Driving Genome Size Research Articles

Genome size variation and evolution during invasive range expansion in an introduced plant.

Plants demonstrate exceptional variation in genome size across species, and their genome sizes can also vary dramatically across individuals and populations within species. This aspect of genetic variation can have consequences for traits and fitness, but few studies attributed genome size differentiation to ecological and evolutionary processes. Biological invasions present particularly useful natural laboratories to infer selective agents that might drive genome size shifts across environments and population histories. Here, we test hypotheses for the evolutionary causes of genome size variation across 14 invading populations of yellow starthistle, Centaurea solstitialis, in California, United States. We use a survey of genome sizes and trait variation to ask: (1) Is variation in genome size associated with developmental trait variation? (2) Are genome sizes smaller toward the leading edge of the expansion, consistent with selection for "colonizer" traits? Or alternatively, does genome size increase toward the leading edge of the expansion, consistent with predicted consequences of founder effects and drift? (3) Finally, are genome sizes smaller at higher elevations, consistent with selection for shorter development times? We found that 2C DNA content varied 1.21-fold among all samples, and was associated with flowering time variation, such that plants with larger genomes reproduced later, with lower lifetime capitula production. Genome sizes increased toward the leading edge of the invasion, but tended to decrease at higher elevations, consistent with genetic drift during range expansion but potentially strong selection for smaller genomes and faster development time at higher elevations. These results demonstrate how genome size variation can contribute to traits directly tied to reproductive success, and how selection and drift can shape that variation. We highlight the influence of genome size on dynamics underlying a rapid range expansion in a highly problematic invasive plant.

Characterization of genome‐wide long terminal repeat retrotransposons provide insights into trait evolution of four grapevine species

AbstractGrapevine is one of the most economically important crops in the world. Although long terminal repeat (LTR) retrotransposons are thought to have played an important role in plants, its distribution in grapevine is not clear. Here, we identified genome‐wide intact LTR retrotransposons in a total of six high‐quality grapevine genomes from Vitis vinifera L., Vitis sylvestris C.C. Gmel., Vitis riparia Michx. and Vitis amurensis Rupr. with an average of 2938 per genome. Among them, the Copia superfamily (particularly for Ale) is a major component of the LTR retrotransposon in grapevine. Insertion time and copy number analysis revealed that the expansion of 70% LTR retrotransposons concentrating on approximately 2.5 Ma was able to drive genome size variation. Phylogenetic tree and syntenic analyses showed that most LTR retrotransposons in these genomes formed and evolved after species divergence. Furthermore, the function and expression of genes inserted by LTR retrotransposons in V. vinifera (Pinot noir) and V. riparia were explored. The length and expression of genes related to starch metabolism and quinone synthesis pathway in Pinot noir and environmental adaptation pathway in V. riparia were significantly affected by LTR retrotransposon insertion. The results improve the understanding of LTR retrotransposons in grapevine genomes and provide insights for its potential contribution to grapevine trait evolution.

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.

The m6A pathway protects the transcriptome integrity by restricting RNA chimera formation in plants.

Global, segmental, and gene duplication-related processes are driving genome size and complexity in plants. Despite their evolutionary potentials, those processes can also have adverse effects on genome regulation, thus implying the existence of specialized corrective mechanisms. Here, we report that an N6-methyladenosine (m6A)-assisted polyadenylation (m-ASP) pathway ensures transcriptome integrity in Arabidopsis thaliana Efficient m-ASP pathway activity requires the m6A methyltransferase-associated factor FIP37 and CPSF30L, an m6A reader corresponding to an YT512-B Homology Domain-containing protein (YTHDC)-type domain containing isoform of the 30-kD subunit of cleavage and polyadenylation specificity factor. Targets of the m-ASP pathway are enriched in recently rearranged gene pairs, displayed an atypical chromatin signature, and showed transcriptional readthrough and mRNA chimera formation in FIP37- and CPSF30L-deficient plants. Furthermore, we showed that the m-ASP pathway can also restrict the formation of chimeric gene/transposable-element transcript, suggesting a possible implication of this pathway in the control of transposable elements at specific locus. Taken together, our results point to selective recognition of 3'-UTR m6A as a safeguard mechanism ensuring transcriptome integrity at rearranged genomic loci in plants.

Non-Mendelian assortment of homologous autosomes of different sizes in males is the ancestral state in the Caenorhabditis lineage

Organismal genome sizes vary by six orders of magnitude and appear positively correlated with organismal size and complexity. Neutral models have been proposed to explain the broad patterns of genome size variation based on organism population sizes. In the Caenorhabditis genus, hermaphrodite genomes are smaller than those of gonochoristic species. One possible driving force for this genome size difference could be non-random chromosome segregation. In Caenorhabditis elegans, chromosome assortment is non-independent and violates Mendel’s second law. In males, the shorter homologue of a heterozygous autosome pair preferentially co-segregates with the X chromosome while the longer one preferentially co-segregates with the nullo-X (O) chromosome in a process we call “skew”. Since hermaphrodites preferentially receive the shorter chromosomes and can start populations independently, their genome size would be predicted to decrease over evolutionary time. If skew is an important driver for genome size reduction in hermaphroditic Caenorhabditis species, then it should be present in all congeneric species. In this study, we tested this hypothesis and found that skew is present in all eight examined species. Our results suggest that skew is likely the ancestral state in this genus. More speculatively, skew may drive genome size patterns in hermaphroditic species in other nematodes.

The mitochondrial genomes of the acoelomorph worms Paratomella rubra, Isodiametra pulchra and Archaphanostoma ylvae

Acoels are small, ubiquitous - but understudied - marine worms with a very simple body plan. Their internal phylogeny is still not fully resolved, and the position of their proposed phylum Xenacoelomorpha remains debated. Here we describe mitochondrial genome sequences from the acoels Paratomella rubra and Isodiametra pulchra, and the complete mitochondrial genome of the acoel Archaphanostoma ylvae. The P. rubra and A. ylvae sequences are typical for metazoans in size and gene content. The larger I. pulchra mitochondrial genome contains both ribosomal genes, 21 tRNAs, but only 11 protein-coding genes. We find evidence suggesting a duplicated sequence in the I. pulchra mitochondrial genome. The P. rubra, I. pulchra and A. ylvae mitochondria have a unique genome organisation in comparison to other metazoan mitochondrial genomes. We found a large degree of protein-coding gene and tRNA overlap with little non-coding sequence in the compact P. rubra genome. Conversely, the A. ylvae and I. pulchra genomes have many long non-coding sequences between genes, likely driving genome size expansion in the latter. Phylogenetic trees inferred from mitochondrial genes retrieve Xenacoelomorpha as an early branching taxon in the deuterostomes. Sequence divergence analysis between P. rubra sampled in England and Spain indicates cryptic diversity.

Assessment of the bimodality in the distribution of bacterial genome sizes.

Bacterial genome sizes have previously been shown to exhibit a bimodal distribution. This phenomenon has prompted discussion regarding the evolutionary forces driving genome size in bacteria and its ecological significance. We investigated the level of inherent redundancy in the public database and the effect it has on the shape of the apparent bimodal distribution. Our study reveals that there is a significant bias in the genome sequencing efforts towards a certain group of species, and that correcting the bias using species nomenclature and clustering of the 16S rRNA gene, results in a unimodal rather than the previously published bimodal distribution. The true genome size distribution and its wider ecological implications will soon emerge as we are currently witnessing rapid growth in the number of sequenced genomes from diverse environmental niches across a range of habitats at an unprecedented rate.

NOVEL INSIGHT INTO EVOLUTIONARY PROCESS FROM AVERAGE GENOME SIZE IN MARINE BACTERIOPLANKTONIC BIOTA

Genome evolution is an essential force that shapes biodiversity. Genome reduction has been demonstrated in numerous microorganisms and is interpreted as a means of decreasing material cost during DNA synthesis. However, most of the previous studies have been conducted under pure-culture or endosymbiotic conditions, which greatly restrict horizontal gene transfer between microbial species. In nature, microbes frequently interact with each other and gene exchanges are quite common within the microbiota. The evolutionary trend underlying genome size is still poorly understood. The ocean provides an ideal setting for examining the evolutionary process of microbial genomes under natural conditions. We retrieved bacterial compositional information for marine bacterioplanktonic biota from the Visualization and Analysis of Microbial Population Structures database and compared their average genome size along an ocean depth gradient. The results showed that marine bacterioplanktonic biotas tend to minimize their average genome size in the course of their evolutionary processes and that niche differentiation is probably the major force driving genome size reduction. These findings provide novel insight into the understanding of the evolutionary process underlying microbial genome size and mechanisms for maintaining microbial biodiversity in nature.

Testing the large genome constraint hypothesis: plant traits, habitat and climate seasonality in Liliaceae.

The factors driving genome size evolution in Liliaceae were examined. In particular, we investigated whether species with larger genomes are confined to less stressful environments with a longer vegetative season. We tested our hypotheses by correlating the genome size with other plant traits and environmental variables. To determine the adaptive nature of the genome size, we also compared the performances of Brownian motion (BM) processes with those inferred by Ornstein-Uhlenbeck (OU) models of trait evolution. A positive correlation of genome size with plant size, mean temperature and habitat moisture and a negative correlation with altitude and precipitation seasonality were found. Models of trait evolution revealed a deviation from a drift process or BM. Instead, changes in genome size were significantly associated with precipitation regimes according to an OU process. Specifically, the evolutionary optima towards which the genome size evolves were higher for humid climates and lower for drier ones. Taken together, our results indicate that the genome size increase in Liliaceae is constrained by climate seasonality.

No evidence that sex and transposable elements drive genome size variation in evening primroses.

Genome size varies dramatically across species, but despite an abundance of attention there is little agreement on the relative contributions of selective and neutral processes in governing this variation. The rate of sex can potentially play an important role in genome size evolution because of its effect on the efficacy of selection and transmission of transposable elements (TEs). Here, we used a phylogenetic comparative approach and whole genome sequencing to investigate the contribution of sex and TE content to genome size variation in the evening primrose (Oenothera) genus. We determined genome size using flow cytometry for 30 species that vary in genetic system and find that variation in sexual/asexual reproduction cannot explain the almost twofold variation in genome size. Moreover, using whole genome sequences of three species of varying genome sizes and reproductive system, we found that genome size was not associated with TE abundance; instead the larger genomes had a higher abundance of simple sequence repeats. Although it has long been clear that sexual reproduction may affect various aspects of genome evolution in general and TE evolution in particular, it does not appear to have played a major role in genome size evolution in the evening primroses.

Metabolic ‘engines’ of flight drive genome size reduction in birds

The tendency for flying organisms to possess small genomes has been interpreted as evidence of natural selection acting on the physical size of the genome. Nonetheless, the flight-genome link and its mechanistic basis have yet to be well established by comparative studies within a volant clade. Is there a particular functional aspect of flight such as brisk metabolism, lift production or maneuverability that impinges on the physical genome? We measured genome sizes, wing dimensions and heart, flight muscle and body masses from a phylogenetically diverse set of bird species. In phylogenetically controlled analyses, we found that genome size was negatively correlated with relative flight muscle size and heart index (i.e. ratio of heart to body mass), but positively correlated with body mass and wing loading. The proportional masses of the flight muscles and heart were the most important parameters explaining variation in genome size in multivariate models. Hence, the metabolic intensity of powered flight appears to have driven genome size reduction in birds.

Co-evolution between transposable elements and their hosts: a major factor in genome size evolution?

Most models of genome size evolution emphasize changes in relative rates of and/or the efficacy of selection on insertions and deletions. However, transposable elements (TEs) are a major contributor to genome size evolution, and since they experience their own selective pressures for expansion, genome size changes may in part be driven by the dynamics of co-evolution between TEs and their hosts. Under this perspective, predictions about the conditions that allow for genome expansion may be altered. In this review, we outline the evidence for TE-host co-evolution, discuss the conditions under which these dynamics can change, and explore the possible contribution to the evolution of genome size. Aided partly by advances in our understanding of the mechanisms of TE silencing via small RNAs, there is growing evidence that the evolution of transposition rates can be important in driving genome expansion and contraction. Shifts in genome size and transposon abundance associated with interspecific hybridization and changes in mating system are consistent with an important role for transposition rate evolution, although other possible explanations persist. More understanding of the potential for the breakdown of host silencing mechanisms and/or the potential for TEs to evade host immune responses will improve our understanding of the importance of changes in TE activity in driving genome size evolution.

Sizing up Arabidopsis genome evolution

Plant genomes vary tremendously in size, even among close relatives (Bennett and Leitch, 2010). In addition, there is considerable variation in related features such as chromosome number and size, number of genes and transposable element (TE) content. There have been several attempts to shed light on both the relative importance of these contributors, and the relative role of mutation versus natural selection, in driving genome size evolution. However, our ability to understand the evolution of genome size to date has been limited, due in part to the lack of large-scale genomic information from closely related species. With the recent publication of the complete genome of the primarily self-incompatible plant Arabidopsis lyrata (Hu et al., 2011), a close relative of the workhorse of plant genetics Arabidopsis thaliana, many of these questions can now be approached with increased strength under a comparative framework.

The shrunken genome of Arabidopsis thaliana

This paper examines macro and micro-level patterns of genome size evolution in the Brassicaceae. A phylogeny of 25 relatives of Arabidopsis thaliana was reconstructed using four molecular markers under both parsimony and Bayesian methods. Reconstruction of genome size (C value) evolution as a discrete character and as a continuous character was also performed. In addition, size dynamics in small chromosomal regions were assessed by comparing genomic clones generated for Arabidopsis lyrata and for Boechera stricta to the fully sequenced genome of A. thaliana. The results reveal a sevenfold variation in genome size among the taxa investigated and that the small genome size of A. thaliana is derived. Our results also indicate that the genome is free to increase or decrease in size across these evolutionary lineages without a directional bias. These changes are accomplished by insertions and deletions at both large and small-scales occurring mostly in intergenic regions, with repetitive sequences and transposable elements implicated in genome size increases. The focus upon taxa relatively closely related to the model organism A. thaliana, and the combination of complementary approaches, allows for unique insights into the processes driving genome size changes.

Evolution of Genome Size in the Grasses

The grasses (Poaceae) exhibit marked conservation of gene content and order (synteny and colinearity), a feature that promises the extension of genomic information from one grass species to another using a unified comparative approach. Grasses also show striking differences in the size of their genomes. Since this complicates the treatment of the grass family as a model genetic system, there is need to better understand the patterns and processes that drive genome size evolution. This requires knowledge of phylogenetic relationships, especially deep branching patterns that unify the grass subfamilies. In this study, a phylogeny of 66 grass species with known genome size, most of them diploid, was assembled. The phylogeny described relationships integrated from shared and derived characteristics in molecular and morphological data and the branching order of basal lineages recently inferred from RNA structure and large‐scale chromosomal rearrangements. Evolutionary changes in genome size that exclude the effect of polyploidization were traced along the branches of the tree using parsimony methods of character state reconstruction. Most levels of change did not exceed twofold, and few exceeded threefold. The frequency of changes in genome size appears to decrease exponentially with the magnitude of change. The ratio of increases‐to‐decreases in genome size increased in the order Ehrhartoideae, PACCAD (panicoids, arundinoids, chloridoids, centothecoids, aristidoids, and danthonioids), and Pooideae clades. However, there were clear patterns of increase and decrease in all major clades, and notable genome size changes in the Pooideae and Chloridoideae subfamilies. This shows different tendencies in genome size diversification in these major grass lineages. Depending on the tracing method, the genome of the ancestor of the grass family had 3.0 to 5.2 pg DNA per 2C nucleus. Results extend early proposals that suggest genome size has both increased and decreased along grass lineages, and show that different models of character evolution imparted different frequencies and levels of change along the branches of the trees.