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Mitochondrial-nuclear interactions: compensatory evolution or variable functional constraint among vertebrate oxidative phosphorylation genes?

Zhang F, Broughton RE - Genome Biol Evol (2013)

Bottom Line: The results from a combined analysis of all OXPHOS subunits fit the predictions of the hypothesis.However, results from two OXPHOS complexes did not fit this pattern when analyzed separately.We found that the d(N) of nu OXPHOS genes for "core" subunits (those involved in the major catalytic activity) was lower than that of "noncore" subunits, whereas there was no significant difference in d(N) between genes for nu non-OXPHOS and core subunits.

View Article: PubMed Central - PubMed

Affiliation: Oklahoma Biological Survey and Department of Biology, University of Oklahoma.

ABSTRACT
Oxidative phosphorylation (OXPHOS), the major energy-producing pathway in aerobic organisms, includes protein subunits encoded by both mitochondrial (mt) and nuclear (nu) genomes. How these independent genomes have coevolved is a long-standing question in evolutionary biology. Although mt genes evolve faster than most nu genes, maintenance of OXPHOS structural stability and functional efficiency may involve correlated evolution of mt and nu OXPHOS genes. The nu OXPHOS genes might be predicted to exhibit accelerated evolutionary rates to accommodate the elevated substitution rates of mt OXPHOS subunits with which they interact. Evolutionary rates of nu OXPHOS genes should, therefore, be higher than that of nu genes that are not involved in OXPHOS (nu non-OXPHOS). We tested the compensatory evolution hypothesis by comparing the evolutionary rates (synonymous substitution rate dS and nonsynonymous substitution rate dN) among 13 mt OXPHOS genes, 60 nu OXPHOS genes, and 77 nu non-OXPHOS genes in vertebrates (7 fish and 40 mammal species). The results from a combined analysis of all OXPHOS subunits fit the predictions of the hypothesis. However, results from two OXPHOS complexes did not fit this pattern when analyzed separately. We found that the d(N) of nu OXPHOS genes for "core" subunits (those involved in the major catalytic activity) was lower than that of "noncore" subunits, whereas there was no significant difference in d(N) between genes for nu non-OXPHOS and core subunits. This latter finding suggests that compensatory changes play a minor role in the evolution of OXPHOS genes and that the observed accelerated nu substitution rates are due largely to reduced functional constraint on noncore subunits.

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Related in: MedlinePlus

Comparison of synonymous substitution rate (dS) and nonsynonymous substitution rate (dN) among mitochondrial oxidative phosphorylation (mt OXPHOS), nuclear OXPHOS (nu OXPHOS), and non-OXPHOS genes in 7 fishes (A, B) and 40 mammals (C, D). Whisker-ends are at the 5th and 95th percentiles. *P < 0.05, **P < 0.01, ***P < 0.001.
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evt129-F2: Comparison of synonymous substitution rate (dS) and nonsynonymous substitution rate (dN) among mitochondrial oxidative phosphorylation (mt OXPHOS), nuclear OXPHOS (nu OXPHOS), and non-OXPHOS genes in 7 fishes (A, B) and 40 mammals (C, D). Whisker-ends are at the 5th and 95th percentiles. *P < 0.05, **P < 0.01, ***P < 0.001.

Mentions: We estimated the total synonymous and nonsynonymous substitution rates on each tree for fishes (fig. 1A) and mammals (fig. 1B) separately using maximum likelihood methods. Because neither dS nor dN was normally distributed and each exhibited significant variance heterogeneity, nonparametric statistics were used to compare the different groups of genes. We found significant differences (Kruskal–Wallis) in dS and dN among the three groups of genes: 13 mt OXPHOS genes, 60 nu OXPHOS genes, and 77 non-OXPHOS genes (table 1). The dS of mt OXPHOS genes was significantly higher than that of nu OXPHOS and non-OXPHOS genes in both (fig. 2A and C). The dS of mt and nu genes were 16.02 ± 9.64 and 2.02 ± 0.87, respectively, in fishes and 72.27 ± 26.56 and 8.85 ± 4.15, respectively, in mammals. No significant difference of the dS was detected between nu OXPHOS genes and non-OXPHOS genes (fig. 2A and C). We note that a small number of mt genes had exceptionally high dS values, which may indicate substitutional saturation, leading to violation of the assumptions of the maximum likelihood estimation method. As predicted, the dN of mt OXPHOS genes was significantly higher than that of nu OXPHOS genes, which in turn was significantly higher than that of non-OXPHOS genes (fig. 2B and D).Fig. 2.—


Mitochondrial-nuclear interactions: compensatory evolution or variable functional constraint among vertebrate oxidative phosphorylation genes?

Zhang F, Broughton RE - Genome Biol Evol (2013)

Comparison of synonymous substitution rate (dS) and nonsynonymous substitution rate (dN) among mitochondrial oxidative phosphorylation (mt OXPHOS), nuclear OXPHOS (nu OXPHOS), and non-OXPHOS genes in 7 fishes (A, B) and 40 mammals (C, D). Whisker-ends are at the 5th and 95th percentiles. *P < 0.05, **P < 0.01, ***P < 0.001.
© Copyright Policy - creative-commons
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3814189&req=5

evt129-F2: Comparison of synonymous substitution rate (dS) and nonsynonymous substitution rate (dN) among mitochondrial oxidative phosphorylation (mt OXPHOS), nuclear OXPHOS (nu OXPHOS), and non-OXPHOS genes in 7 fishes (A, B) and 40 mammals (C, D). Whisker-ends are at the 5th and 95th percentiles. *P < 0.05, **P < 0.01, ***P < 0.001.
Mentions: We estimated the total synonymous and nonsynonymous substitution rates on each tree for fishes (fig. 1A) and mammals (fig. 1B) separately using maximum likelihood methods. Because neither dS nor dN was normally distributed and each exhibited significant variance heterogeneity, nonparametric statistics were used to compare the different groups of genes. We found significant differences (Kruskal–Wallis) in dS and dN among the three groups of genes: 13 mt OXPHOS genes, 60 nu OXPHOS genes, and 77 non-OXPHOS genes (table 1). The dS of mt OXPHOS genes was significantly higher than that of nu OXPHOS and non-OXPHOS genes in both (fig. 2A and C). The dS of mt and nu genes were 16.02 ± 9.64 and 2.02 ± 0.87, respectively, in fishes and 72.27 ± 26.56 and 8.85 ± 4.15, respectively, in mammals. No significant difference of the dS was detected between nu OXPHOS genes and non-OXPHOS genes (fig. 2A and C). We note that a small number of mt genes had exceptionally high dS values, which may indicate substitutional saturation, leading to violation of the assumptions of the maximum likelihood estimation method. As predicted, the dN of mt OXPHOS genes was significantly higher than that of nu OXPHOS genes, which in turn was significantly higher than that of non-OXPHOS genes (fig. 2B and D).Fig. 2.—

Bottom Line: The results from a combined analysis of all OXPHOS subunits fit the predictions of the hypothesis.However, results from two OXPHOS complexes did not fit this pattern when analyzed separately.We found that the d(N) of nu OXPHOS genes for "core" subunits (those involved in the major catalytic activity) was lower than that of "noncore" subunits, whereas there was no significant difference in d(N) between genes for nu non-OXPHOS and core subunits.

View Article: PubMed Central - PubMed

Affiliation: Oklahoma Biological Survey and Department of Biology, University of Oklahoma.

ABSTRACT
Oxidative phosphorylation (OXPHOS), the major energy-producing pathway in aerobic organisms, includes protein subunits encoded by both mitochondrial (mt) and nuclear (nu) genomes. How these independent genomes have coevolved is a long-standing question in evolutionary biology. Although mt genes evolve faster than most nu genes, maintenance of OXPHOS structural stability and functional efficiency may involve correlated evolution of mt and nu OXPHOS genes. The nu OXPHOS genes might be predicted to exhibit accelerated evolutionary rates to accommodate the elevated substitution rates of mt OXPHOS subunits with which they interact. Evolutionary rates of nu OXPHOS genes should, therefore, be higher than that of nu genes that are not involved in OXPHOS (nu non-OXPHOS). We tested the compensatory evolution hypothesis by comparing the evolutionary rates (synonymous substitution rate dS and nonsynonymous substitution rate dN) among 13 mt OXPHOS genes, 60 nu OXPHOS genes, and 77 nu non-OXPHOS genes in vertebrates (7 fish and 40 mammal species). The results from a combined analysis of all OXPHOS subunits fit the predictions of the hypothesis. However, results from two OXPHOS complexes did not fit this pattern when analyzed separately. We found that the d(N) of nu OXPHOS genes for "core" subunits (those involved in the major catalytic activity) was lower than that of "noncore" subunits, whereas there was no significant difference in d(N) between genes for nu non-OXPHOS and core subunits. This latter finding suggests that compensatory changes play a minor role in the evolution of OXPHOS genes and that the observed accelerated nu substitution rates are due largely to reduced functional constraint on noncore subunits.

Show MeSH
Related in: MedlinePlus