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Hymenoptera exhibit a reciprocal pattern of
centrosome inheritance.
We
tackled the issue of de novo
centrosome formation by examining the origin of the centrosome in
unfertilized jewel wasp embryos (Nasonia
vitripennis). This species is a member of the large insect
order hymenoptera (ants, wasps, and bees). Fertilized hymenoptera
embryos develop into diploid females while unfertilized embryos develop
into haploid males. By following centrosome, spindle and nuclear
behavior in real time during early embryogenesis, we discovered that
centrosomes were assembled before the first mitotic division but were
inherited differently in unfertilized and fertilized eggs. In
both cases, large numbers of microtubule organicing centers (MTOCs)
appeared at the cortex of the egg after completion of meiosis. In
unfertilized eggs, the MTOCs migrated inwards. Two of them became
stably associated with the female pronucleus, and the remaining
cytoplasmic asters rapidly disappeared. These MTOCs appear to be
canonical centrosomes because they contain g-tubulin, CP190, and
centrioles, and they undergo duplication. In fertilized eggs, the
Nasonia sperm
brought in paternally derived centrosomes, similar to Drosophila melanogaster. At
pronuclear fusion, the diploid zygotic nucleus was associated only with
paternally derived centrosomes. None of the cytoplasmic asters
associated with the zygotic nucleus and, as in unfertilized eggs, they
rapidly degenerated. Therefore, unfertilized male eggs inherit
maternal centrosomes whereas fertilized female eggs inherit paternal
centrosomes. This is the first system described in which
centrosomes are reciprocally inherited. This work is published in
Current Biology (Tram
and Sullivan 2000).
Centrosomes in
unfertilized Hymenopteran embryos form from specialized organelles
derived from the female oocyte
Recently we discovered that these maternally derived
centrosomes originate from accessory nuclei (AN), which are
specialized organelles derived from the oocyte nuclear envelope in
Hymenopteran species. In the parasitic wasps Nasonia vitripennis and Muscidifurax uniraptor, the
position and number of AN in mature oocytes correspond to the position
and number of maternal centrosomes in early embryos. These AN
also contain high concentrations of g-tubulin. In the honeybee, Apis mellifera, distinct g-tubulin
foci are present in each AN. Additionally, the Hymenopteran
homolog of the Drosophila
centrosomal protein Dgrip84 localizes on the outer surfaces of
AN.
Cytoplasmic bodies are accessory nuclei organelles present in
Hymenopteran oocytes.
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These organelles
disintegrate in the late oocyte, leaving
behind small g-tubulin foci, which likely seed the formation of
maternal centrosomes. Accessory nuclei, therefore, may have
played a significant role in the evolution of haplodiploidy in
Hymenopteran insects. This work is published in Current Biology
(Ferree
et al. 2006). These results indicate that Nasonia and hymenoptera may be
excellent model systems to study centrosome biogenesis and germline
inheritance.
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