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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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Phylogeny of the seven fishes (Betancur-R et al. 2013) (A) and 40 mammals (Meredith et al. 2011) (B) used in this study.
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evt129-F1: Phylogeny of the seven fishes (Betancur-R et al. 2013) (A) and 40 mammals (Meredith et al. 2011) (B) used in this study.

Mentions: A few recent investigations have addressed mt–nu coevolution at the molecular level but have been restricted to a few genes or a small number of species (e.g., nu genes CYC1 and UQCRFS1, and mt gene MT-CYTB [Willett and Burton 2001], or genes involved in OXPHOS complex IV [Goldberg et al. 2003]). Here, we describe a broader study of 73 OXPHOS genes and a comparison between OXPHOS and 77 non-OXPHOS housekeeping genes. Under a compensatory evolution scenario, we predicted that dN of mt OXPHOS > nu OXPHOS > nu non-OXPHOS genes. We tested the compensatory substitution model by comparing the evolutionary rates (both dS and dN) of 13 mt protein-coding genes (mt OXPHOS genes), 60 nu OXPHOS genes, and 77 non-OXPHOS genes in 47 vertebrate species, including 7 fishes and 40 mammals. The seven fish species are phylogenetically disparate, spanning some 250 Myr of evolutionary history (Betancur-R et al. 2013) (fig. 1A), whereas most of the mammal lineages emerged within the last 80 Myr (Meredith et al. 2011) (fig. 1B).Fig. 1.—


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

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

Phylogeny of the seven fishes (Betancur-R et al. 2013) (A) and 40 mammals (Meredith et al. 2011) (B) used in this study.
© Copyright Policy - creative-commons
Related In: Results  -  Collection

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

evt129-F1: Phylogeny of the seven fishes (Betancur-R et al. 2013) (A) and 40 mammals (Meredith et al. 2011) (B) used in this study.
Mentions: A few recent investigations have addressed mt–nu coevolution at the molecular level but have been restricted to a few genes or a small number of species (e.g., nu genes CYC1 and UQCRFS1, and mt gene MT-CYTB [Willett and Burton 2001], or genes involved in OXPHOS complex IV [Goldberg et al. 2003]). Here, we describe a broader study of 73 OXPHOS genes and a comparison between OXPHOS and 77 non-OXPHOS housekeeping genes. Under a compensatory evolution scenario, we predicted that dN of mt OXPHOS > nu OXPHOS > nu non-OXPHOS genes. We tested the compensatory substitution model by comparing the evolutionary rates (both dS and dN) of 13 mt protein-coding genes (mt OXPHOS genes), 60 nu OXPHOS genes, and 77 non-OXPHOS genes in 47 vertebrate species, including 7 fishes and 40 mammals. The seven fish species are phylogenetically disparate, spanning some 250 Myr of evolutionary history (Betancur-R et al. 2013) (fig. 1A), whereas most of the mammal lineages emerged within the last 80 Myr (Meredith et al. 2011) (fig. 1B).Fig. 1.—

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