Genome Size Evolution Research Articles

Which factors contribute most to genome size variation within angiosperms?

Genome size varies greatly across the flowering plants and has played an important role in shaping their evolution. It has been reported that many factors correlate with the variation in genome size, but few studies have systematically explored this at the genomic level. Here, we scan genomic information for 74 species from 74 families in 38 orders covering the major groups of angiosperms (the taxonomic information was acquired from the latest Angiosperm Phylogeny Group (APG IV) system) to evaluate the correlation between genome size variation and different genome characteristics: polyploidization, different types of repeat sequence content, and the dynamics of long terminal repeat retrotransposons (LTRs). Surprisingly, we found that polyploidization shows no significant correlation with genome size, while LTR content demonstrates a significantly positive correlation. This may be due to genome instability after polyploidization, and since LTRs occupy most of the genome content, it may directly result in most of the genome variation. We found that the LTR insertion time is significantly negatively correlated with genome size, which may reflect the competition between insertion and deletion of LTRs in each genome, and that the old insertions are usually easy to recognize and eliminate. We also noticed that most of the LTR burst occurred within the last 3 million years, a timeframe consistent with the violent climate fluctuations in the Pleistocene. Our findings enhance our understanding of genome size evolution within angiosperms, and our methods offer immediate implications for corresponding research in other datasets.

Genome Size Estimation of Callipogon relictus Semenov (Coleoptera: Cerambycidae), an Endangered Species and a Korea Natural Monument.

Simple SummaryThe longhorned beetle Calipogon relictus has been considered as a class I endangered species since 2012 in Korea. In an attempt towards beetle conservation, we estimated its genome size at 1.8 ± 0.2 Gb, representing one of the largest cerambycid genomes. This study provides useful insight at the genome level and facilitates the development of an effective conservation strategy.We estimated the genome size of a relict longhorn beetle, Callipogon relictus Semenov (Cerambycidae: Prioninae)—the Korean natural monument no. 218 and a Class I endangered species—using a combination of flow cytometry and k-mer analysis. The two independent methods enabled accurate estimation of the genome size in Cerambycidae for the first time. The genome size of C. relictus was 1.8 ± 0.2 Gb, representing one of the largest cerambycid genomes studied to date. An accurate estimation of genome size of a critically endangered longhorned beetle is a major milestone in our understanding and characterization of the C. relictus genome. Ultimately, the findings provide useful insight into insect genomics and genome size evolution, particularly among beetles.

Draft Genome Assemblies and Annotations of Agrypnia vestita Walker, and Hesperophylax magnus Banks Reveal Substantial Repetitive Element Expansion in Tube Case-Making Caddisflies (Insecta: Trichoptera).

Trichoptera (caddisflies) play an essential role in freshwater ecosystems; for instance, larvae process organic material from the water and are food for a variety of predators. Knowledge on the genomic diversity of caddisflies can facilitate comparative and phylogenetic studies thereby allowing scientists to better understand the evolutionary history of caddisflies. Although Trichoptera are the most diverse aquatic insect order, they remain poorly represented in terms of genomic resources. To date, all long-read based genomes have been sequenced from individuals in the retreat-making suborder, Annulipalpia, leaving ∼275 Ma of evolution without high-quality genomic resources. Here, we report the first long-read based de novo genome assemblies of two tube case-making Trichoptera from the suborder Integripalpia, Agrypnia vestita Walker and Hesperophylax magnus Banks. We find that these tube case-making caddisflies have genome sizes that are at least 3-fold larger than those of currently sequenced annulipalpian genomes and that this pattern is at least partly driven by major expansion of repetitive elements. In H. magnus, long interspersed nuclear elements alone exceed the entire genome size of some annulipalpian counterparts suggesting that caddisflies have high potential as a model for understanding genome size evolution in diverse insect lineages.

Unexpectedly high mutation rate of a deep-sea hyperthermophilic anaerobic archaeon.

Deep-sea hydrothermal vents resemble the early Earth, and thus the dominant Thermococcaceae inhabitants, which occupy an evolutionarily basal position of the archaeal tree and take an obligate anaerobic hyperthermophilic free-living lifestyle, are likely excellent models to study the evolution of early life. Here, we determined that unbiased mutation rate of a representative species, Thermococcus eurythermalis, exceeded that of all known free-living prokaryotes by 1-2 orders of magnitude, and thus rejected the long-standing hypothesis that low mutation rates were selectively favored in hyperthermophiles. We further sequenced multiple and diverse isolates of this species and calculated that T. eurythermalis has a lower effective population size than other free-living prokaryotes by 1-2 orders of magnitude. These data collectively indicate that the high mutation rate of this species is not selectively favored but instead driven by random genetic drift. The availability of these unusual data also helps explore mechanisms underlying microbial genome size evolution. We showed that genome size is negatively correlated with mutation rate and positively correlated with effective population size across 30 bacterial and archaeal lineages, suggesting that increased mutation rate and random genetic drift are likely two important mechanisms driving microbial genome reduction. Future determinations of the unbiased mutation rate of more representative lineages with highly reduced genomes such as Prochlorococcus and Pelagibacterales that dominate marine microbial communities are essential to test these hypotheses.

Variation and Evolution of Genome Size in Gymnosperms

Abstract Gymnosperms show a significantly higher mean (1C=18.16, 1Cx=16.80) and a narrow range (16.89-fold) of genome sizes as compared with angiosperms. Among the 12 families the largest ranges of 1C values is shown by Ephedraceae (4.73-fold) and Cupressaceae (4.45-fold) which are partly due to polyploidy as 1Cx values vary 2.41 and 1.37-fold respectively. In rest of the families which have only diploid taxa the range of 1C values is from 1.18-fold (Cycadaeae) to 4.36-fold (Podocarpaceae). The question is how gymnosperms acquired such big genome sizes despite the rarity of recent instances of polyploidy. A general survey of different families and genera shows that gymnosperms have experienced both increase and decrease in their genome size during evolution. Various genomic components which have accounted for these large genomes have been discussed. The major contributors are the transposable elements particularly LTR-retrotransposons comprising of Ty3gypsy, Ty1copia and gymny superfamilies which are most widespread. The genomes of gymnosperms have been acquiring diverse LTR-RTs in their long evolution in the absence of any efficient mechanism of their elimination. The epigenetic machinery which silences these large tracts of repeat sequences into the stretches of heterochromatin and the adaptive value of these silenced repeat sequences need further investigation.

Quantum Patterns of Genome Size Variation in Angiosperms

Aims: The discontinuous pattern of genome size variation in angiosperms is an unsolved problem related to genome evolution. In this study, we introduced a genome evolution operator and solved the related eigenvalue equation to deduce the discontinuous pattern. Background: Genome is a well-defined system for studying the evolution of species. One of the basic problems is the genome size evolution. The DNA amounts for angiosperm species are highly variable, differing over 1000-fold. One big surprise is the discovery of the discontinuous distribution of nuclear DNA amounts in many angiosperm genera. Objective: The discontinuous distribution of nuclear DNA amounts has certain regularity, much like a group of quantum states in atomic physics. The quantum pattern has not been explained by all the evolutionary theories so far and we shall interpret it through the quantum simulation of genome evolution. Methods: We introduced a genome evolution operator H to deduce the distribution of DNA amount. The nuclear DNA amount in angiosperms is studied from the eigenvalue equation of the genome evolution operator H. The operator H is introduced by physical simulation and it is defined as a function of the genome size N and the derivative with respect to the size. Results: The discontinuity of DNA size distribution and its synergetic occurrence in related angiosperms species are successfully deduced from the solution of the equation. The results agree well with the existing experimental data of Aloe, Clarkia, Nicotiana, Lathyrus, Allium and other genera. Conclusion: The success of our approach may infer the existence of a set of genomic evolutionary equations satisfying classical-quantum duality. The classical phase of evolution means it obeys the classical deterministic law, while the quantum phase means it obeys the quantum stochastic law. The discontinuity of DNA size distribution provides novel evidences on the quantum evolution of angiosperms. It has been realized that the discontinuous pattern is due to the existence of some unknown evolutionary constraints. However, our study indicates that these constraints on the angiosperm genome essentially originate from quantum.

Genome Size Evolution and Dynamics in Iris, with Special Focus on the Section Oncocyclus.

Insights into genome size dynamics and its evolutionary impact remain limited by the lack of data for many plant groups. One of these is the genus Iris, of which only 53 out of c. 260 species have available genome sizes. In this study, we estimated the C-values for 41 species and subspecies of Iris mainly from the Eastern Mediterranean region. We constructed a phylogenetic framework to shed light on the distribution of genome sizes across subgenera and sections of Iris. Finally, we tested evolutionary models to explore the mode and tempo of genome size evolution during the radiation of section Oncocyclus. Iris as a whole displayed a great variety of C-values; however, they were unequally distributed across the subgenera and sections, suggesting that lineage-specific patterns of genome size diversification have taken place within the genus. The evolutionary model that best fitted our data was the speciational model, as changes in genome size appeared to be mainly associated with speciation events. These results suggest that genome size dynamics may have contributed to the radiation of Oncocyclus irises. In addition, our phylogenetic analysis provided evidence that supports the segregation of the Lebanese population currently attributed to Iris persica as a distinct species.

Genome Size of 17 Species From Caelifera (Orthoptera) and Determination of Internal Standards With Very Large Genome Size in Insecta.

Comparative studies of insect genome size show that Orthoptera is a unique group of Insecta with a significantly enlarged genome. To determine a suitable internal standard for a large genome and to compare the effects of different internal standards on estimates of genome size, we used four internal standards to estimate nuclear DNA content in nine insect species with large genomes. The results showed that the combination of two internal standards, Locusta migratoria (♂1C = 6.20 pg, ♀1C = 6.60 pg) and Periplaneta americana♂ (1C = 3.41 pg), was suitable for estimating large genome of Caelifera by flow cytometry. Using these two internal standards, we estimated the genome sizes of 17 species of Caelifera (12 genera in Acrididae, 2 genera in Pamphagidae, 1 genus in Pyrgomorphidae) using flow cytometry. Genomes ranged from 6.57 pg (Shirakiacris shirakii) to 18.64 pg (Bryodemella holdereri), the largest described in insects to date. These species showed significant genomic dimorphism based on sex: females had a 0.56 pg larger genome than males on average, which might be due to the sex chromosome determinism mechanism of X0(♂)/XX(♀). To test the results obtained by flow cytometry, we used k-mers of Illumina sequencing data to gauge the C-value of Calliptamus abbreviatus and Haplotropis brunneriana. The results of the two methods are slightly different. Genomes were estimated to be about 0.28 and 0.26 pg smaller, respectively, than the flow cytometry values. Furthermore, we also reconstructed the evolutionary relationships of these taxa and discuss the genome size evolution in a phylogenetic framework.

Evolutionary dynamics of genome size in a radiation of woody plants.

Plant genome size ranges widely, providing many opportunities to examine how genome size variation affects plant form and function. We analyzed trends in chromosome number, genome size, and leaf traits for the woody angiosperm clade Viburnum to examine the evolutionary associations, functional implications, and possible drivers of genome size. Chromosome counts and genome size estimates were mapped onto a Viburnum phylogeny to infer the location and frequency of polyploidization events and trends in genome size evolution. Genome size was analyzed with leaf anatomical and physiological data to evaluate the influence of genome size on plant function. We discovered nine independent polyploidization events, two reductions in base chromosome number, and substantial variation in genome size with a slight trend toward genome size reduction in polyploids. We did not find strong relationships between genome size and the functional and morphological traits that have been highlighted at broader phylogenetic scales. Polyploidization events were sometimes associated with rapid radiations, demonstrating that polyploid lineages can be highly successful. Relationships between genome size and plant physiological function observed at broad phylogenetic scales may be largely irrelevant to the evolutionary dynamics of genome size at smaller scales. The view that plants readily tolerate changes in ploidy and genome size, and often do so, appears to apply to Viburnum.

Evolutionary dynamics of transposable elements and satellite DNAs in polyploid Spartina species

Repeated sequences and polyploidy play a central role in plant genome dynamics. Here, we analyze the evolutionary dynamics of repeats in tetraploid and hexaploid Spartina species that diverged during the last 10 million years within the Chloridoideae, one of the poorest investigated grass lineages. From high-throughput genome sequencing, we annotated Spartina repeats and determined what sequence types account for the genome size variation among species. We examined whether differential genome size evolution correlated with ploidy levels and phylogenetic relationships. We also examined the tempo of repeat sequence dynamics associated with allopatric speciation over the last 3–6 million years between hexaploid species that diverged on the American and European Atlantic coasts and tetraploid species from North and South America. The tetraploid S. spartinae, whose phylogenetic placement has been debated, exhibits a similar repeat content as hexaploid species, suggesting common ancestry. Genome expansion or contraction resulting from repeat dynamics seems to be explained mostly by the contrasting divergence times between species, rather than by genome changes triggered by ploidy level change per se. One 370 bp satellite may be exhibiting ‘meiotic drive’ and driving chromosome evolution in S. alterniflora. Our results provide crucial insights for investigating the genetic and epigenetic consequences of such differential repeat dynamics on the ecology and distribution of the meso- and neopolyploid Spartina species.

Genome Evolution: Mutation Is the Main Driver of Genome Size in Prokaryotes

Despite intense research on genome architecture since the 2000s, genome-size evolution in prokaryotes has remained puzzling. Using a phylogenetic approach, a new study found that increased mutation rate is associated with gene loss and reduced genome size in prokaryotes.

Inflorescence preformation prior to winter: a surprisingly widespread strategy that drives phenology of temperate perennial herbs.

Organ preformation in overwintering buds of perennial plants has been known for almost two centuries. It is hypothesized to underlie fast growth and early flowering, but its frequency, phylogenetic distribution, and ecological relevance have never been systematically examined. We microscopically observed inflorescence preformation in overwintering buds (IPB) in the autumn. We studied a phylogenetically and ecologically representative set of 330 species of temperate perennial angiosperms and linked these observations with quantitative data on species' flowering phenology, genome size, and ecology. IPB was observed in 34% of species examined (in 14% species the stamens and/or pistils were already developed). IPB is fairly phylogenetically conserved and frequent in many genera (Alchemilla, Carex, Euphorbia, Geranium, Primula, Pulmonaria) or families (Ranunculaceae, Euphorbiaceae, Violaceae, Boraginaceae). It was found in species of any genome size, although it was almost universal in those with large genomes. Compared with non-IPB species, IPB species flowered 38d earlier on average and were more common in shaded and undisturbed habitats. IPB is a surprisingly widespread adaptation for early growth in predictable (undisturbed) conditions. It contributes to temporal niche differentiation and has important consequences for understanding plant phenology, genome size evolution, and phylogenetic structure of plant communities.

Is the evolution of carnivory connected with genome size reduction?

As repeatedly shown, the remarkable variation in the genome size of angiosperms can be shaped by extrinsic selective pressures, including nutrient availability. Carnivory has evolved independently in 10 angiosperm clades, but all carnivorous plants share a common affinity to nutrient-poor habitats. As such, carnivory and genome reduction could be responses to the same environmental pressure. Indeed, the smallest genomes among flowering plants are found in the carnivorous family Lentibulariaceae, where a unique mutation in cytochrome c oxidase (COX) is suspected to promote genome miniaturization. Despite these hypotheses, a phylogenetically informed test of genome size and nutrient availability across carnivorous clades has so far been missing. Using linear mixed models, we compared genome sizes of 127 carnivorous plants from 7 diverse angiosperm clades with 1072 of their noncarnivorous relatives. We also tested whether genome size in Lentibulariaceae reflects the presence of the COX mutation. The genome sizes of carnivorous plants do not differ significantly from those of their noncarnivorous relatives. Based on available data, no significant association between the COX mutation and genome miniaturization could be confirmed, not even when considering polyploidy. Carnivory alone does not seem to significantly affect genome size decrease. Plausibly, it might actually counterbalance the effect of nutrient limitation on genome size evolution. The role of the COX mutation in genome miniaturization needs to be evaluated by analysis of a broader data set because current knowledge of its presence across Lentibulariaceae covers less than 10% of the species diversity in this family.

Genome size evolution: towards new model systems for old questions.

Genome size (GS) variation is a fundamental biological characteristic; however, its evolutionary causes and consequences are the topic of ongoing debate. Whether GS is a neutral trait or one subject to selective pressures, and how strong these selective pressures are, may remain open questions. Fundamentally, the genomic sequences responsible for this variation directly impact the potential evolutionary outcomes and, equally, are the targets of different evolutionary pressures. For example, duplications and deletions of genic regions (large or small) can have immediate and drastic phenotypic effects, while an expansion or contraction of non-coding DNA is less likely to cause catastrophic phenotypic effects. However, in the long term, the accumulation or deletion of ncDNA is likely to have larger effects. Modern sequencing technologies are allowing for the dissection of these proximate causes, but a combination of these new technologies with more traditional evolutionary experiments and approaches could revolutionize this debate and potentially resolve many of these arguments. Here, I discuss an ambitious way forward for GS research, putting it in context of historical debates, theories and sometimes contradictory evidence, and highlighting the promise of combining new sequencing technologies and analytical developments with more traditional experimental evolution approaches.

Increased Mutation Rate Is Linked to Genome Reduction in Prokaryotes

The evolutionary processes that drive variation in genome size across the tree of life remain unresolved. Effective population size (Ne) is thought to play an important role in shaping genome size [1-3]-a key example being the reduced genomes of insect endosymbionts, which undergo population bottlenecks during transmission [4]. However, the existence of reduced genomes in marine and terrestrial prokaryote species with large Ne indicate that genome reduction is influenced by multiple processes [3]. One candidate process is enhanced mutation rate, which can increase adaptive capacity but can also promote gene loss. To investigate evolutionary forces associated with prokaryotic genome reduction, we performed molecular evolutionary and phylogenomic analyses of nine lineages from five bacterial and archaeal phyla. We found that gene-loss rate strongly correlated with synonymous substitution rate (a proxy for mutation rate) in seven of the nine lineages. However, gene-loss rate showed weak or no correlation with the ratio of nonsynonymous/synonymous substitution rate (dN/dS). These results indicate that genome reduction is largely associated with increased mutation rate, while the association between gene loss and changes in Ne is less well defined. Lineages with relatively high dS and dN, as well as smaller genomes, lacked multiple DNA repair genes, providing a proximate cause for increased mutation rates. Our findings suggest that similar mechanisms drive genome reduction in both intracellular and free-living prokaryotes, with implications for developing a comprehensive theory of prokaryote genome size evolution.

A deep dive into the ancestral chromosome number and genome size of flowering plants.

Chromosome number and genome variation in flowering plants have stimulated growing speculation about the ancestral chromosome number of angiosperms, but estimates so far remain equivocal. We used a probabilistic approach to model haploid chromosome number (n) changes along a phylogeny embracing more than 10000 taxa, to reconstruct the ancestral chromosome number of the common ancestor of extant angiosperms and the most recent common ancestor for single angiosperm families. Independently, we carried out an analysis of 1C genome size evolution, including over 5000 taxa. Our analyses revealed an ancestral haploid chromosome number for angiosperms of n=7, a diploid status, and an ancestral 1Cof1.73pg. For 160 families, inferred ancestral n are provided for the first time. Both descending dysploidy and polyploidy played crucial roles in chromosome number evolution. While descending dysploidy is equally distributed early and late across the phylogeny, polyploidy is detected mainly towards the tips. Similarly, 1C genome size also increases (or decreases) significantly in late-branching lineages. Therefore, no evidence exists of a clear link between ancestral chromosome numbers and ancient polyploidization events, suggesting that further insights are needed to elucidate the organization of genome packaging into chromosomes.

Genome Size Evolution Mediated by Gypsy Retrotransposons in Brassicaceae

The dynamic activity of transposable elements (TEs) contributes to the vast diversity of genome size and architecture among plants. Here, we examined the genomic distribution and transposition activity of long terminal repeat retrotransposons (LTR-RTs) in Arabidopsis thaliana (Ath) and three of its relatives, Arabidopsis lyrata (Aly), Eutrema salsugineum (Esa), and Schrenkiella parvula (Spa), in Brassicaceae. Our analyses revealed the distinct evolutionary dynamics of Gypsyretrotransposons, which reflects the different patterns of genome size changes of the four species over the past million years. The rate of Gypsy transposition in Aly is approximately five times more rapid than that of Ath and Esa, suggesting an expanding Aly genome. Gypsy insertions in Esa are strictly confined to pericentromeric heterochromatin and associated with dramatic centromere expansion. In contrast, Gypsy insertions in Spa have been largely suppressed over the last million years, likely as a result of a combination of an inherent molecular mechanism of preferential DNA removal and purifying selection at Gypsy elements. Additionally, species-specific clades of Gypsy elements shaped the distinct genome architectures of Aly and Esa.

Contribution to the knowledge of genome size evolution in edible blueberries (genus Vaccinium)

Contribution to the knowledge of genome size evolution in edible blueberries (genus Vaccinium)

Environmental pressures on stomatal size may drive plant genome size evolution: evidence from a natural experiment with Cape geophytes.

The idea that genome (size) evolution in eukaryotes could be driven by environmental factors is still vigorously debated. In extant plants, genome size correlates positively with stomatal size, leading to the idea that conditions enabling the existence of large stomata in fossil plants also supported growth of their genome size. We test this inductive assumption in drought-adapted, prostrate-leaved Cape (South Africa) geophytes where, compared with their upright-leaved geophytic ancestors, stomata develop in a favourably humid microclimate formed underneath their leaves. Stomatal parameters (leaf cuticle imprints) and genome size (flow cytometry) were measured in 16 closely related geophytic species pairs from seven plant families. In each pair, representing a different genus, we contrasted a prostrate-leaved species with its upright-leaved phylogenetic relative, the latter whose stomata are exposed to the ambient arid climate. Except for one, all prostrate-leaves species had larger stomata, and in 13 of 16 pairs they also had larger genomes than their upright-leaved relatives. Stomatal density and theoretical maximum conductance were less in prostrate-leaved species with small guard cells (<1 pL) but showed no systematic difference in species pairs with larger guard cells (>1 pL). Giant stomata were observed in the prostrate-leaved Satyrium bicorne (89-137 µm long), despite its relatively small genome (2C = 9 Gbp). Our results imply that climate, through selection on stomatal size, might be able to drive genome size evolution in plants. The data support the idea that plants from 'greenhouse' geological periods with large stomata might have generally had larger genome sizes when compared with extant plants, though this might not have been solely due to higher atmospheric CO2 in these periods but could also have been due to humid conditions prevailing at fossil deposit sites.

Mitogenomics reveals phylogenetic relationships of Arcoida (Mollusca, Bivalvia) and multiple independent expansions and contractions in mitochondrial genome size

Arcoida, comprising about 570 species of blood cockles, is an ecologically and economically important lineage of bivalve molluscs. Current classification of arcoids is largely based on morphology, which shows widespread homoplasy. Despite two recent studies employing multi-locus analyses with broad sampling of Arcoida, evolutionary relationships among major lineages remain controversial. Interestingly, mitochondrial genomes of several ark shell species are 2–3 times larger than those found in most bilaterians, and are among the largest bilaterian mitochondrial genomes reported to date. These results highlight the need of detailed phylogenetic study to explore evolutionary relationships within Arcoida so that the evolution of mitochondrial genome size can be understood. To this end, we sequenced 17 mitochondrial genomes and compared them with publicly available data, including those from other lineages of Arcoida with emphasis on the subclade Arcoidea species. Our phylogenetic analyses indicate that Noetiidae, Cucullaeidae and Glycymerididae are nested within a polyphyletic Arcidae. Moreover, we find multiple independent expansions and potential contractions of mitochondrial genome size, suggesting that the large mitochondrial genome is not a shared ancestral feature in Arcoida. We also examined tandem repeats and inverted repeats in non-coding regions and investigated the presence of such repeats with relation to genome size variation. Our results suggest that tandem repeats might facilitate intraspecific mitochondrial genome size variation, and that inverted repeats, which could be derived from transposons, might be responsible for mitochondrial genome expansions and contractions. We show that mitochondrial genome size in Arcoida is more dynamic than previously understood and provide insights into evolution of mitochondrial genome size variation in metazoans.