Most cited article - PubMed ID 28035749
Genome Compositional Organization in Gars Shows More Similarities to Mammals than to Other Ray-Finned Fish
Fishes of the genus Carassius are useful experimental vertebrate models for the study of evolutionary biology and cytogenetics. Carassius demonstrates diverse biological characteristics, such as variation in ploidy levels and chromosome numbers, and presence of microchromosomes. Those Carassius polyploids with ≥150 chromosomes have microchromosomes, but the origin of microchromosomes, especially in European populations, is unknown. We used cytogenetics to study evolution of tandem repeats (U1 and U2 small nuclear DNAs and H3 histone) and microchromosomes in Carassius from the Czech Republic. We tested the hypotheses whether the number of tandem repeats was affected by polyploidization or divergence between species and what mechanism drives evolution of microchromosomes. Tandem repeats were found in tetraploid and hexaploid Carassius gibelio, and tetraploid Carassius auratus and Carassius carassius in conserved numbers, with the exception of U1 small nuclear DNA in C. auratus. This conservation indicates reduction and/or loss in the number of copies per locus in hexaploids and may have occurred by divergence rather than polyploidization. To study the evolution of microchromosomes, we used the whole microchromosome painting probe from hexaploid C. gibelio and hybridized it to tetraploid and hexaploid C. gibelio, and tetraploid C. auratus and C. carassius. Our results revealed variation in the number of microchromosomes in hexaploids and indicated that the evolution of the Carassius karyotype is governed by macrochromosome fissions followed by segmental duplication in pericentromeric areas. These are potential mechanisms responsible for the presence of microchromosomes in Carassius hexaploids. Differential efficacy of one or both of these mechanisms in different tetraploids could ensure variability in chromosome number in polyploids in general.
- Keywords
- FISH, U1 and U2 snDNAs, chromosome painting, histone H3, polyploidy, teleost fish,
- MeSH
- Cyprinidae * MeSH
- Cytogenetic Analysis MeSH
- Polyploidy MeSH
- Segmental Duplications, Genomic * MeSH
- Tandem Repeat Sequences MeSH
- Tetraploidy MeSH
- Animals MeSH
- Check Tag
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
Fish speciation was accompanied by changes in the urogenital system anatomy. In evolutionarily modern Teleostei, male reproductive tracts are fully separated from the excretory system, while in evolutionarily ancient Chondrostei and Holostei, the excretory and reproductive tracts are not separated. Sturgeon post-testicular sperm maturation (PTSM) occurring as a result of sperm/urine mixing is phenomenologically well described, while, in holosteans, functional intimacy of seminal ducts with kidney ducts and the existence of PTSM still need to be addressed. In Lepisosteus platostomus (Holostei), sperm samples were collected from testes (TS), efferent ducts (EDS), and Wolffian ducts (WDS). While WDS was motile, no motility was found in TS and EDS. The existence of PTSM was checked by in vitro PTSM procedure. After TS and EDS incubation in seminal fluid from WDS, no more than 5% motile spermatozoa were observed in TS, whereas in EDS the motility percentage was up to 75%. Experimental dyeing of urogenital ducts in gars and sturgeons revealed some differences in the interconnection between sperm ducts and kidneys. It is concluded that post-testicular sperm maturation occurs in gars and suggests that infraclass Holostei occupies an intermediate evolutionary position between Teleostei and Chondrostei in the anatomical arrangement of the urogenital system.
- MeSH
- Sperm Motility MeSH
- Genitalia, Male MeSH
- Fishes anatomy & histology MeSH
- Semen MeSH
- Spermatozoa MeSH
- Testis * MeSH
- Sperm Maturation * MeSH
- Animals MeSH
- Check Tag
- Male MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
The organization of the genome nucleotide (AT/GC) composition in vertebrates remains poorly understood despite the numerous genome assemblies available. Particularly, the origin of the AT/GC heterogeneity in amniotes, in comparison to the homogeneity in anamniotes, is controversial. Recently, several exceptions to this dichotomy were confirmed in an ancient fish lineage with mammalian AT/GC heterogeneity. Hence, our current knowledge necessitates a reevaluation considering this fact and utilizing newly available data and tools. We analyzed fish genomes in silico with as low user input as possible to compare previous approaches to assessing genome composition. Our results revealed a disparity between previously used plots of GC% and histograms representing the authentic distribution of GC% values in genomes. Previous plots heavily reduced the range of GC% values in fish to comply with the alleged AT/GC homogeneity and AT-richness of their genomes. We illustrate how the selected sequence size influences the clustering of GC% values. Previous approaches that disregarded chromosome and genome sizes, which are about three times smaller in fish than in mammals, distorted their results and contributed to the persisting confusion about fish genome composition. Chromosome size and their transposons may drive the AT/GC heterogeneity apparent on mammalian chromosomes, whereas far less in fishes.
- Keywords
- AT/GC genome composition, GC-content evolution transposons, natural breaks,
- MeSH
- Genome Size MeSH
- Isochores * genetics MeSH
- Fishes * genetics MeSH
- Chromosomes, Mammalian MeSH
- Mammals MeSH
- Cluster Analysis MeSH
- Animals MeSH
- Check Tag
- Animals MeSH
- Publication type
- Journal Article MeSH
- Names of Substances
- Isochores * MeSH
Cytogenetic and compositional studies considered fish genomes rather poor in guanine-cytosine content (GC%) because of a putative "sharp increase in genic GC% during the evolution of higher vertebrates". However, the available genomic data have not been exploited to confirm this viewpoint. In contrast, further misunderstandings in GC%, mostly of fish genomes, originated from a misapprehension of the current flood of data. Utilizing public databases, we calculated the GC% in animal genomes of three different, technically well-established fractions: DNA (entire genome), cDNA (complementary DNA), and cds (exons). Our results across chordates help set borders of GC% values that are still incorrect in literature and show: (i) fish in their immense diversity possess comparably GC-rich (or even GC-richer) genomes as higher vertebrates, and fish exons are GC-enriched among vertebrates; (ii) animal genomes generally show a GC-enrichment from the DNA, over cDNA, to the cds level (i.e., not only the higher vertebrates); (iii) fish and invertebrates show a broad(er) inter-quartile range in GC%, while avian and mammalian genomes are more constrained in their GC%. These results indicate no sharp increase in the GC% of genes during the transition to higher vertebrates, as stated and numerously repeated before. We present our results in 2D and 3D space to explore the compositional genome landscape and prepared an online platform to explore the AT/GC compositional genome evolution.
- Keywords
- AT/GC evolution, GC content, GC landscape pipeline, compositional cytogenomics, genome evolution,
- MeSH
- DNA MeSH
- Genomics MeSH
- DNA, Complementary MeSH
- Evolution, Molecular MeSH
- Vertebrates * genetics MeSH
- Fishes * genetics MeSH
- Mammals genetics MeSH
- Animals MeSH
- Check Tag
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- DNA MeSH
- DNA, Complementary MeSH
Our novel Python-based tool EVANGELIST allows the visualization of GC and repeats percentages along chromosomes in sequenced genomes and has enabled us to perform quantitative large-scale analyses on the chromosome level in fish and other vertebrates. This is a different approach from the prevailing analyses, i.e., analyses of GC% in the coding sequences that make up not more than 2% in human. We identified GC content (GC%) elevations in microchromosomes in ancient fish lineages similar to avian microchromosomes and a large variability in the relationship between the chromosome size and their GC% across fish lineages. This raises the question as to what extent does the chromosome size drive GC% as posited by the currently accepted explanation based on the recombination rate. We ascribe the differences found across fishes to varying GC% of repetitive sequences. Generally, our results suggest that the GC% of repeats and proportion of repeats are independent of the chromosome size. This leaves an open space for another mechanism driving the GC evolution in vertebrates.
- Keywords
- GC content, GC-biased gene conversion, chromosome size, linkage group, microchromosomes,
- MeSH
- Chromosomes genetics MeSH
- Cytogenetics * MeSH
- Genome genetics MeSH
- Evolution, Molecular * MeSH
- Vertebrates classification genetics MeSH
- Birds classification genetics MeSH
- Recombination, Genetic genetics MeSH
- Repetitive Sequences, Nucleic Acid MeSH
- Fishes classification genetics MeSH
- Base Composition genetics MeSH
- Animals MeSH
- Check Tag
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
The study of fish cytogenetics has been impeded by the inability to produce G-bands that could assign chromosomes to their homologous pairs. Thus, the majority of karyotypes published have been estimated based on morphological similarities of chromosomes. The reason why chromosome G-banding does not work in fish remains elusive. However, the recent increase in the number of fish genomes assembled to the chromosome level provides a way to analyse this issue. We have developed a Python tool to visualize and quantify GC percentage (GC%) of both repeats and unique DNA along chromosomes using a non-overlapping sliding window approach. Our tool profiles GC% and simultaneously plots the proportion of repeats (rep%) in a color scale (or vice versa). Hence, it is possible to assess the contribution of repeats to the total GC%. The main differences are the GC% of repeats homogenizing the overall GC% along fish chromosomes and a greater range of GC% scattered along fish chromosomes. This may explain the inability to produce G-banding in fish. We also show an occasional banding pattern along the chromosomes in some fish that probably cannot be detected with traditional qualitative cytogenetic methods.
- Keywords
- AT/GC heterogeneity, GC-profile, chromosome banding, fish cytogenetics, repeats organization,
- MeSH
- Genome * MeSH
- Gorilla gorilla classification genetics MeSH
- Karyotyping methods MeSH
- Cats MeSH
- Chromosome Mapping methods statistics & numerical data MeSH
- Chromosome Banding MeSH
- Fishes classification genetics MeSH
- Software * MeSH
- Tandem Repeat Sequences MeSH
- Base Composition * MeSH
- Animals MeSH
- Check Tag
- Cats MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
Critically endangered sturgeons, having undergone three whole genome duplication events, represent an exceptional example of ploidy plasticity in vertebrates. Three extant ploidy groups, combined with autopolyploidization, interspecific hybridization and the fertility of hybrids are important issues in sturgeon conservation and aquaculture. Here we demonstrate that the sturgeon genome can undergo numerous alterations of ploidy without severe physiological consequences, producing progeny with a range of ploidy levels and extremely high chromosome numbers. Artificial suppression of the first mitotic division alone, or in combination with suppression of the second meiotic division of functionally tetraploid zygotes (4n, C-value = 4.15) of Siberian sturgeon Acipenser baerii and Russian sturgeon A. gueldenstaedtii resulted in progeny of various ploidy levels-diploid/hexaploid (2n/6n) mosaics, hexaploid, octoploid juveniles (8n), and dodecaploid (12n) larvae. Counts between 477 to 520 chromosomes in octoploid juveniles of both sturgeons confirmed the modal chromosome numbers of parental species had been doubled. This exceeds the highest previously documented chromosome count among vertebrates 2n ~ 446 in the cyprinid fish Ptychobarbus dipogon.
BACKGROUND: Teleost fish genome size has been repeatedly demonstrated to positively correlate with the proportion of transposable elements (TEs). This finding might have far-reaching implications for our understanding of the evolution of nucleotide composition across vertebrates. Genomes of fish and amphibians are GC homogenous, with non-teleost gars being the single exception identified to date, whereas birds and mammals are AT/GC heterogeneous. The exact reason for this phenomenon remains controversial. Since TEs make up significant proportions of genomes and can quickly accumulate across genomes, they can potentially influence the host genome with their own GC content (GC%). However, the GC% of fish TEs has so far been neglected. RESULTS: The genomic proportion of TEs indeed correlates with genome size, although not as linearly as previously shown with fewer genomes, and GC% negatively correlates with genome size in the 33 fish genome assemblies analysed here (excluding salmonids). GC% of fish TE consensus sequences positively correlates with the corresponding genomic GC% in 29 species tested. Likewise, the GC contents of the entire repetitive vs. non-repetitive genomic fractions correlate positively in 54 fish species in Ensembl. However, among these fish species, there is also a wide variation in GC% between the main groups of TEs. Class II DNA transposons, predominant TEs in fish genomes, are significantly GC-poorer than Class I retrotransposons. The AT/GC heterogeneous gar genome contains fewer Class II TEs, a situation similar to fugu with its extremely compact and also GC-enriched but AT/GC homogenous genome. CONCLUSION: Our results reveal a previously overlooked correlation between GC% of fish genomes and their TEs. This applies to both TE consensus sequences as well as the entire repetitive genomic fraction. On the other hand, there is a wide variation in GC% across fish TE groups. These results raise the question whether GC% of TEs evolves independently of GC% of the host genome or whether it is driven by TE localization in the host genome. Answering these questions will help to understand how genomic GC% is shaped over time. Long-term accumulation of GC-poor(er) Class II DNA transposons might indeed have influenced AT/GC homogenization of fish genomes and requires further investigation.
- Keywords
- GC content, Genome evolution, Nucleotide composition, Teleost fish, Transposon,
- Publication type
- Journal Article MeSH
Cichlid fishes are the subject of scientific interest because of their rapid adaptive radiation, resulting in extensive ecological and taxonomic diversity. In this study, we examined 11 morphologically distinct cichlid species endemic to Barombi Mbo, the largest crater lake in western Cameroon, namely Konia eisentrauti, Konia dikume, Myaka myaka, Pungu maclareni, Sarotherodon steinbachi, Sarotherodon lohbergeri, Sarotherodon linnellii, Sarotherodon caroli, Stomatepia mariae, Stomatepia pindu, and Stomatepia mongo. These species supposedly evolved via sympatric ecological speciation from a common ancestor, which colonized the lake no earlier than one million years ago. Here we present the first comparative cytogenetic analysis of cichlid species from Barombi Mbo Lake using both conventional (Giemsa staining, C-banding, and CMA3/DAPI staining) and molecular (fluorescence in situ hybridization with telomeric, 5S, and 28S rDNA probes) methods. We observed stability on both macro and micro-chromosomal levels. The diploid chromosome number was 2n = 44, and the karyotype was invariably composed of three pairs of meta/submetacentric and 19 pairs of subtelo/acrocentric chromosomes in all analysed species, with the same numbers of rDNA clusters and distribution of heterochromatin. The results suggest the evolutionary stability of chromosomal set; therefore, the large-scale chromosomal rearrangements seem to be unlikely associated with the sympatric speciation in Barombi Mbo.
- Keywords
- African endemic fishes, FISH, Karyotype, adaptive radiation, chromosome banding, chromosome stasis, cytotaxonomy, rDNA,
- MeSH
- Adaptation, Biological genetics radiation effects MeSH
- Biological Evolution MeSH
- Chromosomal Instability radiation effects MeSH
- Cichlids genetics MeSH
- In Situ Hybridization, Fluorescence MeSH
- Lakes MeSH
- Karyotype MeSH
- Karyotyping MeSH
- Chromosome Mapping MeSH
- Chromosome Banding MeSH
- Telomere genetics MeSH
- Animals MeSH
- Check Tag
- Animals MeSH
- Publication type
- Journal Article MeSH
- Geographicals
- Cameroon MeSH
Arowanas (Osteoglossinae) are charismatic freshwater fishes with six species and two genera (Osteoglossum and Scleropages) distributed in South America, Asia, and Australia. In an attempt to provide a better assessment of the processes shaping their evolution, we employed a set of cytogenetic and genomic approaches, including i) molecular cytogenetic analyses using C- and CMA3/DAPI staining, repetitive DNA mapping, comparative genomic hybridization (CGH), and Zoo-FISH, along with ii) the genotypic analyses of single nucleotide polymorphisms (SNPs) generated by diversity array technology sequencing (DArTseq). We observed diploid chromosome numbers of 2n = 56 and 54 in O. bicirrhosum and O. ferreirai, respectively, and 2n = 50 in S. formosus, while S. jardinii and S. leichardti presented 2n = 48 and 44, respectively. A time-calibrated phylogenetic tree revealed that Osteoglossum and Scleropages divergence occurred approximately 50 million years ago (MYA), at the time of the final separation of Australia and South America (with Antarctica). Asian S. formosus and Australian Scleropages diverged about 35.5 MYA, substantially after the latest terrestrial connection between Australia and Southeast Asia through the Indian plate movement. Our combined data provided a comprehensive perspective of the cytogenomic diversity and evolution of arowana species on a timescale.
- Keywords
- DArTseq, Gondwana, biogeography, evolution, genetic diversity,
- MeSH
- Principal Component Analysis MeSH
- Biological Evolution * MeSH
- Genetic Variation MeSH
- Genomics * MeSH
- Genotyping Techniques MeSH
- Karyotype MeSH
- Chromosome Mapping MeSH
- Chromosome Banding MeSH
- Fishes genetics MeSH
- Geography MeSH
- Animals MeSH
- Check Tag
- Animals MeSH
- Publication type
- Journal Article MeSH
- Comparative Study MeSH