Oocyte selection is concurrent with meiosis resumption in the coenocystic oogenesis of Oikopleura

Oogenesis in the tunicate, Oikopleura, is unusual for a chordate, in that the thousands of nuclei comprising the entire germline are contained in a unique giant cell, the coenocyst. We examined progression through meiotic prophase I in concert with cellular mechanisms implicated in selection, growth and maturation of oocytes in this shared cytoplasm. Unlike sister vertebrates, no germinal vesicle was formed and maternal transcripts were instead synthesized by polyploid nurse nuclei present in equal numbers to transcriptionally quiescent meiotic nuclei. Meiosis resumption was concomitant with MAPK cascade activation during which pERK translocated to nurse nuclei. Simultaneously, the coenocyst partitioned into hundreds of synchronously growing oocytes. Significantly, only the subset of meiotic nuclei selected to populate maturing oocytes displayed histone H3 serine 28 phosphorylation. Disruption of the MAPK cascade, or microtubule dynamics, did not inhibit meiotic resumption but generated oocytes with multiple nurse and meiotic nuclei. As these supernumerary nuclei also became H3S28P enriched, growing oocytes defined a selective kinase environment in the common coenocyst cytoplasm. Vitellogenesis preceded the timing of oocyte selection among excess germ line nuclei in contrast to Drosophila and vertebrates. This unique feature enables late adjustment of oocyte number in accordance with the cytoplasmic volume of the germline cyst accumulated during vitellogenesis.