New Genes in
            <i>Drosophila</i>
            Quickly Become Essential

Chen, Sidi; Zhang, Yong E.; Long, Manyuan

doi:10.1126/science.1196380

Cited by 271 publications

(375 citation statements)

References 24 publications

(36 reference statements)

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“…Remarkably, among testis-specific lncRNAs, the proportion of functional lncRNAs was similar along the sampled evolutionary ages (Supplemental Table S2), suggesting that, as in the formation of essential genes (Chen et al 2010), a constant proportion of young lncRNAs quickly acquire important functions. Furthermore, although our analysis was limited to testis-biased lncRNAs, we hypothesize that across the entire pool of lncRNAs, functional sequences may be likely to accumulate in a stationary tempo and maintained at a constant proportion, around 30%.…”

Section: Functionality May Be Only Accumulated Within a Constant Propmentioning

confidence: 98%

“…6A), we observed a constant fraction of functional ones (∼35%) within each evolutionary age group (Supplemental Table S2), including old (>40 million years ago [Mya]) and young RNAs. A previous study found that ∼30% of new protein-coding genes quickly become essential (Chen et al 2010). In addition, we investigated the sequence conservation of all surveyed lncRNAs and compared the conservation of the RNAs with that of protein-coding genes.…”

Section: Cold Spring Harbor Laboratory Press On May 12 2018 -Publishmentioning

confidence: 99%

“…All lncRNAs emerging more than 40 million years ago were regarded as old lncRNAs (Chen et al 2010), and the young lncRNAs were further divided into two or three age groups to calculate the relative proportion of functional lncRNAs and study the emergence of lncRNA functionalization. Sequence conservation was assessed by PhastCons score.…”

Section: Evolutionary Age and Sequence Conservation Analysis Of Lncrnasmentioning

confidence: 99%

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Critical roles of long noncoding RNAs in Drosophila spermatogenesis

et al. 2016

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Long noncoding RNAs (lncRNAs), a recently discovered class of cellular RNAs, play important roles in the regulation of many cellular developmental processes. Although lncRNAs have been systematically identified in various systems, most of them have not been functionally characterized in vivo in animal models. In this study, we identified 128 testis-specific Drosophila lncRNAs and knocked out 105 of them using an optimized three-component CRISPR/Cas9 system. Among the lncRNA knockouts, 33 (31%) exhibited a partial or complete loss of male fertility, accompanied by visual developmental defects in late spermatogenesis. In addition, six knockouts were fully or partially rescued by transgenes in a trans configuration, indicating that those lncRNAs primarily work in trans. Furthermore, gene expression profiles for five lncRNA mutants revealed that testis-specific lncRNAs regulate global gene expression, orchestrating late male germ cell differentiation. Compared with coding genes, the testis-specific lncRNAs evolved much faster. Moreover, lncRNAs of greater functional importance exhibited higher sequence conservation, suggesting that they are under constant evolutionary selection. Collectively, our results reveal critical functions of rapidly evolving testis-specific lncRNAs in late Drosophila spermatogenesis.

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Section: Functionality May Be Only Accumulated Within a Constant Propmentioning

confidence: 98%

Section: Cold Spring Harbor Laboratory Press On May 12 2018 -Publishmentioning

confidence: 99%

Section: Evolutionary Age and Sequence Conservation Analysis Of Lncrnasmentioning

confidence: 99%

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Critical roles of long noncoding RNAs in Drosophila spermatogenesis

et al. 2016

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“…Matches with identity ≥50%, length ≥35%, and significance <10 −3 were kept, and gene families containing more than two copies were removed. D. melanogaster pairs were supplemented with those from Chen et al (49). 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).…”

Section: Methodsmentioning

confidence: 99%

Neofunctionalization of young duplicate genes in Drosophila

Assis

Bachtrog

2013

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

183

331

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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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“…More recently, Chen et al [21] reported that a significant fraction of new genes in the Drosophila genus are essential, despite their relatively recent appearance. Many of these ''new'' genes are actually chimeric; products of either illegitimate recombination or retroposition.…”

Section: Domain Shuffling Goes Systems Biologymentioning

confidence: 99%

Domain shuffling and the increasing complexity of biological networks

Souza

2012

BioEssays

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New Genes in Drosophila Quickly Become Essential

Cited by 271 publications

References 24 publications

Critical roles of long noncoding RNAs in Drosophila spermatogenesis

Critical roles of long noncoding RNAs in Drosophila spermatogenesis

Neofunctionalization of young duplicate genes in Drosophila

Domain shuffling and the increasing complexity of biological networks

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