MBE Advance Access published online on February 21, 2008
Molecular Biology and Evolution, doi:10.1093/molbev/msn047
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Research Article |
Genesis and expansion of metazoan transcription factor gene classes
1 School of Integrative Biology, The University of Queensland, Brisbane QLD 4072, Australia
2 School of Biological Sciences, The University of Reading, Whiteknights, Reading, RG6 6BX, United Kingdom
3 Institute of Molecular Bioscience, The University of Queensland, Brisbane QLD 4072, Australia
4 DOE Joint Genome Institute, 2800 Mitchell Avenue, Walnut Creek, CA 94598, USA
5 Center for Integrative Genomics, Department of Molecular and Cell Biology, University of California, Berkeley, CA 94720, USA
6 Department of Zoology, University of Oxford, South Parks Road, Oxford, OX1 3PS, United Kingdom
* To whom correspondence should be addressed. Tel: +61 7 3365 2467. Fax: +61 7 3365 1655. E-mail: b.degnan{at}uq.edu.au.
Received for publication November 26, 2007. Revision received February 5, 2008. Accepted for publication February 12, 2008.
We know little about the genomic events that led to the advent of a multicellular grade of organization in animals, one of the most dramatic transitions in evolution. Metazoan multicellularity is correlated with the evolution of embryogenesis, which presumably was underpinned by a gene regulatory network reliant on the differential activation of signalling pathways and transcription factors. Many transcription factor genes that play critical roles in bilaterian development largely appear to have evolved before the divergence of cnidarian and bilaterian lineages. In contrast, sponges seem to have a more limited suite of transcription factors, suggesting that the developmental regulatory gene repertoire changed markedly during early metazoan evolution. Using whole genome information from the sponge Amphimedon queenslandica, a range of eumetazoans, and the choanoflagellate Monosiga brevicollis, we investigate the genesis and expansion of homeobox, Sox, T-box, and Fox transcription factor genes. Comparative analyses reveal that novel transcription factor domains (such as Paired, POU, and T-box) arose very early in metazoan evolution, prior to the separation of extant metazoan phyla but after the divergence of choanoflagellate and metazoan lineages. Phylogenetic analyses indicate that transcription factor classes then gradually expanded at the base of Metazoa before the bilaterian radiation, with each class following a different evolutionary trajectory. Based on the limited number of transcription factors in the Amphimedon genome, we infer that the genome of the metazoan last common ancestor included fewer gene members in each class than are present in extant eumetazoans. Transcription factor orthologues present in sponge, cnidarian, and bilaterian genomes may represent part of the core metazoan regulatory network underlying the origin of animal development and multicellularity.
Key Words: developmental genes • Amphimedon queenslandica • sponge • homeodomain • Sox • Fox • T-box
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