Distinct molecular strategies for Hox-mediated limb suppression in Drosophila: from cooperativity to dispensability/antagonism in TALE partnership

PLoS Genet. 2013;9(3):e1003307. doi: 10.1371/journal.pgen.1003307. Epub 2013 Mar 7.

Abstract

The emergence following gene duplication of a large repertoire of Hox paralogue proteins underlies the importance taken by Hox proteins in controlling animal body plans in development and evolution. Sequence divergence of paralogous proteins accounts for functional specialization, promoting axial morphological diversification in bilaterian animals. Yet functionally specialized paralogous Hox proteins also continue performing ancient common functions. In this study, we investigate how highly divergent Hox proteins perform an identical function. This was achieved by comparing in Drosophila the mode of limb suppression by the central (Ultrabithorax and AbdominalA) and posterior class (AbdominalB) Hox proteins. Results highlight that Hox-mediated limb suppression relies on distinct modes of DNA binding and a distinct use of TALE cofactors. Control of common functions by divergent Hox proteins, at least in the case studied, relies on evolving novel molecular properties. Thus, changes in protein sequences not only provide the driving force for functional specialization of Hox paralogue proteins, but also provide means to perform common ancient functions in distinct ways.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Body Patterning / genetics
  • DNA-Binding Proteins* / genetics
  • DNA-Binding Proteins* / metabolism
  • Drosophila melanogaster* / genetics
  • Drosophila melanogaster* / growth & development
  • Evolution, Molecular
  • Extremities / growth & development*
  • Gene Duplication / genetics
  • Gene Expression Regulation, Developmental
  • Homeodomain Proteins* / classification
  • Homeodomain Proteins* / genetics
  • Homeodomain Proteins* / metabolism
  • Sequence Homology, Amino Acid

Substances

  • DNA-Binding Proteins
  • Homeodomain Proteins

Grants and funding

Work was supported by Grants from Agence Nationale pour la Recherche (ANR), l'Association pour la Recherche contre le Cancer (ARC), la Fondation pour la Recherche Medicale (FRM), and an Indo-French CEFIPRA grant. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.