The Drosophila early ovarian transcriptome provides insight to the molecular causes of recombination rate variation across genomes

Abstract

BackgroundEvidence in yeast indicates that gene expression is correlated with recombination activity and double-strand break (DSB) formation in some hotspots. Studies of nucleosome occupancy in yeast and mice also suggest that open chromatin influences the formation of DSBs. In Drosophila melanogaster, high-resolution recombination maps show an excess of DSBs within annotated transcripts relative to intergenic sequences. The impact of active transcription on recombination landscapes, however, remains unexplored in a multicellular organism. We then investigated the transcription profile during early meiosis in D. melanogaster females to obtain a glimpse at the relevant transcriptional dynamics during DSB formation, and test the specific hypothesis that DSBs preferentially target transcriptionally active genomic regions.ResultsOur study of transcript profiles of early- and late-meiosis using mRNA-seq revealed, 1) significant differences in gene expression, 2) new genes and exons, 3) parent-of-origin effects on transcription in early-meiosis stages, and 4) a nonrandom genomic distribution of transcribed genes. Importantly, genomic regions that are more actively transcribed during early meiosis show higher rates of recombination, and we ruled out DSB preference for genic regions that are not transcribed.ConclusionsOur results provide evidence in a multicellular organism that transcription during the initial phases of meiosis increases the likelihood of DSB and give insight into the molecular determinants of recombination rate variation across the D. melanogaster genome. We propose that a model where variation in gene expression plays a role altering the recombination landscape across the genome could provide a molecular, heritable and plastic mechanism to observed patterns of recombination variation, from the high level of intra-specific variation to the known influence of environmental factors and stress conditions.

Whole-Genome Analysis of Individual Meiotic Events in Drosophila melanogaster Reveals That Noncrossover Gene Conversions Are Insensitive to Interference and the Centromere Effect

“…Analyzing our current dataset, we detected no motifs enriched over background using 201 of the SCO events defined by two SNPs ≤500 bp apart ( Figure S6 ). This finding suggests that either several motifs may be associated with COs, as reported by Comeron et al (2012) , or that crossovers in D. melanogaster may be associated with open chromatin and transcription in early meiosis ( Adrian and Comeron 2013 ). Either one of these possibilities would make a true crossover-associated motif difficult to detect in a dataset of this size.…”

Whole‐genome patterns of linkage disequilibrium across flycatcher populations clarify the causes and consequences of fine‐scale recombination rate variation in birds

“…Different recombination intensities at hotspots have been reported in three commercial chicken breeds, where similar associations between recombination and genomic features were observed (Pengelly et al., ). One possible explanation for the variation in recombination intensity at hotspots in species without PRDM9 is that differences in gene expression during meiosis results in differences in the likelihood of DSB and thereby recombination frequency between individuals and between species (Adrian & Comeron, ; Petes, ). In the next section, we further discuss a possible mechanistic link between location of recombination hotspots and regions of transcription regulation, the epigenetic modifications of which are inherently related to gene expression.…”

Genomic correlates of recombination rate and its variability across eight recombination maps in the western honey bee (Apis mellifera L.)

“…This interpretation also fits most of the motifs identified in previous studies [ 25 , 26 ]. Any particular motif might provide specific binding sites for factors that facilitate chromatin access for the recombination initiation factors, resulting in recombination hotspots [ 22 , 37 ]. However, the honey bee genome seems to be devoid of distinct hotspots [ 25 ], corroborating our interpretation that no specific, cis-acting motifs control recombination rate in the honey bee genome.…”

“…The GC content of the honey bee genome is only 33% on average with a strong bimodal distribution ranging from 10-70% [ 20 ] and genes are overly abundant in genome regions with lower than average GC content [ 21 ]. Thus, DNA structure and accessibility may be one mechanistic explanation [ 22 ]. Quantitative or qualitative differences in the recombination apparatus may also cause the overall excess of recombination in honey bees.…”