Nme gene family evolutionary history reveals pre-metazoan origins and high conservation between humans and the sea anemone, Nematostella vectensis

Background

The Nme gene family is involved in multiple physiological and pathological processes such as cellular differentiation, development, metastatic dissemination, and cilia functions. Despite the known importance of Nme genes and their use as clinical markers of tumor aggressiveness, the associated cellular mechanisms remain poorly understood. Over the last 20 years, several non-vertebrate model species have been used to investigate Nme functions. However, the evolutionary history of the family remains poorly understood outside the vertebrate lineage. The aim of the study was thus to elucidate the evolutionary history of the Nme gene family in Metazoans.

Methodology/Principal Findings

Using a total of 21 eukaryote species including 14 metazoans, the evolutionary history of Nme genes was reconstructed in the metazoan lineage. We demonstrated that the complexity of the Nme gene family, initially thought to be restricted to chordates, was also shared by the metazoan ancestor. We also provide evidence suggesting that the complexity of the family is mainly a eukaryotic innovation, with the exception of Nme8 that is likely to be a choanoflagellate/metazoan innovation. Highly conserved gene structure, genomic linkage, and protein domains were identified among metazoans, some features being also conserved in eukaryotes. When considering the entire Nme family, the starlet sea anemone is the studied metazoan species exhibiting the most conserved gene and protein sequence features with humans. In addition, we were able to show that most of the proteins known to interact with human NME proteins were also found in starlet sea anemone.

Conclusion/Significance

Together, our observations further support the association of Nme genes with key cellular functions that have been conserved throughout metazoan evolution. Future investigations of evolutionarily conserved Nme gene functions using the starlet sea anemone could shed new light on a wide variety of key developmental and cellular processes.     

Evolutionary history of the vertebrate mitogen activated protein kinases family

Background

The mitogen activated protein kinases (MAPK) family pathway is implicated in diverse cellular processes and pathways essential to most organisms. Its evolution is conserved throughout the eukaryotic kingdoms. However, the detailed evolutionary history of the vertebrate MAPK family is largely unclear.

Methodology/Principal Findings

The MAPK family members were collected from literatures or by searching the genomes of several vertebrates and invertebrates with the known MAPK sequences as queries. We found that vertebrates had significantly more MAPK family members than invertebrates, and the vertebrate MAPK family originated from 3 progenitors, suggesting that a burst of gene duplication events had occurred after the divergence of vertebrates from invertebrates. Conservation of evolutionary synteny was observed in the vertebrate MAPK subfamilies 4, 6, 7, and 11 to 14. Based on synteny and phylogenetic relationships, MAPK12 appeared to have arisen from a tandem duplication of MAPK11 and the MAPK13-MAPK14 gene unit was from a segmental duplication of the MAPK11-MAPK12 gene unit. Adaptive evolution analyses reveal that purifying selection drove the evolution of MAPK family, implying strong functional constraints of MAPK genes. Intriguingly, however, intron losses were specifically observed in the MAPK4 and MAPK7 genes, but not in their flanking genes, during the evolution from teleosts to amphibians and mammals. The specific occurrence of intron losses in the MAPK4 and MAPK7 subfamilies might be associated with adaptive evolution of the vertebrates by enhancing the gene expression level of both MAPK genes.

Conclusions/Significance

These results provide valuable insight into the evolutionary history of the vertebrate MAPK family.     

Endopolyploidy in vertebrate liver: An evolutionary perspective

Hepatocyte nuclei in several species of vertebrates were examined, to establish the frequency of polyploidy and related parameters along evolutionary lines. Nuclei were compared in terms of volume, DNA content, ploidy ranges and internal organization. Several trends emerged. When present, heterochromatin occupied 20–25% of nuclear profile areas, irrespective of nuclear volume and ploidy; the volume of heterochromatin, however, increased in direct proportion to ploidy level. Regardless of internal organization, ploidy and species, a direct correlation emerged between the volumes of nuclei and their absolute DNA content. Results are discussed in terms of structural and genic DNA.     

Chitinase family GH18: evolutionary insights from the genomic history of a diverse protein family

Background  

Chitinases (EC.3.2.1.14) hydrolyze the β-1,4-linkages in chitin, an abundant N-acetyl-β-D-glucosamine polysaccharide that is a structural component of protective biological matrices such as insect exoskeletons and fungal cell walls. The glycoside hydrolase 18 (GH18) family of chitinases is an ancient gene family widely expressed in archea, prokaryotes and eukaryotes. Mammals are not known to synthesize chitin or metabolize it as a nutrient, yet the human genome encodes eight GH18 family members. Some GH18 proteins lack an essential catalytic glutamic acid and are likely to act as lectins rather than as enzymes. This study used comparative genomic analysis to address the evolutionary history of the GH18 multiprotein family, from early eukaryotes to mammals, in an effort to understand the forces that shaped the human genome content of chitinase related proteins.     

The evolutionary history of crustacean segmentation: a fossil-based perspective

The evolution of segmentation in Crustacea, that is, the formation of sclerotized and jointed body somites and arrangement of somites into tagmata, is viewed in light of historical traits and functional constraints. The set of Early to Late Cambrian 'Orsten' arthropods have informed our current views of crustacean evolution considerably. These three-dimensionally preserved fossils document ancient morphologies, as opposed to purely hypothetical models and, because of the unusual preservation of larval stages, provide us with unparalleled insight into the morphogenesis of body somites and their structural equipment. The variety of evolutionary levels represented in the 'Orsten' including lobopodians, tardigrades, and pentastomids also allows phylogenetic interpretations far beyond the Crustacea. The 'Orsten' evidence and data from representatives of the Lower Cambrian Chengjiang biota in southwestern China, including phylogenetically earlier forms, form the major source of our morphology-based review of structural and functional developments that led toward the Crustacea. The principal strategy of arthropods is the simultaneous development of head somites, as expressed in a basal "head larva," and a successive addition of postcephalic somites from a preterminal budding zone with progressive maturation of metameric structures. This can be recognized in the developmental patterns of extant and fossil representatives of several euarthropod taxa, particularly crustaceans, trilobites, and chelicerates (at least basally). The development of these taxa points to an early somite-poor and free-living hatching stage. Embryonic development to a late stage within an egg, as occurring in recent onychophorans and certain in-group euarthropods, is regarded as achieved several times convergently.     

Eph family functions from an evolutionary perspective

Eph receptor tyrosine kinases and ephrins have been identified in organisms ranging from sponges to flies and worms to chick, mice and humans, thus allowing their function to be approached also from an evolutionary perspective. The structural analysis of Eph/ephrin crystals is providing hints for the existence of Eph and ephrin folds in plants and suggests a mechanism for triggering bi-directional signalling.     

Soluble galactoside-binding vertebrate lectins: a protein family with common properties

1. Soluble galactoside-binding lectins could play a key role in vertebrates by specifical binding to complementary glycoconjugates. 2. Their expression and localization are developmentally regulated. 3. They constitute a large family of structurally related proteins which contain a series of conserved aminoacids. 4. Their functional role could vary from an organ to another, and the same lectin may probably mediate several biological activities.     

Cabbage family affairs: the evolutionary history of Brassicaceae

Life without the mustard family (Brassicaceae) would be a world without many crop species and the model organism Arabidopsis (Arabidopsis thaliana) that has revolutionized our knowledge in almost every field of modern plant biology. Despite this importance, research breakthroughs in understanding family-wide evolutionary patterns and processes within this flowering plant family were not achieved until the past few years. In this review, we examine recent outcomes from diverse botanical disciplines (taxonomy, systematics, genomics, paleobotany and other fields) to synthesize for the first time a holistic view on the evolutionary history of the mustard family.     

Strong evolutionary conservation of broadly expressed protein isoforms in the troponin I gene family and other vertebrate gene families

The sequences of the adenylate kinase gene (adk) and the RecA gene (recA) were determined from the same isolates ofNeisseria gonorrhoeae, N. meningitidis, N. lactamica, N. polysaccharea, N. cinerea, N. mucosa, N. pharyngis var.flava, N. flavescens, andN. animalis. The patterns of sequence divergence observed atadk andrecA were very different. Dendrograms constructed from therecA data using two different algorithms were statistically robust and were congruent with each other and with the relationships between the species previously proposed using other data. In contrast, the dendrograms derived from theadk data were noncongruent with each other, and with those from therecA data, and were statistically poorly supported. These results, along with the uniform distribution of pairwise sequence divergences between the species atadk, suggest there has been a history of interspecies recombination within theadk gene of the humanNeisseria species which has obscured the phylogenetic relationships between the species. This view was supported by Sawyer's runs test, and the Index of Association (I_A) between codons, which provided significant evidence for interspecies recombination between theadk genes from the humanNeisseria species, but no evidence of interspecies recombination between therecA sequences.     

Phylogenetic perspective on the relationships and evolutionary history of the Acipenseriformes

The Acipenseriformes, as one of the earliest extant vertebrates, plays an important role in the evolution of fishes and even the whole vertebrates. Here we collected and analyzed all complete mitochondrial genomes of Acipenseriformes species. Phylogenetic analyses demonstrated that the polytomous branch included Acipenseridae and Polyodontidae formed five clades. The Polyodontidae clade and the Scaphirhynchus clade both were monophyletic group, whereas the Acipenser species and the Huso species both were polyphyletic group. The Bayesian divergence times showed that the origin time for Acipenseriformes was at 318.0 Mya, which was similar to the some previous results of 312.1 Mya, 346.9 Mya and 389.7 Mya. The result was in good consistent with the paleontological data available and the split time of the Pacific and Atlantic Oceans from the Jurassic to the Cretaceous (Laurasia splits in North America and Eurasia). The dN/dS ratios showed the evolutionary rates gradually slow down in five major Acipenseriformes clades from the Clade A (the Pacific sturgeons species) to Clade C (the genus Scaphirhynchus), which was related to the process of geographical formation.     

Immunoglobulin CH gene family in hominoids and its evolutionary history.

The organization of the human immunoglobulin CH gene suggests that a gene duplication involving the C gamma-C gamma-C epsilon-C alpha region has occurred during evolution. We previously showed that both chimpanzee and gorilla have two 5'-C epsilon-C alpha-3', as in human, and that orangutan, gibbon, and Old World monkeys have one C epsilon gene and one, two, and one C alpha gene(s), respectively. In addition to these clustered CH genes, there is one processed C epsilon pseudogene in each species. The present study revealed that orangutan and crab-eating macaque (an Old World monkey) both have one 5'-C epsilon-C alpha-3' and that gibbon has two 5'-C epsilon-C alpha-3', one C epsilon gene of which is completely deleted. By Southern analysis, the number of C gamma genes in all the nonhuman hominoids was estimated to be four to five, as in human, in comparison with two for crab-eating macaque. The C mu and C delta genes were estimated to be present as single copies in both hominoids and crab-eating macaque. Furthermore, it was proved that there are two copies of the C epsilon 5'-flanking region in both the orangutan and the gibbon genomes. These results show that gene duplication including the C gamma-C gamma-C epsilon-C alpha genes occurred in the common ancestor of hominoids and that subsequent deletion of the C epsilon gene (in orangutan, including one of the C alpha genes) occurred independently in each hominoid species.     

The evolutionary history of the amylase multigene family in Drosophila pseudoobscura

In Drosophila pseudoobscura, the amylase (Amy) multigene family is contained within a series of inversions, or gene arrangements, on the third chromosome. The Standard (ST), Santa Cruz (SC), and Tree Line (TL) inversions are central to the phylogeny of arrangements, and have clusters of other arrangements derived from them. The gene arrangements belonging to each of these three clusters have a characteristic number of Amy genes, ranging from three in ST to two in SC to one in TL. This distribution pattern can reflect a history of either duplications or deletions, although the data available in the past did not permit a decision between these alternatives. We provide unambiguous evidence that three Amy genes were present before the divergence of the ST, SC, and TL arrangements. Thus, the current status of the Amy multigene family is the result of deletions in the TL and SC arrangements, which created three new pseudogenes: TL Amy2-psi, TL Amy3-psi, and SC Amy3- psi. Analysis of pseudogene sequences revealed that, in the SC and ST arrangements, pseudogene evolution has been retarded, most likely due to the homogenization effect of gene conversion. Finally, by determining the original copy number, we have reconstructed the evolutionary history of the Amy multigene family and linked it with the evolution of the central gene arrangements.      

Phylogenetic relationships and evolutionary history of the reef fish family Labridae

The family Labridae (including scarines and odacines) contains 82 genera and about 600 species of fishes that inhabit coastal and continental shelf waters in tropical and temperate oceans throughout the world. The Labridae (the wrasses) is the fifth largest fish family and second largest marine fish family, and is one of the most morphologically and ecologically diversified families of fishes in size, shape, and color. Labrid phylogeny is a long-standing problem in ichthyology that is part of the larger question of relationships within the suborder Labroidei. A phylogenetic analysis of labrids was conducted to investigate relationships among the six classical tribes of wrasses, the affinities of the wrasses to the parrotfishes (scarines), and the broad phylogenetic structure among labrid genera. Four gene fragments were sequenced from 98 fish species, including 84 labrid fishes and 14 outgroup taxa. Taxa were chosen from all major labrid clades and most major global ocean regions where labrid fishes exist, as well as cichlid, pomacentrid, and embiotocid outgroups. From the mitochondrial genome we sequenced portions of 12S rRNA (1000 bp) and 16S rRNA (585 bp), which were aligned by using a secondary structure model. From the nuclear genome, we sequenced part of the protein-coding genes RAG2 (846 bp) and Tmo4C4 (541 bp). Maximum likelihood, maximum parsimony, and Bayesian analyses on the resulting 2972 bp of DNA sequence produced similar topologies that confirm the monophyly of a family Labridae that includes the parrotfishes and butterfishes and strong support for many previously identified taxonomic subgroups. The tribe Hypsigenyini (hogfishes, tuskfishes) is the sister group to the remaining labrids and includes odacines and the chisel-tooth wrasse Pseudodax moluccanus, a species previously considered close to scarines. Cheilines and scarines are sister-groups, closely related to the temperate Labrini, and pseudocheilines and cheilines are split in all phylogenies. The razorfishes (novaculines) and temperate pseudolabrines form successive sister clades to the large crown group radiation of the Julidini. The cleaner wrasses (Labrichthyini) are nested within this radiation and several julidine genera do not appear to be monophyletic (e.g., Coris and Halichoeres). Invasion of temperate water by this predominantly tropical group has occurred multiple times and the reconstruction of biogeography assuming an Indo-Pacific ancestor results in five different lineages invading the Atlantic/Caribbean region. Functional novelties in the feeding apparatus have allowed labrid fishes to occupy nearly every feeding guild in reef environments, and trophic variation is a central axis of diversification in this family.     

Tachykinin and tachykinin receptor of an ascidian, Ciona intestinalis: evolutionary origin of the vertebrate tachykinin family

Tachykinins (TKs) are the most prevalent vertebrate brain/gut peptides. In this study, we originally identified authentic TKs and their receptor from a protochordate, Ciona intestinalis. The Ciona TK (Ci-TK) precursor, like mammalian gamma-preprotachykinin A (gamma-PPTA), encodes two TKs, Ci-TK-I and -II, including the -FXGLM-NH(2) vertebrate TK consensus. Mass spectrometry of the neural extract revealed the production of both Ci-TKs. Ci-TK-I contains several Substance P (SP)-typical amino acids, whereas a Thr is exceptionally located at position 4 from the C terminus of Ci-TK-II. The Ci-TK gene encodes both Ci-TKs in the same exon, indicating no alternative generation of Ci-TKs, unlike the PPTA gene. These results suggested that the alternative splicing of the PPTA gene was established during evolution of vertebrates. The only Ci-TK receptor, Ci-TK-R, was equivalently activated by Ci-TK-I, SP, and neurokinin A at physiological concentrations, whereas Ci-TK-II showed 100-fold less potent activity, indicating that the ligand selectivity of Ci-TK-R is distinct from those of vertebrate TK receptors. Ci-TK-I, like SP, also elicited the typical contraction on the guinea pig ileum. The Ci-TK gene was expressed in neurons of the brain ganglion, small cells in the intestine, and the zone 7 in the endostyle, which corresponds to the vertebrate thyroid gland. Furthermore, the Ci-TK-R mRNA was distributed in these three tissues plus the gonad. These results showed that Ci-TKs play major roles in sexual behavior and feeding in protochordates as brain/gut peptides and endocrine/paracrine molecules. Taken together, our data revealed the biochemical and structural origins of vertebrate TKs and their receptors.     

Recent evolutionary history of American Onchocerca volvulus, based on analysis of a tandemly repeated DNA sequence family

Polymerase chain reaction (PCR) products were characterized for a repeated sequence family (designated "O-150") of the human filarial parasite Onchocerca volvulus. In phylogenetic inferences, the O-150 sequences clustered into closely related groups, suggesting that concerted evolution maintains sequence homology in this family. Using a novel mathematical model based on a nested application of an analysis of variance, we demonstrated that African rainforest and savannah strain parasite populations are significantly different. In contrast, parasites collected in the New World are indistinguishable from African savannah strains of O. volvulus. This finding supports the hypothesis that onchocerciasis was recently introduced into the New World, possibly as a result of the slave trade.      

Phylogenomic analysis reveals dynamic evolutionary history of the Drosophila heterochromatin protein 1 (HP1) gene family

Heterochromatin is the gene-poor, satellite-rich eukaryotic genome compartment that supports many essential cellular processes. The functional diversity of proteins that bind and often epigenetically define heterochromatic DNA sequence reflects the diverse functions supported by this enigmatic genome compartment. Moreover, heterogeneous signatures of selection at chromosomal proteins often mirror the heterogeneity of evolutionary forces that act on heterochromatic DNA. To identify new such surrogates for dissecting heterochromatin function and evolution, we conducted a comprehensive phylogenomic analysis of the Heterochromatin Protein 1 gene family across 40 million years of Drosophila evolution. Our study expands this gene family from 5 genes to at least 26 genes, including several uncharacterized genes in Drosophila melanogaster. The 21 newly defined HP1s introduce unprecedented structural diversity, lineage-restriction, and germline-biased expression patterns into the HP1 family. We find little evidence of positive selection at these HP1 genes in both population genetic and molecular evolution analyses. Instead, we find that dynamic evolution occurs via prolific gene gains and losses. Despite this dynamic gene turnover, the number of HP1 genes is relatively constant across species. We propose that karyotype evolution drives at least some HP1 gene turnover. For example, the loss of the male germline-restricted HP1E in the obscura group coincides with one episode of dramatic karyotypic evolution, including the gain of a neo-Y in this lineage. This expanded compendium of ovary- and testis-restricted HP1 genes revealed by our study, together with correlated gain/loss dynamics and chromosome fission/fusion events, will guide functional analyses of novel roles supported by germline chromatin.