Dataset Information

DNA Transposon Expansion is Associated with Genome Size Increase in Mudminnows.

ABSTRACT: Genome sizes of eukaryotic organisms vary substantially, with whole-genome duplications (WGD) and transposable element expansion acting as main drivers for rapid genome size increase. The two North American mudminnows, Umbra limi and Umbra pygmaea, feature genomes about twice the size of their sister lineage Esocidae (e.g., pikes and pickerels). However, it is unknown whether all Umbra species share this genome expansion and which causal mechanisms drive this expansion. Using flow cytometry, we find that the genome of the European mudminnow is expanded similarly to both North American species, ranging between 4.5 and 5.4 pg per diploid nucleus. Observed blocks of interstitially located telomeric repeats in U. limi suggest frequent Robertsonian rearrangements in its history. Comparative analyses of transcriptome and genome assemblies show that the genome expansion in Umbra is driven by the expansion of DNA transposon and unclassified repeat sequences without WGD. Furthermore, we find a substantial ongoing expansion of repeat sequences in the Alaska blackfish Dallia pectoralis, the closest relative to the family Umbridae, which might mark the beginning of a similar genome expansion. Our study suggests that the genome expansion in mudminnows, driven mainly by transposon expansion, but not WGD, occurred before the separation into the American and European lineage.

SUBMITTER: Lehmann R

PROVIDER: S-EPMC8557787 | biostudies-literature | 2021 Oct

REPOSITORIES: biostudies-literature

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DNA Transposon Expansion is Associated with Genome Size Increase in Mudminnows.

Lehmann Robert R Kovařík Aleš A Ocalewicz Konrad K Kirtiklis Lech L Zuccolo Andrea A Tegner Jesper N JN Wanzenböck Josef J Bernatchez Louis L Lamatsch Dunja K DK Symonová Radka R

Genome biology and evolution 20211001 10

Genome sizes of eukaryotic organisms vary substantially, with whole-genome duplications (WGD) and transposable element expansion acting as main drivers for rapid genome size increase. The two North American mudminnows, Umbra limi and Umbra pygmaea, feature genomes about twice the size of their sister lineage Esocidae (e.g., pikes and pickerels). However, it is unknown whether all Umbra species share this genome expansion and which causal mechanisms drive this expansion. Using flow cytometry, we ...[more]

PMID: 34599322

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Project description:BackgroundThe causes and consequences of genome size variation across Eukaryotes, which spans five orders of magnitude, have been hotly debated since before the advent of genome sequencing. Previous studies have mostly examined variation among larger taxonomic units (e.g., orders, or genera), while comparisons among closely related species are rare. Rotifers of the Brachionus plicatilis species complex exhibit a seven-fold variation in genome size and thus represent a unique opportunity to study such changes on a relatively short evolutionary timescale. Here, we sequenced and analysed the genomes of four species of this complex with nuclear DNA contents spanning 110-422 Mbp. To establish the likely mechanisms of genome size change, we analysed both sequencing read libraries and assemblies for signatures of polyploidy and repetitive element content. We also compared these genomes to that of B. calyciflorus, the closest relative with a sequenced genome (293 Mbp nuclear DNA content).ResultsDespite the very large differences in genome size, we saw no evidence of ploidy level changes across the B. plicatilis complex. However, repetitive element content explained a large portion of genome size variation (at least 54%). The species with the largest genome, B. asplanchnoidis, has a strikingly high 44% repetitive element content, while the smaller B. plicatilis genomes contain between 14 and 25% repetitive elements. According to our analyses, the B. calyciflorus genome contains 39% repetitive elements, which is substantially higher than previously reported (21%), and suggests that high repetitive element load could be widespread in monogonont rotifers.ConclusionsEven though the genome sizes of these species are at the low end of the metazoan spectrum, their genomes contain substantial amounts of repetitive elements. Polyploidy does not appear to play a role in genome size variations in these species, and these variations can be mostly explained by changes in repetitive element content. This contradicts the naïve expectation that small genomes are streamlined, or less complex, and that large variations in nuclear DNA content between closely related species are due to polyploidy.

Project description:BACKGROUND:Repetitive sequences (RSs) are redundant, complex at times, and often lineage-specific, representing significant "building" materials for genes and genomes. According to their origins, sequence characteristics, and ways of propagation, repetitive sequences are divided into transposable elements (TEs) and satellite sequences (SSs) as well as related subfamilies and subgroups hierarchically. The combined changes attributable to the repetitive sequences alter gene and genome architectures, such as the expansion of exonic, intronic, and intergenic sequences, and most of them propagate in a seemingly random fashion and contribute very significantly to the entire mutation spectrum of mammalian genomes. PRINCIPAL FINDINGS:Our analysis is focused on evolutional features of TEs and SSs in the intronic sequence of twelve selected mammalian genomes. We divided them into four groups-primates, large mammals, rodents, and primary mammals-and used four non-mammalian vertebrate species as the out-group. After classifying intron size variation in an intron-centric way based on RS-dominance (TE-dominant or SS-dominant intron expansions), we observed several distinct profiles in intron length and positioning in different vertebrate lineages, such as retrotransposon-dominance in mammals and DNA transposon-dominance in the lower vertebrates, amphibians and fishes. The RS patterns of mouse and rat genes are most striking, which are not only distinct from those of other mammals but also different from that of the third rodent species analyzed in this study-guinea pig. Looking into the biological functions of relevant genes, we observed a two-dimensional divergence; in particular, genes that possess SS-dominant and/or RS-free introns are enriched in tissue-specific development and transcription regulation in all mammalian lineages. In addition, we found that the tendency of transposons in increasing intron size is much stronger than that of satellites, and the combined effect of both RSs is greater than either one of them alone in a simple arithmetic sum among the mammals and the opposite is found among the four non-mammalian vertebrates. CONCLUSIONS:TE- and SS-derived RSs represent major mutational forces shaping the size and composition of vertebrate genes and genomes, and through natural selection they either fine-tune or facilitate changes in size expansion, position variation, and duplication, and thus in functions and evolutionary paths for better survival and fitness. When analyzed globally, not only are such changes significantly diversified but also comprehensible in lineages and biological implications.

Project description:BACKGROUND: Nuclear genome size varies 300 000-fold, whereas transcriptome size varies merely 17-fold. In the largest genomes nearly all DNA is non-genic secondary DNA, mostly intergenic but also within introns. There is now compelling evidence that secondary DNA is functional, i.e. positively selected by organismal selection, not the purely neutral or 'selfish' outcome of mutation pressure. The skeletal DNA theory argued that nuclear volumes are genetically determined primarily by nuclear DNA amounts, modulated somewhat by genes affecting the degree of DNA packing or unfolding; the huge spread of nuclear genome sizes is the necessary consequence of the origin of the nuclear envelope and the nucleation of its assembly by DNA, plus the adaptively significant 300 000-fold range of cell volumes and selection for balanced growth by optimizing karyoplasmic volume ratios (essentially invariant with cell volume in growing/multiplying cells). This simple explanation of the C-value paradox is refined here in the light of new insights into the nature of heterochromatin and the nuclear lamina, the genetic control of cell volume, and large-scale eukaryote phylogeny, placing special emphasis on protist test cases of the basic principles of nuclear genome size evolution. GENOME MINIATURIZATION: and Expansion Intracellular parasites (e.g. Plasmodium, microsporidia) dwarfed their genomes by gene loss and eliminating virtually all secondary DNA. The primary driving forces for genome reduction are metabolic and spatial economy and cell multiplication speed. Most extreme nuclear shrinkage yielded genomes as tiny as 0.38 Mb (making the nuclear genome size range effectively 1.8 million-fold!) in some minute enslaved nuclei (nucleomorphs) of cryptomonads and chlorarachneans, chimaeric cells that also retain a separate normal large nucleus. The latter shows typical correlation between genome size and cell volume, but nucleomorphs do not despite co-existing in the same cell for >500 My. Thus mutation pressure does not inexorably increase genome size; selection can eliminate essentially all non-coding DNA if need be. Nucleomorphs and microsporidia even reduced gene size. Expansion of secondary DNA in the main nucleus, and in large-celled eukaryotes generally, must be positively selected for function. Ciliate nuclear dimorphism provides a key test that refutes the selfish DNA and strongly supports the skeletal DNA/karyoplasmic ratio interpretation of genome size evolution. GENETIC CONTROL OF CELL VOLUME IS MULTIGENIC: The quantitatively proportional correlation between genome size and cell size cannot be explained by purely mutational theories, as eukaryote cell volumes are causally determined by cell cycle control genes, not by DNA amounts.

Dataset Information

DNA Transposon Expansion is Associated with Genome Size Increase in Mudminnows.

Publications

DNA Transposon Expansion is Associated with Genome Size Increase in Mudminnows.

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