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Adaptive threonine increase in transmembrane regions of mitochondrial proteins in higher primates.

Kitazoe Y, Kishino H, Hasegawa M, Nakajima N, Thorne JL, Tanaka M - PLoS ONE (2008)

Bottom Line: This Thr increase involved the replacement of hydrophobic AAs in the membrane interior.Because crucial roles of Thr and Ser in membrane proteins have been proposed to be the formation of hydrogen bonds enhancing helix-helix interactions, the Thr increase detected in the higher primates might be adaptive by serving to reinforce stability of mt proteins in the inner membrane.The correlation between Thr composition in the membrane interior and the longevity of animals is striking, especially because some mt functions are thought to be involved in aging.

View Article: PubMed Central - PubMed

Affiliation: Center of Medical Information Science, Kochi Medical School, Nankoku, Kochi, Japan. kitazoey@kochi-u.ac.jp

ABSTRACT

Background: The mitochondrial (mt) gene tree of placental mammals reveals a very strong acceleration of the amino acid (AA) replacement rate and a change in AA compositional bias in the lineage leading to the higher primates (simians), in contrast to the nuclear gene tree. Whether this acceleration and compositional bias were caused by adaptive evolution at the AA level or directional mutation pressure at the DNA level has been vigorously debated.

Methodology/principal findings: Our phylogenetic analysis indicates that the rate acceleration in the simian lineage is accompanied by a marked increase in threonine (Thr) residues in the transmembrane helix regions of mt DNA-encoded proteins. This Thr increase involved the replacement of hydrophobic AAs in the membrane interior. Even after accounting for lack of independence due to phylogeny, a regression analysis reveals a statistical significant positive correlation between Thr composition and longevity in primates.

Conclusion/significance: Because crucial roles of Thr and Ser in membrane proteins have been proposed to be the formation of hydrogen bonds enhancing helix-helix interactions, the Thr increase detected in the higher primates might be adaptive by serving to reinforce stability of mt proteins in the inner membrane. The correlation between Thr composition in the membrane interior and the longevity of animals is striking, especially because some mt functions are thought to be involved in aging.

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Related in: MedlinePlus

Hoa→Thr flows on a placental mammal tree.The tree was reconstructed with a multidimensional vector space (MVS) method from 62 complete mt AA sequences [2]. The upper and lower half circles on the ancestral nodes and terminals represent the numbers of Hoa and Thr, respectively, relative to those of the root sequence. The decrease of Hoa and the increase of Thr were expressed by gradational changes from dark colors toward light ones of four grades (see the insertion). We defined the root sequence as the most recent common ancestor of Afrotheria and Xenarthra, and estimated the node sequences by applying the maximum parsimony algorithm to three groups of Hoa, Thr and Rma (the remaining AAs except for Hoa and Thr) (Materials and Methods).
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pone-0003343-g001: Hoa→Thr flows on a placental mammal tree.The tree was reconstructed with a multidimensional vector space (MVS) method from 62 complete mt AA sequences [2]. The upper and lower half circles on the ancestral nodes and terminals represent the numbers of Hoa and Thr, respectively, relative to those of the root sequence. The decrease of Hoa and the increase of Thr were expressed by gradational changes from dark colors toward light ones of four grades (see the insertion). We defined the root sequence as the most recent common ancestor of Afrotheria and Xenarthra, and estimated the node sequences by applying the maximum parsimony algorithm to three groups of Hoa, Thr and Rma (the remaining AAs except for Hoa and Thr) (Materials and Methods).

Mentions: Mitochondria supply most cellular energy and influence cell growth, human disease, and probably aging [1]. A better understanding of mt protein functions may be possible by detecting adaptive evolution that occurred in specific lineages of the mt gene tree of the placental mammals. Interestingly, the mt gene tree displays elevated rates of AA replacement in lineages leading to the simians, rodents, and hedgehogs (Figure 1) [2]. Although the nuclear gene tree also shows rate accelerations in the lineages of rodents and hedgehogs, no significant acceleration is observed in the primate lineage [3], [4] whereas the mt branch lengths of the simians (relative to the total branch lengths) are twice as long as those on the nuclear gene tree. This feature of the mt gene tree suggests that the simian lineage experienced a particularly unusual event in molecular evolution. One hypothesis is that an episode of adaptive evolution occurred in the simian lineage [5]–[9]. Another hypothesis is that the acceleration and compositional bias were caused by a higher rate of directional mutation [10], [11]. The adaptive hypothesis is supported by a highly significant acceleration of nonsynonymous changes, in contrast to a rather homogeneous rate of synonymous changes. The mutation bias explanation is supported by the existence of directional nucleotide mutation pressure at the fourfold-degenerate third nucleotide sites (FD3rd) in codons [12]–[14], and also by the duration of the single-stranded state of the 12 mt protein-coding genes (except for NADH dehydrogenase subunit 6) during replication [12].


Adaptive threonine increase in transmembrane regions of mitochondrial proteins in higher primates.

Kitazoe Y, Kishino H, Hasegawa M, Nakajima N, Thorne JL, Tanaka M - PLoS ONE (2008)

Hoa→Thr flows on a placental mammal tree.The tree was reconstructed with a multidimensional vector space (MVS) method from 62 complete mt AA sequences [2]. The upper and lower half circles on the ancestral nodes and terminals represent the numbers of Hoa and Thr, respectively, relative to those of the root sequence. The decrease of Hoa and the increase of Thr were expressed by gradational changes from dark colors toward light ones of four grades (see the insertion). We defined the root sequence as the most recent common ancestor of Afrotheria and Xenarthra, and estimated the node sequences by applying the maximum parsimony algorithm to three groups of Hoa, Thr and Rma (the remaining AAs except for Hoa and Thr) (Materials and Methods).
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2553178&req=5

pone-0003343-g001: Hoa→Thr flows on a placental mammal tree.The tree was reconstructed with a multidimensional vector space (MVS) method from 62 complete mt AA sequences [2]. The upper and lower half circles on the ancestral nodes and terminals represent the numbers of Hoa and Thr, respectively, relative to those of the root sequence. The decrease of Hoa and the increase of Thr were expressed by gradational changes from dark colors toward light ones of four grades (see the insertion). We defined the root sequence as the most recent common ancestor of Afrotheria and Xenarthra, and estimated the node sequences by applying the maximum parsimony algorithm to three groups of Hoa, Thr and Rma (the remaining AAs except for Hoa and Thr) (Materials and Methods).
Mentions: Mitochondria supply most cellular energy and influence cell growth, human disease, and probably aging [1]. A better understanding of mt protein functions may be possible by detecting adaptive evolution that occurred in specific lineages of the mt gene tree of the placental mammals. Interestingly, the mt gene tree displays elevated rates of AA replacement in lineages leading to the simians, rodents, and hedgehogs (Figure 1) [2]. Although the nuclear gene tree also shows rate accelerations in the lineages of rodents and hedgehogs, no significant acceleration is observed in the primate lineage [3], [4] whereas the mt branch lengths of the simians (relative to the total branch lengths) are twice as long as those on the nuclear gene tree. This feature of the mt gene tree suggests that the simian lineage experienced a particularly unusual event in molecular evolution. One hypothesis is that an episode of adaptive evolution occurred in the simian lineage [5]–[9]. Another hypothesis is that the acceleration and compositional bias were caused by a higher rate of directional mutation [10], [11]. The adaptive hypothesis is supported by a highly significant acceleration of nonsynonymous changes, in contrast to a rather homogeneous rate of synonymous changes. The mutation bias explanation is supported by the existence of directional nucleotide mutation pressure at the fourfold-degenerate third nucleotide sites (FD3rd) in codons [12]–[14], and also by the duration of the single-stranded state of the 12 mt protein-coding genes (except for NADH dehydrogenase subunit 6) during replication [12].

Bottom Line: This Thr increase involved the replacement of hydrophobic AAs in the membrane interior.Because crucial roles of Thr and Ser in membrane proteins have been proposed to be the formation of hydrogen bonds enhancing helix-helix interactions, the Thr increase detected in the higher primates might be adaptive by serving to reinforce stability of mt proteins in the inner membrane.The correlation between Thr composition in the membrane interior and the longevity of animals is striking, especially because some mt functions are thought to be involved in aging.

View Article: PubMed Central - PubMed

Affiliation: Center of Medical Information Science, Kochi Medical School, Nankoku, Kochi, Japan. kitazoey@kochi-u.ac.jp

ABSTRACT

Background: The mitochondrial (mt) gene tree of placental mammals reveals a very strong acceleration of the amino acid (AA) replacement rate and a change in AA compositional bias in the lineage leading to the higher primates (simians), in contrast to the nuclear gene tree. Whether this acceleration and compositional bias were caused by adaptive evolution at the AA level or directional mutation pressure at the DNA level has been vigorously debated.

Methodology/principal findings: Our phylogenetic analysis indicates that the rate acceleration in the simian lineage is accompanied by a marked increase in threonine (Thr) residues in the transmembrane helix regions of mt DNA-encoded proteins. This Thr increase involved the replacement of hydrophobic AAs in the membrane interior. Even after accounting for lack of independence due to phylogeny, a regression analysis reveals a statistical significant positive correlation between Thr composition and longevity in primates.

Conclusion/significance: Because crucial roles of Thr and Ser in membrane proteins have been proposed to be the formation of hydrogen bonds enhancing helix-helix interactions, the Thr increase detected in the higher primates might be adaptive by serving to reinforce stability of mt proteins in the inner membrane. The correlation between Thr composition in the membrane interior and the longevity of animals is striking, especially because some mt functions are thought to be involved in aging.

Show MeSH
Related in: MedlinePlus