Subfunctionalization of duplicated genes as a transition state to neofunctionalization

Rastogi, Shruti; Liberles, David A.

doi:10.1186/1471-2148-5-28

Cited by 327 publications

(151 citation statements)

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“…A duplicated enzyme or transcription factor will, if not lost, likely be subject to subfunctionalization [17], [18], a process that may in turn lead to neofunctionalization [19], [20]. To extend the model to the case where a second nutrient is present in the environment, we mimic a gene duplication event by adding a set of variables where “A” is replaced with “B”.…”

Section: Resultsmentioning

confidence: 99%

Is Transcriptional Regulation of Metabolic Pathways an Optimal Strategy for Fitness?

et al. 2007

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BackgroundTranscriptional regulation of the genes in metabolic pathways is a highly successful strategy, which is virtually universal in microorganisms. The lac operon of E. coli is but one example of how enzyme and transporter production can be made conditional on the presence of a nutrient to catabolize.MethodologyWith a minimalist model of metabolism, cell growth and transcriptional regulation in a microorganism, we explore how the interaction between environmental conditions and gene regulation set the growth rate of cells in the phase of exponential growth. This in silico model, which is based on biochemical rate equations, does not describe a specific organism, but the magnitudes of its parameters are chosen to match realistic values. Optimizing the parameters of the regulatory system allows us to quantify the fitness benefit of regulation. When a second nutrient and its metabolic pathway are introduced, the system must further decide whether and how to activate both pathways.ConclusionsEven the crudest transcriptional network is shown to substantially increase the fitness of the organism, and this effect persists even when the range of nutrient levels is kept very narrow. We show that maximal growth is achieved when pathway activation is a more or less steeply graded function of the nutrient concentration. Furthermore, we predict that bistability of the system is a rare phenomenon in this context, but outline a situation where it may be selected for.

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Section: Resultsmentioning

confidence: 99%

Is Transcriptional Regulation of Metabolic Pathways an Optimal Strategy for Fitness?

et al. 2007

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“…This process of subfunctionalization is important because it has been described as a transition state for further neofunctionalization. The latter is a process that involves the retention of the ancestral function of one gene while another duplicate acquires new functions (43). The description and characterization of these processes are essential in this system to understand the evolution of roles in the ADP-Glc PPase family.…”

Section: Discussionmentioning

confidence: 99%

Ostreococcus tauri ADP-glucose Pyrophosphorylase Reveals Alternative Paths for the Evolution of Subunit Roles

Kuhn¹,

Falaschetti²,

Ballícora

2009

Journal of Biological Chemistry

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ADP-glucose pyrophosphorylase controls starch synthesis in plants and is an interesting case to study the evolution and differentiation of roles in heteromeric enzymes. It includes two homologous subunits, small (S) and large (L), that originated from a common photosynthetic eukaryotic ancestor. In present day organisms, these subunits became complementary after loss of certain roles in a process described as subfunctionalization. For instance, the potato tuber enzyme has a noncatalytic L subunit that complements an S subunit with suboptimal allosteric properties. To understand the evolution of catalysis and regulation in this family, we artificially synthesized both subunit genes from the unicellular alga Ostreococcus tauri. This is among the most ancient species in the green lineage that diverged from the ancestor of all green plants and algae. After heterologous gene expression, we purified and characterized the proteins. The O. tauri enzyme was not redox-regulated, suggesting that redox regulation of ADP-glucose pyrophosphorylases appeared later in evolution. The S subunit had a typical low apparent affinity for the activator 3-phosphoglycerate, but it was atypically defective in the catalytic efficiency (V max /K m ) for the substrate Glc-1-P. The L subunit needed the S subunit for soluble expression. In the presence of a mutated S subunit (to avoid interference), the L subunit had a high apparent affinity for 3-phosphoglycerate and substrates suggesting a leading role in catalysis. Therefore, the subfunctionalization of the O. tauri enzyme was different from previously described cases. To the best of our knowledge, this is the first biochemical description of a system with alternative subfunctionalization paths.Starch synthesis in photosynthetic eukaryotes such as higher plants and unicellular algae is controlled by a heterotetrameric ADP-glucose pyrophosphorylase (ADP-Glc PPase, 4 EC 2.7.7.27). This enzyme catalyzes the reaction of ATP and Glc-1-P to form ADP-glucose (ADP-Glc) and PP i , and it is primarily activated by 3-phosphoglycerate (3-PGA) and inhibited by P i . In photosynthetic eukaryotes the enzyme includes two distinct S and L homologous subunits (S 2 L 2 or ␣ 2 ␤ 2 ), but in photosynthetic bacteria the enzyme is a homotetramer (␣ 4 ). There has been debate regarding the role of the different subunits of ADP-Glc PPase. The S subunit homotetramer from potato (Solanum tuberosum) tuber (StuS), Arabidopsis thaliana (APS1), and barley (Hordeum vulgare) endosperm have a catalytic function with defective regulatory properties (1-3). It is not clear if there is a set of universal roles for the L subunit in plants. The L subunit from potato tuber (StuL) is catalytically deficient and plays more of a regulatory role by modifying the apparent affinity of the S subunit toward allosteric regulators (1, 4). On the other hand, the Arabidopsis APL1 and APL2 isoforms have both catalytic and regulatory functions, whereas the APL3 and APL4 isoforms behave like StuL (2, 5). The maize (Zea mays) endosperm L subunit...

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“…If this is the case, the 3R-WGD should have contributed to the emergence of different gene functions among lineages and, consequently, to the various aspects of teleost diversity. Such lineage-specific evolution of duplicate genes includes both loss of gene function and sub-neofunctionalization between duplicates (partitioning of the ancestral functions of the pre-duplicate gene leading to long-term persistence and adaptive evolution of the duplicates; Ohno 1970; Force et al 1999;He and Zhang 2005;Rastogi and Liberles 2005). However, very few studies have examined the lineage-specific loss or persistence of duplicate genes derived from the 3R-WGD; therefore, there are few estimates of the effect of 3R-WGD on the current organization of teleost genomes (e.g., Sémon and Wolfe 2007a;Sato et al 2009a).…”

Section: R-wgd and Genetic Diversitymentioning

confidence: 99%

Teleost fish with specific genome duplication as unique models of vertebrate evolution

Sato

Nishida

2010

Environ Biol Fish

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Whole-genome duplication (WGD) is believed to be one of the major evolutionary events that shaped the genome organization of vertebrates. Here, we review recent research on vertebrate genome evolution, specifically on WGD and its consequences for gene and genome evolution in teleost fishes. Recent genome analyses confirmed that all vertebrates experienced two rounds of WGD early in their evolution, and that teleosts experienced a subsequent additional third-round (3R)-WGD. The 3R-WGD was estimated to have occurred 320-400 million years ago in a teleost ancestor, but after its divergence from a common ancestor with living non-teleost actinopterygians (Bichir, Sturgeon, Bowfin, and Gar) based on the analyses of teleost-specific duplicate genes. This 3R-WGD was confirmed by synteny analysis and ancestral karyotype inference using the genome sequences of Tetraodon and medaka. Most of the tetrapods, on the other hand, have not experienced an additional WGD; however, they have experienced repeated chromosomal rearrangements throughout the whole genome. Therefore, different types of chromosomal events have characterized the genomes of teleosts and tetrapods, respectively. The 3R-WGD is useful to investigate the consequences of WGD because it is an evolutionarily recent WGD and thus teleost genomes retain many more WGD-derived duplicates and "traces" of their evolution. In addition, the remarkable morphological, physiological, and ecological diversity of teleosts may facilitate understanding of macrophenotypic evolution on the basis of genetic/genomic information. We highlight the teleosts with 3R-WGD as unique models for future studies on ecology and evolution taking advantage of emerging genomics technologies and systems biology environments.

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Subfunctionalization of duplicated genes as a transition state to neofunctionalization

Cited by 327 publications

References 16 publications

Is Transcriptional Regulation of Metabolic Pathways an Optimal Strategy for Fitness?

Is Transcriptional Regulation of Metabolic Pathways an Optimal Strategy for Fitness?

Ostreococcus tauri ADP-glucose Pyrophosphorylase Reveals Alternative Paths for the Evolution of Subunit Roles

Teleost fish with specific genome duplication as unique models of vertebrate evolution

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