Abstract
BackgroundGATA transcription factors influence many developmental processes, including the specification of embryonic germ layers. The GATA gene family has significantly expanded in many animal lineages: whereas diverse cnidarians have only one GATA transcription factor, six GATA genes have been identified in many vertebrates, five in many insects, and eleven to thirteen in Caenorhabditis nematodes. All bilaterian animal genomes have at least one member each of two classes, GATA123 and GATA456.ResultsWe have identified one GATA123 gene and one GATA456 gene from the genomic sequence of two invertebrate deuterostomes, a cephalochordate (Branchiostoma floridae) and a hemichordate (Saccoglossus kowalevskii). We also have confirmed the presence of six GATA genes in all vertebrate genomes, as well as additional GATA genes in teleost fish. Analyses of conserved sequence motifs and of changes to the exon-intron structure, and molecular phylogenetic analyses of these deuterostome GATA genes support their origin from two ancestral deuterostome genes, one GATA 123 and one GATA456. Comparison of the conserved genomic organization across vertebrates identified eighteen paralogous gene families linked to multiple vertebrate GATA genes (GATA paralogons), providing the strongest evidence yet for expansion of vertebrate GATA gene families via genome duplication events.ConclusionFrom our analysis, we infer the evolutionary birth order and relationships among vertebrate GATA transcription factors, and define their expansion via multiple rounds of whole genome duplication events. As the genomes of four independent invertebrate deuterostome lineages contain single copy GATA123 and GATA456 genes, we infer that the 0R (pre-genome duplication) invertebrate deuterostome ancestor also had two GATA genes, one of each class. Synteny analyses identify duplications of paralogous chromosomal regions (paralogons), from single ancestral vertebrate GATA123 and GATA456 chromosomes to four paralogons after the first round of vertebrate genome duplication, to seven paralogons after the second round of vertebrate genome duplication, and to fourteen paralogons after the fish-specific 3R genome duplication. The evolutionary analysis of GATA gene origins and relationships may inform understanding vertebrate GATA factor redundancies and specializations.
Highlights
GATA transcription factors influence many developmental processes, including the specification of embryonic germ layers
Identification of hemichordate and cephalochordate GATA sequences While we recently concluded that the genome of the ancestor to both deuterostomes and protostomes encoded two GATA transcription factors [6,7], another group [8] suggested that at least five GATA factors were encoded by the genome of the last common ancestor of fruit flies, nematodes, and vertebrates, with subsequent losses occurring in some deuterostome lineages
An initial reciprocal blast suggested that these fragments encode distinct GATA1/2/3 and GATA4/5/6 orthologs, and this initial assignment was supported by the phylogenetic analyses below; we refer to these as BfloGATA123 and BfloGATA456
Summary
GATA transcription factors influence many developmental processes, including the specification of embryonic germ layers. The GATA gene family has significantly expanded in many animal lineages: whereas diverse cnidarians have only one GATA transcription factor, six GATA genes have been identified in many vertebrates, five in many insects, and eleven to thirteen in Caenorhabditis nematodes. Most animal genomes include multiple GATA transcription factor genes with widely conserved developmental roles[1]. The GATA transcription factor family is a relatively small and evolutionary tractable gene family, with only six members present in mammals, five in insects, and eleven in the nematode C. elegans. This gene family has undergone significant expansion in bilaterians compared to lower metazoans. Only a single GATA gene has been found in two cnidarian genomes currently sequenced [4]
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