Abstract
In the males of lecanoid coccids, or mealybugs, an entire, paternally derived, haploid chromosome set becomes heterochromatic after the seventh embryonic mitotic cycle. In females, both haploid sets are euchromatic throughout the life cycle. In mealybugs, as in all homopteran species, chromosomes are holocentric. Holocentric chromosomes are characterized by the lack of a localized centromere and consequently of a localized kinetic activity. In monocentric species, sister chromatid cohesion and monopolar attachment play a pivotal role in regulating chromosome behavior during the two meiotic divisions. Both these processes rely upon the presence of a single, localized centromere and as such cannot be properly executed by holocentric chromosomes. Here we furnish further evidence that meiosis is inverted in both sexes of mealybugs and we suggest how this might represent an adaptation to chromosome holocentrism. Moreover, we reveal that at the second meiotic division in males a monopolar spindle is formed, to which only euchromatic chromosomes become attached. By this mechanism the paternally derived, heterochromatic, haploid chromosome set strictly segregates from the euchromatic one, and it is then excluded from the genetic continuum as a result of meiotic drive.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Albertson DG, Thomson JN (1993) Segregation of holocentric chromosomes at meiosis in the nematode Caenorhabditis elegans. Chromosome Res 1:15–26
Bongiorni S, Prantera G (2003) Imprinted facultative heterochromatization in mealybugs. Genetica 117:271–279
Bongiorni S, Cintio O, Prantera G (1999) The relationship between DNA methylation and chromosome imprinting in the Coccid Planococcus citri. Genetics 151:1471–1478
Bongiorni S, Mazzuoli M, Masci S, Prantera G (2001) Facultative heterochromatization in parahaploid male mealybugs: involvement of a heterochromatin-associated protein. Development 128:3809–3817
Brown SW, Nur U (1964) Heterochromatic chromosomes in the coccids. Science 145:130–136
Cenci G, Bonaccorsi S, Pisano C, Verni F, Gatti M (1994) Chromatin and microtubule organization during premeiotic, meiotic and early postmeiotic stages of Drosophila melanogaster spermatogenesis. J Cell Sci 107:3521–3534
Chandra HS (1962) Inverse meiosis in triploid females of the mealybug, Planococcus citri. Genetics 47:1441–1454
Dej KJ, Orr-Weaver TL (2000) Separation anxiety at the centromere. Trends Cell Biol 10:392–399
Dernburg AF (2001) Here, there, and everywhere: kinetochore function on holocentric chromosomes. J Cell Biol 153:F33–F38
Esteban MR, Campos MC, Perondini AL, Goday C (1997) Role of microtubules and microtubule organizing centers on meiotic chromosome elimination in Sciara ocellaris. J Cell Sci 110:721–730
Gerbi SA (1986) Unusual chromosome movements in sciarid flies. Results Probl Cell Differ 13:71–104
Goday C, Pimpinelli S (1989) Centromere organization in meiotic chromosomes of Parascaris univalens. Chromosoma 98:160–166
Howe M, McDonald KL, Albertson DG, Meyer BJ (2001) HIM-10 is required for kinetochore structure and function on Caenorhabditis elegans chromosomes. J Cell Biol 153:1227–1238
Hughes-Schrader S (1948) Cytology of coccids (Coccoidea, Homoptera). Adv Genet 2:1-203
Nasmyth K (2001) Disseminating the genome: joining, resolving, and separating sister chromatids during mitosis and meiosis. Annu Rev Genet. 35:673–745
Nur U (1967) Reversal of heterochromatization and the activity of the paternal chromosome set in the male mealybug. Genetics 56:375–389
Nur U (1990) Heterochromatization and euchromatization of whole genomes in scale insects (Coccoidea: Homoptera). Dev Suppl: 29–34
Pisano C, Bonaccorsi S, Gatti M (1993) The kl-3 loop of the Y chromosome of Drosophila melanogaster binds a tektin-like protein. Genetics 133:569–579
Suja JA, del Cerro AL, Page J, Rufas JS, Santos JL (2000) Meiotic sister chromatid cohesion in holocentric sex chromosomes of three heteropteran species is maintained in the absence of axial elements. Chromosoma 109:35–43
Toth A, Rabitsch KP, Galova M, Schleiffer A, Buonomo SB, Nasmyth K (2000) Functional genomics identifies monopolin: a kinetochore protein required for segregation of homologs during meiosis I. Cell 103:1155–1168
Walker MY, Hawley RS (2000) Hanging on to your homolog: the roles of pairing, synapsis and recombination in the maintenance of homolog adhesion. Chromosoma 109:3-9
Wrensch DL, Kethley JB, Norton RA (1993) Cytogenetics of holokinetic chromosomes and inverted meiosis: keys to the evolutionary success of mites, with generalizations on eukaryotes. In: Houck MA (ed) Mites: ecological and evolutionary analyses of life history patterns. Chapman and Hall, New York, London, pp 282–343
Acknowledgements
We are indebted to Barbara Wakimoto for helpful suggestions and critical reading of the manuscript. This work was supported by grants from the Italian MIUR to G.P.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by E.A. Nigg
Rights and permissions
About this article
Cite this article
Bongiorni, S., Fiorenzo, P., Pippoletti, D. et al. Inverted meiosis and meiotic drive in mealybugs. Chromosoma 112, 331–341 (2004). https://doi.org/10.1007/s00412-004-0278-4
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00412-004-0278-4