Modular development of the teleost trunk along the dorsoventral axis and zic1/zic4 as selector genes in the dorsal module

Development. 2013 Apr;140(7):1486-96. doi: 10.1242/dev.088567. Epub 2013 Mar 5.

Abstract

Teleost fish exhibit remarkable diversity in morphology, such as fins and coloration, particularly on the dorsal side. These structures are evolutionary adaptive because their back is highly visible to other individuals. However, owing to the late phenotypic appearance (from larva to adult) and lack of appropriate mutants, the genetic mechanisms that regulate these dorsoventrally asymmetric external patterns are largely unknown. To address this, we have analyzed the spontaneous medaka mutant Double anal fin (Da), which exhibits a mirror-image duplication of the ventral half across the lateral midline from larva to adult. Da is an enhancer mutant for zic1 and zic4 in which their expression in dorsal somites is lost. We show that the dorsoventral polarity in Da somites is lost and then demonstrate using transplantation techniques that somites and their derived tissues globally determine the multiple dorsal-specific characteristics of the body (fin morphology and pigmentation) from embryo to adult. Intriguingly, the zic1/zic4 expression in the wild type persists throughout life in the dorsal parts of somite derivatives, i.e. the myotome, dermis and vertebrae, forming a broad dorsal domain in the trunk. Comparative analysis further implies a central role for zic1/zic4 in morphological diversification of the teleost body. Taken together, we propose that the teleost trunk consists of dorsal/ventral developmental modules and that zic1/zic4 in somites function as selector genes in the dorsal module to regulate multiple dorsal morphologies.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Body Patterning / genetics*
  • Cells, Cultured
  • Embryo, Nonmammalian
  • Fishes / embryology
  • Fishes / genetics
  • Fishes / metabolism
  • Gene Expression Regulation, Developmental
  • Genes, Switch / genetics
  • Genes, Switch / physiology
  • Models, Biological
  • Oryzias / embryology
  • Oryzias / genetics
  • Oryzias / metabolism
  • Phenotype
  • Somites / embryology
  • Somites / metabolism
  • Thorax / embryology*
  • Thorax / metabolism
  • Transcription Factors / genetics
  • Transcription Factors / physiology*
  • Zinc Fingers / genetics

Substances

  • Transcription Factors