Genetic basis of transcriptome diversity in Drosophila melanogaster

Abstract

Understanding how DNA sequence variation is translated into variation for complex phenotypes has remained elusive but is essential for predicting adaptive evolution, for selecting agriculturally important animals and crops, and for personalized medicine. Gene expression may provide a link between variation in DNA sequence and organismal phenotypes, and its abundance can be measured efficiently and accurately. Here we quantified genome-wide variation in gene expression in the sequenced inbred lines of the Drosophila melanogaster Genetic Reference Panel (DGRP), increasing the annotated Drosophila transcriptome by 11%, including thousands of novel transcribed regions (NTRs). We found that 42% of the Drosophila transcriptome is genetically variable in males and females, including the NTRs, and is organized into modules of genetically correlated transcripts. We found that NTRs often were negatively correlated with the expression of protein-coding genes, which we exploited to annotate NTRs functionally. We identified regulatory variants for the mean and variance of gene expression, which have largely independent genetic control. Expression quantitative trait loci (eQTLs) for the mean, but not for the variance, of gene expression were concentrated near genes. Notably, the variance eQTLs often interacted epistatically with local variants in these genes to regulate gene expression. This comprehensive characterization of population-scale diversity of transcriptomes and its genetic basis in the DGRP is critically important for a systems understanding of quantitative trait variation.

Microenvironmental Gene Expression Plasticity Among IndividualDrosophila melanogaster

“…As expected from previous studies of gene expression using pools of individuals, we observed massive differences in gene expression due to sex (Table 1 and Table S1) (Jin et al 2001; Arbeitman et al 2002; Parisi et al 2003; Ranz et al 2003; Harbison et al 2005; Wayne et al 2007; Zhang et al 2007; Ayroles et al 2009; Huylmans and Parsch 2014; Huang et al 2015). Of the 15,674 genes detected in the experiment, 14,883, or 95%, were differentially expressed between males and females (FDR < 0.05).…”

“…Duplicate libraries prepared for 118 flies indicated that the technical effects were very small relative to the biological effects (Lin et al 2016). In addition, residual heterozygosity in chromosomal inversions does not appear to be a factor, in agreement with a recent assessment of gene expression in pooled flies of the DGRP (Huang et al 2015). Thus, the biological sources of gene expression differences among individuals are much greater than these potential technical sources.…”

“…We expected that genotype, with multiple differences in gene regulators, enhancers, and silencers, would profoundly influence gene expression, as demonstrated previously in pools of individual flies (Jin et al 2001; Harbison et al 2005; Wayne et al 2007; Ayroles et al 2009; Huang et al 2015). Indeed, most of the 15,674 annotated transcripts we detected were differentially expressed among the DGRP genotypes (Table 1 and Table S1); 10,401 (66.4% of detected genes; FDR < 0.05) of the transcripts had genetic differences, and 7148 (45.6%) of genetically variable transcripts were also expressed in a sexually dimorphic manner.…”

Evolution and plasticity of the transcriptome under temperature fluctuations in the fungal plant pathogen Zymoseptoria tritici

“…Although high, this amount of variation in Z. tritici remains comparable to former results coming from many other studies highlighting the natural variation of transcription within species, mostly using eQTL mapping ( e.g. Brem, 2002; Schadt et al, 2003; Huang et al, 2015; Zan et al, 2016; Osada et al, 2017).…”

A-to-I RNA editing uncovers hidden signals of adaptive genome evolution in animals

“…GSE67505). The expression data 492 was obtained from pooled RNA-Seq data for the DGRP2 lines, as described in the original 493 study [43]. The published expression tables are given separately for male and females in FPKM 494…”