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Abstract
BackgroundLbx/ladybird genes originated as part of the metazoan cluster of Nk homeobox genes. In all animals investigated so far, both the protostome genes and the vertebrate Lbx1 genes were found to play crucial roles in neural and muscle development. Recently however, additional Lbx genes with divergent expression patterns were discovered in amniotes. Early in the evolution of vertebrates, two rounds of whole genome duplication are thought to have occurred, during which 4 Lbx genes were generated. Which of these genes were maintained in extant vertebrates, and how these genes and their functions evolved, is not known.ResultsHere we searched vertebrate genomes for Lbx genes and discovered novel members of this gene family. We also identified signature genes linked to particular Lbx loci and traced the remnants of 4 Lbx paralogons (two of which retain Lbx genes) in amniotes. In teleosts, that have undergone an additional genome duplication, 8 Lbx paralogons (three of which retain Lbx genes) were found. Phylogenetic analyses of Lbx and Lbx-associated genes show that in extant, bony vertebrates only Lbx1- and Lbx2-type genes are maintained. Of these, some Lbx2 sequences evolved faster and were probably subject to neofunctionalisation, while Lbx1 genes may have retained more features of the ancestral Lbx gene. Genes at Lbx1 and former Lbx4 loci are more closely related, as are genes at Lbx2 and former Lbx3 loci. This suggests that during the second vertebrate genome duplication, Lbx1/4 and Lbx2/3 paralogons were generated from the duplicated Lbx loci created during the first duplication event.ConclusionOur study establishes for the first time the evolutionary history of Lbx genes in bony vertebrates, including the order of gene duplication events, gene loss and phylogenetic relationships. Moreover, we identified genetic hallmarks for each of the Lbx paralogons that can be used to trace Lbx genes as other vertebrate genomes become available. Significantly, we show that bony vertebrates only retained copies of Lbx1 and Lbx2 genes, with some Lbx2 genes being highly divergent. Thus, we have established a base on which the evolution of Lbx gene function in vertebrate development can be evaluated.
Highlights
Ladybird homeobox (Lbx)/ladybird genes originated as part of the metazoan cluster of Nk homeobox genes
Three Lbx genes were identified in the teleosts Takifugu rubripes, Tetraodon nigroviridis, Gasterosteus aculeatus, and two genes in Oryzias latipes (Medaka), while only one lbx/ladybird gene was retrieved for the invertebrate deuterostomes
Investigating the organisation of this former LBX3/TLX3 locus, we found that TLX3 is on one side linked to the gene that encodes for Ranbinding protein 17 (RANBP17, a member of the Exportin protein family), the gene encoding for the gamma-aminobutyric acid receptor (GABRP), a further KCNIP gene, KCNIP1, the Lymphocyte cytosolic protein gene LCP2, the Forkhead transcription factor gene FOXI1, the Dedicator of cytokinesis gene DOCK2, the coil-coil domain encoding CCDC99 gene, followed by SLIT3
Summary
Lbx/ladybird genes originated as part of the metazoan cluster of Nk homeobox genes. In all animals investigated so far, both the protostome genes and the vertebrate Lbx genes were found to play crucial roles in neural and muscle development. In the evolution of vertebrates, two rounds of whole genome duplication are thought to have occurred, during which 4 Lbx genes were generated. In all chordate relatives of vertebrates investigated so far, such as the urochordates Oikopleura dioica and Ciona intestinalis and the cephalochordate Branchiostoma floridae (amphioxus), only a single lbx gene has been found [3]. It is, safe to assume that prior to the two rounds of vertebrate genome duplication, only a single Lbx gene existed
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