Origin of Metazoan Patterning Systems and the Role of ANTP‐Class Homeobox Genes

Abstract

The origin (Metazoa) is considered a key event in the history of life on Earth. Understanding the molecular mechanisms underlying the emergence of animals has become one of the principal aims of research in many laboratories. These research programs are propelled by the many genome projects (past and present) carried out in labs around the world. A thorough comparison of the structure and composition of genomes provides us with a unique opportunity to understand the evolution of animals as products of their genome dynamics. One major focus of attention has been the characterisation of families of transcriptional regulators in different lineages and the careful analysis of their patterns of evolutionary change. Needless to say, these comparisons make full sense only in the context of parallel analysis of their expression domains and their historical changes. Among the most studied families of transcription factors (those with critical involvement in processes such as regulation of axial polarity, proliferation or differentiation) is the so‐called ANTP (for Anntenapedia)‐class of homeodomain proteins. Importantly, this class of proteins is specific to the metazoans, and the diversification of its members appears to follow a clear phyletic pattern of variation.

The knowledge of the changes in composition and expression domains of the major families of ANTP‐class homeobox genes in the early divergent metazoan phyla (Porifera, Ctenophora, Placozoa, Cnidaria) plus in the bilaterian Xenacoelomorpha has been advancing. The current scarcity of knowledge seems to restrict the advancement of our understanding, which needs further research to expand.

Key Concepts

  • Homeobox‐containing genes encode for transcription factors. The homeobox sequence is translated into the homeodomain.
  • The homeobox genes are grouped into classes and families. The ANTP class of homeobox genes is metazoan‐specific.
  • Phylogenetic relationships at the origin of Metazoa are unresolved. They provide a framework for putative evolutionary scenarios of any gene family.
  • Hox and Parahox genes control specific aspects of the main metazoan body axis. They are the best studied families of ANTP class homeobox genes.
  • Homeobox genes of the ANTP class control basic aspects of development, such as proliferation and differentiation of cells and tissues.
  • Family assignments within the ANTP class are, sometimes, difficult, given the low phylogenetic signal provided by just the homeodomain. Other additional motifs in the protein sequence (such as interaction domains or specific peptides) can be critical in determining affinities.

Keywords: homeobox; ANTP class; evolution; phylogenetic relationships; metazoan; body patterning

Figure 1. Phylogenetic relationships among the early branching metazoan phyla. The presence of Hox and ParaHox genes is indicated by purple and orange stars, respectively. The deduced parsimonious emergence of these gene families in the frame of each tree topology is indicated with circles. The alternate topologies are based on the studies of (a) Porifera sister to the remaining metazoans (Philippe et al., or Nosenko et al., ); (b) Ctenophora as sister to the remaining metazoans (Dunn et al., ; Hejnol et al., ; or Moroz et al., ); (c) Ctenophora + Porifera as sister groups (Ryan et al., ); (d) Xenacoelomorpha (dotted green branches) as sister to the remaining bilaterians (diamond; Hejnol et al., ) or as members of Deuterostomia (circle; Philippe et al. 2011). This drawing is based on data presented in Figure 1 of Whelan et al. ().
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Further Reading

Budd GE (2013) At the origin of animals: the revolutionary cambrian fossil record. Current Genomics 14 (6): 344–354.

Bürglin TR (2011) Homeodomain subtypes and functional diversity. Subcellular Biochemistry 52: 95–122.

Merabet S and Galliot B (2015) The TALE face of Hox proteins in animal evolution. Frontiers in Genetics 6: 267. DOI: 10.3389/fgene.2015.00267.eCollection 2015.

Telford MJ, Budd GE and Philippe H (2015) Phylogenomic insights into animal evolution. Current Biology 25 (19): R876–R887.

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Thomas‐Chollier, Morgane, and Martinez, Pedro(Feb 2016) Origin of Metazoan Patterning Systems and the Role of ANTP‐Class Homeobox Genes. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0022852.pub2]