Eccentric position of the germinal vesicle and cortical flow during oocyte maturation specify the animal-vegetal axis of ascidian embryos

Abstract

The animal-vegetal (A-V) axis is already set in unfertilized eggs. It plays crucial roles in coordinating germ-layer formation. However, how the A-V axis is set has not been well studied. In ascidians, unfertilized eggs are already polarized along the axis in terms of cellular components. This polarization occurs during oocyte maturation. Oocytes within the gonad have the germinal vesicle (GV) close to the future animal pole. When the GVs of full-grown oocytes were experimentally translocated to the opposite pole by centrifugal force, every aspect that designates A-V polarity was reversed in the eggs and embryos. This was confirmed by examining the cortical allocation of the meiotic spindle, the position of the polar body emission, the polarized distribution of mitochondria and postplasmic/PEM mRNA, the direction of the cortical flow during oocyte maturation, the cleavage pattern and germ-layer formation during embryogenesis. Therefore, the eccentric position of the GV triggers subsequent polarizing events and establishes the A-V axis in eggs and embryos. We emphasize important roles of the cortical flow. This is the first report in which the A-V axis was experimentally and completely reversed in animal oocytes before fertilization.

Bulk Actin Dynamics Drive Phase Segregation in Zebrafish Oocytes

“…Embryogenesis typically begins by reorganizing the cytoplasm within the oocyte (ooplasm). Seminal studies in tunicates have shown that the segregation of maternal determinants within the oocyte establish the blueprint for embryo patterning (Wilson, 1900;Satoh, 1994;Prodon et al, 2008Prodon et al, , 2009Nishida et al, 2017). Subsequent work in both vertebrate and invertebrate model organisms has demonstrated a common and essential role of ooplasmic reorganization for oocyte maturation and embryo patterning (Schuh and Ellenberg, 2008;Nance et al, 2003;Nance and Zallen, 2011).…”

“…In the nematode Caenorhabditis elegans, for instance, cortical actomyosin network flows are required for anterior-posterior polarization by accumulating cortex associated polarization cues at the anterior pole of the oocyte and zygote (Nance et al, 2003;Munro et al, 2004). Likewise in ascidians, cortical actomyosin flows are critical for germ layer specification by driving the segregation of maternal determinants within the oocyte (Prodon et al, 2008;Nishida et al, 2017). Finally, in starfish oocytes, periodic cortical actomyosin contraction waves trigger ooplasm flows by dynamically changing oocyte shape (Klughammer et al, 2018).…”