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The structure, splicing, synteny and expression of lamprey COE genes and the evolution of the COE gene family in chordates

Abstract

COE genes encode transcription factors that have been found in all metazoans examined to date. They possess a distinctive domain structure that includes a DNA-binding domain (DBD), an IPT/TIG domain and a helix-loop-helix (HLH) domain. An intriguing feature of the COE HLH domain is that in jawed vertebrates it is composed of three helices, compared to two in invertebrates. We report the isolation and expression of two COE genes from the brook lamprey Lampetra planeri and compare these to COE genes from the lampreys Lethenteron japonicum and Petromyzon marinus. Molecular phylogenetic analyses do not resolve the relationship of lamprey COE genes to jawed vertebrate paralogues, though synteny mapping shows that they all derive from duplication of a common ancestral genomic region. All lamprey genes encode conserved DBD, IPT/TIG and HLH domains; however, the HLH domain of lamprey COE-A genes encodes only two helices while COE-B encodes three helices. We also identified COE-B splice variants encoding either two or three helices in the HLH domain, along with other COE-A and COE-B splice variants affecting the DBD and C-terminal transactivation regions. In situ hybridisation revealed expression in the lamprey nervous system including the brain, spinal cord and cranial sensory ganglia. We also detected expression of both genes in mesenchyme in the pharyngeal arches and underlying the notochord. This allows us to establish the primitive vertebrate expression pattern for COE genes and compare this to that of invertebrate chordates and other animals to develop a model for COE gene evolution in chordates.

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Acknowledgements

We thank the Forestry Commission of England for permission to collect lamprey embryos and Dr. Jo Begbie for access to histology facilities. RL-R was supported by the Mexican National Council for Science and Technology (CONACYT). CP was supported by a Royal Society Newton International Fellowship and by an EMBO Long-Term Fellowship.

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Correspondence to Sebastian M. Shimeld.

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Communicated by Karen E. Sears

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Lara-Ramírez, R., Poncelet, G., Patthey, C. et al. The structure, splicing, synteny and expression of lamprey COE genes and the evolution of the COE gene family in chordates. Dev Genes Evol 227, 319–338 (2017). https://doi.org/10.1007/s00427-017-0591-6

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Keywords

  • COE
  • Ebf
  • Neurogenesis
  • Lamprey
  • Cranial ganglia
  • Pharyngeal arch
  • Brain