Dataset Information

Evolution of the Alx homeobox gene family: parallel retention and independent loss of the vertebrate Alx3 gene.

ABSTRACT: The Alx gene family is implicated in craniofacial development and comprises two to four homeobox genes in each vertebrate genome analyzed. Using phylogenetics and comparative genomics, we show that the common ancestor of jawed vertebrates had three Alx genes descendent from the two-round genome duplications (Alx1, Alx3, Alx4), compared with a single amphioxus gene. Later in evolution one of the paralogues, Alx3, was lost independently from at least three different vertebrate lineages, whereas Alx1 and Alx4 were consistently retained. Comparison of spatial gene expression patterns reveals that the three mouse genes have equivalent craniofacial expression to the two chick and frog genes, suggesting that redundancy compensated for gene loss. We suggest that multiple independent loss of one Alx gene was predisposed by extensive and persistent overlap in gene expression between Alx paralogues. Even so, it is unclear whether it was coincidence or evolutionary bias that resulted in the same Alx gene being lost on each occasion, rather than different members of the gene family.

SUBMITTER: McGonnell IM

PROVIDER: S-EPMC3166657 | biostudies-literature | 2011 Jul-Aug

REPOSITORIES: biostudies-literature

ACCESS DATA

Publications

Evolution of the Alx homeobox gene family: parallel retention and independent loss of the vertebrate Alx3 gene.

McGonnell Imelda M IM Graham Anthony A Richardson Joanna J Fish Jennifer L JL Depew Michael J MJ Dee Chris T CT Holland Peter W H PW Takahashi Tokiharu T

Evolution & development 20110701 4

The Alx gene family is implicated in craniofacial development and comprises two to four homeobox genes in each vertebrate genome analyzed. Using phylogenetics and comparative genomics, we show that the common ancestor of jawed vertebrates had three Alx genes descendent from the two-round genome duplications (Alx1, Alx3, Alx4), compared with a single amphioxus gene. Later in evolution one of the paralogues, Alx3, was lost independently from at least three different vertebrate lineages, whereas Al ...[more]

PMID: 21740507

Similar Datasets

Project description:BackgroundThe vertebrate tetraspanin family has many features which make it suitable for preserving the imprint of ancient sequence evolution and amenable for phylogenomic analysis. So we believe that an in-depth analysis of the tetraspanin evolution not only provides more complete understanding of tetraspanin biology, but offers new insights into the influence of the two rounds of whole genome duplication (2R-WGD) at the origin of vertebrates.ResultsA detailed phylogeny of vertebrate tetraspanins was constructed by using multiple lines of information, including sequence-based phylogenetics, key structural features, intron configuration and genomic synteny. In particular, a total of 38 modern tetraspanin ortholog lineages in bony vertebrates have been identified and subsequently classified into 17 ancestral lineages existing before 2R-WGD. Based on this phylogeny, we found that the ohnolog retention rate of tetraspanins after 2R-WGD was three times as the average (a rate similar to those of transcription factors and protein kinases). This high rate didn't increase the tetrapanin family size, but changed the family composition, possibly by displacing vertebrate-specific gene lineages with the lineages conserved across deuterostomes. We also found that the period from 2R-WGD to recent time is controlled by gene losses. Meanwhile, positive selection has been detected on 80% of the branches right after 2R-WGDs, which declines significantly on both magnitude and extensity on the following speciation branches. Notably, the loss of mammalian RDS2 is accompanied by strong positive selection on mammalian ROM1, possibly due to gene loss-induced compensatory evolution.ConclusionsFirst, different from transcription factors and kinases, high duplicate retention rate after 2R-WGD didn't increase the tetraspanin family size but just reshaped the family composition. Second, the evolution of tetraspanins right after 2R-WGD had been impacted by a massive wave of gene loss and positive selection on coding sequences. Third, the lingering effect of 2R-WGD on tetraspanin gene loss and positive selection might last for 300-400 million years.

Project description:BackgroundLIM homeobox (Lhx) transcription factors are unique to the animal lineage and have patterning roles during embryonic development in flies, nematodes and vertebrates, with a conserved role in specifying neuronal identity. Though genes of this family have been reported in a sponge and a cnidarian, the expression patterns and functions of the Lhx family during development in non-bilaterian phyla are not known.ResultsWe identified Lhx genes in two cnidarians and a placozoan and report the expression of Lhx genes during embryonic development in Nematostella and the demosponge Amphimedon. Members of the six major LIM homeobox subfamilies are represented in the genomes of the starlet sea anemone, Nematostella vectensis, and the placozoan Trichoplax adhaerens. The hydrozoan cnidarian, Hydra magnipapillata, has retained four of the six Lhx subfamilies, but apparently lost two others. Only three subfamilies are represented in the haplosclerid demosponge Amphimedon queenslandica. A tandem cluster of three Lhx genes of different subfamilies and a gene containing two LIM domains in the genome of T. adhaerens (an animal without any neurons) indicates that Lhx subfamilies were generated by tandem duplication. This tandem cluster in Trichoplax is likely a remnant of the original chromosomal context in which Lhx subfamilies first appeared. Three of the six Trichoplax Lhx genes are expressed in animals in laboratory culture, as are all Lhx genes in Hydra. Expression patterns of Nematostella Lhx genes correlate with neural territories in larval and juvenile polyp stages. In the aneural demosponge, A. queenslandica, the three Lhx genes are expressed widely during development, including in cells that are associated with the larval photosensory ring.ConclusionsThe Lhx family expanded and diversified early in animal evolution, with all six subfamilies already diverged prior to the cnidarian-placozoan-bilaterian last common ancestor. In Nematostella, Lhx gene expression is correlated with neural territories in larval and juvenile polyp stages. This pattern is consistent with a possible role in patterning the Nematostella nervous system. We propose a scenario in which Lhx genes play a homologous role in neural patterning across eumetazoans.

Dataset Information

Evolution of the Alx homeobox gene family: parallel retention and independent loss of the vertebrate Alx3 gene.

Publications

Evolution of the Alx homeobox gene family: parallel retention and independent loss of the vertebrate Alx3 gene.

Similar Datasets

OmicsDI is part of the ELIXIR infrastructure

Tweets