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

Abstract

How the embryonic body axis is generated is a fundamental question in developmental biology. The molecular mechanisms involved in this process have been the subject of intensive studies using traditional model organisms during the last few decades, and the results have provided crucial information for understanding the formation of animal body plans. In particular, studies exploring the molecular nature of Spemann's organizer have revealed the intricate interactions underlying several signaling pathways (namely the Wnt/b-catenin, Nodal and Bmp pathways) that pattern the dorsoventral (DV) axis in vertebrate embryos. Furthermore, recent comparative studies have shown that many of these signaling interactions are also employed in other non-vertebrate model organisms for their early embryonic axis patterning. These results suggest that there is deep homology in DV patterning mechanisms among bilaterian animals and that these mechanisms may be traced back to the common ancestor of cnidarians and bilaterians. However, the mechanism by which the DV axis became inverted in the chordate lineage relative to the DV axis in other bilaterian animals remains unclear. Cephalochordata (i.e., amphioxus) represent a basal chordate group which occupies a key phylogenetic position for explorations of the origin of the chordate body plan. In this review, we summarize what is currently known regarding the developmental mechanisms that establish the DV axis in amphioxus embryos. By comparing this to what is known in vertebrates, we can start to hypothesize about the ancestral DV patterning mechanisms in chordates and discuss their possible evolutionary origins.

Morphological Stasis and Proteome Innovation in Cephalochordates

“…In the present work, we have also selected key developmental genes that are known to be critical for determining anteroposterior (AP) and dorvosventral (DV) patterning, and left-right (LR) asymmetric development of amphioxus [ 8 , 27 , 28 , 29 , 30 ]. Sequences of the latter group of B. belcheri proteins were downloaded from the Chinese Lancelet Genome website [ 26 ].…”

The gastropod Lottia peitaihoensis as a model to study the body patterning of trochophore larvae

“…Alternatively, it is possible that some of these reports may represent other aspects of organizer signaling that have not been linked to the molecular logic mentioned above. This speculation is particularly noteworthy with regard to Activin/Nodal signaling (Lanza & Seaver, 2018, 2020a, 2020b), given the role of Nodal signaling in the DV patterning of various deuterostomes (Duboc & Lepage, 2008; Kozmikova & Yu, 2017). The D‐quadrant organizer: (II) deep links among various developmental effects and the transitions of body axesWhen inhibiting organizer function in L. peitaihoensis , either by inhibiting MAPK signaling or knocking down BMP2/4 or Chordin, the BMP signaling gradient before gastrulation is eliminated, followed by the loss of the DV axis (radial development) (Tan et al, 2022).…”

“…Alternatively, it is possible that some of these reports may represent other aspects of organizer signaling that have not been linked to the molecular logic mentioned above. This speculation is particularly noteworthy with regard to Activin/Nodal signaling (Lanza & Seaver, 2018, 2020a, 2020b), given the role of Nodal signaling in the DV patterning of various deuterostomes (Duboc & Lepage, 2008; Kozmikova & Yu, 2017).…”

Molecular asymmetry in the cephalochordate embryo revealed by single-blastomere transcriptome profiling

“…We thus set out to examine the molecular functions of four newly identified amphioxus genes with asymmetrically localized transcripts. Because gene-specific functional experiments are technically challenging in amphioxus embryos, we used zebrafish embryos as a surrogate in vivo model, with which amphioxus shares similar axial patterning mechanisms [21,36]. Synthesized mRNA of amphioxus zfp665/198050, soxB1b/130889, tbx2/124781 and foxn1/4b/247432 were injected separately into zebrafish zygotes, and the resulting phenotypes were assessed at 2 to 3 days post-fertilization.…”