A revised spiralian homeobox gene classification incorporating new polychaete transcriptomes reveals a diverse TALE class and a divergent Hox gene

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Abstract

The diversity of mechanisms and capacity for regeneration across the Metazoa present an intriguing challenge in evolutionary biology, impacting on the burgeoning field of regenerative medicine. Broad taxonomic sampling is essential to improve our understanding of regeneration, and studies outside of the traditional model organisms have proved extremely informative. Within the historically under-studied Spiralia, the Annelida have an impressive variety of tractable regenerative systems. The biomeralising, blastema-less regeneration of the head appendage (operculum) of the serpulid polychaete keelworm Spirobranchus (formerly Pomatoceros) lamarcki is one such system. To profile potential regulatory mechanisms, we classified the homeobox gene content of opercular regeneration transcriptomes. As a result of retrieving several difficult-to-classify homeobox sequences, we performed an extensive search and phylogenetic analysis of the TALE and PRD-class homeobox gene content of a broad selection of lophotrochozoan genomes. These analyses contribute to our increasing understanding of the diversity, taxonomic extent, rapid evolution, and radical flexibility of these recently discovered homeobox gene radiations. Our expansion and integration of previous nomenclature systems helps to clarify their cryptic orthology. We also describe an unusual divergent S. lamarcki Antp gene, a previously unclassified lophotrochozoan orphan gene family (Lopx), and a number of novel Nk class orphan genes. The expression and potential involvement of many of these lineage- and clade-restricted homeobox genes in S. lamarcki operculum regeneration provides an example of diversity in regenerative mechanisms, as well as significantly improving our understanding of homeobox gene evolution.
Original languageEnglish
Pages (from-to)2151–2167
Number of pages17
JournalGenome Biology and Evolution
Volume10
Issue number9
Early online date7 Jul 2018
DOIs
Publication statusPublished - 1 Sept 2018

Keywords

  • Spirobranchus lamarcki
  • Regeneration
  • Operculum
  • Biomineralization
  • NK genes
  • PRD class genes

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