Establishment of lateral organ asymmetries in the invertebrate chordate, Ciona intestinalis.

ABSTRACT:

Background

The evolutionary emergence and diversification of the chordates appear to involve dramatic changes in organ morphogenesis along the left/right axis. However, the ancestral chordate mechanism for establishing lateral asymmetry remains ambiguous. Additionally, links between the initial establishment of lateral asymmetry and subsequent asymmetries in organ morphogenesis are poorly characterized.

Results

To explore asymmetric organ morphogenesis during chordate evolution, we have begun to characterize left/right patterning of the heart and endodermal organs in an invertebrate chordate, Ciona intestinalis. Here, we show that Ciona has a laterally asymmetric, right-sided heart. Our data indicate that cardiac lateral asymmetry requires H⁺/K⁺ ion flux, but is independent of Nodal signaling. Our pharmacological inhibitor studies show that ion flux is required for polarization of epidermal cilia and neurula rotation and suggest that ion flux functions synergistically with chorion contact to drive cardiac laterality. Live imaging analysis revealed that larval heart progenitor cells undergo a lateral shift without displaying any migratory behaviors. Furthermore, we find that this passive shift corresponds with the emergence of lateral asymmetry in the endoderm, which is also ion flux dependent.

Conclusions

Our data suggest that ion flux promotes laterally asymmetric morphogenesis of the larval endoderm rudiment leading to a passive, Nodal-independent shift in the position of associated heart progenitor cells. These findings help to refine hypotheses regarding ancestral chordate left/right patterning mechanisms and how they have diverged within invertebrate and vertebrate chordate lineages.

SUBMITTER: Palmquist K 

PROVIDER: S-EPMC5526266 | biostudies-literature | 2017

REPOSITORIES: biostudies-literature