Rapid evolution of expression and regulatory divergences after yeast gene duplication

Gu, Xun; Zhang, Zhongqi; Huang, Wei

doi:10.1073/pnas.0409186102

Cited by 171 publications

(153 citation statements)

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“…Previous studies comparing gene expression levels of duplicate genes revealed that expression divergence between copies occurs rapidly (31)(32)(33)(34)(35)(36)(37)(38) and can be asymmetric (32,35,38). However, our analysis is unique in that it uses expression data and phylogenetic relationships among genes to explicitly classify the evolutionary processes underlying the retention of duplicates on a genome-wide scale.…”

Section: Discussionmentioning

confidence: 99%

Neofunctionalization of young duplicate genes in Drosophila

Assis

Bachtrog

2013

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

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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Section: Discussionmentioning

confidence: 99%

Neofunctionalization of young duplicate genes in Drosophila

Assis

Bachtrog

2013

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

191

332

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“…In this regard, diverse authors have proposed that while paralogues may retain similar functionality, gene expression rapidly diverges immediately after duplication events (Gu et al, , 2002Li et al, 2005), implying that alterations in gene expression precede potential changes in function. Furthermore, it has been postulated that paralogous genes which diverge in function contribute to evolutionary innovation at a biochemical level (Evangelisti & Wagner, 2004;Gu et al, 2005Gu et al, , 2002Zhang et al, 1998). In order to corroborate these observations, we analysed the metabolic divergence of paralogous genes.…”

Section: Databasesmentioning

confidence: 90%

New insights into the regulatory networks of paralogous genes in bacteria

et al. 2010

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Extensive genomic studies on gene duplication in model organisms such as Escherichia coli and Saccharomyces cerevisiae have recently been undertaken. In these models, it is commonly considered that a duplication event may include a transcription factor (TF), a target gene, or both. Following a gene duplication episode, varying scenarios have been postulated to describe the evolution of the regulatory network. However, in most of these, the TFs have emerged as the most important and in some cases the only factor shaping the regulatory network as the organism responds to a natural selection process, in order to fulfil its metabolic needs. Recent findings concerning the regulatory role played by elements other than TFs have indicated the need to reassess these early models. Thus, we performed an exhaustive review of paralogous gene regulation in E. coli and Bacillus subtilis based on published information, available in the NCBI PubMed database and in well-established regulatory databases. Our survey reinforces the notion that despite TFs being the most prominent components shaping the regulatory networks, other elements are also important. These include small RNAs, riboswitches, RNA-binding proteins, sigma factors, protein-protein interactions and DNA supercoiling, which modulate the expression of genes involved in particular metabolic processes or induce a more complex response in terms of the regulatory networks of paralogous genes in an integrated interplay with TFs. IntroductionGene duplication is one of the main sources of functional divergence in organisms (Babu et al., 2004;Conant & Wolfe, 2008;Gelfand, 2006;Lynch & Conery, 2000;Teichmann & Babu, 2004). In order to fulfil an organism's metabolic needs, selection processes modify the regulation of the paralogous gene copies, taking advantage of a repertoire of new functions. Duplication events may include genes coding for transcription factors (TFs), permitting a more versatile adaptation of the functional diversity gained from the duplication of structural genes. Different aspects of the evolution of the regulatory networks of paralogous genes have been examined, including the co-evolution of the upstream regulatory regions and their corresponding TFs; the likely consequences of gain, loss, and replacement of TFs in the regulatory networks of paralogous genes (Gelfand, 2006;Teichmann & Babu, 2004); and also the topological and dynamic properties of the regulatory networks (Babu et al., 2006;Balaji et al., 2007; Luscombe et al., 2004). This review will consider the fascinating repertoire of additional mechanisms other than TFs, which help regulate the expression of paralogous genes in Escherichia coli and Bacillus subtilis. This analysis is derived from an extensive compilation of the regulatory information available from the NCBI PubMed database and deposited in the E. TFs are essential elements in the regulatory networks of paralogous genes TFs are the most prominent and usually the only regulatory element taken into account in any of the aforementioned stu...

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“…As an initial effort to spark interests in exploring these important issues and also motivated by discoveries that duplicated genes can develop divergent regulation and expression pattern, [18][19][20] we have recently characterized the profiles of histone modifications in the human segmental duplications. 21 We found that the two regions www.landesbioscience.com Epigenetics 251…”

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confidence: 99%

Gene duplication in the epigenomic era: Roles of chromatin modifications

Zheng

2008

Epigenetics

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Rapid evolution of expression and regulatory divergences after yeast gene duplication

Cited by 171 publications

References 34 publications

Neofunctionalization of young duplicate genes in Drosophila

Neofunctionalization of young duplicate genes in Drosophila

New insights into the regulatory networks of paralogous genes in bacteria

Gene duplication in the epigenomic era: Roles of chromatin modifications

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