High intrinsic: Rate of DNA loss in Drosophila

Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, Massachusetts 02138, USA.
Nature (Impact Factor: 41.46). 12/1996; 384(6607):346-9. DOI: 10.1038/384346a0
Source: PubMed


Pseudogenes are common in mammals but virtually absent in Drosophila. All putative Drosophila pseudogenes show patterns of molecular evolution that are inconsistent with the lack of functional constraints. The absence of bona fide pseudogenes is not only puzzling, it also hampers attempts to estimate rates and patterns of neutral DNA change. The estimation problem is especially acute in the case of deletions and insertions, which are likely to have large effects when they occur in functional genes and are therefore subject to strong purifying selection. We propose a solution to this problem by taking advantage of the propensity of retrotransposable elements without long terminal repeats (non-LTR) to create non-functional, 'dead-on-arrival' copies of themselves as a common by-product of their transpositional cycle. Phylogenetic analysis of a non-LTR element, Helena, demonstrates that copies lose DNA at an unusually high rate, suggesting that lack of pseudogenes in Drosophila is the product of rampant deletion of DNA in unconstrained regions. This finding has important implications for the study of genome evolution in general and the 'C-value paradox' in particular.

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    • "For DNA loss, several mechanisms have been suggested such as transposon-mediated excision, replication slippage, and 'illegitimate recombination' (Petrov, et al. 1996, Devos, et al. 2002, Hu, et al. 2011). In our opinion, deletion-biased DSB repair seems to be the most likely cause for genome shrinkage (Kirik, et al. 2000, Puchta 2005), for several reasons: i) DSB repair is an ubiquitous requirement; ii) hypomorphic or hypermorphic mutants of single DSB repair components may result in a bias between repair pathway variants; iii) even a small bias towards either deletions or insertions can have an evolutionary impact; the more so because misrepair events in plant shoot meristems, if viable, may be transferred via germ cells to the next generation; iv) erroneous DSB repair encompasses phenomena such as transposon-mediated excision, replication slippage and illegitimate recombination, the latter for instance via the 'single strand annealing' pathway; and v) chromosome rearrangements are the result of DSB misrepair and even large interstitial deletions, or translocations resulting in dysploid chromosome number reduction, can be survived if no essential genes are lost (Schubert and Lysak 2011). "
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    ABSTRACT: The C-value paradox remains incompletely resolved after >40 yr and is exemplified by 2,350-fold variation in genome sizes of flowering plants. The carnivorous Lentibulariaceae genus Genlisea, displaying a 25-fold range of genome sizes, is a promising subject to study mechanisms and consequences of evolutionary genome size variation. Applying genomic, phylogenetic, and cytogenetic approaches, we uncovered bidirectional genome size evolution within the genus Genlisea. The Genlisea nigrocaulis Steyerm. genome (86 Mbp) has probably shrunk by retroelement silencing and deletion-biased double-strand break (DSB) repair, from an ancestral size of 400 to 800 Mbp to become one of the smallest among flowering plants. The G. hispidula Stapf genome has expanded by whole-genome duplication (WGD) and retrotransposition to 1550 Mbp. Genlisea hispidula became allotetraploid after the split from the G. nigrocaulis clade ~29 Ma. Genlisea pygmaea A. St.-Hil. (179 Mbp), a close relative of G. nigrocaulis, proved to be a recent (auto)tetraploid. Our analyses suggest a common ancestor of the genus Genlisea with an intermediate 1C value (400–800 Mbp) and subsequent rapid genome size evolution in opposite directions. Many abundant repeats of the larger genome are absent in the smaller, casting doubt on their functionality for the organism, while recurrent WGD seems to safeguard against the loss of essential elements in the face of genome shrinkage. We cannot identify any consistent differences in habitat or life strategy that correlate with genome size changes, raising the possibility that these changes may be selectively neutral.
    Full-text · Article · Sep 2015 · The Plant Genome
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    • "Simple conservation of sequence and expression provides strong validation of the physical presence of transcripts, but it does not imply function unless it is measured relative to the probability of occurrence by chance. Analysis of defective D. melanogaster transposons (Petrov et al. 1996) suggests that neutral DNA has a half-life of ;0.19 ss (see Methods). We calculated a 0.16 ss half-life for nonexpressed intergenic DNA. "
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    ABSTRACT: Accurate gene model annotation of reference genomes is critical for making them useful. The modENCODE project has improved the D. melanogaster genome annotation by using deep and diverse high-throughput data. Since transcriptional activity that has been evolutionarily conserved is likely to have an advantageous function, we have performed large-scale interspecific comparisons to increase confidence in predicted annotations. To support comparative genomics, we filled in divergence gaps in the Drosophila phylogeny by generating draft genomes for eight new species. For comparative transcriptome analysis, we generated mRNA expression profiles on 81 samples from multiple tissues and developmental stages of 15 Drosophila species, and we performed cap analysis of gene expression in D. melanogaster and D. pseudoobscura. We also describe conservation of four distinct core promoter structures composed of combinations of elements at three positions. Overall, each type of genomic feature shows a characteristic divergence rate relative to neutral models, highlighting the value of multispecies alignment in annotating a target genome that should prove useful in the annotation of other high priority genomes, especially human and other mammalian genomes that are rich in noncoding sequences. We report that the vast majority of elements in the annotation are evolutionarily conserved, indicating that the annotation will be an important springboard for functional genetic testing by the Drosophila community.
    Preview · Article · Sep 2014
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    • "In Cryptobranchus, as in plethodontid salamanders, slower rates of DNA loss reflect fewer and smaller deletion events per substitution than are found in other vertebrate taxa (Sun, Arriaza, et al. 2012). Indels 30 bp in length have long been attributed to uncharacterized errors in DNA replication and/or recombination (Petrov et al. 1996; Kvikstad et al. 2007). Recently, comparative genomic analyses have begun to leverage natural variation in indel dynamics, across both genomes and lineages , to reveal the specific mechanisms of indel formation (Kvikstad et al. 2007, 2009; Hu et al. 2011; Nam and Ellegren 2012). "
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    ABSTRACT: Among animals, genome sizes range from 20 Mb to 130 Gb, with 380-fold variation across vertebrates. Most of the largest vertebrate genomes are found in salamanders, an amphibian clade of 660 species. Thus, salamanders are an important system for studying causes and consequences of genomic gigantism. Previously, we showed that plethodontid salamander genomes accumulate higher levels of LTR retrotransposons than do other vertebrates, although the evolutionary origins of such sequences remained unexplored. We also showed that some salamanders in the family Plethodontidae have relatively slow rates of DNA loss through small insertions and deletions. Here, we present new data from Cryptobranchus alleganiensis, the hellbender. Cryptobranchus and Plethodontidae span the basal phylogenetic split within salamanders; thus, analyses incorporating these taxa can shed light on the genome of the ancestral crown salamander lineage, which underwent expansion. We show that high levels of LTR retrotransposons likely characterize all crown salamanders, suggesting that disproportionate expansion of this TE class contributed to genomic expansion. Phylogenetic and age distribution analyses of salamander LTR retrotransposons indicate that salamanders' high TE levels reflect persistence and diversification of ancestral TEs rather than horizontal transfer events. Finally, we show that relatively slow DNA loss rates through small indels likely characterize all crown salamanders, suggesting that a decreased DNA loss rate contributed to genomic expansion at the clade's base. Our identification of shared genomic features across phylogenetically distant salamanders is a first step towards identifying the evolutionary processes underlying accumulation and persistence of high levels of repetitive sequence in salamander genomes.
    Full-text · Article · Jun 2014 · Genome Biology and Evolution
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