Centrosome inheritance in starfish zygotes: selective loss of the maternal centrosome after fertilization.
The mature egg inherits a centrosome from the second meiotic spindle, and the sperm introduces a second centrosome at fertilization. Since only one of these centrosomes survives to be used in development, specific mechanisms must exist to control centrosome inheritance. To investigate how centrosome inheritance is controlled we used starfish eggs as a model system, because they undergo meiosis after fertilization. As a result, the fate of the maternal and paternal centrosomes can be followed by light microscopy and experimentally manipulated in vivo. We show initially that only the paternal centrosome is used in starfish zygote development; the maternal centrosome retained from meiosis II is functionally lost before first mitosis. We then tested a number of possible ways in which the zygote could exert this differential control over the stability of centrosomes initially residing in the same cytoplasm. The results of these experiments can be summarized as follows: (1) Although the microtubule organizing center activity of the maternal centrosome is not degraded after meiosis, the ability of this centrosome to double at successive mitoses is lost. (2) The sperm centrosome is not "masked" from cytoplasmic conditions which could destabilize all centrosomes during or after the meiotic sequence. (3) The functional loss of the maternal centrosome is not due to its cortical location. (4) The loss of this doubling capacity is determined by the egg, not by putative inhibitory factors from the fertilizing sperm. (5) The destabilization of the maternal centrosome is not due to the complete loss of its centrioles. Together, these results demonstrate that all maternal centrosomes are equivalent and that they are intrinsically different from the paternal centrosome. This intrinsic difference, in concert with a change in cytoplasmic conditions after meiosis, determines the selective loss of the maternal centrosome inherited from the meiosis II spindle.
Sluder
G
G
Worcester Foundation for Experimental Biology, Shrewsbury, Massachusetts 01545.
Miller
F J
FJ
Lewis
K
K
Davison
E D
ED
Rieder
C L
CL
D000818:Animals; D002502:Centrioles / Q000648:ultrastructure*; D003593:Cytoplasm / Q000648:ultrastructure; D005260:Female; D008297:Male; D008540:Meiosis; D008870:Microtubules / Q000648:ultrastructure; D008938:Mitosis; D015388:Organelles / Q000648:ultrastructure*; D013094:Spermatozoa / Q000648:ultrastructure; D008941:Spindle Apparatus / Q000648:ultrastructure; D013215:Starfish / Q000196:embryology*; D015053:Zygote / Q000648:ultrastructure*