Acquisition of the dorsal structures in chordate amphioxus

Abstract

Acquisition of dorsal structures, such as notochord and hollow nerve cord, is likely to have had a profound influence upon vertebrate evolution. Dorsal formation in chordate development thus has been intensively studied in vertebrates and ascidians. However, the present understanding does not explain how chordates acquired dorsal structures. Here we show that amphioxus retains a key clue to answer this question. In amphioxus embryos, maternal nodal mRNA distributes asymmetrically in accordance with the remodelling of the cortical cytoskeleton in the fertilized egg, and subsequently lefty is first expressed in a patch of blastomeres across the equator where wnt8 is expressed circularly and which will become the margin of the blastopore. The lefty domain co-expresses zygotic nodal by the initial gastrula stage on the one side of the blastopore margin and induces the expression of goosecoid, not-like, chordin and brachyury1 genes in this region, as in the oral ectoderm of sea urchin embryos, which provides a basis for the formation of the dorsal structures. The striking similarity in the gene regulations and their respective expression domains when comparing dorsal formation in amphioxus and the determination of the oral ectoderm in sea urchin embryos suggests that chordates derived from an ambulacrarian-type blastula with dorsoventral inversion.

Dorsal-ventral patterning in amphioxus: current understanding, unresolved issues, and future directions

“…2) (Wang et al, 2016b). Lrp5/6,Axin,Gsk3b,APC,Gro,Ckla,Ckl3b,and (Holland et al, 2005;Kozmikova et al, 2013;Lin et al, 2006;Morov et al, 2016;Onai et al, 2010;Qian et al, 2013;Schubert et al, 2000a;Schubert et al, 2000b;Wang et al, 2016a;Yasui et al, 2002;Yu et al, 2007), and this report (Fig. 5).…”

“…This may indicate the existence of previously unrecognized cytoplasmic/ cortical movement in fertilized amphioxus eggs, similar to what has been observed in ascidian (Sardet et al, 2007) or Xenopus eggs . Furthermore, this report showed that the active form of the Arp2/3 complex moves to the animal pole in the cortical region of amphioxus zygotes, and that this movement influences the distribution of maternal Nodal mRNA toward the animal pole (Morov et al, 2016) (Fig. 4).…”

“…Here, the chromatin de-condenses as the oocyte undergoes its second maturation division, and subsequently, the second pothese observations, the authors suggested that the sperm entry points and the location of the male pronuclei are inconsistent with the stereotypical movement of the male pronucleus, and hence, the sperm entry site is not important for establishing the DV polarity in amphioxus embryos (Morov et al, 2016). These authors also showed that in amphioxus, the active form of the Arp2/3 complex, which functions during the activation of the cytoskeletal reorganization of the cell (Mullins et al, 1998;Pollard, 2007), changes its distribution within the egg during the first several minutes of development after fertilization (Morov et al, 2016). This may indicate the existence of previously unrecognized cytoplasmic/ cortical movement in fertilized amphioxus eggs, similar to what has been observed in ascidian (Sardet et al, 2007) or Xenopus eggs .…”

“…The gathering of mitochondria near the fusing pronuclei establishes an asymmetry in the fertilized egg and likely influences the position of the DV axis Holland and Onai, 2012). On the other hand, a recent report showed that sperm can enter the amphioxus egg anywhere, with some preference for the region along the equator (Morov et al, 2016). It also showed that at 5 min after fertilization, the male pronucleus does not show any regional preference (Fig 3B), and the male and female pronuclei meet on one side of the animal hemisphere near the equator approximately 20 min after fertilization (Morov et al, 2016).…”

“…4). Although there are no data showing the localization of phosphorylated Smad2/3 protein, which would indicate the region of activity of Nodal/Vg1 signaling, functional experiments that used pharmacological inhibitors of Smad2/3-mediated signaling showed that Nodal is an essential maternal factor mediating the specification of the dorsal region in the early amphioxus embryo (Morov et al, 2016;Onai et al, 2010).…”