Genome reduction by deletion of paralogs in the marine cyanobacterium Prochlorococcus

Several isolates of the marine cyanobacterial genus Prochlorococcus have smaller genome sizes than those of the closely related genus Synechococcus. In order to test whether loss of protein-coding genes has contributed to genome size reduction in Prochlorococcus, we reconstructed events of gene family evolution over a strongly supported phylogeny of 12 Prochlorococcus genomes and 9 Synechococcus genomes. Significantly, more events both of loss of paralogs within gene families and of loss of entire gene families occurred in Prochlorococcus than in Synechococcus. The number of nonancestral gene families in genomes of both genera was positively correlated with the extent of genomic islands (GIs), consistent with the hypothesis that horizontal gene transfer (HGT) is associated with GIs. However, even when only isolates with comparable extents of GIs were compared, significantly more events of gene family loss and of paralog loss were seen in Prochlorococcus than in Synechococcus, implying that HGT is not the primary reason for the genome size difference between the two genera.     

Ancient large-scale genome duplications: phylogenetic and linkage analyses shed light on chordate genome evolution

Paralogous genes from several families were found in four human chromosome regions (4p16, 5q33-35, 8p12-21, and 10q24-26), suggesting that their common ancestral region underwent several rounds of large- scale duplication. Searches in the EMBL databases, followed by phylogenetic analyses, showed that cognates (orthologs) of human duplicated genes can be found in other vertebrates, including bony fishes. In contrast, within each family, only one gene showing the same high degree of similarity with all the duplicated mammalian genes was found in nonvertebrates (echinoderms, insects, nematodes). This indicates that large-scale duplications occurred after the echinoderms/chordates split and before the bony vertebrate radiation. It has been suggested that two rounds of gene duplication occurred in the vertebrate lineage after the separation of Amphioxus and craniate (vertebrates + Myxini) ancestors. Before these duplications, the genes that have led to the families of paralogous genes in vertebrates must have been physically linked in the craniate ancestor. Linkage of some of these genes can be found in the Drosophila melanogaster and Caenorhabditis elegans genomes, suggesting that they were linked in the triploblast Metazoa ancestor.      

Genomic view of the evolution of the complement system

The recent accumulation of genomic information of many representative animals has made it possible to trace the evolution of the complement system based on the presence or absence of each complement gene in the analyzed genomes. Genome information from a few mammals, chicken, clawed frog, a few bony fish, sea squirt, fruit fly, nematoda and sea anemone indicate that bony fish and higher vertebrates share practically the same set of complement genes. This suggests that most of the gene duplications that played an essential role in establishing the mammalian complement system had occurred by the time of the teleost/mammalian divergence around 500 million years ago (MYA). Members of most complement gene families are also present in ascidians, although they do not show a one-to-one correspondence to their counterparts in higher vertebrates, indicating that the gene duplications of each gene family occurred independently in vertebrates and ascidians. The C3 and factor B genes, but probably not the other complement genes, are present in the genome of the cnidaria and some protostomes, indicating that the origin of the central part of the complement system was established more than 1,000 MYA.     

Are all fishes ancient polyploids?

Euteleost fishes seem to have more copies of many genes than their tetrapod relatives. Three different mechanisms could explain the origin of these 'extra' fish genes. The duplicates may have been produced during a fish-specific genome duplication event. A second explanation is an increased rate of independent gene duplications in fish. A third possibility is that after gene or genome duplication events in the common ancestor of fish and tetrapods, the latter lost more genes. These three hypotheses have been tested by phylogenetic tree reconstruction. Phylogenetic analyses of sequences from human, mouse, chicken, frog (Xenopus laevis), zebrafish (Danio rerio) and pufferfish (Takifugu rubripes) suggest that ray-finned fishes are likely to have undergone a whole genome duplication event between 200 and 450 million years ago. We also comment here on the evolutionary consequences of this ancient genome duplication.     

Isochore pattern and gene distribution in the chicken genome

We report here investigations on the isochore pattern and the distribution of genes in the chromosomes of chicken. In spite of large differences in genome size and karyotype, the compositional properties and the gene distribution of the chicken genome are very similar to those recently published for the human genome, which is a good representative of most mammalian genomes. In fact, this similarity, which extends to the relative amounts and, also, to a large extent at least, to the average base composition of isochore families, is most interesting in view of the very large distance of mammals and birds for a common ancestor, which goes back to 310–340 million years ago. This raises important questions about genome evolution in vertebrates.     

Evolutionary diversification of the avian fatty acid-binding proteins

Phylogenetic analysis of avian and other vertebrate fatty acid binding proteins (FABPs) supported the hypothesis that several gene duplications within this family occurred prior to the most recent common ancestor (MRCA) of tetrapods and bony fishes. The chicken genome encodes two liver-expressed FABPs: (1) L-FABP or FABP1; and (2) Lb-FABP. We propose that the latter be designated FABP10, because in our phylogenetic analysis it clustered with zebrafish FABP10. Bioinformatic analysis of across-tissue gene expression patterns in the chicken showed some congruence with phylogenetic relationships. On the basis of expression, chicken FABP genes seemed to form two major groups: (1) a cluster of genes many of which showed predominant expression in the digestive system (FABP1, FABP2, FABP6, FABP10, RBP1, and CRABP1); and (2) a cluster of genes most of which had predominant expression in tissues other than those of the digestive system, including muscle and the central nervous system (FABP3, FABP4, FABP5, FABP7, and PMP2). Since these clusters corresponded to major clusters in the phylogenetic tree as well, it seems a plausible hypothesis that the earliest duplication in the vertebrate FABP family led to the divergence of a gut-specialized gene from a gene expressed mainly in nervous and muscular systems. Data on gene expression in livers of two lines of chickens selected for high growth and low growth showed differences between FABP1 and FABP10 expressions in the liver, supporting the hypothesis of functional divergence between the two chicken liver-expressed FABPs related to food intake.     

Evolutionary diversification of the vertebrate transferrin multi-gene family

In a phylogenetic analysis of vertebrate transferrins (TFs), six major clades (subfamilies) were identified: (a) S, the mammalian serotransferrins; (b) ICA, the mammalian inhibitor of carbonic anhydrase (ICA) homologs; (c) L, the mammalian lactoferrins; (d) O, the ovotransferrins of birds and reptiles; (e) M, the melanotransferrins of bony fishes, amphibians, reptiles, birds, and mammals; and (f) M-like, a newly identified TF subfamily found in bony fishes, amphibians, reptiles, and birds. A phylogenetic tree based on the joint alignment of N-lobes and C-lobes supported the hypothesis that three separate events of internal duplication occurred in vertebrate TFs: (a) in the common ancestor of the M subfamily, (b) in the common ancestor of the M-like subfamily, and (c) in the common ancestor of other vertebrate TFs. The S, ICA, and L subfamilies were found only in placental mammals, and the phylogenetic analysis supported the hypothesis that these three subfamilies arose by gene duplication after the divergence of placental mammals from marsupials. The M-like subfamily was unusual in several respects, including the presence of a uniquely high proportion of clade-specific conserved residues, including distinctive but conserved residues in the sites homologous to those functioning in carbonate binding of human serotransferrin. The M-like family also showed an unusually high proportion of cationic residues in the positively charged region corresponding to human lactoferrampin, suggesting a distinctive role of this region in the M-like subfamily, perhaps in antimicrobial defense.     

Evolution of the lung surfactant proteins in birds and mammals

Phylogenetic analyses of the families of mammalian lung surfactant proteins (SP-A, SP-B, SP-C, and SP-D) supported the hypothesis that these proteins have diverged between birds and mammals as a result of lineage-specific gene duplications and deletions. Homologs of mammalian genes encoding SP-B, SP-C, and SP-D appear to have been deleted in chickens, whereas there was evidence of avian-specific duplications of the genes encoding SP-A and presaposin. Analysis of the genes closely linked to human SP-B, SP-C, and SP-D genes revealed that all three of these genes are closely linked to genes having orthologs on chicken chromosome 6 and also to genes lacking chicken orthologs. These relationships suggest that all of the lung surfactant protein genes, as well as certain related genes, may have been linked in the ancestor of humans and chickens. Further, they imply that the loss of surfactant protein genes in the avian lineages formed part of major genomic rearrangement events that involved the loss of other genes as well. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

The evolutionary relationships between the two bacteria Escherichia coli and Haemophilus influenzae and their putative last common ancestor

We have tried to approach the nature of the last common ancestor to Haemophilus influenzae and Escherichia coli and to determine how each bacterium could have diverged from this putative organism. The approach used was exhaustive analysis of the homologous proteins coded by genes present in these bacteria, using as criteria for sequence relatedness an alignment of at least 80 amino acid residues and a PAM distance (number of accepted point mutations per 100 residues separating two sequences) below 250. Evolutionarily significant similarities were found between 1,345 H. influenzae proteins (85% of the total genome) and 3,058 E. coli. proteins (75% of the total genome), many of them belonging to families of various sizes (from 666 doublets to 35 large groups of more than 10 members). Nearly all the genes found by this approach to be duplicated in both bacteria were already duplicated in their last common ancestor. This was deduced from (1) the comparison of the respective distributions of evolutionary distances between orthologs (genes separated only by speciation events) and paralogs (genes duplicated in the same genome) and (2) the analysis of the phylogenetic trees reconstructed for each family of paralogs containing at least two members belonging to each bacterium. The distributions of the different categories of homologs show a significant loss of paralogous genes in H. influenzae (reduction proportional to the genome size), of many sequences which are still present in one copy in E. coli, and of some entire gene families. Phylogenetic trees also confirmed this recent loss of paralogous genes in H. influenzae. Thus, the genome size of the last common ancestor of these two bacteria would have been close to that of present-day E. coli, and the evolution of H. influenzae toward a parasitic life led to an important decrease in its genome size by some mechanism of streamlining. During this recent evolution, the memory of the gene order present in the last common ancestor has been blurred, but a few short conserved chromosomal fragments can still be detected in present-day E. coli and H. influenzae.      

Ancient and recent duplications of the rainbow trout Wilms' tumor gene.

The Wilms' tumor suppressor (WT1) gene plays an important role in the development and functioning of the genitourinary system, and mutations in this gene are associated with nephroblastoma formation in humans. Rainbow trout (Oncorhynchus mykiss) is one of the rare animal models that readily form nephroblastomas, yet trout express three distinct WT1 genes, one of which is duplicated and inherited tetrasomically. Sequence analyses suggest an ancient gene duplication in the common ancestor of bony fishes resulted in the formation of two WT1 gene families, that conserve the splicing variations of tetrapod WT1, and a second duplication event occurred in the trout lineage. The WT1 genes of one family map to linkage groups 6 and 27 in the trout genome map. Reverse transcribed polymerase chain reaction (RT-PCR) expression analysis demonstrated little difference in W     

Conserved synteny between the Ciona genome and human paralogons identifies large duplication events in the molecular evolution of the insulin-relaxin gene family

The aims of the study were to outline the sequence of eventsthat gave rise to the vertebrate insulin-relaxin gene familyand the chromosomal regions in which they reside. We analyzedthe gene content surrounding the human insulin/relaxin geneswith respect to what family they belonged to and if the duplicationhistory of investigated families parallels the evolution ofthe insulin-relaxin family members. Markov Clustering and phylogeneticanalysis were used to determine family identity. More than 15%of the genes belonged to families that have paralogs in theregions, defining two sets of quadruplicate paralogy regions.Thereby, the localization of insulin/relaxin genes in humansis in accordance with those regions on human chromosomes 1,11, 12, 19q (insulin/insulin-like growth factors) and 1, 6p/15q,9/5, 19p (insulin-like factors/relaxins) were formed duringtwo genome duplications. We compared the human genome with thatof Ciona intestinalis, a species that split from the vertebratelineage before the two suggested genome duplications. Two insulin-likeorthologs were discovered in addition to the already describedCi-insulin gene. Conserved synteny between the Ciona regionshosting the insulin-like genes and the two sets of human paralogonsimplies their common origin. Linkage of the two human paralogons,as seen in human chromosome 1, as well as the two regions hostingthe Ciona insulin-like genes suggests that a segmental duplicationgave rise to the region prior to the genome doublings. Thus,preserved gene content provides support that genome duplication(s)in addition to segmental and single-gene duplications shapedthe genomes of extant vertebrates.     

Evolution of vertebrate rod and cone phototransduction genes

Vertebrate cones and rods in several cases use separate but related components for their signal transduction (opsins, G-proteins, ion channels, etc.). Some of these proteins are also used differentially in other cell types in the retina. Because cones, rods and other retinal cell types originated in early vertebrate evolution, it is of interest to see if their specific genes arose in the extensive gene duplications that took place in the ancestor of the jawed vertebrates (gnathostomes) by two tetraploidizations (genome doublings). The ancestor of teleost fishes subsequently underwent a third tetraploidization. Our previously reported analyses showed that several gene families in the vertebrate visual phototransduction cascade received new members in the basal tetraploidizations. We here expand these data with studies of additional gene families and vertebrate species. We conclude that no less than 10 of the 13 studied phototransduction gene families received additional members in the two basal vertebrate tetraploidizations. Also the remaining three families seem to have undergone duplications during the same time period but it is unclear if this happened as a result of the tetraploidizations. The implications of the many early vertebrate gene duplications for functional specialization of specific retinal cell types, particularly cones and rods, are discussed.     

A comprehensive expression analysis of all members of a gene family encoding cell-wall enzymes allowed us to predict cis-regulatory regions involved in cell-wall construction in specific organs of Arabidopsis.

The Arabidopsis thaliana genome sequencing project has revealed that multigene families, such as those generated by genome duplications, are more abundant among plant genomes than among animal genomes. To gain insight into the evolutionary implications of the multigene families in higher plants, we examined the XTH gene family, a group of genes encoding xyloglucan endotransglucosylase/hydrolase, which are responsible for cell-wall construction in plants. Expression analysis of all members (33 genes) of this family, using quantitative real-time RT-PCR, revealed that most members exhibit distinct expression profiles in terms of tissue specificity and responses to hormonal signals, with some members exhibiting similar expression patterns. By comparing the flanking sequences of individual genes, we identified four sets of large-segment duplications and two sets of solitary gene duplications. In each set of gene duplicates, long nucleotide sequences, ranging from one to two hundred base pairs, are conserved. Furthermore, gene duplicates exhibit similar organ-specific expression profiles. These facts allowed us to predict putative cis-regulatory regions, particularly those responsible for cell-wall construction, and hence for morphogenesis, that are specific for certain organs or tissues in plants.     

Comparative genomics and bioenergetics.

Bacterial and archaeal complete genome sequences have been obtained from a wide range of evolutionary lines, which allows some general conclusions about the phylogenetic distribution and evolution of bioenergetic pathways to be drawn. In particular, I searched in the complete genomes for key enzymes involved in aerobic and anaerobic respiratory pathways and in photosynthesis, and mapped them into an rRNA tree of sequenced species. The phylogenetic distribution of these enzymes is very irregular, and clearly shows the diverse strategies of energy conservation used by prokaryotes. In addition, a thorough phylogenetic analysis of other bioenergetic protein families of wide distribution reveals a complex evolutionary history for the respective genes. A parsimonious explanation for these complex phylogenetic patterns and for the irregular distribution of metabolic pathways is that the last common ancestor of Bacteria and Archaea contained several members of every gene family as a consequence of previous gene or genome duplications, while different patterns of gene loss occurred during the evolution of every gene family. This would imply that the last universal ancestor was a bioenergetically sophisticated organism. Finally, important steps that occurred during the evolution of energetic machineries, such as the early evolution of aerobic respiration and the acquisition of eukaryotic mitochondria from a proteobacterium ancestor, are supported by the analysis of the complete genome sequences.     

Early vertebrate chromosome duplications and the evolution of the neuropeptide Y receptor gene regions

Background  

One of the many gene families that expanded in early vertebrate evolution is the neuropeptide (NPY) receptor family of G-protein coupled receptors. Earlier work by our lab suggested that several of the NPY receptor genes found in extant vertebrates resulted from two genome duplications before the origin of jawed vertebrates (gnathostomes) and one additional genome duplication in the actinopterygian lineage, based on their location on chromosomes sharing several gene families. In this study we have investigated, in five vertebrate genomes, 45 gene families with members close to the NPY receptor genes in the compact genomes of the teleost fishes Tetraodon nigroviridis and Takifugu rubripes. These correspond to Homo sapiens chromosomes 4, 5, 8 and 10.     

Gene relocations within chloroplast genomes of Jasminum and Menodora (Oleaceae) are due to multiple, overlapping inversions

The chloroplast (cp) DNA sequence of Jasminum nudiflorum (Oleaceae-Jasmineae) is completed and compared with the large single-copy region sequences from 6 related species. The cp genomes of the tribe Jasmineae (Jasminum and Menodora) show several distinctive rearrangements, including inversions, gene duplications, insertions, inverted repeat expansions, and gene and intron losses. The ycf4-psaI region in Jasminum section Primulina was relocated as a result of 2 overlapping inversions of 21,169 and 18,414 bp. The 1st, larger inversion is shared by all members of the Jasmineae indicating that it occurred in the common ancestor of the tribe. Similar rearrangements were also identified in the cp genome of Menodora. In this case, 2 fragments including ycf4 and rps4-trnS-ycf3 genes were moved by 2 additional inversions of 14 and 59 kb that are unique to Menodora. Other rearrangements in the Oleaceae are confined to certain regions of the Jasminum and Menodora cp genomes, including the presence of highly repeated sequences and duplications of coding and noncoding sequences that are inserted into clpP and between rbcL and psaI. These insertions are correlated with the loss of 2 introns in clpP and a serial loss of segments of accD. The loss of the accD gene and clpP introns in both the monocot family Poaceae and the eudicot family Oleaceae are clearly independent evolutionary events. However, their genome organization is surprisingly similar despite the distant relationship of these 2 angiosperm families.     

OrthoParaMap: Distinguishing orthologs from paralogs by integrating comparative genome data and gene phylogenies

Background  

In eukaryotic genomes, most genes are members of gene families. When comparing genes from two species, therefore, most genes in one species will be homologous to multiple genes in the second. This often makes it difficult to distinguish orthologs (separated through speciation) from paralogs (separated by other types of gene duplication). Combining phylogenetic relationships and genomic position in both genomes helps to distinguish between these scenarios. This kind of comparison can also help to describe how gene families have evolved within a single genome that has undergone polyploidy or other large-scale duplications, as in the case of Arabidopsis thaliana – and probably most plant genomes.     

The genome sizes of megabats (Chiroptera: Pteropodidae) are remarkably constrained

It has long been recognized that bats and birds contain less DNA in their genomes than their non-flying relatives. It has been suggested that this relates to the high metabolic demands of powered flight, a notion that is supported by the fact that pterosaurs also appear to have exhibited small genomes. Given the long-standing interest in this question, it is surprising that almost no data have been presented regarding genome size diversity among megabats (family Pteropodidae). The present study provides genome size estimates for 43 species of megabats in an effort to fill this gap and to test the hypothesis that all bats, and not just microbats, possess small genomes. Intriguingly, megabats appear to be even more constrained in terms of genome size than the members of other bat families.     

Eukaryote genome duplication - where's the evidence?

Several eukaryotes, including maize, yeast and Xenopus, are degenerate polyploids formed by relatively recent whole-genome duplications. Ohno's conjecture that more ancient genome duplications occurred in an ancestor of vertebrates is probably at least partly true but the present shortage of gene sequence and map information from vertebrates makes it difficult to either prove or disprove this hypothesis. Candidate paralogous segments in mammalian genomes have been identified but the lack of statistical rigour means that many of the proposals in the literature are probably artefacts.