Sequence shortening in the rodent ancestor

Laurie, Steve; Toll-Riera, Macarena; Radó-Trilla, Núria; Albà, M. Mar

doi:10.1101/gr.121897.111

Cited by 19 publications

(29 citation statements)

References 51 publications

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“…S2 and Dataset S4). Microdeletions are slightly smaller in size in human and macaque than in mouse and rat (by 0.46 bp on average), which is in agreement with a previous study (63). In summary, we observe substantial variation in the rate and size spectrum of DNA microdeletion between and within eutherian and avian orders.…”

Section: Resultssupporting

confidence: 92%

“…5A), about 3.5× higher as those for the human lineage, in agreement with previous analyses of a smaller number of mammals (29,36,37,62,63). All other mammalian lineages we analyzed exhibit microdeletion rates that are intermediate between those of human and rodents, except for the common ancestor of bats (Chiroptera), which displays the lowest microdeletion rate in our analysis.…”

Section: Resultssupporting

confidence: 91%

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Dynamics of genome size evolution in birds and mammals

Kapusta

Suh

Feschotte

2017

Proc. Natl. Acad. Sci. U.S.A.

370

358

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Genome size in mammals and birds shows remarkably little interspecific variation compared with other taxa. However, genome sequencing has revealed that many mammal and bird lineages have experienced differential rates of transposable element (TE) accumulation, which would be predicted to cause substantial variation in genome size between species. Thus, we hypothesize that there has been covariation between the amount of DNA gained by transposition and lost by deletion during mammal and avian evolution, resulting in genome size equilibrium. To test this model, we develop computational methods to quantify the amount of DNA gained by TE expansion and lost by deletion over the last 100 My in the lineages of 10 species of eutherian mammals and 24 species of birds. The results reveal extensive variation in the amount of DNA gained via lineage-specific transposition, but that DNA loss counteracted this expansion to various extents across lineages. Our analysis of the rate and size spectrum of deletion events implies that DNA removal in both mammals and birds has proceeded mostly through large segmental deletions (>10 kb). These findings support a unified "accordion" model of genome size evolution in eukaryotes whereby DNA loss counteracting TE expansion is a major determinant of genome size. Furthermore, we propose that extensive DNA loss, and not necessarily a dearth of TE activity, has been the primary force maintaining the greater genomic compaction of flying birds and bats relative to their flightless relatives.genome size evolution | DNA loss | transposable elements | amniotes | flight T he nature and relative importance of the molecular mechanisms and evolutionary forces underlying genome size variation has been the subject of intense research and debate (1-7). Variation in genome sizes may not always occur at a level where natural selection is strong enough to prevent genetic drift to determine their fate (neutral or effectively neutral variation) (3). Additionally, the fixation probability of slightly deleterious deletions or insertions would be higher in species with smaller effective population sizes, where natural selection acts less efficiently (3,8). On the other hand, a number of correlative associations between genome size and phenotypic traits, such as cell size (9, 10) and metabolic rate associated with powered flight (11, 12), suggest that natural selection and adaptive processes also shape genome size evolution. Teasing apart the relative importance of these two forces (drift and selection) requires a better understanding of the mode and processes by which DNA is gained and lost over long evolutionary periods in different taxa. Thus, establishing an integrated view of the contribution of gain and loss of DNA to genome size variation (or lack thereof) remains an important goal in genome biology (e.g., refs. 1, 2, 13, and 14).Most studies of genome size evolution have focused on taxa with extensive variation in genome sizes, such as flowering plants (15)(16)(17)(18)(19)(20), conifers (21), insects (22-...

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Section: Resultssupporting

confidence: 92%

Section: Resultssupporting

confidence: 91%

Dynamics of genome size evolution in birds and mammals

Kapusta

Suh

Feschotte

2017

Proc. Natl. Acad. Sci. U.S.A.

370

358

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“…It is consistent with the previously reported rodent lineage deletion bias (Laurie et al 2012) and demonstrates that this bias applies to transcriptional regulatory sequence to at least the same extent as protein-coding sequence (Taylor et al 2004).…”

Section: Resultssupporting

confidence: 80%

“…1D). This is consistent with reports of genome-wide excess deletions early in the rodent lineage (Laurie et al 2012). The deletion excess in rodents may also explain more subtle differences between human and mouse promoter evolution.…”

Section: Frequent Promoter Turnover In Mouse and Humansupporting

confidence: 81%

The frequent evolutionary birth and death of functional promoters in mouse and human

et al. 2015

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Promoters are central to the regulation of gene expression. Changes in gene regulation are thought to underlie much of the adaptive diversification between species and phenotypic variation within populations. In contrast to earlier work emphasizing the importance of enhancer evolution and subtle sequence changes at promoters, we show that dramatic changes such as the complete gain and loss (collectively, turnover) of functional promoters are common. Using quantitative measures of transcription initiation in both humans and mice across 52 matched tissues, we discriminate promoter sequence gains from losses and resolve the lineage of changes. We also identify expression divergence and functional turnover between orthologous promoters, finding only the latter is associated with local sequence changes. Promoter turnover has occurred at the majority (>56%) of protein-coding genes since humans and mice diverged. Tissue-restricted promoters are the most evolutionarily volatile where retrotransposition is an important, but not the sole, source of innovation. There is considerable heterogeneity of turnover rates between promoters in different tissues, but the consistency of these in both lineages suggests that the same biological systems are similarly inclined to transcriptional rewiring. The genes affected by promoter turnover show evidence of adaptive evolution. In mice, promoters are primarily lost through deletion of the promoter containing sequence, whereas in humans, many promoters appear to be gradually decaying with weak transcriptional output and relaxed selective constraint. Our results suggest that promoter gain and loss is an important process in the evolutionary rewiring of gene regulation and may be a significant source of phenotypic diversification.

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“…We have previously found that, in alignments of orthologous mammalian proteins, both amino acid tandem repeats and LCRs are more often associated with insertions than with deletions [27], suggesting that repetitive regions have a greater tendency to expand than to contract. The accumulation of certain LCRs over time will depend on the intrinsic rate of slippage of the triplets encoding the underlying amino acid repeats, as well as the strength and mode of selection acting on the LCRs.…”

Section: Introductionmentioning

confidence: 99%

Dissecting the role of low-complexity regions in the evolution of vertebrate proteins

Radó-Trilla

Albà

2012

BMC Evol Biol

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BackgroundLow-complexity regions (LCRs) in proteins are tracts that are highly enriched in one or a few amino acids. Given their high abundance, and their capacity to expand in relatively short periods of time through replication slippage, they can greatly contribute to increase protein sequence space and generate novel protein functions. However, little is known about the global impact of LCRs on protein evolution.ResultsWe have traced back the evolutionary history of 2,802 LCRs from a large set of homologous protein families from H.sapiens, M.musculus, G.gallus, D.rerio and C.intestinalis. Transcriptional factors and other regulatory functions are overrepresented in proteins containing LCRs. We have found that the gain of novel LCRs is frequently associated with repeat expansion whereas the loss of LCRs is more often due to accumulation of amino acid substitutions as opposed to deletions. This dichotomy results in net protein sequence gain over time. We have detected a significant increase in the rate of accumulation of novel LCRs in the ancestral Amniota and mammalian branches, and a reduction in the chicken branch. Alanine and/or glycine-rich LCRs are overrepresented in recently emerged LCR sets from all branches, suggesting that their expansion is better tolerated than for other LCR types. LCRs enriched in positively charged amino acids show the contrary pattern, indicating an important effect of purifying selection in their maintenance.ConclusionWe have performed the first large-scale study on the evolutionary dynamics of LCRs in protein families. The study has shown that the composition of an LCR is an important determinant of its evolutionary pattern.

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Sequence shortening in the rodent ancestor

Cited by 19 publications

References 51 publications

Dynamics of genome size evolution in birds and mammals

Dynamics of genome size evolution in birds and mammals

The frequent evolutionary birth and death of functional promoters in mouse and human

Dissecting the role of low-complexity regions in the evolution of vertebrate proteins

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