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Gene duplication and the evolution of moonlighting proteins.

Espinosa-Cantú A, Ascencio D, Barona-Gómez F, DeLuna A - Front Genet (2015)

Bottom Line: Dosage amplification and incomplete subfunctionalization appear to be prevalent in the maintenance of multifunctionality.We discuss the role of gene-expression divergence and paralog responsiveness in moonlighting proteins with overlapping biochemical properties.Future studies analyzing multifunctional genes in a more systematic and comprehensive manner will not only enable a better understanding of how this emerging class of protein behavior originates and is maintained, but also provide new insights on the mechanisms of evolution by gene duplication.

View Article: PubMed Central - PubMed

Affiliation: Laboratorio Nacional de Genómica para la Biodiversidad (Langebio), Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional (CINVESTAV), Irapuato, Mexico.

ABSTRACT
Gene duplication is a recurring phenomenon in genome evolution and a major driving force in the gain of biological functions. Here, we examine the role of gene duplication in the origin and maintenance of moonlighting proteins, with special focus on functional redundancy and innovation, molecular tradeoffs, and genetic robustness. An overview of specific examples-mainly from yeast-suggests a widespread conservation of moonlighting behavior in duplicate genes after long evolutionary times. Dosage amplification and incomplete subfunctionalization appear to be prevalent in the maintenance of multifunctionality. We discuss the role of gene-expression divergence and paralog responsiveness in moonlighting proteins with overlapping biochemical properties. Future studies analyzing multifunctional genes in a more systematic and comprehensive manner will not only enable a better understanding of how this emerging class of protein behavior originates and is maintained, but also provide new insights on the mechanisms of evolution by gene duplication.

No MeSH data available.


The fate of moonlighting proteins after gene duplication. The interplay between different mechanisms of gene evolution by duplication (including amplification) influence the origin, retention, and loss of moonlighting proteins. (I) Gene duplication may enable the origin or retention of moonlighting proteins over time by selection for dosage amplification of one or more molecular functions in the ancestor (e.g., yeast Rpl2A/Rpl2B). (II) Incomplete subfunctionalization of one or more molecular activities in the ancestor may enable the origin or retention of moonlighting behaviors as a result of neutral evolution (e.g., yeast Eno1/Eno2). In this scenario, the subfunctionalization may act on gene expression or protein activity, e.g., substrate specificity. (III) In contrast, duplication may result in the loss of moonlighting behaviors of one of the paralogs (e.g., yeast Gal1/Gal3), or of in both gene products (e.g., chicken argininosuccinate lyase/δ-crystallins) by complete specialization of their molecular activities.
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Figure 1: The fate of moonlighting proteins after gene duplication. The interplay between different mechanisms of gene evolution by duplication (including amplification) influence the origin, retention, and loss of moonlighting proteins. (I) Gene duplication may enable the origin or retention of moonlighting proteins over time by selection for dosage amplification of one or more molecular functions in the ancestor (e.g., yeast Rpl2A/Rpl2B). (II) Incomplete subfunctionalization of one or more molecular activities in the ancestor may enable the origin or retention of moonlighting behaviors as a result of neutral evolution (e.g., yeast Eno1/Eno2). In this scenario, the subfunctionalization may act on gene expression or protein activity, e.g., substrate specificity. (III) In contrast, duplication may result in the loss of moonlighting behaviors of one of the paralogs (e.g., yeast Gal1/Gal3), or of in both gene products (e.g., chicken argininosuccinate lyase/δ-crystallins) by complete specialization of their molecular activities.

Mentions: With the evolutionary models of gene duplication in mind, we examined available databases of moonlighting proteins described to date (Hernandez et al., 2014; Mani et al., 2015). Many of these proteins have gone through gene duplication events. In the specific example of the budding yeast Saccharomyces cerevisiae, for which extensive functional data is available, over 30 such multifunctional proteins have been described. This set includes 14 genes with paralogs that originated either from the whole-genome duplication or from small-scale duplication events (Table 1). Therefore, it is tempting to speculate that duplication dynamics have played a role in the origins and maintenance of gene multifunctionality. In what follows, we present different scenarios of evolution of moonlighting proteins by gene duplication, starting from ancestral monofunctional or multifunctional states and driven by neutral or adaptive evolution (see Figure 1).


Gene duplication and the evolution of moonlighting proteins.

Espinosa-Cantú A, Ascencio D, Barona-Gómez F, DeLuna A - Front Genet (2015)

The fate of moonlighting proteins after gene duplication. The interplay between different mechanisms of gene evolution by duplication (including amplification) influence the origin, retention, and loss of moonlighting proteins. (I) Gene duplication may enable the origin or retention of moonlighting proteins over time by selection for dosage amplification of one or more molecular functions in the ancestor (e.g., yeast Rpl2A/Rpl2B). (II) Incomplete subfunctionalization of one or more molecular activities in the ancestor may enable the origin or retention of moonlighting behaviors as a result of neutral evolution (e.g., yeast Eno1/Eno2). In this scenario, the subfunctionalization may act on gene expression or protein activity, e.g., substrate specificity. (III) In contrast, duplication may result in the loss of moonlighting behaviors of one of the paralogs (e.g., yeast Gal1/Gal3), or of in both gene products (e.g., chicken argininosuccinate lyase/δ-crystallins) by complete specialization of their molecular activities.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4493404&req=5

Figure 1: The fate of moonlighting proteins after gene duplication. The interplay between different mechanisms of gene evolution by duplication (including amplification) influence the origin, retention, and loss of moonlighting proteins. (I) Gene duplication may enable the origin or retention of moonlighting proteins over time by selection for dosage amplification of one or more molecular functions in the ancestor (e.g., yeast Rpl2A/Rpl2B). (II) Incomplete subfunctionalization of one or more molecular activities in the ancestor may enable the origin or retention of moonlighting behaviors as a result of neutral evolution (e.g., yeast Eno1/Eno2). In this scenario, the subfunctionalization may act on gene expression or protein activity, e.g., substrate specificity. (III) In contrast, duplication may result in the loss of moonlighting behaviors of one of the paralogs (e.g., yeast Gal1/Gal3), or of in both gene products (e.g., chicken argininosuccinate lyase/δ-crystallins) by complete specialization of their molecular activities.
Mentions: With the evolutionary models of gene duplication in mind, we examined available databases of moonlighting proteins described to date (Hernandez et al., 2014; Mani et al., 2015). Many of these proteins have gone through gene duplication events. In the specific example of the budding yeast Saccharomyces cerevisiae, for which extensive functional data is available, over 30 such multifunctional proteins have been described. This set includes 14 genes with paralogs that originated either from the whole-genome duplication or from small-scale duplication events (Table 1). Therefore, it is tempting to speculate that duplication dynamics have played a role in the origins and maintenance of gene multifunctionality. In what follows, we present different scenarios of evolution of moonlighting proteins by gene duplication, starting from ancestral monofunctional or multifunctional states and driven by neutral or adaptive evolution (see Figure 1).

Bottom Line: Dosage amplification and incomplete subfunctionalization appear to be prevalent in the maintenance of multifunctionality.We discuss the role of gene-expression divergence and paralog responsiveness in moonlighting proteins with overlapping biochemical properties.Future studies analyzing multifunctional genes in a more systematic and comprehensive manner will not only enable a better understanding of how this emerging class of protein behavior originates and is maintained, but also provide new insights on the mechanisms of evolution by gene duplication.

View Article: PubMed Central - PubMed

Affiliation: Laboratorio Nacional de Genómica para la Biodiversidad (Langebio), Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional (CINVESTAV), Irapuato, Mexico.

ABSTRACT
Gene duplication is a recurring phenomenon in genome evolution and a major driving force in the gain of biological functions. Here, we examine the role of gene duplication in the origin and maintenance of moonlighting proteins, with special focus on functional redundancy and innovation, molecular tradeoffs, and genetic robustness. An overview of specific examples-mainly from yeast-suggests a widespread conservation of moonlighting behavior in duplicate genes after long evolutionary times. Dosage amplification and incomplete subfunctionalization appear to be prevalent in the maintenance of multifunctionality. We discuss the role of gene-expression divergence and paralog responsiveness in moonlighting proteins with overlapping biochemical properties. Future studies analyzing multifunctional genes in a more systematic and comprehensive manner will not only enable a better understanding of how this emerging class of protein behavior originates and is maintained, but also provide new insights on the mechanisms of evolution by gene duplication.

No MeSH data available.