In the zebra finch (Taeniopygia guttata), there is a germ-line-restricted chromosome regularly present in males and females. A reexamination of male and female meiosis in the zebra finch showed that this element forms a euchromatic bivalent in oocytes, but it is always a single, heterochromatic element in spermatocytes. Immunostaining with anti-MLH1 showed that the bivalent in oocytes has two or three foci with a localized pattern, indicating the regular occurrence of recombination. In male meiosis, the single restricted chromosome forms an axis that contains the cohesin subunit SMC3, and the associated chromatin is densely packed until late pachytene. Electron microscopy of thin-sectioned seminiferous tubules shows that the restricted chromosome is eliminated in postmeiotic stages in the form of packed chromatin inside a micronucleus, visible in the cytoplasm of young spermatids. The selective condensation of the restricted chromosome during early meiotic prophase in males is interpreted as a strategy to avoid the triggering of asynaptic checkpoints, but this condensation is reversed prior to the final condensation that leads to its (ulterior) elimination. Recombination during female meiosis may prevent the genetic attrition of the restricted chromosome and, along with the elimination in male germ cells, ensures its regular transmission through females.
Mitotic and meiotic analysis with light and electron microscopy was performed in male and female zebra finches (Taeniopygia guttata). Somatic cells from bone marrow have a 2n = 80 and show the usual sex chromosome mechanism of birds ZZ (male)/ZW (female). In the germ lines of both sexes, a single accessory chromosome was regularly present in all the cells examined from all the individual birds. In synaptonemal complex (SC) spreads of pachytene oocytes and spermatocytes, this accessory chromosome forms a single axis, but it behaves differentially in male and female meiosis. While this accessory chromosome is euchromatic in oocytes, it is strongly heterochromatic in spermatocytes. In pachytene spermatocytes, the accessory chromosome adopts a morphology strikingly similar to that of the XY body ('sex vesicle') of mammalian spermatocytes. This accessory chromosome is eliminated during male meiosis and forms a cytoplasmic dense body in young spermatids that shows strong fluorescence with DAPI. The presence of this germ line-restricted chromosome does not affect the behaviour of the ZW pair in oocytes, as the sex chromosomes pair regularly and show a localized recombination nodule. It is suggested that this accessory chromosome has transcriptional activity during oogenesis, and thus it is regularly transmitted through preferential segregation during female meiosis.
We report here that a germline-restricted chromosome (GRC) is regularly present in males and females of the Bengalese finch (Lonchura domestica). While the GRC is euchromatic in oocytes, in spermatocytes this chromosome is cytologically seen as entirely heterochromatic and presumably inactive. The GRC is observed in the cytoplasm of secondary spermatocytes, indicating that its elimination from the nucleus occurs during the first meiotic division. By immunofluorescence on microspreads, we investigated the presence of histone H3 modifications throughout male meiosis, as well as in postmeiotic stages. We found that the GRC is highly enriched in di- and trimethylated histone H3 at lysine 9 during prophase I, in agreement with the presumed inactive state of this chromosome. At metaphase I, dimethylated histone H3 is no longer detectable on the GRC and its chromatin is more faintly stained with DAPI. The condensed GRC is underphosphorylated at serine 10 compared to the regular chromosomes during metaphase I, being phosphorylated later at this site after the first meiotic division. From these results, we proposed that trimethylation of histone H3 at lysine 9 on the GRC chromatin increases during metaphase I. This hypermethylated state at lysine 9 may preclude the phosphorylation of the adjacent serine 10 residue, providing an example of cross-talk of histone H3 modifications as described in experimental systems. The differential underphosphorylation of the GRC chromatin before elimination is interpreted as a cytologically detectable byproduct of deficient activity of Aurora B kinase, which is responsible for the phosphorylation of H3 at serine 10 during mitosis and meiosis.
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