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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) between mitochondrial (mt) and nuclear (nu) genes in each complex in 7 fishes (A, B) and 40 mammals (C, D). Complex II is composed of subunits encoded only by nu genes. Whisker-ends are at the 5th and 95th percentiles. *P < 0.05, **P < 0.01, ***P < 0.001.
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evt129-F3: Comparison of synonymous substitution rate (dS) and nonsynonymous substitution rate (dN) between mitochondrial (mt) and nuclear (nu) genes in each complex in 7 fishes (A, B) and 40 mammals (C, D). Complex II is composed of subunits encoded only by nu genes. Whisker-ends are at the 5th and 95th percentiles. *P < 0.05, **P < 0.01, ***P < 0.001.

Mentions: Estimates of dS and dN were assessed for each OXPHOS complexes. The dS of mt genes was higher than that of nu genes in all four complexes (complex II is composed of subunits only encoded by nu genes) (fig. 3A and C). The dN of mt genes was not consistently higher than that of nu genes in all complexes. For example, the dN of mt genes in complex III was lower than that of nu genes in fishes (fig. 3B) whereas higher than that of nu genes in mammals (fig. 3D); the dN of mt genes in complex IV was significantly lower than that of nu genes in fishes (fig. 3B) and lower than that of nu genes in mammals (fig. 3D).Fig. 3.—


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) between mitochondrial (mt) and nuclear (nu) genes in each complex in 7 fishes (A, B) and 40 mammals (C, D). Complex II is composed of subunits encoded only by nu genes. 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-F3: Comparison of synonymous substitution rate (dS) and nonsynonymous substitution rate (dN) between mitochondrial (mt) and nuclear (nu) genes in each complex in 7 fishes (A, B) and 40 mammals (C, D). Complex II is composed of subunits encoded only by nu genes. Whisker-ends are at the 5th and 95th percentiles. *P < 0.05, **P < 0.01, ***P < 0.001.
Mentions: Estimates of dS and dN were assessed for each OXPHOS complexes. The dS of mt genes was higher than that of nu genes in all four complexes (complex II is composed of subunits only encoded by nu genes) (fig. 3A and C). The dN of mt genes was not consistently higher than that of nu genes in all complexes. For example, the dN of mt genes in complex III was lower than that of nu genes in fishes (fig. 3B) whereas higher than that of nu genes in mammals (fig. 3D); the dN of mt genes in complex IV was significantly lower than that of nu genes in fishes (fig. 3B) and lower than that of nu genes in mammals (fig. 3D).Fig. 3.—

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