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Predictive Models of Recombination Rate Variation across the Drosophila melanogaster Genome.

ABSTRACT: In all eukaryotic species examined, meiotic recombination, and crossovers in particular, occur non-randomly along chromosomes. The cause for this non-random distribution remains poorly understood but some specific DNA sequence motifs have been shown to be enriched near crossover hotspots in a number of species. We present analyses using machine learning algorithms to investigate whether DNA motif distribution across the genome can be used to predict crossover variation in Drosophila melanogaster, a species without hotspots. Our study exposes a combinatorial non-linear influence of motif presence able to account for a significant fraction of the genome-wide variation in crossover rates at all genomic scales investigated, from 20% at 5-kb to almost 70% at 2,500-kb scale. The models are particularly predictive for regions with the highest and lowest crossover rates and remain highly informative after removing sub-telomeric and -centromeric regions known to have strongly reduced crossover rates. Transcriptional activity during early meiosis and differences in motif use between autosomes and the X chromosome add to the predictive power of the models. Moreover, we show that population-specific differences in crossover rates can be partly explained by differences in motif presence. Our results suggest that crossover distribution in Drosophila is influenced by both meiosis-specific chromatin dynamics and very local constitutive open chromatin associated with DNA motifs that prevent nucleosome stabilization. These findings provide new information on the genetic factors influencing variation in recombination rates and a baseline to study epigenetic mechanisms responsible for plastic recombination as response to different biotic and abiotic conditions and stresses.

SUBMITTER: Adrian AB

PROVIDER: S-EPMC5010912 | biostudies-literature | 2016 Sep

REPOSITORIES: biostudies-literature

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Predictive Models of Recombination Rate Variation across the Drosophila melanogaster Genome.

Adrian Andrew B AB Corchado Johnny Cruz JC Comeron Josep M JM

Genome biology and evolution 20160902 8

In all eukaryotic species examined, meiotic recombination, and crossovers in particular, occur non-randomly along chromosomes. The cause for this non-random distribution remains poorly understood but some specific DNA sequence motifs have been shown to be enriched near crossover hotspots in a number of species. We present analyses using machine learning algorithms to investigate whether DNA motif distribution across the genome can be used to predict crossover variation in Drosophila melanogaster ...[more]

PMID: 27492232

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Project description:Estimating fine-scale recombination maps of Drosophila from population genomic data is a challenging problem, in particular because of the high background recombination rate. In this paper, a new computational method is developed to address this challenge. Through an extensive simulation study, it is demonstrated that the method allows more accurate inference, and exhibits greater robustness to the effects of natural selection and noise, compared to a well-used previous method developed for studying fine-scale recombination rate variation in the human genome. As an application, a genome-wide analysis of genetic variation data is performed for two Drosophila melanogaster populations, one from North America (Raleigh, USA) and the other from Africa (Gikongoro, Rwanda). It is shown that fine-scale recombination rate variation is widespread throughout the D. melanogaster genome, across all chromosomes and in both populations. At the fine-scale, a conservative, systematic search for evidence of recombination hotspots suggests the existence of a handful of putative hotspots each with at least a tenfold increase in intensity over the background rate. A wavelet analysis is carried out to compare the estimated recombination maps in the two populations and to quantify the extent to which recombination rates are conserved. In general, similarity is observed at very broad scales, but substantial differences are seen at fine scales. The average recombination rate of the X chromosome appears to be higher than that of the autosomes in both populations, and this pattern is much more pronounced in the African population than the North American population. The correlation between various genomic features-including recombination rates, diversity, divergence, GC content, gene content, and sequence quality-is examined using the wavelet analysis, and it is shown that the most notable difference between D. melanogaster and humans is in the correlation between recombination and diversity.

Project description:Meiotic recombination is a fundamental evolutionary process. It not only generates diversity, but influences the efficacy of natural selection and genome evolution. There can be significant heterogeneity in recombination rates within and between species, however this variation is not well understood outside of a few model taxa, particularly in forest trees. Eucalypts are forest trees of global economic importance, and dominate many Australian ecosystems. We studied recombination rate in Eucalyptus globulus using genetic linkage maps constructed in 10 unrelated individuals, and markers anchored to the Eucalyptus reference genome. This experimental design provided the replication to study whether recombination rate varied between individuals and chromosomes, and allowed us to study the genomic attributes and population genetic parameters correlated with this variation.Recombination rate varied significantly between individuals (range?=?2.71 to 3.51 centimorgans/megabase [cM/Mb]), but was not significantly influenced by sex or cross type (F1 vs. F2). Significant differences in recombination rate between chromosomes were also evident (range?=?1.98 to 3.81 cM/Mb), beyond those which were due to variation in chromosome size. Variation in chromosomal recombination rate was significantly correlated with gene density (r?=?0.94), GC content (r?=?0.90), and the number of tandem duplicated genes (r?=?-0.72) per chromosome. Notably, chromosome level recombination rate was also negatively correlated with the average genetic diversity across six species from an independent set of samples (r?=?-0.75).The correlations with genomic attributes are consistent with findings in other taxa, however, the direction of the correlation between diversity and recombination rate is opposite to that commonly observed. We argue this is likely to reflect the interaction of selection and specific genome architecture of Eucalyptus. Interestingly, the differences amongst chromosomes in recombination rates appear stable across Eucalyptus species. Together with the strong correlations between recombination rate and features of the Eucalyptus reference genome, we maintain these findings provide further evidence for a broad conservation of genome architecture across the globally significant lineages of Eucalyptus.

Dataset Information

Predictive Models of Recombination Rate Variation across the Drosophila melanogaster Genome.

Publications

Predictive Models of Recombination Rate Variation across the Drosophila melanogaster Genome.

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