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The evolutionary diversification of LSF and Grainyhead transcription factors preceded the radiation of basal animal lineages.

ABSTRACT: BACKGROUND:The transcription factors of the LSF/Grainyhead (GRH) family are characterized by the possession of a distinctive DNA-binding domain that bears no clear relationship to other known DNA-binding domains, with the possible exception of the p53 core domain. In triploblastic animals, the LSF and GRH subfamilies have diverged extensively with respect to their biological roles, general expression patterns, and mechanism of DNA binding. For example, Grainyhead (GRH) homologs are expressed primarily in the epidermis, and they appear to play an ancient role in maintaining the epidermal barrier. By contrast, LSF homologs are more widely expressed, and they regulate general cellular functions such as cell cycle progression and survival in addition to cell-lineage specific gene expression. RESULTS:To illuminate the early evolution of this family and reconstruct the functional divergence of LSF and GRH, we compared homologs from 18 phylogenetically diverse taxa, including four basal animals (Nematostella vectensis, Vallicula multiformis, Trichoplax adhaerens, and Amphimedon queenslandica), a choanoflagellate (Monosiga brevicollis) and several fungi. Phylogenetic and bioinformatic analyses of these sequences indicate that (1) the LSF/GRH gene family originated prior to the animal-fungal divergence, and (2) the functional diversification of the LSF and GRH subfamilies occurred prior to the divergence between sponges and eumetazoans. Aspects of the domain architecture of LSF/GRH proteins are well conserved between fungi, choanoflagellates, and metazoans, though within the Metazoa, the LSF and GRH families are clearly distinct. We failed to identify a convincing LSF/GRH homolog in the sequenced genomes of the algae Volvox carteri and Chlamydomonas reinhardtii or the amoebozoan Dictyostelium purpureum. Interestingly, the ancestral GRH locus has become split into two separate loci in the sea anemone Nematostella, with one locus encoding a DNA binding domain and the other locus encoding the dimerization domain. CONCLUSIONS:In metazoans, LSF and GRH proteins play a number of roles that are essential to achieving and maintaining multicellularity. It is now clear that this protein family already existed in the unicellular ancestor of animals, choanoflagellates, and fungi. However, the diversification of distinct LSF and GRH subfamilies appears to be a metazoan invention. Given the conserved role of GRH in maintaining epithelial integrity in vertebrates, insects, and nematodes, it is noteworthy that the evolutionary origin of Grh appears roughly coincident with the evolutionary origin of the epithelium.

SUBMITTER: Traylor-Knowles N

PROVIDER: S-EPMC2873413 | biostudies-literature | 2010 Apr

REPOSITORIES: biostudies-literature

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The evolutionary diversification of LSF and Grainyhead transcription factors preceded the radiation of basal animal lineages.

Traylor-Knowles Nikki N Hansen Ulla U Dubuc Timothy Q TQ Martindale Mark Q MQ Kaufman Les L Finnerty John R JR

BMC evolutionary biology 20100418

<h4>Background</h4>The transcription factors of the LSF/Grainyhead (GRH) family are characterized by the possession of a distinctive DNA-binding domain that bears no clear relationship to other known DNA-binding domains, with the possible exception of the p53 core domain. In triploblastic animals, the LSF and GRH subfamilies have diverged extensively with respect to their biological roles, general expression patterns, and mechanism of DNA binding. For example, Grainyhead (GRH) homologs are expre ...[more]

PMID: 20398424

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Project description:BACKGROUND: Basic helix-loop-helix and homeodomain transcription factors have been shown to specify all different neuronal cell subtypes composing the vertebrate retina. The appearance of gene paralogs of such retina-specific transcription factors in lower vertebrates, with differently evolved function and/or conserved non-coding elements, might provide an important source for the generation of neuronal diversity within the vertebrate retinal architecture. In line with this hypothesis, we investigated the evolution of the homeobox Barhl family of transcription factors, barhl1 and barhl2, in the teleost and tetrapod lineages. In tetrapod barhl2, but not barhl1, is expressed in the retina and is important for amacrine cell specification. Zebrafish has three barhl paralogs: barhl1.1, barhl1.2 and barhl2, but their precise spatio-temporal retinal expression, as well as their function is yet unknown. RESULTS: Here we performed a meticulous expression pattern comparison of all known barhl fish paralogs and described a novel barhl paralog in medaka. Our detailed analysis of zebrafish barhl gene expression in wild type and mutant retinas revealed that only barhl1.2 and barhl2 are present in the retina. We also showed that these two paralogs are expressed in distinct neuronal lineages and are differently regulated by Atoh7, a key retinal-specific transcription factor. Finally, we found that the two retained medaka fish barhl paralogs, barhl1 and barhl2, are both expressed in the retina, in a pattern reminiscent of zebrafish barhl1.2 and barhl2 respectively. By performing phylogenetic and synteny analysis, we provide evidence that barhl retinal expression domain is an ancestral feature, probably lost in tetrapods due to functional redundancy. CONCLUSIONS: Functional differences among retained paralogs of key retina-specific transcription factors between teleosts and tetrapods might provide important clues for understanding their potential impact on the generation of retinal neuronal diversity. Intriguingly, within teleosts, retention of zebrafish barhl1.2 and its medaka ortholog barhl1 appears to correlate with the acquisition of distinct signalling mechanisms by the two genes within distinct retinal cell lineages. Our findings provide a starting point for the study of barhl gene evolution in relation to the generation of cell diversity in the vertebrate retina.

Project description:BackgroundDiet is a key component of a species ecological niche and plays critical roles in guiding the trajectories of evolutionary change. Previous studies suggest that dietary evolution can influence the rates and patterns of species diversification, with omnivorous (animal and plant, 'generalist') diets slowing down diversification compared to more restricted ('specialist') herbivorous and carnivorous diets. This hypothesis, here termed the "dietary macroevolutionary sink" hypothesis (DMS), predicts that transitions to omnivorous diets occur at higher rates than into any specialist diet, and omnivores are expected to have the lowest diversification rates, causing an evolutionary sink into a single type of diet. However, evidence for the DMS hypothesis remains conflicting. Here, we present the first test of the DMS hypothesis in a lineage of ectothermic tetrapods-the prolific Liolaemidae lizard radiation from South America.ResultsAncestral reconstructions suggest that the stem ancestor was probably insectivorous. The best supported trait model is a diet-dependent speciation rate, with independent extinction rates. Herbivory has the highest net diversification rate, omnivory ranks second, and insectivory has the lowest. The extinction rate is the same for all three diet types and is much lower than the speciation rates. The highest transition rate was from omnivory to insectivory, and the lowest transition rates were between insectivory and herbivory.ConclusionsOur findings challenge the core prediction of the DMS hypothesis that generalist diets represent an 'evolutionary sink'. Interestingly, liolaemid lizards have rapidly and successfully proliferated across some of the world's coldest climates (at high elevations and latitudes), where species have evolved mixed arthropod-plant (omnivore) or predominantly herbivore diets. This longstanding observation is consistent with the higher net diversification rates found in both herbivory and omnivory. Collectively, just like the evolution of viviparity has been regarded as a 'key adaptation' during the liolaemid radiation across cold climates, our findings suggest that transitions from insectivory to herbivory (bridged by omnivory) are likely to have played a role as an additional key adaptation underlying the exceptional diversification of these reptiles across extreme climates.

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The evolutionary diversification of LSF and Grainyhead transcription factors preceded the radiation of basal animal lineages.

Publications

The evolutionary diversification of LSF and Grainyhead transcription factors preceded the radiation of basal animal lineages.

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