of the paternal chromosome set in the male mealy bug. Genetics 56:375–389PubMedGoogle Scholar
  27. Pepling ME, de Cuevas M, Spradling AC (1999) Germline cysts: a conserved phase of germ cell development? Trends Cell Biol 9:257–262CrossRefPubMedGoogle Scholar
  28. Sims RJ III, Nishioka K, Reinberg D (2003) Histone lysine methylation: a signature for chromatin function. Trends Genet 19:629–639CrossRefPubMedGoogle Scholar
  29. Strahl B, Allis C (2000) The language of covalent histone modifications. Nature 403:41–45CrossRefPubMedGoogle Scholar
  30. Surani MAH, Barton SC, Norris ML (1984) Development of reconstituted mouse eggs suggests imprinting of the genome during gametogenesis. Nature 308:548–550PubMedGoogle Scholar
  31. Surani MA (1991) Genomic imprinting: Developmental significance and molecular mechanism. Curr Opin Genet Dev 1:241–246 PubMedGoogle Scholar
  32. Telfer W (1975) Development and physiology of the oocyte–nurse cell syncytium. In: Treherne JE, Berridge MJ, Wigglesworth VB (eds) Advances in insect physiology, vol 11. Academic, London, pp 223–319Google Scholar
  33. Turner B (2000) Histone acetylation and an epigenetic code. Bioessays 22:836–845CrossRefPubMedGoogle Scholar
  34. de Villena FP-M, de la Casa-Esperòn E, Sapienza C (2000) Natural selection and the function of genome imprinting: beyond the silenced minority. Trends Genet 16:573–579CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  1. 1.Department of Genetics and Molecular BiologyUniversity of Rome “La Sapienza”RomeItaly

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