Sex-Biased Transcriptome Evolution in Drosophila

Assis, Raquel; Zhou, Qi; Bachtrog, Doris

doi:10.1093/gbe/evs093

Cited by 183 publications

(290 citation statements)

References 43 publications

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“…We first compared their expression in wild-type ovary and testis tissues, and found higher overall abundances of splicing factors in ovary than in testis (paired Wilcox rank sum test, P = 2.98e-10), with more genes in the set displaying ovary-rather than testisbiased expression ( Figure 5A). This is particularly noteworthy because it contrasts with the general pattern of all expressed genes, with more genes displaying testis-rather than ovarybiased expression [Table S8; see also (PARISI et al 2003;ASSIS et al 2012)]. In agreement with the higher abundance of splicing factors in ovary, we also observed an overall lower IR rate in ovary than in testis ( Figure S6, P < 2.2e-16).…”

Section: The Expression Of Splicing Factors Differs Between Ovary Andsupporting

confidence: 74%

“…These sex-specific and sex-biased phenotypes partially emerge from regulatory differences in gene expression. While sex differences in gene expression are observed in several tissues, they are especially manifested in the gonads (MEIKLEJOHN et al 2003;PARISI et al 2003;ELLEGREN AND PARSCH 2007;ZHANG et al 2007;ASSIS et al 2012;PARSCH AND ELLEGREN 2013;PERRY et al 2014) and are often traced to variation in the sex chromosomes (GIBSON et al 2002;LEMOS et al 2008;SACKTON et al 2011;COOLON et al 2015). In Drosophila, the X-chromosome is relatively large with thousands of protein-coding genes, with experimental evidence confirming population genetic predictions about the consequences of X-linked variation.…”

Section: Introductionmentioning

confidence: 90%

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The Y Chromosome Modulates Splicing and Sex-Biased Intron Retention Rates in Drosophila

Wang¹,

Branco²,

Lemos³

2018

Genetics

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The Drosophila Y chromosome is a 40MB segment of mostly repetitive DNA; it harbors a handful of protein coding genes and a disproportionate amount of satellite repeats, transposable elements, and multicopy DNA arrays. Intron retention (IR) is a type of alternative splicing (AS) event by which one or more introns remain within the mature transcript. IR recently emerged as a deliberate cellular mechanism to modulate gene expression levels and has been implicated in multiple biological processes. However, the extent of sex differences in IR and the contribution of the Y chromosome to the modulation of alternative splicing and intron retention rates has not been addressed. Here we showed pervasive intron retention (IR) in the fruit fly Drosophila melanogaster with thousands of novel IR events, hundreds of which displayed extensive sex-bias.

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Section: The Expression Of Splicing Factors Differs Between Ovary Andsupporting

confidence: 74%

Section: Introductionmentioning

confidence: 90%

The Y Chromosome Modulates Splicing and Sex-Biased Intron Retention Rates in Drosophila

Wang¹,

Branco²,

Lemos³

2018

Genetics

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“…Using an FDR < 0.05 as a cutoff for genes with FPKM > 1 in at least one sample (SI Appendix, Methods and Table S1), significant sex-biased gene expression was found in 80% (10,427/ 13,050) of N. vitripennis and 76% (9,565/12,618) of N. giraulti genes (Table 1), indicating substantial sex-biased expression in a haplodiploid species with no sex chromosomes. This percentage is even greater than the proportion of sex-biased genes in Drosophila, which have qualitatively distinct sex chromosomes (31). Strikingly, extremely strong sex differences were also found in these two Nasonia species: 429 genes showed >100-fold and 60 showed >1,000-fold difference in N. vitripennis (SI Appendix, Fig.…”

Section: Resultsmentioning

confidence: 92%

Genetic and epigenetic architecture of sex-biased expression in the jewel wasps Nasonia vitripennis and giraulti

Wang

Werren

Clark

2015

Proc. Natl. Acad. Sci. U.S.A.

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There is extraordinary diversity in sexual dimorphism (SD) among animals, but little is known about its epigenetic basis. To study the epigenetic architecture of SD in a haplodiploid system, we performed RNA-seq and whole-genome bisulfite sequencing of adult females and males from two closely related parasitoid wasps, Nasonia vitripennis and Nasonia giraulti. More than 75% of expressed genes displayed significantly sex-biased expression. As a consequence, expression profiles are more similar between species within each sex than between sexes within each species. Furthermore, extremely male-and female-biased genes are enriched for totally different functional categories: male-biased genes for key enzymes in sexpheromone synthesis and female-biased genes for genes involved in epigenetic regulation of gene expression. Remarkably, just 70 highly expressed, extremely male-biased genes account for 10% of all transcripts in adult males. Unlike expression profiles, DNA methylomes are highly similar between sexes within species, with no consistent sex differences in methylation found. Therefore, methylation changes cannot explain the extensive level of sex-biased gene expression observed. Female-biased genes have smaller sequence divergence between species, higher conservation to other hymenopterans, and a broader expression range across development. Overall, female-biased genes have been recruited from genes with more conserved and broadly expressing "house-keeping" functions, whereas male-biased genes are more recently evolved and are predominately testis specific. In summary, Nasonia accomplish a striking degree of sex-biased expression without sex chromosomes or epigenetic differences in methylation. We propose that methylation provides a general signal for constitutive gene expression, whereas other sex-specific signals cause sex-biased gene expression.sex-biased expression | DNA methylation | RNA-seq | WGBS-seq | fatty acid desaturase

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“…Quantile-normalized RNA-seq data for carcass, female head, ovary, male head, testis, and accessory gland tissues of each species were obtained as described by Assis et al (50). We restricted our analysis to gene pairs in which both copies are expressed in at least one tissue [i.e., fragments per kilobase of exon per million fragments mapped (FPKM) ≥ 1 for D. melanogaster and FPKM ≥ 4 for D. pseudoobscura (50)]. These expression cutoffs were also used in our alternate classification approach, based on expression localization patterns (see Classification of Evolutionary Processes by Expression Localization Patterns).…”

Section: Methodsmentioning

confidence: 99%

Neofunctionalization of young duplicate genes in Drosophila

Assis

Bachtrog

2013

Proc. Natl. Acad. Sci. U.S.A.

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191

332

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Gene duplication is a key source of genetic innovation that plays a role in the evolution of phenotypic complexity. Although several evolutionary processes can result in the long-term retention of duplicate genes, their relative contributions in nature are unknown. Here we develop a phylogenetic approach for comparing genome-wide expression profiles of closely related species to quantify the roles of conservation, neofunctionalization, subfunctionalization, and specialization in the preservation of duplicate genes. Application of our method to pairs of young duplicates in Drosophila shows that neofunctionalization, the gain of a novel function in one copy, accounts for the retention of almost twothirds of duplicate genes. Surprisingly, novel functions nearly always originate in younger (child) copies, whereas older (parent) copies possess functions similar to those of ancestral genes. Further examination of such pairs reveals a strong bias toward RNAmediated duplication events, implicating asymmetric duplication and positive selection in the evolution of new functions. Moreover, we show that young duplicate genes are expressed primarily in testes and that their expression breadth increases over evolutionary time. This finding supports the "out-of-testes" hypothesis, which posits that testes are a catalyst for the emergence of new genes that ultimately evolve functions in other tissues. Thus, our study highlights the importance of neofunctionalization and positive selection in the retention of young duplicates in Drosophila and illustrates how duplicates become incorporated into novel functional networks over evolutionary time.G ene duplication produces two copies of an existing gene.Evolutionary theory predicts that functional redundancy of duplicate genes causes one copy to undergo a brief period of relaxed selection after duplication (1). In nearly all cases, this should result in an accumulation of deleterious mutations and pseudogenization of the copy within a few million years (2). However, most sequenced eukaryotic genomes contain many functional duplicates, some of which are hundreds of millions of years old (3-8), suggesting that duplicate genes play important roles in evolution.Four processes can result in the evolutionary preservation of duplicate genes: conservation, neofunctionalization, subfunctionalization, and specialization. Under conservation, ancestral functions are maintained in both copies, likely because increased gene dosage is beneficial (1). Under neofunctionalization, one copy retains its ancestral functions, and the other acquires a novel function (1). Under subfunctionalization, mutations damage different functions of each copy, such that both copies are required to preserve all ancestral gene functions (9, 10). Finally, under specialization, subfunctionalization and neofunctionalization act in concert, producing two copies that are functionally distinct from each other and from the ancestral gene (11). Theoretical work has shown that different conditions can result in the retention of...

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Sex-Biased Transcriptome Evolution in Drosophila

Cited by 183 publications

References 43 publications

The Y Chromosome Modulates Splicing and Sex-Biased Intron Retention Rates in Drosophila

The Y Chromosome Modulates Splicing and Sex-Biased Intron Retention Rates in Drosophila

Genetic and epigenetic architecture of sex-biased expression in the jewel wasps Nasonia vitripennis and giraulti

Neofunctionalization of young duplicate genes in Drosophila

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