Abstract
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.
Similar content being viewed by others
References
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 410:120–124
Braun RE, Behringer RR, Peschon JJ, Brinster RL, Palmiter RD (1989) Genetically haploid spermatids are phenotypically diploid. Nature 337:373–376
Brown SW (1969) Developmental control of heterochromatization in coccids. Genetics Suppl 61:191–198
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 110–181
Brown SW, Nelson-Rees A (1961) Radiation analysis of a lecanoid genetic system. Genetics 46:983–1007
Brown SW, Nur U (1964) Heterochromatic chromosomes in the coccids. Science 154:130–136
Buning J (1994) The insect ovary: ultrastructure, previtellogenic growth and evolution. Chapman & Hall, London
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 105:2103–2110
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 111:22–36
de Cuevas M, Lilly MA, Spradling AC (1997) Germline cyst formation in Drosophila. Annu Rev Genet 31:405–428
Epstein H, James TC, Singh PB (1992) Cloning and expression of Drosophila HP1 homologs from a mealybug, Planococcus citri. J Cell Sci 101:463–474
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 51:37–49
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 110:93–101
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 17:1870–1881
Grewal SIS, Elgin SCR (2002) Heterochromatin: new possibilities for the inheritance of structure. Curr Opin Genet Dev 12:178–187
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 131:1243–1259
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 109:2779–2788
Hughes-Schrader S (1948) Cytology of coccids (Coccoidea–Homoptera). Adv Genet 2:127–203
James TC, Elgin SCR (1986) Identification of a nonhistone chromosomal protein associated with heterochromatin in Drosophila melanogaster and its gene. Mol Cell Biol 6:3862–3872
Jenuwein T, Allis CD (2001) Translating the histone code. Science 293:1074–1080
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 410:116–120
Li Y, Kirschmann DA, Wallrath LL (2002) Does heterochromatin protein 1 always follow code? Proc Natl Acad Sci USA 99:16462–16469
Li Y, Danze, JR, Alvarez P, Belmont AS, Wallrath LL (2003) Effects of tethering HP1 to euchromatic regions of the Drosophila genome. Development 130:1817–1824
Nelson-Rees W (1960) A study of sex predetermination in the mealy bug Planococcus citri (Risso). J Exp Zool 144:111–137
Noguchi T, Miller KG (2003) A role for actin dynamics in individualization during spermatogenesis in Drosophila melanogaster. Development 130:1805–1816
Nur U (1967) Reversal of heterochromatization and the activity of the paternal chromosome set in the male mealy bug. Genetics 56:375–389
Pepling ME, de Cuevas M, Spradling AC (1999) Germline cysts: a conserved phase of germ cell development? Trends Cell Biol 9:257–262
Sims RJ III, Nishioka K, Reinberg D (2003) Histone lysine methylation: a signature for chromatin function. Trends Genet 19:629–639
Strahl B, Allis C (2000) The language of covalent histone modifications. Nature 403:41–45
Surani MAH, Barton SC, Norris ML (1984) Development of reconstituted mouse eggs suggests imprinting of the genome during gametogenesis. Nature 308:548–550
Surani MA (1991) Genomic imprinting: Developmental significance and molecular mechanism. Curr Opin Genet Dev 1:241–246
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 223–319
Turner B (2000) Histone acetylation and an epigenetic code. Bioessays 22:836–845
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 16:573–579
Acknowledgements
We thank T.C. James for providing us with the anti-HP1 antibody (C1A9), Prof. S. Pimpinelli for the anti-MeLy9-H3, and Prof. M. Gatti for the anti-α-spectrin antibody. The research was supported by Ministero dell’Istruzione, dell’Università e della Ricerca (MIUR).
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by A. Spradling
Rights and permissions
About this article
Cite this article
Buglia, G.L., Ferraro, M. Germline cyst development and imprinting in male mealybug Planococcus citri. Chromosoma 113, 284–294 (2004). https://doi.org/10.1007/s00412-004-0317-1
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00412-004-0317-1