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

Karl Palmquist,Brad Davidson

doi:10.1186/s13227-017-0075-9

Abstract

BackgroundThe 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.ResultsTo 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.ConclusionsOur 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.

Highlights

The evolutionary emergence and diversification of the chordates appear to involve dramatic changes in organ morphogenesis along the left/right axis
Directed lateral asymmetry of the Ciona heart The recent characterization of Ciona embryonic left– right patterning has failed to ascertain if embryonic asymmetry translates into post-metamorphic asymmetry
By St. 25, the trunk region displays laterally asymmetric lobes (Fig. 1c′′). This overall morphological asymmetry is associated with a lateral shift of the heart progenitor cells to one side of the endostyle (Fig. 1c′′)

Summary

Introduction

The evolutionary emergence and diversification of the chordates appear to involve dramatic changes in organ morphogenesis along the left/right axis. Links between the initial establishment of lateral asymmetry and subsequent asymmetries in organ morphogenesis are poorly characterized. Broad conservation of axial signaling is thought to reflect a deeply homologous, ancestral embryonic patterning mechanism at the base of the bilateria. The process by which the initial axial signals coordinate subsequent organ morphogenesis and how this process has been altered to generate novel traits remains poorly defined. This is true for the more recently characterized LR molecular axis [1]. Errors in embryonic LR axis formation underlie prevalent congenital abnormalities in organ form and function [2, 3]

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Discussion

Conclusion