Ancestral and novel roles of Pax family genes in mollusks

BMC Evol Biol. 2017 Mar 16;17(1):81. doi: 10.1186/s12862-017-0919-x.

Abstract

Background: Pax genes are transcription factors with significant roles in cell fate specification and tissue differentiation during animal ontogeny. Most information on their tempo-spatial mode of expression is available from well-studied model organisms where the Pax-subfamilies Pax2/5/8, Pax6, and Paxα/β are mainly involved in the development of the central nervous system (CNS), the eyes, and other sensory organs. In certain taxa, Pax2/5/8 seems to be additionally involved in the development of excretion organs. Data on expression patterns in lophotrochozoans, and in particular in mollusks, are very scarce for all the above-mentioned Pax-subfamilies, which hampers reconstruction of their putative ancestral roles in bilaterian animals. Thus, we studied the developmental expression of Pax2/5/8, Pax6, and the lophotrochozoan-specific Paxβ in the worm-shaped mollusk Wirenia argentea, a member of Aplacophora that together with Polyplacophora forms the Aculifera, the proposed sister taxon to all primarily single-shelled mollusks (Conchifera).

Results: All investigated Pax genes are expressed in the developing cerebral ganglia and in the ventral nerve cords, but not in the lateral nerve cords of the tetraneural nervous system. Additionally, Pax2/5/8 is expressed in epidermal spicule-secreting or associated cells of the larval trunk and in the region of the developing protonephridia. We found no indication for an involvement of the investigated Pax genes in the development of larval or adult sensory organs of Wirenia argentea.

Conclusions: Pax2/5/8 seems to have a conserved role in the development of the CNS, whereas expression in the spicule-secreting tissues of aplacophorans and polyplacophorans suggests co-option in aculiferan skeletogenesis. The Pax6 expression pattern in Aculifera largely resembles the common bilaterian expression during CNS development. All data available on Paxβ expression argue for a common role in lophotrochozoan neurogenesis.

Keywords: Aculifera; Development; EvoDevo; Evolution; Gene expression; Lophotrochozoa; Mollusca; Neurogenesis; Pax genes; Tetraneural nervous system.

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Eye / metabolism
  • Larva / growth & development
  • Mollusca / classification
  • Mollusca / genetics*
  • Mollusca / growth & development
  • Mollusca / metabolism
  • Paired Box Transcription Factors / chemistry
  • Paired Box Transcription Factors / genetics*
  • Paired Box Transcription Factors / metabolism*
  • Phylogeny
  • Sequence Alignment

Substances

  • Paired Box Transcription Factors