Centrosome inheritance in starfish zygotes. II: Selective suppression of the maternal centrosome during meiosis

Although both gametes may contribute a centrosome to the zygote at fertilization, only one of these centrosomes is used in development. Thus, specific mechanisms must exist to control centrosome inheritance in all sexually reproducing organisms. We use starfish as a model system to characterize these control mechanisms because the eggs complete meiosis I and meiosis II after fertilization; this allows us to directly follow the fate of all parental centrosomes in vivo. Only the paternal centrosome is used in starfish development. Although the microtubule organizing center activity of the maternal centrosome persists, the functional loss of this centrosome involves the suppression of its ability to double, or reproduce, at successive mitoses (Sluder et al., 1989. Dev. Biol. 131, 567-579). To determine when the reproductive capacity of the maternal centrosome is degraded, we transfer meiosis I and meiosis II spindles from just fertilized eggs into other zygotes that are in prophase of first mitosis. Meiosis I spindles are stable during first mitosis and are disassembled in first telophase in concert with the host spindle. In 61% of the cases a variable number of formerly meiotic centrosomes are active at second mitosis and reproduce in a normal fashion between subsequent mitoses. However, when meiosis II spindles are transferred in the same manner, in only 26% of the cases do any of the centrosomes persist past first mitosis or reproduce in a normal fashion thereafter. In the remainder of the cases the remnants of the maternal centrosomes organize a single monaster that does not double between mitoses. Control transfers of first mitosis spindles indicate that these results are not due to nonspecific damage to the meiotic spindles or to the recipient zygotes. These observations indicate that the reproductive capacity of maternal centrosomes is degraded during meiosis I, not during oogenesis. Our results also show that the cytoplasmic conditions which eliminate this reproductive capacity are no longer active once the zygote has entered the first mitotic cell cycle.