Abstract
BackgroundThe 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.ResultsOf 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).ConclusionsComparisons 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.
Highlights
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
The S. kowalevskii genome contains a single copy of all bilaterian Fox family members with two notable exceptions; we failed to identify a representative of FoxH, which was likely secondarily lost in hemichordates and echinoderms [20] since it is present in the mollusc Lottia gigantea [33]
The FoxQ2 family is represented by three paralogs in S. kowalevskii (Figure 1)
Summary
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. The development of animal body plans and associated morphological innovations are a result of genetic and cellular mechanisms acting in space and time Developmental regulation of these mechanisms has many layers of complexity, and involves interacting suites of transcription factors that form core conserved regulatory kernels [1]. Four of these families have subsequently been further divided: FoxL into FoxL1 and FoxL2, FoxN into FoxN1/4 and FoxN2/3, FoxQ into FoxQ1 and FoxQ2, and FoxJ into FoxJ1 and FoxJ2 [30] This has led to the identification of a total number of 24 Fox families, making it possible to compare their orthologs in different species to gain insights into the evolution of this large transcription factor family and their roles in metazoan developmental programs
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