Comprehensive survey of carapacial ridge-specific genes in turtle implies co-option of some regulatory genes in carapace evolution

Evol Dev. 2005 Jan-Feb;7(1):3-17. doi: 10.1111/j.1525-142X.2005.05002.x.

Abstract

The turtle shell is an evolutionary novelty in which the developmental pattern of the ribs is radically modified. In contrast to those of other amniotes, turtle ribs grow laterally into the dorsal dermis to form a carapace. The lateral margin of carapacial primordium is called the carapacial ridge (CR), and is thought to play an essential role in carapace patterning. To reveal the developmental mechanisms underlying this structure, we systematically screened for genes expressed specifically in the CR of the Chinese soft-shelled turtle, Pelodiscus sinensis, using microbead-based differential cDNA analysis and real-time reverse transcription-polymerase chain reaction. We identified orthologs of Sp5, cellular retinoic acid-binding protein-I (CRABP-I), adenomatous polyposis coli down-regulated 1 (APCDD1), and lymphoid enhancer-binding factor-1 (LEF-1). Although these genes are conserved throughout the major vertebrate lineages, comparison of their expression patterns with those in chicken and mouse indicated that these genes have acquired de novo expression in the CR in the turtle lineage. In association with the expression of LEF-1, the nuclear localization of beta-catenin protein was detected in the CR ectoderm, suggesting that the canonical Wnt signaling triggers carapace development. These findings indicate that the acquisition of the turtle shell did not involve the creation of novel genes, but was based on the co-option of pre-existing genes.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Body Patterning
  • Cell Lineage
  • Cell Nucleus / metabolism
  • Chickens
  • Cloning, Molecular
  • Cytoskeletal Proteins / metabolism
  • DNA / metabolism
  • DNA Primers / chemistry
  • DNA, Complementary / metabolism
  • DNA-Binding Proteins / metabolism
  • Developmental Biology*
  • Ectoderm / metabolism
  • Evolution, Molecular*
  • Gene Expression Regulation, Developmental*
  • Genes, Regulator
  • Immunohistochemistry
  • In Situ Hybridization
  • Intracellular Signaling Peptides and Proteins / metabolism
  • Limb Buds / embryology
  • Lymphoid Enhancer-Binding Factor 1
  • Membrane Proteins
  • Models, Biological
  • Phylogeny
  • Receptors, Retinoic Acid / metabolism
  • Reverse Transcriptase Polymerase Chain Reaction
  • Signal Transduction
  • Temperature
  • Time Factors
  • Trans-Activators / metabolism
  • Transcription Factors / metabolism
  • Turtles
  • beta Catenin

Substances

  • Apcdd1 protein, mouse
  • Cytoskeletal Proteins
  • DNA Primers
  • DNA, Complementary
  • DNA-Binding Proteins
  • Intracellular Signaling Peptides and Proteins
  • Lymphoid Enhancer-Binding Factor 1
  • Membrane Proteins
  • Receptors, Retinoic Acid
  • Trans-Activators
  • Transcription Factors
  • beta Catenin
  • retinoic acid binding protein I, cellular
  • DNA