Identifying concerted evolution and gene conversion in mammalian gene pairs lasting over 100 million years

Background  

Concerted evolution occurs in multigene families and is characterized by stretches of homogeneity and higher sequence similarity between paralogues than between orthologues. Here we identify human gene pairs that have undergone concerted evolution, caused by ongoing gene conversion, since at least the human-mouse divergence. Our strategy involved the identification of duplicated genes with greater similarity within a species than between species. These genes were required to be present in multiple mammalian genomes, suggesting duplication early in mammalian divergence. To eliminate genes that have been conserved due to strong purifying selection, our analysis also required at least one intron to have retained high sequence similarity between paralogues.     

250 million years of bindin evolution

Bindin plays a central role in sperm-egg attachment and fusion in sea urchins (echinoids). Previous studies determined the DNA sequence of bindin in two orders of the class Echinoidea, representing 10% of all echinoid species. We report sequences of mature bindin from five additional genera, representing four new orders, including the distantly related sand dollars, heart urchins, and pencil urchins. The six orders in which bindin is now known include 70% of all echinoids, and indicate that bindin was present in the common ancestor of all extant sea urchins more than 250 million years ago. Over this span of evolutionary time there has been (1). remarkable conservation in the core region of bindin, particularly in a stretch of 29 amino acids that has not changed at all; (2). conservation of a motif of basic amino acids at the cleavage site between preprobindin and mature bindin; (3). more than a twofold change in length of mature bindin; and (4). emergence of high variation in the sequences outside the core, including the insertion of glycine-rich repeats in the bindins of some orders, but not others.     

Interhomologue sequence variation of alpha satellite DNA from human chromosome 17: Evidence for concerted evolution along haplotypic lineages

Alpha satellite DNA is a family of tandemly repeated DNA found at the centromeres of all primate chromosomes. Different human chromosomes 17 in the population are characterized by distinct alpha satellite haplotypes, distinguished by the presence of variant repeat forms that have precise monomeric deletions. Pairwise comparisons of sequence diversity between variant repeat units from each haplotype show that they are closely related in sequence. Direct sequencing of PCR-amplified alpha satellite reveals heterogeneous positions between the repeat units on a chromosome as two bands at the same position on a sequencing ladder. No variation was detected in the sequence and location of these heterogeneous positions between chromosomes 17 from the same haplotype, but distinct patterns of variation were detected between chromosomes from different haplotypes. Subsequent sequence analysis of individual repeats from each haplotype confirmed the presence of extensive haplotype-specific sequence variation. Phylogenetic inference yielded a tree that suggests these chromosome 17 repeat units evolve principally along haplotypic lineages. These studies allow insight into the relative rates and/or timing of genetic turnover processes that lead to the homogenization of tandem DNA families. Correspondence to: H.F. Willard     

Phylogenomics,molecular evolution,and estimated ages of lineages from the deep phylogeny of Poaceae

The deeply diverging subfamilies of grasses: Anomochlooideae, Pharoideae, and Puelioideae, today inhabit tropical forest floors as sparsely distributed depauperate lineages. The BEP/PACMAD grasses, which make up the majority of the family, are the result of a more recent radiation. Species in the deeply diverging subfamilies were here investigated to better understand molecular evolutionary processes and ages of divergence. Complete chloroplast genomes (plastomes) of Pharus latifolius L., P. lappulaceus Aubl., and Puelia olyriformis (Franch.) Clayton were determined. Four plastome loci from seven species of the deep subfamilies were also sequenced. Phylogenetic and mutation analyses and divergence estimations were conducted on all sequences together with homologous sequences from other Poaceae. Mutation analyses surveyed insertion/deletion mutations across the plastomes, clarified a trend in the molecular evolution of the rpoC2 locus, and indicated unique pseudogenizations in the plastomes of Pharus and Puelia. Phylogenetic analyses largely confirmed earlier multi-gene phylogenies. Phylogenomic and divergence analyses produced estimated origins of the crown nodes of Anomochlooideae at 65–104 Ma, Pharoideae at 44–71 Ma, and Puelioideae at 62–96 Ma. The upper ends of our estimated ranges are in general agreement with previous estimates. However, the lower ends of our ranges are considerably older than previous estimates, reflecting the influence of the less commonly used oldest fossil calibration point. The deeply diverging subfamilies exhibited the accumulation of numerous substitution and indel mutations consistent with a long evolutionary history that predated the radiation of the BEP/PACMAD grasses. We hypothesize that relatively rapid warming and drying in Africa at 55–56.5 Ma may have acted as selective forces stimulating adaptive radiations of grasses from the African tropical forests into diverse habitats.     

A genomic view of 500 million years of cnidarian evolution

Cnidarians (corals, anemones, jellyfish and hydras) are a diverse group of animals of interest to evolutionary biologists, ecologists and developmental biologists. With the publication of the genome sequences of Hydra and Nematostella, whose last common ancestor was the stem cnidarian, researchers are beginning to see the genomic underpinnings of cnidarian biology. Cnidarians are known for the remarkable plasticity of their morphology and life cycles. This plasticity is reflected in the Hydra and Nematostella genomes, which differ to an exceptional degree in size, base composition, transposable element content and gene conservation. It is now known what cnidarian genomes, given 500 million years, are capable of; as we discuss here, the next challenge is to understand how this genomic history has led to the striking diversity seen in this group.     

Eight million years of maintained heterozygosity in chromosome homologs of cercopithecine monkeys

Chromosoma - In the Cercopithecini ancestor two chromosomes, homologous to human chromosomes 20 and 21, fused to form the Cercopithecini specific 20/21 association. In some individuals from the...     

Species specificity in major urinary proteins by parallel evolution

Species-specific chemosignals, pheromones, regulate social behaviors such as aggression, mating, pup-suckling, territory establishment, and dominance. The identity of these cues remains mostly undetermined and few mammalian pheromones have been identified. Genetically-encoded pheromones are expected to exhibit several different mechanisms for coding 1) diversity, to enable the signaling of multiple behaviors, 2) dynamic regulation, to indicate age and dominance, and 3) species-specificity. Recently, the major urinary proteins (Mups) have been shown to function themselves as genetically-encoded pheromones to regulate species-specific behavior. Mups are multiple highly related proteins expressed in combinatorial patterns that differ between individuals, gender, and age; which are sufficient to fulfill the first two criteria. We have now characterized and fully annotated the mouse Mup gene content in detail. This has enabled us to further analyze the extent of Mup coding diversity and determine their potential to encode species-specific cues.Our results show that the mouse Mup gene cluster is composed of two subgroups: an older, more divergent class of genes and pseudogenes, and a second class with high sequence identity formed by recent sequential duplications of a single gene/pseudogene pair. Previous work suggests that truncated Mup pseudogenes may encode a family of functional hexapeptides with the potential for pheromone activity. Sequence comparison, however, reveals that they have limited coding potential. Similar analyses of nine other completed genomes find Mup gene expansions in divergent lineages, including those of rat, horse and grey mouse lemur, occurring independently from a single ancestral Mup present in other placental mammals. Our findings illustrate that increasing genomic complexity of the Mup gene family is not evolutionarily isolated, but is instead a recurring mechanism of generating coding diversity consistent with a species-specific function in mammals.     

Phylogenetics of Puya (Bromeliaceae): Placement, major lineages, and evolution of Chilean species

Puya (Bromeliaceae), a large genus of terrestrial bromeliads found throughout a range of elevations in the Andes and central Chile, is of great systematic, evolutionary, and biogeographical interest. This first molecular phylogenetic study of Puya and related bromeliads employs matK, trnS-trnG, rps16, and PHYC sequences. Chloroplast DNA, nuclear DNA, and combined DNA data all place Puya closest to subfamily Bromelioideae. Nuclear and combined data support Puya as monophyletic, and the two subgenera are nonmonophyletic. All data indicate that the Chilean species of Puya are early diverging within the genus, consistent with Chilean genera as the first-diverging members of subfamily Bromelioideae. Central Chile is identified as a key region for understanding the biogeographical history of Bromeliaceae, as is true with other South American plant groups. A complicated history involving early chloroplast capture and later secondary hybridization and/or introgression is seen in Chilean lineages. These events help explain the occurrence of sterile inflorescence tips, floral color and shape, and leaf indument. The ecological radiation of Puya appears coincident with the final, recent rise of the Andes and subsequent high-elevation habitat diversification. Additionally, geographical distribution, rather than moisture or elevational adaptations, correlates to species relationships. Evolution of CAM photosynthesis has occurred multiple times.     

Neurotrophic activities of trk receptors conserved over 600 million years of evolution

The trk family of receptor tyrosine kinases is crucial for neuronal survival in the vertebrate nervous system, however both C. elegans and Drosophila lack genes encoding trks or their ligands. The only invertebrate representative of this gene family identified to date is Ltrk from the mollusk Lymnaea. Did trophic functions of trk receptors originate early in evolution, or were they an innovation of the vertebrates? Here we show that the Ltrk gene conserves a similar exon/intron order as mammalian trk genes in the region encoding defined extracellular motifs, including one exon encoding a putative variant immunoglobulin-like domain. Chimeric receptors containing the intracellular and transmembrane domains of Ltrk undergo ligand-induced autophosphorylation followed by MAP kinase activation in transfected cells. The chimeras are internalized similarly to TrkA in PC12 cells, and their stimulation leads to differentiation and neurite extension. Knock-down of endogenous Ltrk expression compromises outgrowth and survival of Lymnaea neurons cultured in CNS-conditioned medium. Thus, Ltrk is required for neuronal survival, suggesting that trophic activities of the trk receptor family originated before the divergence of molluscan and vertebrate lineages approximately 600 million years ago.     

Journey through the past: 150 million years of plant genome evolution

The genome sequence of the plant model organism Arabidopsis thaliana was presented in December of the year 2000. Since then, the 125 Mb sequence has revealed many of its evolutionary secrets. Through comparative analyses with other plant genomes, we know that the genome of A. thaliana, or better that of its ancestors, has undergone at least three whole genome duplications during the last 120 or so million years. The first duplication seems to have occurred at the dawn of dicot evolution, while the later duplications probably occurred <70 million years ago (Ma). One of those younger genome-wide duplications might be linked to the K-T extinction. Following these duplication events, the ancestral A. thaliana genome was hugely rearranged and gene copies have been massively lost. During the last 10 million years of its evolution, almost half of its genome was lost due to hundreds of thousands of small deletions. Here, we reconstruct plant genome evolution from the early angiosperm ancestor to the current A. thaliana genome, covering about 150 million years of evolution characterized by gene and genome duplications, genome rearrangements and genome reduction.     

The genomic impact of 100 million years of social evolution in seven ant species

Ants (Hymenoptera, Formicidae) represent one of the most successful eusocial taxa in terms of both their geographic distribution and species number. The publication of seven ant genomes within the past year was a quantum leap for socio- and ant genomics. The diversity of social organization in ants makes them excellent model organisms to study the evolution of social systems. Comparing the ant genomes with those of the honeybee, a lineage that evolved eusociality independently from ants, and solitary insects suggests that there are significant differences in key aspects of genome organization between social and solitary insects, as well as among ant species. Altogether, these seven ant genomes open exciting new research avenues and opportunities for understanding the genetic basis and regulation of social species, and adaptive complex systems in general.     

Satellite-DNA diversification and the evolution of major lineages in Cardueae (Carduoideae Asteraceae)

In a previous work, we characterized the HinfI satellite DNA family in the subtribe Centaureinae (Cardueae) demonstrating that a “library” of eight HinfI subfamilies would exist in the common ancestor of all Centaureinae, which were differentially amplified in different lineages. Now, we extend our study by analyzing a total of 219 additional repeats from fifteen species belonging to Carlininae, Echinopsinae and Carduinae, and comparing them to those of Centaureinae. Most HinfI sequences belonged to the subfamily II, although a few sequences of other subfamilies were detected in some species. Additionally, a new subfamily characteristic of several Carduinae species was discovered. Although phylogenetic trees grouped sequences by subfamily affinity instead of species provenance, when comparing repeats of the same subfamily, the degree of divergence between any pair of sequences was related to the evolutionary distance between the species compared in most cases. Exceptions were in comparisons between sequences of some Centaureinae species, and between sequences of some Carduinae species and those of Centaureinae. Our results demonstrate that: (1) At least nine HinfI subfamilies would exist in the common ancestor of Cardueae, each one differentially amplified in different lineages; (2) After differential spreading, sequences of each subfamily evolved concertedly through molecular drive, resulting in the gradual divergence of repeats between different species; (3) The rate to which concerted evolution occurred was different between lineages according to the evolutionary history of each one.     

Intron distribution in Plantae: 500 million years of stasis during land plant evolution

Little is known about the evolution of the intron-exon organization in the more primitive groups of land plants, and the intron distribution among Plantae (glauco-, rhodo-, chloro- and streptophytes) has not been investigated so far. The present study is focused on some key species such as the liverwort Marchantia polymorpha, representing the most ancient lineage of land plants, and the streptophycean green alga Mesostigma viride, branching prior to charophycean green algae and terrestrial plants. The intron distribution of six genes for sugar phosphate metabolism was analyzed including four different glyceraldehyde-3-phosphate dehydrogenases (GAPDH), the sedoheptulose-1,7-bisphosphatase (SBP) and the glucose-6-phosphate isomerase (GPI). We established 15 new sequences including three cDNA and twelve genomic clones with up to 24 introns per gene, which were identified in the GPI of Marchantia. The intron patterns of all six genes are completely conserved among seed plants, lycopods, mosses and even liverworts. This intron stasis without any gain of novel introns seem to last for nearly 500 million years and may be characteristic for land plants in general. Some unique intron positions in Mesostigma document that a uniform distribution is no common trait of all streptophytes, but it may correlate with the transition to terrestrial habitats. However, the respective genes of chlorophycean green algae display largely different patterns, thus indicating at least one phase of massive intron rearrangement in the green lineage. We moreover included rhodophyte and glaucophyte reference sequences in our analyses and, even if the well documented monophyly of Plantae is not reflected by a uniform intron distribution, at least one GPI intron is strictly conserved for 1.5 billion years.     

HeT-A and TART, two Drosophila retrotransposons with a bona fide role in chromosome structure for more than 60 million years

Drosophila telomeres have been maintained by retrotransposition for at least 60 MY, which predates the separation of extant species of this genus. Studies of D. melanogaster, D. yakuba, and D. virilis show that, in Drosophila, telomeres are composed of two non-LTR retrotransposons, HeT-A and TART. Far from being static, HeT-A and TART evolve faster than Drosophila euchromatic genes. In spite of their high rate of sequence change, HeT-A and TART maintain their basic structures and unusual individual features. The maintenance of their separate identities suggests that HeT-A and TART cooperate either in the process of retrotransposition onto the chromosome end, or in the formation of telomere chromatin by transposed DNA copies. The telomeric retrotransposons and the Drosophila genome constitute an example of a robust symbiotic relationship between mobile elements and the genome.     

Meiotic segregation of a homeologous chromosome pair

During meiosis, the alignment of homologous chromosomes facilitates their subsequent migration away from one another to opposite spindle poles at anaphase I. Recombination is part of the mechanism by which chromosomes identify their homologous partners, and serves to link the homologs in a way that, in some organisms, has been shown to promote proper attachment to the meiotic spindle. We have built a diploid strain that contains a pair of homeologous chromosomes V': one is derived from Saccharomyces cerevisiae and one originates from S. carlsbergensis. Sequence analysis reveals that these chromosomes share 71% sequence identity. The homeologs experience high levels of meiotic double-stranded breaks. Despite their relatedness and their competence to initiate recombination, the meiotic segregation behavior of the homeologous chromosomes suggests that, in most meioses, they are partitioned by a meiotic segregation system that has been shown previously to partition non-exchange chromosomes and pairs with no homology. Though the homeologous chromosomes show a degree of meiotic segregation fidelity similar to that of other non-exchange pairs, our data provide evidence that their limited sequence homology may provide some bias in meiotic partner choice.     

Effectiveness of ph gene in inducing homoeologous chromosome pairing in agrotricum

Summary We observed pairing, when the ph gene was present, between wheat (Triticum aestivum L. em. Thell.) chromosome 4B, and an Agropyron intermedium (Host) Beauv. chromosome (Ai) carrying a gene resistant to wheat streak mosaic (WSM). In a monosomic addition polyhaploid [2n = 22 = 19' + 5B' (ph) + 4B' + Ai'], we recorded an average of 4.1 bivalents and 0.3 trivalents per cell. Induced homoeologous pairing was most effective when both 5B chromosomes carrying ph gene were present. Our data suggest that chromosome 4B of wheat and the Agropyron chromosome (Ai) carrying a gene for resistance to WSM are homoeologous and that it is possible to use either ph mutant or nullisomic 5B stock to induce genetic recombination between the two chromosomes.Contribution No. 1657-j, Kansas State Agric. Expt. Sta., Manhattan, KS. The research is partially supported by a grant from Kansas Wheat Commission     

Functional conservation of an insect odorant receptor gene across 250 million years of evolution

Pest insects have a profound negative impact on agriculture and human health. Significant global losses of crops, stored agricultural products, timber and livestock can be attributed to damage and destruction by insects . Blood-feeding insects such as mosquitoes, flies and ticks transmit many of humanity's most devastating infectious diseases. Insect-borne diseases account for more than one million annual fatalities, and insect-associated illnesses surpass 300 million annual reported cases . The medical and economic impact of these animals can be ascribed in part to the sensitivity and selectivity of their olfactory systems, essential for location of their preferred plant and animal hosts.