Antagonizing retinoic acid and FGF/MAPK pathways control posterior body patterning in the invertebrate chordate Ciona intestinalis

PLoS One. 2012;7(9):e46193. doi: 10.1371/journal.pone.0046193. Epub 2012 Sep 25.

Abstract

Vertebrate embryos exploit the mutual inhibition between the RA and FGF signalling pathways to coordinate the proliferative elongation of the main body axis with the progressive patterning and differentiation of its neuroectodermal and paraxial mesodermal structures. The evolutionary history of this patterning system is still poorly understood. Here, we investigate the role played by the RA and FGF/MAPK signals during the development of the tail structures in the tunicate Ciona intestinalis, an invertebrate chordate belonging to the sister clade of vertebrates, in which the prototypical chordate body plan is established through very derived morphogenetic processes. Ciona embryos are constituted of few cells and develop according to a fixed lineage; elongation of the tail occurs largely by rearrangement of postmitotic cells; mesoderm segmentation and somitogenesis are absent. We show that in the Ciona embryo, the antagonism of the RA and FGF/MAPK signals is required to control the anteroposterior patterning of the tail epidermis. We also demonstrate that the RA, FGF/MAPK and canonical Wnt pathways control the anteroposterior patterning of the tail peripheral nervous system, and reveal the existence of distinct subpopulations of caudal epidermal neurons with different responsiveness to the RA, FGF/MAPK and canonical Wnt signals. Our data provide the first demonstration that the use of the antagonism between the RA and FGF signals to pattern the main body axis predates the emergence of vertebrates and highlight the evolutionary plasticity of this patterning strategy, showing that in different chordates it can be used to pattern different tissues within the same homologous body region.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Body Patterning / genetics
  • Body Patterning / physiology*
  • Butadienes / pharmacology
  • Ciona intestinalis / drug effects
  • Ciona intestinalis / embryology*
  • Ciona intestinalis / metabolism*
  • Enzyme Inhibitors / pharmacology
  • Fibroblast Growth Factor 2 / pharmacology
  • Fibroblast Growth Factors / antagonists & inhibitors
  • Fibroblast Growth Factors / metabolism*
  • Gene Expression Regulation, Developmental / drug effects
  • Mitogen-Activated Protein Kinases / antagonists & inhibitors
  • Mitogen-Activated Protein Kinases / metabolism*
  • Nitriles / pharmacology
  • Signal Transduction / drug effects
  • Tretinoin / metabolism
  • Tretinoin / pharmacology*

Substances

  • Butadienes
  • Enzyme Inhibitors
  • Nitriles
  • U 0126
  • Fibroblast Growth Factor 2
  • Tretinoin
  • Fibroblast Growth Factors
  • Mitogen-Activated Protein Kinases

Grants and funding

Work was financed by the CNRS and the Agence Nationale pour la Recherche (Programme Blanc “Chor-Evo-Net”). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.