Protein phosphatase 2A is essential to maintain meiotic arrest, and to prevent Ca2+ burst at spawning and eventual parthenogenesis in the larvacean Oikopleura dioica

Unfertilized eggs of most animals are arrested at a certain point in the meiotic cell cycles. Reinitiation of meiosis and the start of embryogenesis are triggered by fertilization. This arrest is essential for preventing parthenogenetic activation and for promoting proper initiation of development by fertilization. In the larvacean Oikopleura dioica, which is a simple model organism for studies of chordate development, the unfertilized egg is arrested at metaphase of meiosis I. We show here that protein phosphatase 2A (PP2A) is essential for maintenance of meiotic arrest after spawning of oocytes. Knockdown (KD) of the maternal PP2A catalytic subunit, which was found in functional screening of maternal factors, caused unfertilized eggs to spontaneously release polar bodies after spawning, and then start pseudo-cleavages without fertilization, namely, parthenogenesis. Parthenogenetic embryos failed to undergo proper mitosis and cytokinesis because of lack of a centrosome, which is to be brought into the egg by a sperm. Activation of the KD oocytes was triggered by possible rise of ambient and intracellular pH upon their release from the gonad into seawater at spawning. Live recording of intracellular calcium level of the KD oocytes indicated that the pH rise caused an aberrant Ca2+ burst, which mimicked the Ca2+ burst that occurs at fertilization. Then, the aberrant Ca2+ burst triggered meiosis resumption through Calcium/calmodulin-dependent protein kinase (CaMK II). Therefore, PP2A is essential for maintenance of meiotic arrest and prevention of parthenogenesis by suppressing the aberrant Ca2+ burst at spawning. •PP2A is essential for maintenance of meiotic arrest in O. dioica oocytes.•Knock down of PP2Ac resulted in parthenogenesis after spawning.•Ambient pH rise at spawning promoted aberrant Ca2+ burst in PP2Ac-KD oocytes.•The aberrant Ca2+ burst led oocytes to reinitiate meiosis and pseudo-cleavages via CaMK II.•O. dioica’s mechanism of meiotic arrest is more similar to that of vertebrates than ascidians.