Specific retention of the protostome-specific PsGEF may parallel with the evolution of mushroom bodies in insect and lophotrochozoan brains

BMC Biol. 2009 May 7;7:21. doi: 10.1186/1741-7007-7-21.

Abstract

Background: Gene gain and subsequent retention or loss during evolution may be one of the underlying mechanisms involved in generating the diversity of metazoan nervous systems. However, the causal relationships acting therein have not been studied extensively.

Results: We identified the gene PsGEF (protostome-specific GEF), which is present in all the sequenced genomes of insects and limpet but absent in those of sea anemones, deuterostomes, and nematodes. In Drosophila melanogaster, PsGEF encodes a short version of a protein with the C2 and PDZ domains, as well as a long version with the C2, PDZ, and RhoGEF domains through alternative splicing. Intriguingly, the exons encoding the RhoGEF domain are specifically deleted in the Daphnia pulex genome, suggesting that Daphnia PsGEF contains only the C2 and PDZ domains. Thus, the distribution of PsGEF containing the C2, PDZ, and RhoGEF domains among metazoans appears to coincide with the presence of mushroom bodies. Mushroom bodies are prominent neuropils involved in the processing of multiple sensory inputs as well as associative learning in the insect, platyhelminth, and annelid brains. In the adult Drosophila brain, PsGEF is expressed in mushroom bodies, antennal lobe, and optic lobe, where it is necessary for the correct axon branch formation of alpha/beta neurons in mushroom bodies. PsGEF genetically interacts with Rac1 but not other Rho family members, and the RhoGEF domain of PsGEF induces actin polymerization in the membrane, thus resulting in the membrane ruffling that is observed in cultured cells with activated forms of Rac.

Conclusion: The specific acquisition of PsGEF by the last common ancestor of protostomes followed by its retention or loss in specific animal species during evolution demonstrates that there are some structural and/or functional features common between insect and lophotrochozoan nervous systems (for example, mushroom bodies), which are absent in all deuterostomes and cnidarians. PsGEF is therefore one of genes associated with the diversity of metazoan nervous systems.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Annelida / anatomy & histology*
  • Axons / metabolism
  • Biological Evolution*
  • Brain / anatomy & histology*
  • Brain / embryology
  • Brain / metabolism
  • Cells, Cultured
  • Daphnia / metabolism
  • Drosophila melanogaster / cytology
  • Drosophila melanogaster / metabolism
  • Exons / genetics
  • Gene Deletion
  • Gene Expression Regulation, Developmental
  • Guanine Nucleotide Exchange Factors / chemistry
  • Guanine Nucleotide Exchange Factors / genetics
  • Guanine Nucleotide Exchange Factors / metabolism*
  • HeLa Cells
  • Humans
  • Insecta / anatomy & histology*
  • Introns / genetics
  • Molecular Sequence Data
  • Mushroom Bodies / anatomy & histology*
  • Organ Specificity
  • Protein Structure, Tertiary
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • rac1 GTP-Binding Protein / metabolism
  • rho GTP-Binding Proteins / metabolism

Substances

  • Guanine Nucleotide Exchange Factors
  • RNA, Messenger
  • rac1 GTP-Binding Protein
  • rho GTP-Binding Proteins