Large-scale DNA editing of retrotransposons accelerates mammalian genome evolution

Carmi, Shai; Church, George M.; Levanon, Erez Y.

doi:10.1038/ncomms1525

Cited by 45 publications

(58 citation statements)

References 50 publications

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“…DNA and RNA editing of retroelements enhances intra-and interspecies diversity. We screened the BMR genome and transcriptome for these, making BMR one of the first organisms to be comprehensively analysed for both types of editing, preceded only by human and mouse 51 .…”

Section: Resultsmentioning

confidence: 99%

Genome-wide adaptive complexes to underground stresses in blind mole rats Spalax

Fang¹,

Nevo²,

Han³

et al. 2014

Nat Commun

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134

148

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The blind mole rat (BMR), Spalax galili, is an excellent model for studying mammalian adaptation to life underground and medical applications. The BMR spends its entire life underground, protecting itself from predators and climatic fluctuations while challenging it with multiple stressors such as darkness, hypoxia, hypercapnia, energetics and high pathonecity. Here we sequence and analyse the BMR genome and transcriptome, highlighting the possible genomic adaptive responses to the underground stressors. Our results show high rates of RNA/DNA editing, reduced chromosome rearrangements, an over-representation of short interspersed elements (SINEs) probably linked to hypoxia tolerance, degeneration of vision and progression of photoperiodic perception, tolerance to hypercapnia and hypoxia and resistance to cancer. The remarkable traits of the BMR, together with its genomic and transcriptomic information, enhance our understanding of adaptation to extreme environments and will enable the utilization of BMR models for biomedical research in the fight against cancer, stroke and cardiovascular diseases.

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Section: Resultsmentioning

confidence: 99%

Genome-wide adaptive complexes to underground stresses in blind mole rats Spalax

Fang¹,

Nevo²,

Han³

et al. 2014

Nat Commun

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134

148

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“…Experiments have shown that the APOBEC3 family can actively inhibit retrotransposition of LTR retroelements in yeasts, mice, and humans (42, 61-63, 77, 78), but whether the LTR elements have evolved or become inactivated from mutations by APOBEC3s is unclear. What is known so far is that a few HERV-K sequences contain the footprint of the G-to-A mutation induced by hA3G only (79). Interestingly, in a recent communication by Carmi et al (79), pairwise comparison of retroelement genomes has identified sequences with clusters of Gto-A mutations that have been attributed by the authors to the APOBEC3 enzymes.…”

Section: Figmentioning

confidence: 99%

Footprint of APOBEC3 on the Genome of Human Retroelements

Anwar

Davenport

Ebrahimi

2013

J Virol

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Almost half of the human genome is composed of transposable elements. The genomic structures and life cycles of some of these elements suggest they are a result of waves of retroviral infection and transposition over millions of years. The reduction of retrotransposition activity in primates compared to that in nonprimates, such as mice, has been attributed to the positive selection of several antiretroviral factors, such as apolipoprotein B mRNA editing enzymes. Among these, APOBEC3G is known to mutate G to A within the context of GG in the genome of endogenous as well as several exogenous retroelements (the underlining marks the G that is mutated). On the other hand, APOBEC3F and to a lesser extent other APOBEC3 members induce G-to-A changes within the nucleotide GA. It is known that these enzymes can induce deleterious mutations in the genome of retroviral sequences, but the evolution and/or inactivation of retroelements as a result of mutation by these proteins is not clear. Here, we analyze the mutation signatures of these proteins on large populations of long interspersed nuclear element (LINE), short interspersed nuclear element (SINE), and endogenous retrovirus (ERV) families in the human genome to infer possible evolutionary pressure and/or hypermutation events. Sequence context dependency of mutation by APOBEC3 allows investigation of the changes in the genome of retroelements by inspecting the depletion of G and enrichment of A within the APOBEC3 target and product motifs, respectively. Analysis of approximately 22,000 LINE-1 (L1), 24,000 SINE Alu, and 3,000 ERV sequences showed a footprint of GG¡AG mutation by APOBEC3G and GA¡AA mutation by other members of the APOBEC3 family (e.g., APOBEC3F) on the genome of ERV-K and ERV-1 elements but not on those of ERV-L, LINE, or SINE.

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“…Because sharply divergent geological, edaphic, climatic, and biotic interfaces abound in nature, we conclude that SS may be a common model of the origin of new species, as envisaged by Darwin. during reverse transcription (among other mechanisms). In some cases, DNA-edited elements successfully enter the genome despite being hypermutated, containing a series of G-to-A mutations (15,16). These sequences enhance genomic diversity and, therefore, increase the potential of developing new traits.…”

mentioning

confidence: 99%

Transcriptome, genetic editing, and microRNA divergence substantiate sympatric speciation of blind mole rat, Spalax

Wang

Knisbacher³

et al. 2016

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

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Incipient sympatric speciation in blind mole rat, Spalax galili, in Israel, caused by sharp ecological divergence of abutting chalkbasalt ecologies, has been proposed previously based on mitochondrial and whole-genome nuclear DNA. Here, we present new evidence, including transcriptome, DNA editing, microRNA, and codon usage, substantiating earlier evidence for adaptive divergence in the abutting chalk and basalt populations. Genetic divergence, based on the previous and new evidence, is ongoing despite restricted gene flow between the two populations. The principal component analysis, neighbor-joining tree, and genetic structure analysis of the transcriptome clearly show the clustered divergent two mole rat populations. Gene-expression level analysis indicates that the population transcriptome divergence is displayed not only by soil divergence but also by sex. Gene ontology enrichment of the differentially expressed genes from the two abutting soil populations highlights reproductive isolation. Alternative splicing variation of the two abutting soil populations displays two distinct splicing patterns. L-shaped F ST distribution indicates that the two populations have undergone divergence with gene flow. Transcriptome divergent genes highlight neurogenetics and nutrition characterizing the chalk population, and energetics, metabolism, musculature, and sensory perception characterizing the abutting basalt population. Remarkably, microRNAs also display divergence between the two populations. The GC content is significantly higher in chalk than in basalt, and stress-response genes mostly prefer nonoptimal codons. The multiple lines of evidence of ecologicalgenomic and genetic divergence highlight that natural selection overrules the gene flow between the two abutting populations, substantiating the sharp ecological chalk-basalt divergence driving sympatric speciation.natural selection | ecological adaptive speciation | DNA editing | microRNA regulation | nonoptimal codon usage

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Large-scale DNA editing of retrotransposons accelerates mammalian genome evolution

Cited by 45 publications

References 50 publications

Genome-wide adaptive complexes to underground stresses in blind mole rats Spalax

Genome-wide adaptive complexes to underground stresses in blind mole rats Spalax

Footprint of APOBEC3 on the Genome of Human Retroelements

Transcriptome, genetic editing, and microRNA divergence substantiate sympatric speciation of blind mole rat, Spalax

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