Evolutionary implications of the mode of D quadrant specification in coelomates with spiral cleavage

Abstract

In annelids, molluscs, echiurans and sipunculids the establishment of the dorsalventral axis of the embryo is associated with D quadrant specification during embryogenesis.This specification occurs in two ways in these phyla. One mechanism specifies the D quadrant via the shunting of a set of cytoplasmic determinants located at the vegetal pole of the egg to one blastomere of the four cell stage embryo. In this case, at the first two cleavages of embryogenesis there is an unequal distribution of cytoplasm, generating one macromere which is larger than the others at the four cell stage. The D quadrant can also be specified by a contact mediated inductive interaction between one of the macromeres at the vegetal pole with micromeres at the animal pole of the embryo. This mechanism operates at a later stage of development than the cytoplasmic localization mechanism and is associated with a pattern of cleavage in which the first two cleavages are equal.An analysis of the phylogenetic relationships within these phyla indicates that the taxa which determine the D quadrant at an early cleavage stage by cytoplasmic localization tend to be derived and lack a larval stage or have larvae with adult characters. Those taxa where the D quadrant is specified by induction include the ancestral groups although some derived groups also use this mechanism.The pulmonate mollusc Lymnaea uses an inductive mechanism for specifying the D quadrant.In these embryos each of the four vegetal macromeres has the potential of becoming the D macromere; however under normal circumstances one of the two vegetal crossfurrow macromeres almost invariably becomes the D quadrant. Experiments are described here in which the size of one of the blastomeres of the four cell stage Lymnaea embryo is increased; this macromere invariably becomes the D quadrant. These experiments suggest that developmental 205 206 Freeman and Lundelius change in relative blastomere size during the first two cleavages in spiralian embryos that normally cleave equally may have provided a route that has led to the establishment of the cytoplasmic localization mechanism of D quadrant formation.

Cytoskeletal Symmetry Breaking and Chirality: From Reconstituted Systems to Animal Development

“…Although the chirality of cell rotations during the first and second round of cell divisions indicates organismal chirality [184], it does not seem to be directly linked to the decisive event at the third round of division [172]. This has been explained by the chirality at the third round of cell divisions more directly influencing the cell arrangement of the organizer, which emerges at the 24-cell stage [174]. Moreover, asymmetric expression of genes of the Nodal pathway [185], which is a conserved gene expression module operating in Deuterostomia, is directly dependent on the chirality of the third round of cell divisions.…”

“…The spirally cleaving glossiphoniid leech Helobdella robusta, which belongs to the Lophotrochoza, shows asymmetric divisions at the first and second round of cell divisions (unlike the snails discussed below) [174]. During the second round of division, the larger D quadrant is generated on the left side of the embryo, which gives rise to bilaterally symmetric mesoderm/ectoderm tissues and inherits unequally segregated developmental determinants.…”

The rise of bilaterians

“…The polar lobe is a transitory structure that forms from the vegetal pole of the egg during cleavage and shunts cytoplasm to one of the blastomeres at the four-cell stage. The descendants of this cell play a major role in setting up the dorsal -ventral axis of the embryo in some genera of extant lophotrochozoan animals (Freeman and Lundelius 1992). These embryos appear to be derived from different species because the egg sizes of embryos producing polar lobes vary.…”

Brefeldin A or monensin inhibits the 3D organizer in gastropod, polyplacophoran, and scaphopod molluscs

“…Dev Genes Evol (2007) 217: I05-118 Organizer specification is different in species undergoing equal versus unequal cleavage (Freeman and Lundelius 1992;Henry et al 2006). In unequal-cleaving and polarlobe-forming species, specification is through the segregation of the maternal determinants to a single vegetal macromere during early divisions .…”