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Functional evolution of pigment synthesis pathways in teleost fish through gen(om)e duplication

Subject Area Evolution, Anthropology
Term from 2007 to 2012
Project identifier Deutsche Forschungsgemeinschaft (DFG) - Project number 51155556
 
Final Report Year 2009

Final Report Abstract

Gene and genome duplications are major mechanisms in evolution of life. Three rounds of genome duplication have occurred in the vertebrate lineage, two rounds during early vertebrate evolution and a third round, the fish-specific genome duplication (FSGD) in the fish lineage. Although the majority of duplicated genes are usually lost after duplication, whole genome duplications are considered to facilitate speciation processes and to provide the genetic raw material for major evolutionary transitions and increases in morphological complexity. In the present study, we have used comparative genomic approaches combining the reconstruction of phylogenetic trees of gene families, their chromosomal location as well as gene function studies (expression analyses and knockdown experiments) to investigate the evolutionary consequences and significance of the three vertebrate genome duplications. First, we have studied the impact of the FSGD on the evolution of pigment cell development and differentiation in fish. The pigmentary system of fishes is the most complex and diverse among vertebrates. Our investigation of more than 120 genes showed that pigmentation genes have been preferentially retained in duplicate after the FSGD so that fish genomes contain around 30% more putative pigmentation genes than tetrapods. Large parts of pigment cell regulatory pathways are present in duplicate being potentially involved in pigmentary innovations in fish. There are also important differences in the retention of duplicated pigmentafion genes among divergent fish lineages. Functional studies of pigment synthesis enzymes in zebrafish and medaka, particularly of the tyrosinase family, revealed lineage-specific functional evolution of duplicated pigmentation genes in fish, but also pointed to anciently conserved gene functions in vertebrates. These results suggest that the FSGD has facilitated the evolution of the pigmentary system in fish. Next, the evolutionary history of the endothelin signaling system consisting of endothelin ligands and receptors was reconstructed. The endothelin system is a key component for the development of a major vertebrate innovation, the neural crest, to which amongst others also the pigment cells belong. Our analysis shows that the endothelin system emerged in an ancestor of the vertebrate lineage and that its members in living vertebrate genomes are derived from the vertebrate whole genome duplications. Each round of genome duplication was followed by co-evolution of the expanding endothelin ligand and receptor repertoires. This supports the importance of genome duplications for the origin and diversification of the neural crest, but also underlines a major role for the integration of newly arising genes into the neural crest regulatory network. In conclusion, the present study supports a major role of whole genome duplication for phenotypic evolution and biodiversity in vertebrates, particulariy in fish.

Publications

  • 2008. The evolution of teleost pigmentation and the fish-specific genome duplicafion. Journal of Fish Biology 73:1891-1918
    Braasch, I., J. N. Volff, and M. Schartl
  • Annual Meeting of the Society for Molecular Biology and Evolution (SMBE) 2008; 5-8 June 2008, Barcelona, Spain. Evolutionary developmental genomics of pigmentation pathways in fish
    Ingo Braasch, Daniel Liedtke, Jean-Nicolas Volff, Manfred Schartl
  • Zoological Institute of the University of Basel, Switzerland, 30 June 2008. Evolution of the vertebrate neural crest and pigmentation pathways by three rounds of genome duplication
    Ingo Braasch
  • 2009. The endothelin system: evolution of vertebrate-specific ligand-receptor interactions by three rounds of genome duplication. Molecular Biology and Evolution, January 27, 2009
    Braasch, I., J. N. Volff, and M. Schartl
  • Evolution by genome duplication: insights from pigmentation pathways in teleost fishes
    Braasch, I., F. Brunet, J. N. Volff, and M. Schartl
  • Functional evolution of tyrp1 genes involved in melanin synthesis after duplication in fish
    Braasch, I., D. Liedtke, J. N. Volff, and M. Schartl
 
 

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