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PubMed1995

Molecular evolution of flower development: diversification of the plant MADS-box regulatory gene family.

Floral homeotic genes that control the specification of meristem and organ identity in developing flowers have been isolated from both Arabidopsis thaliana and Antirrhinum majus. Most of these genes belong to a large family of regulatory genes and possess a characteristic DNA binding domain known as the MADS-box. Members of this gene family display primarily floral-specific expression and are homologous to transcription factors found in several animal and fungal species. Molecular evolutionary analyses reveal that there are appreciable differences in the substitution rates between different domains of these plant MADS-box genes. Phylogenetic analyses also demonstrate that members of the plant MADS-box gene family are organized into several distinct gene groups: the AGAMOUS, APETALA3/PISTILLATA and APETALA1/AGL9 groups. The shared evolutionary history of members of a gene group appear to reflect the distinct functional roles these MADS-box genes play in flower development. Molecular evolutionary analyses also suggest that these different gene groups were established in a relatively short span of evolutionary time and that the various floral homeotic loci originated even before the appearance of the flowering plants.

Amino Acid Sequence↗
PubMed2003

Gene duplication and spectral diversification of cone visual pigments of zebrafish.

Zebrafish is becoming a powerful animal model for the study of vision but the genomic organization and variation of its visual opsins have not been fully characterized. We show here that zebrafish has two red (LWS-1 and LWS-2), four green (RH2-1, RH2-2, RH2-3, and RH2-4), and single blue (SWS2) and ultraviolet (SWS1) opsin genes in the genome, among which LWS-2, RH2-2, and RH2-3 are novel. SWS2, LWS-1, and LWS-2 are located in tandem and RH2-1, RH2-2, RH2-3, and RH2-4 form another tandem gene cluster. The peak absorption spectra (lambdamax) of the reconstituted photopigments from the opsin cDNAs differed markedly among them: 558 nm (LWS-1), 548 nm (LWS-2), 467 nm (RH2-1), 476 nm (RH2-2), 488 nm (RH2-3), 505 nm (RH2-4), 355 nm (SWS1), 416 nm (SWS2), and 501 nm (RH1, rod opsin). The quantitative RT-PCR revealed a considerable difference among the opsin genes in the expression level in the retina. The expression of the two red opsin genes and of three green opsin genes, RH2-1, RH2-3, and RH2-4, is significantly lower than that of RH2-2, SWS1, and SWS2. These findings must contribute to our comprehensive understanding of visual capabilities of zebrafish and the evolution of the fish visual system and should become a basis of further studies on expression and developmental regulation of the opsin genes.

Amino Acid Sequence↗
PubMed2003

Duplication and diversification in the APETALA1/FRUITFULL floral homeotic gene lineage: implications for the evolution of floral development.

Phylogenetic analyses of angiosperm MADS-box genes suggest that this gene family has undergone multiple duplication events followed by sequence divergence. To determine when such events have taken place and to understand the relationships of particular MADS-box gene lineages, we have identified APETALA1/FRUITFULL-like MADS-box genes from a variety of angiosperm species. Our phylogenetic analyses show two gene clades within the core eudicots, euAP1 (including Arabidopsis APETALA1 and Antirrhinum SQUAMOSA) and euFUL (including Arabidopsis FRUITFULL). Non-core eudicot species have only sequences similar to euFUL genes (FUL-like). The predicted protein products of euFUL and FUL-like genes share a conserved C-terminal motif. In contrast, predicted products of members of the euAP1 gene clade contain a different C terminus that includes an acidic transcription activation domain and a farnesylation signal. Sequence analyses indicate that the euAP1 amino acid motifs may have arisen via a translational frameshift from the euFUL/FUL-like motif. The euAP1 gene clade includes key regulators of floral development that have been implicated in the specification of perianth identity. However, the presence of euAP1 genes only in core eudicots suggests that there may have been changes in mechanisms of floral development that are correlated with the fixation of floral structure seen in this clade.

Amino Acid Sequence↗
PubMed2004

Patterns of gene duplication and functional evolution during the diversification of the AGAMOUS subfamily of MADS box genes in angiosperms.

Members of the AGAMOUS (AG) subfamily of MIKC-type MADS-box genes appear to control the development of reproductive organs in both gymnosperms and angiosperms. To understand the evolution of this subfamily in the flowering plants, we have identified 26 new AG-like genes from 15 diverse angiosperm species. Phylogenetic analyses of these genes within a large data set of AG-like sequences show that ancient gene duplications were critical in shaping the evolution of the subfamily. Before the radiation of extant angiosperms, one event produced the ovule-specific D lineage and the well-characterized C lineage, whose members typically promote stamen and carpel identity as well as floral meristem determinacy. Subsequent duplications in the C lineage resulted in independent instances of paralog subfunctionalization and maintained functional redundancy. Most notably, the functional homologs AG from Arabidopsis and PLENA (PLE) from Antirrhinum are shown to be representatives of separate paralogous lineages rather than simple genetic orthologs. The multiple subfunctionalization events that have occurred in this subfamily highlight the potential for gene duplication to lead to dissociation among genetic modules, thereby allowing an increase in morphological diversity.

Amino Acid Sequence↗
PubMed2003

Positive selection during the diversification of class I vomeronasal receptor-like (V1RL) genes, putative pheromone receptor genes, in human and primate evolution.

Vomeronasal receptors are the major receptors for pheromones in vertebrates, and five putative type 1 vomeronasal receptors (V1RL) have been identified in humans. The evolution of the V1RL1 gene in non-human primates, and patterns of selection on V1RL genes, were investigated. The presumed ortholog of V1RL1 was sequenced from 13 species of nonhuman primate, and in eight of these species V1RL1 was a pseudogene. Phylogenetic reconstructions reveal that V1RL1 pseudogene formation occurred independently in multiple primate lineages. Using maximum likelihood estimates of dN/dS ratios in PAML, we show that V1RL genes have evolved under neutral evolution in lineages in which they became a pseudogene. In contrast, among lineages in which V1RL genes contain an open reading frame, the majority of sites are under purifying selection and a minority are under significant positive selection. These results provide an interesting case where all three categories of selection can be teased apart in the same data set using maximum likelihood methods. The finding of positive selection on V1RL genes during primate evolution provides indirect support for the hypothesis that V1RL genes have a function in species-specific pheromone detection in primates.

Amino Acid Sequence↗
PubMed2003

Evolution of the TCP gene family in Asteridae: cladistic and network approaches to understanding regulatory gene family diversification and its impact on morphological evolution.

In the plant subclass Asteridae, bilaterally symmetrical flowers have evolved from a radially symmetrical ancestral phenotype on at least three independent occasions: in the Boraginaceae, Solanaceae, and Lamiales. Development of bilateral flower symmetry has been shown to be determined by the early-acting cycloidea (cyc) and dichotoma (dich) genes in Antirrhinum, a member of the Lamiales. cyc and dich belong to the TCP gene family of putative transcription factors. TCP gene sequences were isolated from 11 Asteridae taxa using an array of degenerate PCR primers. Closely related species exhibiting either ancestral actinomorphic or derived zygomorphic flowers were sampled for each independent origin of bilateral flower symmetry. Cladistic and network-based analyses were performed to establish viable hypotheses regarding the evolution of bilateral symmetry in Asteridae. For the TCP gene family, the use of cladistic phylogenetic analysis to identify orthologous genes is complicated by a paucity of alignable data, frequent gene duplication and extinction, and the possibility of reticulate evolution via intergenic recombination. These complicating factors can be generalized to many regulatory gene families. As an alternative to cladistic analysis, we propose the use of network analysis for the reconstruction of regulatory gene family phylogenetic and functional relationships. Results of analyses support the hypothesis that the origin of bilaterally symmetrical flowers in the Boraginaceae and Solanaceae did not require orthologs or functional analogs of cyc or dich. This suggests that the genetic mechanism that determines bilateral flower symmetry in these taxa is not homologous to that of the Lamiales. Results of analyses are consistent with the hypothesis that the evolution of bilateral floral symmetry in the Lamiales required the origin of a novel gene function subsequent to gene duplication.

Amino Acid Sequence↗
PubMed2003

Bayesian models of episodic evolution support a late precambrian explosive diversification of the Metazoa.

Multicellular animals, or Metazoa, appear in the fossil records between 575 and 509 million years ago (MYA). At odds with paleontological evidence, molecular estimates of basal metazoan divergences have been consistently older than 700 MYA. However, those date estimates were based on the molecular clock hypothesis, which is almost always violated. To relax this hypothesis, we have implemented a Bayesian approach to describe the change of evolutionary rate over time. Analysis of 22 genes from the nuclear and the mitochondrial genomes under the molecular clock assumption produced old date estimates, similar to those from previous studies. However, by allowing rates to vary in time and by taking small species-sampling fractions into account, we obtained much younger estimates, broadly consistent with the fossil records. In particular, the date of protostome-deuterostome divergence was on average 582 +/- 112 MYA. These results were found to be robust to specification of the model of rate change. The clock assumption thus had a dramatic effect on date estimation. However, our results appeared sensitive to the prior model of cladogenesis, although the oldest estimates (791 +/- 246 MYA) were obtained under a suboptimal model. Bayes posterior estimates of evolutionary rates indicated at least one major burst of molecular evolution at the end of the Precambrian when protostomes and deuterostomes diverged. We stress the importance of assumptions about rates on date estimation and suggest that the large discrepancies between the molecular and fossil dates of metazoan divergences might partly be due to biases in molecular date estimation.

Algorithms↗
PubMed2004

Early duplication and functional diversification of the opsin gene family in insects.

Recent analysis of the complete mosquito Anopheles gambiae genome has revealed a far higher number of opsin genes than for either the Drosophila melanogaster genome or any other known insect. In particular, the analysis revealed an extraordinary opsin gene content expansion, whereby half are long wavelength-sensitive (LW) opsin gene duplicates. We analyzed this genomic data in relationship to other known insect opsins to estimate the relative timing of the LW opsin gene duplications and to identify "missing" paralogs in extant species. The inferred branching patterns of the LW opsin gene family phylogeny indicate at least one early gene duplication within insects before the emergence of the orders Orthoptera, Mantodea, Hymenoptera, Lepidoptera, and Diptera. These data predict the existence of one more LW opsin gene than is currently known from most insects. We tested this prediction by using a degenerate PCR strategy to screen the hymenopteran genome for novel LW opsin genes. We isolated two LW opsin gene sequences from each of five bee species, Bombus impatiens, B. terrestris, Diadasia afflicta, D. rinconis, and Osmia rufa, including 1.1 to 1.2 kb from a known (LW Rh1) and 1 kb from a new opsin gene (LW Rh2). Phylogenetic analysis suggests that the novel hymenopteran gene is orthologous to A. gambiae GPRop7, a gene that is apparently missing from D. melanogaster. Relative rate tests show that LW Rh2 is evolving at a slower rate than LW Rh1 and, therefore, may be a useful marker for higher-level hymenopteran systematics. Site-specific rate tests indicate the presence of several amino acid sites between LW Rh1 and LW Rh2 that have undergone shifts in selective constraints after duplication. These sites and others are discussed in relationship to putative structural and functional differences between the two genes.

Amino Acid Sequence↗
PubMed2004

Adaptive evolution drives the diversification of zinc-finger binding domains.

The human genome is estimated to contain 700 zinc-finger genes, which perform many key functions, including regulating transcription. The dramatic increase in the number of these genes as we move from yeast to C. elegans to Drosophila and to humans, as well as the clustered organization of these genes in humans, suggests that gene duplication has played an important role in expanding this family of genes. Using likelihood methods developed by Yang and parsimony methods introduced by Suzuki and Gojobori, we have investigated four clusters of zinc-finger genes on human chromosome 19 and found evidence that positive selection was involved in diversifying the family of zinc-finger binding motifs.

Adaptation, Biological↗
PubMed2005

Evolution of the trnF(GAA) gene in Arabidopsis relatives and the brassicaceae family: monophyletic origin and subsequent diversification of a plastidic pseudogene.

Recently, we used the 5'-trnL(UAA)-trnF(GAA) region of the chloroplast DNA for phylogeographic reconstructions and phylogenetic analysis among the genera Arabidopsis, Boechera, Rorippa, Nasturtium, and Cardamine. Despite the fact that extensive gene duplications are rare among the chloroplast genome of higher plants, within these taxa the anticodon domain of the trnF(GAA) gene exhibit extensive gene duplications with one to eight tandemly repeated copies in close 5' proximity of the functional gene. Interestingly, even in Arabidopsis thaliana we found six putative pseudogenic copies of the functional trnF gene within the 5'-intergenic trnL-trnF spacer. A reexamination of trnL(UAA)-trnF(GAA) regions from numerous published phylogenetic studies among halimolobine, cardaminoid, and other cruciferous taxa revealed not only extensive trnF gene duplications but also favor the hypothesis about a single origin of trnF pseudogene formation during evolution of the Brassicaceae family 16-21 MYA. Conserved sequence motifs from this tandemly repeated region are codistributed nonrandomly throughout the plastome, and we found some similarities with a DNA sequence duplication in the rps7 gene and its adjacent spacer. Our results demonstrate the potential evolutionary dynamics of a plastidic region generally regarded as highly conserved and probably cotranscribed and, as shown here for several genera among cruciferous plants, greatly characterized by parallel gains and losses of duplicated trnF copies.

Arabidopsis↗
PubMed2005

Evolutionary diversification of DNA methyltransferases in eukaryotic genomes.

In eukaryotes, C5-cytosine methylation is a common mechanism associated with a variety of functions such as gene regulation or control of genomic stability. Different subfamilies of eukaryotic methyltransferases (MTases) have been identified, mainly in metazoa, plants, and fungi. In this paper, we used hidden Markov models to detect MTases in completed or almost completed eukaryotic genomes, including different species of Protozoa. A phylogenetic analysis of MTases enabled us to define six subfamilies of MTases, including two new subfamilies. The dnmt1 subfamily that includes all the known MTases with a maintenance activity seems to be absent in the Protozoa. The dnmt2 subfamily seems to be the most widespread, being present even in the nonmethylated Dictyostelium discoideum. We also found two dnmt2 members in the bacterial genus Geobacter, suggesting that horizontal transfers of MTases occurred between eukaryotes and prokaryotes. Even if the direction of transfer cannot be determined, this relationship might be useful for understanding the function of this enigmatic subfamily of MTases. Globally, our analysis reveals a great diversity of MTases in eukaryotes, suggesting the existence of different methylation systems. Our results also suggest acquisitions and losses of different MTases in every eukaryotic lineage studied and that some eukaryotes appear to be devoid of methylation.

DNA Modification Methylases↗
PubMed2006

Diversification and specialization of HIV protease function during in vitro evolution.

Our goal is to understand how enzymes adapt to utilize novel substrates. We and others have shown that directed evolution tends to generate enzyme variants with broadened substrate specificity. Broad-specificity enzymes are generally deleterious to living cells, so this observed trend might be an artifact of the most commonly employed high throughput screens. Here, we demonstrate a more natural and effective screening strategy for directed evolution. The gene encoding model enzyme HIV protease was randomly mutated, and the resulting library was expressed in Escherichia coli cells to eliminate cytotoxic broad-specificity variants. The surviving variants were screened for clones with activity against a reporter enzyme. The wild-type human immunodeficiency virus type I protease (HIV PR) is cytotoxic and exhibits no detectable activity in reactions with beta-galactosidase (BGAL). In contrast, the selected variants were nontoxic and exhibited greater activity and specificity against BGAL than did the wild-type HIV PR in reactions with any substrate. A single round of whole gene random mutagenesis and conventional high-throughput screening does not usually effect complete inversions of substrate specificity. This suggests that a combination of positive and purifying selection engenders more rapid adaptation than positive selection alone.

Adaptation, Biological↗
PubMed2006

Transposon-mediated expansion and diversification of a family of ULP-like genes.

Transposons comprise a major component of eukaryotic genomes, yet it remains controversial whether they are merely genetic parasites or instead significant contributors to organismal function and evolution. In plants, thousands of DNA transposons were recently shown to contain duplicated cellular gene fragments, a process termed transduplication. Although transduplication is a potentially rich source of novel coding sequences, virtually all appear to be pseudogenes in rice. Here we report the results of a genome-wide survey of transduplication in Mutator-like elements (MULEs) in Arabidopsis thaliana, which shows that the phenomenon is generally similar to rice transduplication, with one important exception: KAONASHI (KI). A family of more than 97 potentially functional genes and apparent pseudogenes, evidently derived at least 15 MYA from a cellular small ubiquitin-like modifier-specific protease gene, KI is predominantly located in potentially autonomous non-terminal inverted repeat MULEs and has evolved under purifying selection to maintain a conserved peptidase domain. Similar to the associated transposase gene but unlike cellular genes, KI is targeted by small RNAs and silenced in most tissues but has elevated expression in pollen. In an Arabidopsis double mutant deficient in histone and DNA methylation with elevated KI expression compared to wild type, at least one KI-MULE is mobile. The existence of KI demonstrates that transduplicated genes can retain protein-coding capacity and evolve novel functions. However, in this case, our evidence suggests that the function of KI may be selfish rather than cellular.

Amino Acid Sequence↗
PubMed1992

Structural organization and diversification of Y-linked sequences comprising Su(Ste) genes in Drosophila melanogaster.

Expression of the X-linked repeated Stellate (Ste) genes, which code for a protein with 38% similarity to the beta-subunit of casein kinase II, is suppressed by the Su(Ste) locus on the Y chromosome. The structure and evolution of the Y-linked repeats in the region of the Su(Ste) locus were studied. The 2800 bp repeats consist of three main elements: the region of homology to the Ste genes, an adjacent AT-rich, Y-specific segment, and mobile element 1360 inserted in the Ste sequence. Amplification of repeats was followed by point mutations, deletions, and insertions of mobile elements. DNA sequencing shows that these repeats may be considered as Ste pseudogenes or as damaged variants of a putative gene(s) encoding a protein quite different from the Ste protein as a result of an alternative splicing pattern. A comparison of 5 variants of the Y-Su(Ste) repeats shows a number of recombination events between amplified and diverged sequences that could be due to either multiple unequal mitotic sister-chromatid exchanges or to gene conversion. It is a first demonstration on a molecular level of these processes occurring in heterochromatic non-rDNA tandemly organized sequences in an eukaryotic genome.

Animals↗
PubMed2000

Evolutionary origin, diversification and specialization of eukaryotic MutS homolog mismatch repair proteins.

Most eubacteria, and all eukaryotes examined thus far, encode homologs of the DNA mismatch repair protein MutS. Although eubacteria encode only one or two MutS-like proteins, eukaryotes encode at least six distinct MutS homolog (MSH) proteins, corresponding to conserved (orthologous) gene families. This suggests evolution of individual gene family lines of descent by several duplication/specialization events. Using quantitative phylogenetic analyses (RASA, or relative apparent synapomorphy analysis), we demonstrate that comparison of complete MutS protein sequences, rather than highly conserved C-terminal domains only, maximizes information about evolutionary relationships. We identify a novel, highly conserved middle domain, as well as clearly delineate an N-terminal domain, previously implicated in mismatch recognition, that shows family-specific patterns of aromatic and charged amino acids. Our final analysis, in contrast to previous analyses of MutS-like sequences, yields a stable phylogenetic tree consistent with the known biochemical functions of MutS/MSH proteins, that now assigns all known eukaryotic MSH proteins to a monophyletic group, whose branches correspond to the respective specialized gene families. The rooted phylogenetic tree suggests their derivation from a mitochondrial MSH1-like protein, itself the descendent of the MutS of a symbiont in a primitive eukaryotic precursor.

Adenosine Triphosphatases↗
PubMed2001

Functional diversification of lepidopteran opsins following gene duplication.

A comparative approach was taken for identifying amino acid substitutions that may be under positive Darwinian selection and are correlated with spectral shifts among orthologous and paralogous lepidopteran long wavelength-sensitive (LW) opsins. Four novel LW opsin fragments were isolated, cloned, and sequenced from eye-specific cDNAs from two butterflies, Vanessa cardui (Nymphalidae) and Precis coenia (Nymphalidae), and two moths, Spodoptera exigua (Noctuidae) and Galleria mellonella (Pyralidae). These opsins were sampled because they encode visual pigments having a naturally occurring range of lambda(max) values (510-530 nm), which in combination with previously characterized lepidopteran opsins, provide a complete range of known spectral sensitivities (510-575 nm) among lepidopteran LW opsins. Two recent opsin gene duplication events were found within the papilionid but not within the nymphalid butterfly families through neighbor-joining, maximum parsimony, and maximum likelihood phylogenetic analyses of 13 lepidopteran opsin sequences. An elevated rate of evolution was detected in the red-shifted Papilio Rh3 branch following gene duplication, because of an increase in the amino acid substitution rate in the transmembrane domain of the protein, a region that forms the chromophore-binding pocket of the visual pigment. A maximum likelihood approach was used to estimate omega, the ratio of nonsynonymous to synonymous substitutions per site. Branch-specific tests of selection (free-ratio) identified one branch with omega = 2.1044, but the small number of substitutions involved was not significantly different from the expected number of changes under the neutral expectation of omega = 1. Ancestral sequences were reconstructed with a high degree of certainty from these data. Reconstructed ancestral sequences revealed several instances of convergence to the same amino acid between butterfly and vertebrate cone pigments, and between independent branches of the butterfly opsin tree that are correlated with spectral shifts.

Amino Acid Sequence↗
PubMed2001

Recurrent amplifications and deletions of satellite DNA accompanied chromosomal diversification in South American tuco-tucos (genus Ctenomys, Rodentia: Octodontidae): a phylogenetic approach.

We investigated the relationship between satellite copy number and chromosomal evolution in tuco-tucos (genus Ctenomys), a karyotypically diverse clade of rodents. To explore phylogenetic relationships among 23 species and 5 undescribed forms, we sequenced the complete mitochondrial cytochrome b genes of 27 specimens and incorporated 27 previously published sequences. We then used quantitative dot-blot techniques to assess changes in the copy number of the major Ctenomys satellite DNA (satDNA), named RPCS. Our analysis of the relationship between variation in copy number of RPCS and chromosomal changes employed a maximum-likelihood approach to infer the copy number of the satellite RPCS in the ancestors of each clade. We found that amplifications and deletions of RPCS were associated with extensive chromosomal rearrangements even among closely related species. In contrast, RPCS copy number stability was observed within clades characterized by chromosomal stability. This example reinforces the suspected role of amplification, deletion, and intragenomic movement of satDNA in promoting extensive chromosomal evolution.

Animals↗