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Systems genetics of single nucleotide substitutions at the Drosophila Obp56h locus

ABSTRACT: Individual variation in complex traits results from allelic variants of multiple segregating genes, which are expressed as coregulated ensembles that are modulated by the environment. Coregulated transcriptional networks around focal genes, defined as their ‘transcriptional niches’, are sensitive to genetic and environmental perturbations. Understanding how single base pair substitutions affect this complex genotype-phenotype relationship by perturbing transcriptional niches is possible in Drosophila, which allows precise control of both the genetic background and the environment. We used a two-step CRISPR-Cas9 mediated gene deletion and reinsertion strategy to generate in a common genetic background five single nucleotide substitutions in the D. melanogaster Obp56h gene that correspond to naturally occurring allelic variants. Changes in single base pairs give rise to differential, sexually dimorphic effects on a plethora of fitness traits, including viability, sex ratio, feeding behavior, starvation resistance, recovery from a chill-induced coma, response to heat shock, activity, and sleep traits. These pleiotropic effects are accompanied by sexually dimorphic shifts in the transcriptional niche of Obp56h. Pairwise comparisons between the lines show common coregulated genes along with varying numbers of transcripts unique to one or few Obp56h alleles. Gene ontology enrichment analyses indicate that fundamental cellular processes for each sex underlie the phenotypic pleiotropy revealed by the Obp56h allelic series. Furthermore, different Obp56h alleles in a common genetic background give rise to allele-specific, sexually dimorphic microenvironmental variation. The reverse genetic engineering strategy, illustrated here, can be generally applied to other genes to dissect variation in the genotype-phenotype relationship at single base pair resolution.

ORGANISM(S): Drosophila melanogaster

PROVIDER: GSE178635 | GEO | 2022/03/10

REPOSITORIES: GEO

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Project description:Sexually dimorphic traits are by definition exaggerated in one sex, which may arise from a history of sex-specific selection â in males, females, or both. If this exaggeration comes at a cost, exaggeration is expected to be greater in higher condition individuals (condition-dependent). Although studies using small numbers of morphological traits are generally supportive, this prediction has not been examined at a larger scale. We test this prediction across the trancriptome by determining the condition-dependence of sex-biased (dimorphic) gene expression. We find that high-condition populations are more sexually dimorphic in transcription than low-condition populations. High condition populations have more male-biased genes and more female-biased genes, and a greater degree of sexually dimorphic expression in these genes. Also, condition-dependence in male-biased genes was greater than in a set of unbiased genes. Interestingly, male-biased genes expressed in the testes were not more condition-dependent than those in the soma. By contrast, increased female-biased expression under high condition may be have occurred because of the greater contribution of the ovary-specific transcripts to the entire mRNA pool. We did not find any genomic signatures distinguishing the condition-dependent sex-biased genes. The degree of condition-dependent sexual dimorphism (CDSD) did not differ between the autosomes and the X-chromosome. There was only weak evidence that rates of evolution correlated with CDSD. We suggest that the sensitivity of both female-biased genes and male-biased genes to condition may be akin to the overall heightened sensitivity to condition that life-history and sexually selected traits tend to exhibit. Our results demonstrate that through condition-dependence, early life experience has dramatic effects on sexual dimorphism in the adult transcriptome. There were 8 biologically distinct samples. Each was replicated 6 times for a total of 48 biological samples on 24 arrays. There was no reference or control sample as a loop design was used. Each of the 48 samples are represented separately.

Project description:The data set submitted here contains the raw SNP genotyping data obtained from the analysis of 24 biparental segregating maize (Zea mays L.) populations and their respective parents. The processed and filtered data were used to construct genetic linkage maps which we used in our study of variation of recombination rate in maize. In sexually reproducing organisms, meiotic crossovers ensure the proper segregation of chromosomes and contribute to genetic diversity by shuffling allelic combinations. Such genetic reassortment is exploited in breeding to combine favorable alleles, and in genetic research to identify genetic factors underlying traits of interest via linkage or association-based approaches. Crossover numbers and distributions along chromosomes vary between species, but little is known about their intraspecies variation. In our study, we report on the variation of recombination rates between 22 European maize inbred lines that belong to the Dent and Flint gene pools. We genotyped 23 doubled-haploid populations derived from crosses between these lines with a 50k-SNP array and constructed high-density genetic maps, showing good correspondence with the maize B73 genome sequence assembly. By aligning each genetic map to the B73 sequence, we obtained the recombination rates along chromosomes specific to each population. We identified significant differences in recombination rates at the genome-wide, chromosome, and intrachromosomal levels between populations, as well as significant variation for genome-wide recombination rates among maize lines. Crossover interference analysis using a two-pathway modeling framework revealed a negative association between recombination rate and interference strength. To our knowledge, the present work provides the most comprehensive study on intraspecific variation of recombination rates and crossover interference strength in eukaryotes. Differences found in recombination rates will allow for selection of high or low recombining lines in crossing programs. Our methodology should pave the way for precise identification of genes controlling recombination rates in maize and other organisms.

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Systems genetics of single nucleotide substitutions at the Drosophila Obp56h locus

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