Rapid and asymmetric divergence of duplicate genes in the human gene coexpression network

Chung, Wen Yu; Albert, Réka; Albert, István; Nekrutenko, Anton; Makova, Kateryna D.

doi:10.1186/1471-2105-7-46

Cited by 45 publications

(24 citation statements)

References 51 publications

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“…For example, in multiple eukaryotic species, the expression correlation between a duplicate pair decreases as Ks increases [56], [63]–[65]. Similarly, the fraction of potential protein interaction partners (predicted based on co-expression) shared between a duplicate gene pair in human declines as Ks increases [34]. Therefore, it is not particularly surprising that the overall proportion of duplicates that lose stress responsiveness increases as Ks increases.…”

Section: Resultsmentioning

confidence: 99%

Evolution of Stress-Regulated Gene Expression in Duplicate Genes of Arabidopsis thaliana

et al. 2009

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Due to the selection pressure imposed by highly variable environmental conditions, stress sensing and regulatory response mechanisms in plants are expected to evolve rapidly. One potential source of innovation in plant stress response mechanisms is gene duplication. In this study, we examined the evolution of stress-regulated gene expression among duplicated genes in the model plant Arabidopsis thaliana. Key to this analysis was reconstructing the putative ancestral stress regulation pattern. By comparing the expression patterns of duplicated genes with the patterns of their ancestors, duplicated genes likely lost and gained stress responses at a rapid rate initially, but the rate is close to zero when the synonymous substitution rate (a proxy for time) is >∼0.8. When considering duplicated gene pairs, we found that partitioning of putative ancestral stress responses occurred more frequently compared to cases of parallel retention and loss. Furthermore, the pattern of stress response partitioning was extremely asymmetric. An analysis of putative cis-acting DNA regulatory elements in the promoters of the duplicated stress-regulated genes indicated that the asymmetric partitioning of ancestral stress responses are likely due, at least in part, to differential loss of DNA regulatory elements; the duplicated genes losing most of their stress responses were those that had lost more of the putative cis-acting elements. Finally, duplicate genes that lost most or all of the ancestral responses are more likely to have gained responses to other stresses. Therefore, the retention of duplicates that inherit few or no functions seems to be coupled to neofunctionalization. Taken together, our findings provide new insight into the patterns of evolutionary changes in gene stress responses after duplication and lay the foundation for testing the adaptive significance of stress regulatory changes under highly variable biotic and abiotic environments.

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Section: Resultsmentioning

confidence: 99%

Evolution of Stress-Regulated Gene Expression in Duplicate Genes of Arabidopsis thaliana

et al. 2009

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“…The majority of newly duplicated genes experience a period of relaxed purifying selection, while only a relatively small proportion exhibits a signature of positive selection consequent to the acquisition of new biological functions [66]. Presumably, in between the initial post-duplicational redundancy and eventual neofunctionalisation through genetic divergence, there is a 'half-way house' state in which a gene is relatively free to explore the acquisition of new functions while still being constrained to some extent by selection against the loss of those functions it has already acquired [67]. …”

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confidence: 99%

Exploring the potential relevance of human-specific genes to complex disease

Cooper

Kehrer‐Sawatzki

2011

Human Genomics

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Although human disease genes generally tend to be evolutionarily more ancient than non-disease genes, complex disease genes appear to be represented more frequently than Mendelian disease genes among genes of more recent evolutionary origin. It is therefore proposed that the analysis of human-specific genes might provide new insights into the genetics of complex disease. Cross-comparison with the Human Gene Mutation Database (http://www.hgmd.org) revealed a number of examples of disease-causing and disease-associated mutations in putatively human-specific genes. A sizeable proportion of these were missense polymorphisms associated with complex disease. Since both human-specific genes and genes associated with complex disease have often experienced particularly rapid rates of evolutionary change, either due to weaker purifying selection or positive selection, it is proposed that a significant number of human-specific genes may play a role in complex disease.

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“…Previous studies have shown that the retention of duplicate genes can result in rapid divergence in expression patterns (Farre & Alba, 2010;Ganko, Meyers, & Vision, 2007;Gu, Nicolae, Lu, & Li, 2002;Leite et al, 2018) and is often asymmetric (Chung, Albert, Albert, Nekrutenko, & Makova, 2006;Ganko et al, 2007;Gu, Zhang, & Huang, 2005;Liu et al, 2015;Wagner, 2002). Here clear divergence in expression patterns was observed among lepidopteran Treh genes ( Figure 3).…”

Section: Discussionmentioning

confidence: 77%

Duplication and diversification of trehalase confers evolutionary advantages on lepidopteran insects

Zhou

Katsuma

et al. 2019

Molecular Ecology

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Gene duplication provides a major source of new genes for evolutionary novelty and ecological adaptation. However, the maintenance of duplicated genes and their relevance to adaptive evolution has long been debated. Insect trehalase (Treh) plays key roles in energy metabolism, growth, and stress recovery. Here, we show that the duplication of Treh in Lepidoptera (butterflies and moths) is linked with their adaptation to various environmental stresses. Generally, two Treh genes are present in insects: Treh1 and Treh2. We report three distinct forms of Treh in lepidopteran insects, where Treh1 was duplicated into two gene clusters (Treh1a and Treh1b). These gene clusters differ in gene expression patterns, enzymatic properties, and subcellular localizations, suggesting that the enzymes probably underwent sub‐ and/or neofunctionalization in the lepidopteran insects. Interestingly, selective pressure analysis provided significant evidence of positive selection on duplicate Treh1b gene in lepidopteran insect lineages. Most positively selected sites were located in the alpha‐helical region, and several sites were close to the trehalose binding and catalytic sites. Subcellular adaptation of duplicate Treh1b driven by positive selection appears to have occurred as a result of selected changes in specific sequences, allowing for rapid reprogramming of duplicated Treh during evolution. Our results suggest that gene duplication of Treh and subsequent functional diversification could increase the survival rate of lepidopteran insects through various regulations of intracellular trehalose levels, facilitating their adaptation to diverse habitats. This study provides evidence regarding the mechanism by which gene family expansion can contribute to species adaptation through gene duplication and subsequent functional diversification.

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Rapid and asymmetric divergence of duplicate genes in the human gene coexpression network

Cited by 45 publications

References 51 publications

Evolution of Stress-Regulated Gene Expression in Duplicate Genes of Arabidopsis thaliana

Evolution of Stress-Regulated Gene Expression in Duplicate Genes of Arabidopsis thaliana

Exploring the potential relevance of human-specific genes to complex disease

Duplication and diversification of trehalase confers evolutionary advantages on lepidopteran insects

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