ParaHox gene expression in larval and postlarval development of the polychaete Nereis virens (Annelida, Lophotrochozoa)

BMC Dev Biol. 2008 May 29:8:61. doi: 10.1186/1471-213X-8-61.

Abstract

Background: Transcription factors that encode ANTP-class homeobox genes play crucial roles in determining the body plan organization and specification of different organs and tissues in bilaterian animals. The three-gene ParaHox family descends from an ancestral gene cluster that existed before the evolution of the Bilateria. All three ParaHox genes are reported from deuterostomes and lophotrochozoans, but not to date from any ecdysozoan taxa, and there is evidence that the ParaHox genes, like the related Hox genes, were ancestrally a single chromosomal cluster. However, unlike the Hox genes, there is as yet no strong evidence that the ParaHox genes are expressed in spatial and temporal order during embryogenesis.

Results: We isolated fragments of the three Nereis virens ParaHox genes, then used these as probes for whole-mount in situ hybridization in larval and postlarval worms. In Nereis virens the ParaHox genes participate in antero-posterior patterning of ectodermal and endodermal regions of the digestive tract and are expressed in some cells in the segment ganglia. The expression of these genes occurs in larval development in accordance with the position of these cells along the main body axis and in postlarval development in accordance with the position of cells in ganglia along the antero-posterior axis of each segment. In none of these tissues does expression of the three ParaHox genes follow the rule of temporal collinearity.

Conclusion: In Nereis virens the ParaHox genes are expressed during antero-posterior patterning of the digestive system (ectodermal foregut and hindgut, and endodermal midgut) of Nereis virens. These genes are also expressed during axial specification of ventral neuroectodermal cell domains, where the expression domains of each gene are re-iterated in each neuromere except for the first parapodial segment. These expression domains are probably predetermined and may be directed on the antero-posterior axis by the Hox genes, whose expression starts much earlier during embryogenesis. Our results support the hypothesis that the ParaHox genes are involved in antero-posterior patterning of the developing embryo, but they do not support the notion that these genes function only in the patterning of endodermal tissues.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Body Patterning / genetics
  • Embryo, Nonmammalian / metabolism
  • Gene Expression Regulation, Developmental*
  • Genes, Homeobox*
  • In Situ Hybridization
  • Larva / genetics
  • Larva / growth & development
  • Multigene Family
  • Polychaeta / embryology
  • Polychaeta / genetics
  • Polychaeta / growth & development*
  • Transcription Factors / genetics

Substances

  • Transcription Factors