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The transcription factor NF-κB in the demosponge Amphimedon queenslandica: insights on the evolutionary origin of the Rel homology domain

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Abstract

The Rel/nuclear factor-kappa B (NF-κB) and nuclear factor of activated T-cells (NFAT) transcription factors contribute to the regulation of an assortment of biological processes by binding DNA with high specificity using their Rel homology domain (RHD). Recently, it has been shown that members of these gene families are present in the genome of the anthozoan cnidarian Nematostella vectensis, indicating that they predate the evolution of the most recent ancestor to living bilaterians. By identifying a single NF-κB gene in the genome of the demosponge Amphimedon queenslandica, a representative of an even earlier branching metazoan lineage, we demonstrate here that the Rel/NF-κB family originated at the dawn of the Metazoa. There is no evidence of RHDs in fungal and choanoflagellate genomes, supporting the notion that the RHD is a metazoan-specific innovation. The A. queenslandica gene (AmqNF-κB) encodes a protein that is highly similar in structure to the vertebrate NF-κB p50/p52 proteins, possessing both a RHD and ankyrin (ANK) repeats. The intact AmqNF-κB contrasts with the N. vectensis NF-κB, which lacks ANK repeats, and suggests that the ancestral metazoan NF-κB was configured identically to contemporary vertebrate and sponge forms. AmqNF-κB is expressed during A. queenslandica embryogenesis, suggesting a developmental role.

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Acknowledgement

This work was supported by Australian Research Council grants to B.M.D. We gratefully acknowledge the contribution of The United States Department of Energy Joint Genome Institute in the production of Amphimedon (Reniera) genomic and EST sequences used in this study through the Community Sequencing Program. We thank the Director and staff of the University of Queensland Heron Island Research Station for field assistance; the Great Barrier Reef Marine Park Authority for granting permission to carry out this research; and Maja Adamska, Sandie Degnan, Claire Larroux, and Gemma Richards for their valuable advice.

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  1. School of Integrative Biology, University of Queensland, Brisbane, 4072, Australia

    Marie Gauthier & Bernard M. Degnan

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  1. Marie Gauthier
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  2. Bernard M. Degnan
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Correspondence to Bernard M. Degnan.

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Communicated by M. Q. Martindale

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Fig. S1

Alignments used for the phylogenetic analyses of the RHD-containing proteins (a, b) and the ANK-repeat containing proteins (c) presented in Fig. 4. Abbreviations are as in Figs. 2 and 4 (DOC 61.5 KB)

Fig. S2

The nucleotide and deduced amino acid sequence of A. queenslandica NF-κB cDNA. Exons 1 to 24 are delimited in the text with alternating blue and black text. The cDNA is 3,601-bp long and encodes a protein of 1,095 amino acids (DOC 33.0 KB)

Fig. S3

Comparison of the amino acid sequence of AmqNF-κB ANK domains with other genes containing the ANK-repeat motif. The intron boundaries are shown in red for known sequences (the genomic predictions for NvBcl3 and NvIkB presented gaps and therefore did not permit determination of the intron exon boundaries of the ANK-repeat motif) (DOC 34.5 KB)

Table S1

Sequence ID for genes used for phylogenetic analyses with corresponding Uniprot primary accession numbers (available on the web site http://www.ebi.uniprot.org/index.shtml) and species name (DOC 51.0 KB)

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Gauthier, M., Degnan, B.M. The transcription factor NF-κB in the demosponge Amphimedon queenslandica: insights on the evolutionary origin of the Rel homology domain. Dev Genes Evol 218, 23–32 (2008). https://doi.org/10.1007/s00427-007-0197-5

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