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Open Access Research

The Fox/Forkhead transcription factor family of the hemichordate Saccoglossus kowalevskii

Jens H Fritzenwanker1*, John Gerhart2, Robert M Freeman3 and Christopher J Lowe1

Author Affiliations

1 Hopkins Marine Station of Stanford University, 120 Oceanview Boulevard, Pacific Grove, CA 93950, USA

2 Department of Molecular and Cell Biology, University of California, 142 Life Sciences Addition #3200, Berkeley, CA 94720, USA

3 Department of Systems Biology, Harvard Medical School, 200 Longwood Avenue, Warren Alpert 536, Boston, MA 02115, USA

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EvoDevo 2014, 5:17  doi:10.1186/2041-9139-5-17

Published: 7 May 2014

Abstract

Background

The Fox gene family is a large family of transcription factors that arose early in organismal evolution dating back to at least the common ancestor of metazoans and fungi. They are key components of many gene regulatory networks essential for embryonic development. Although much is known about the role of Fox genes during vertebrate development, comprehensive comparative studies outside vertebrates are sparse. We have characterized the Fox transcription factor gene family from the genome of the enteropneust hemichordate Saccoglossus kowalevskii, including phylogenetic analysis, genomic organization, and expression analysis during early development. Hemichordates are a sister group to echinoderms, closely related to chordates and are a key group for tracing the evolution of gene regulatory mechanisms likely to have been important in the diversification of the deuterostome phyla.

Results

Of the 22 Fox gene families that were likely present in the last common ancestor of all deuterostomes, S. kowalevskii has a single ortholog of each group except FoxH, which we were unable to detect, and FoxQ2, which has three paralogs. A phylogenetic analysis of the FoxQ2 family identified an ancestral duplication in the FoxQ2 lineage at the base of the bilaterians. The expression analyses of all 23 Fox genes of S. kowalevskii provide insights into the evolution of components of the regulatory networks for the development of pharyngeal gill slits (foxC, foxL1, and foxI), mesoderm patterning (foxD, foxF, foxG), hindgut development (foxD, foxI), cilia formation (foxJ1), and patterning of the embryonic apical territory (foxQ2).

Conclusions

Comparisons of our results with data from echinoderms, chordates, and other bilaterians help to develop hypotheses about the developmental roles of Fox genes that likely characterized ancestral deuterostomes and bilaterians, and more recent clade-specific innovations.

Keywords:
Hemichordate; Saccoglossus kowalevskii; Fox cluster; Deuterostome evolution; Gene regulatory networks; Gill slits; Gut patterning; EH-I-like motif; FoxQ2; Fox genes; Forkhead; Fork head