Dataset Information

Alternative Splicing within and between Drosophila Species, Sexes, Tissues, and Developmental Stages.

ABSTRACT: Alternative pre-mRNA splicing ("AS") greatly expands proteome diversity, but little is known about the evolutionary landscape of AS in Drosophila and how it differs between embryonic and adult stages or males and females. Here we study the transcriptomes from several tissues and developmental stages in males and females from four species across the Drosophila genus. We find that 20-37% of multi-exon genes are alternatively spliced. While males generally express a larger number of genes, AS is more prevalent in females, suggesting that the sexes adopt different expression strategies for their specialized function. While the number of total genes expressed increases during early embryonic development, the proportion of expressed genes that are alternatively spliced is highest in the very early embryo, before the onset of zygotic transcription. This indicates that females deposit a diversity of isoforms into the egg, consistent with abundant AS found in ovary. Cluster analysis by gene expression ("GE") levels shows mostly stage-specific clustering in embryonic samples, and tissue-specific clustering in adult tissues. Clustering embryonic stages and adult tissues based on AS profiles results in stronger species-specific clustering, suggesting that diversification of splicing contributes to lineage-specific evolution in Drosophila. Most sex-biased AS found in flies is due to AS in gonads, with little sex-specific splicing in somatic tissues.

SUBMITTER: Gibilisco L

PROVIDER: S-EPMC5147784 | biostudies-literature | 2016 Dec

REPOSITORIES: biostudies-literature

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Alternative Splicing within and between Drosophila Species, Sexes, Tissues, and Developmental Stages.

Gibilisco Lauren L Zhou Qi Q Mahajan Shivani S Bachtrog Doris D

PLoS genetics 20161209 12

Alternative pre-mRNA splicing ("AS") greatly expands proteome diversity, but little is known about the evolutionary landscape of AS in Drosophila and how it differs between embryonic and adult stages or males and females. Here we study the transcriptomes from several tissues and developmental stages in males and females from four species across the Drosophila genus. We find that 20-37% of multi-exon genes are alternatively spliced. While males generally express a larger number of genes, AS is mo ...[more]

PMID: 27935948

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Project description:This is a prepublication dataset that should change as updates are made to the underling genomes and annotations. Additional samples may be deposited and some samples may fail quality control. Please contact Haiwang Yang <haiwang.yang@nih.gov> for details. The RNA-seq data set contains the transcriptional profiling of eight sexed tissue types (head, thorax, carcass, abdomen w/o gonad, gonad, other reproductive tract, genitalia, and digestive system) and/or whole adult flies from five strains of Drosophila grimshawi, two strains of D. silvestris, and one strain each of D. hemipeza, D. heteroneura, and D. hawaiiensis. Samples were collected in duplicate to quadruplicate from sexually mature sexed adults (4-5 weeks post eclosion), which had been allowed to freely mate. Single-end stranded 76bp PolyA+ RNA-seq was performed on all samples. Libraries were multiplexed with indexed adaptors, and some were also prepared as mixed libraries with RNA from genetically distant species: Drosophila melanogaster (GSE81142) and Anopheles stephensi (GEO entry in preparation). All whole adult samples were prepared from single flies. Tissues were pooled from 3-5 individuals depending on the size of both the tissue and the species. For the G1 strain (reference assembly strain) of D. grimshawi, we profiled seven adult tissues for each sex in addition to whole flies. Samples were whole fly (one fly per sample), head (5 flies), thorax (5 flies), abdomen w/o gonad (5 flies), gonad (testes or ovaries) (5 flies), other reproductive tract (accessory gland and male reproductive duct or female spermatheca and oviduct; 10 flies per sample), genitalia (10 flies), and digestive system (proventriculus, crop, salivary gland, gut, and renal tubule; 5 flies). We prepared sexed single fly whole body samples in quadruplicate for ZA27Z2, ZA27Z3, and Mo010 strains of D. grimshawi. We also prepared sex-specific head, carcass, gonad, other reproductive tract with genitalia with duplicate for Wm1041 strain of D. grimshawi and other species - D. silvestris (Y11R6 and U26B9 strains), D. hemipeza (W40B14 strain), D. heteroneura (W48B6 strain), and D. hawaiiensis (Y17P5 strain). We used reduced number of flies for the non-grimshawi species (i.e., 3 heads, gonads or carcasses per sample, and 6 reproductive tracts plus genitalia per sample).

Project description:BackgroundDynamic activation and inactivation of gene regulatory DNA produce the expression changes that drive the differentiation of cellular lineages. Identifying regulatory regions active during developmental transitions is necessary to understand how the genome specifies complex developmental programs and how these processes are disrupted in disease. Gene regulatory dynamics are mediated by many factors, including the binding of transcription factors (TFs) and the methylation and acetylation of DNA and histones. Genome-wide maps of TF binding and DNA and histone modifications have been generated for many cellular contexts; however, given the diversity and complexity of animal development, these data cover only a small fraction of the cellular and developmental contexts of interest. Thus, there is a need for methods that use existing epigenetic and functional genomics data to analyze the thousands of contexts that remain uncharacterized.ResultsTo investigate the utility of histone modification data in the analysis of cellular contexts without such data, I evaluated how well genome-wide H3K27ac and H3K4me1 data collected in different developmental stages, tissues, and species were able to predict experimentally validated heart enhancers active at embryonic day 11.5 (E11.5) in mouse. Using a machine-learning approach to integrate the data from different contexts, I found that E11.5 heart enhancers can often be predicted accurately from data from other contexts, and I quantified the contribution of each data source to the predictions. The utility of each dataset correlated with nearness in developmental time and tissue to the target context: data from late developmental stages and adult heart tissues were most informative for predicting E11.5 enhancers, while marks from stem cells and early developmental stages were less informative. Predictions based on data collected in non-heart tissues and in human hearts were better than random, but worse than using data from mouse hearts.ConclusionsThe ability of these algorithms to accurately predict developmental enhancers based on data from related, but distinct, cellular contexts suggests that combining computational models with epigenetic data sampled from relevant contexts may be sufficient to enable functional characterization of many cellular contexts of interest.

Dataset Information

Alternative Splicing within and between Drosophila Species, Sexes, Tissues, and Developmental Stages.

Publications

Alternative Splicing within and between Drosophila Species, Sexes, Tissues, and Developmental Stages.

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