Limits...
Natural selection and adaptive evolution of leptin in the ochotona family driven by the cold environmental stress.

Yang J, Wang ZL, Zhao XQ, Wang de P, Qi de L, Xu BH, Ren YH, Tian HF - PLoS ONE (2008)

Bottom Line: Our results show that positive selection (PS) acts on pika leptin, while nine PS sites located within the functionally significant segment 85-119 of leptin and one unique motif appeared only in pika lineages-the ATP synthase alpha and beta subunit signature site.Our findings support the viewpoint that adaptive evolution may occur in pika leptin, which may play important roles in pikas' ecological adaptation to extreme environmental stress.We speculate that cold, and probably not hypoxia, may be the primary environmental factor for driving adaptive evolution of pika leptin.

View Article: PubMed Central - PubMed

Affiliation: Key Laboratory of Qinghai-Tibetan Plateau Biological Evolution and Adaptation, Northwest Institute of Plateau Biology, The Chinese Academy of Sciences, Xining, Qinghai, China.

ABSTRACT

Background: Environmental stress can accelerate the evolutionary rate of specific stress-response proteins and create new functions specialized for different environments, enhancing an organism's fitness to stressful environments. Pikas (order Lagomorpha), endemic, non-hibernating mammals in the modern Holarctic Region, live in cold regions at either high altitudes or high latitudes and have a maximum distribution of species diversification confined to the Qinghai-Tibet Plateau. Variations in energy metabolism are remarkable for them living in cold environments. Leptin, an adipocyte-derived hormone, plays important roles in energy homeostasis.

Methodology/principal findings: To examine the extent of leptin variations within the Ochotona family, we cloned the entire coding sequence of pika leptin from 6 species in two regions (Qinghai-Tibet Plateau and Inner Mongolia steppe in China) and the leptin sequences of plateau pikas (O. curzonia) from different altitudes on Qinghai-Tibet Plateau. We carried out both DNA and amino acid sequence analyses in molecular evolution and compared modeled spatial structures. Our results show that positive selection (PS) acts on pika leptin, while nine PS sites located within the functionally significant segment 85-119 of leptin and one unique motif appeared only in pika lineages-the ATP synthase alpha and beta subunit signature site. To reveal the environmental factors affecting sequence evolution of pika leptin, relative rate test was performed in pikas from different altitudes. Stepwise multiple regression shows that temperature is significantly and negatively correlated with the rates of non-synonymous substitution (Ka) and amino acid substitution (Aa), whereas altitude does not significantly affect synonymous substitution (Ks), Ka and Aa.

Conclusions/significance: Our findings support the viewpoint that adaptive evolution may occur in pika leptin, which may play important roles in pikas' ecological adaptation to extreme environmental stress. We speculate that cold, and probably not hypoxia, may be the primary environmental factor for driving adaptive evolution of pika leptin.

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Related in: MedlinePlus

Multiple alignments of leptin amino acids sequences.Residues identical to Gorilla leptin are presented as dots (.). The predicted motifs are shaded by different colors [protein kinase C phosphorylation sites (PKC) are yellow; casein kinase II phosphorylation sites (CK2) are red; N-glycosylation sites are green). Underlined amino acid sequences indicate the motif of the ATP synthase α and β subunit signature site. The numbers at the right are the total numbers of amino acids. Two cysteine residues at 96 and 146 are indicated by asterisks.
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pone-0001472-g001: Multiple alignments of leptin amino acids sequences.Residues identical to Gorilla leptin are presented as dots (.). The predicted motifs are shaded by different colors [protein kinase C phosphorylation sites (PKC) are yellow; casein kinase II phosphorylation sites (CK2) are red; N-glycosylation sites are green). Underlined amino acid sequences indicate the motif of the ATP synthase α and β subunit signature site. The numbers at the right are the total numbers of amino acids. Two cysteine residues at 96 and 146 are indicated by asterisks.

Mentions: A 646-bp fragment in pikas and a 565-bp fragment from both Lepus oiostolus and Oryctolagus cuniculus, which contained the complete coding region, were cloned, respectively. These sequences were submitted to GenBank and were assigned the following accession numbers: DQ983189 (Ochotona curzoniae); EF091861 (Ochtona nubrica); EF091863 (Ochotona cansus cansus 1); EF091864 (Ochotona cansus cansus 2); EF091862 (Ochotona annecten); EF091860 (Ochotona daurica bedfordi); DQ983190 (Lepus oiostolus), and DQ983191 (Oryctolagus cuniculus). The deduced amino acid sequences were composed of 167 amino acids and encoded an apparent signal peptide sequence of 21 amino acids with the signal cleavage site between Ala-21 and Val-22. Thus, the mature secreted protein had a predicted molecular weight of 16.086 kDa and a pI of 6.3. To reveal the evolutionary divergence in leptin sequences among lineages, we assembled and analyzed 20 sequences representing samples from different lineages in vertebrates. The result of the multiple alignments for amino acid sequences is shown in Figure 1.


Natural selection and adaptive evolution of leptin in the ochotona family driven by the cold environmental stress.

Yang J, Wang ZL, Zhao XQ, Wang de P, Qi de L, Xu BH, Ren YH, Tian HF - PLoS ONE (2008)

Multiple alignments of leptin amino acids sequences.Residues identical to Gorilla leptin are presented as dots (.). The predicted motifs are shaded by different colors [protein kinase C phosphorylation sites (PKC) are yellow; casein kinase II phosphorylation sites (CK2) are red; N-glycosylation sites are green). Underlined amino acid sequences indicate the motif of the ATP synthase α and β subunit signature site. The numbers at the right are the total numbers of amino acids. Two cysteine residues at 96 and 146 are indicated by asterisks.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2194619&req=5

pone-0001472-g001: Multiple alignments of leptin amino acids sequences.Residues identical to Gorilla leptin are presented as dots (.). The predicted motifs are shaded by different colors [protein kinase C phosphorylation sites (PKC) are yellow; casein kinase II phosphorylation sites (CK2) are red; N-glycosylation sites are green). Underlined amino acid sequences indicate the motif of the ATP synthase α and β subunit signature site. The numbers at the right are the total numbers of amino acids. Two cysteine residues at 96 and 146 are indicated by asterisks.
Mentions: A 646-bp fragment in pikas and a 565-bp fragment from both Lepus oiostolus and Oryctolagus cuniculus, which contained the complete coding region, were cloned, respectively. These sequences were submitted to GenBank and were assigned the following accession numbers: DQ983189 (Ochotona curzoniae); EF091861 (Ochtona nubrica); EF091863 (Ochotona cansus cansus 1); EF091864 (Ochotona cansus cansus 2); EF091862 (Ochotona annecten); EF091860 (Ochotona daurica bedfordi); DQ983190 (Lepus oiostolus), and DQ983191 (Oryctolagus cuniculus). The deduced amino acid sequences were composed of 167 amino acids and encoded an apparent signal peptide sequence of 21 amino acids with the signal cleavage site between Ala-21 and Val-22. Thus, the mature secreted protein had a predicted molecular weight of 16.086 kDa and a pI of 6.3. To reveal the evolutionary divergence in leptin sequences among lineages, we assembled and analyzed 20 sequences representing samples from different lineages in vertebrates. The result of the multiple alignments for amino acid sequences is shown in Figure 1.

Bottom Line: Our results show that positive selection (PS) acts on pika leptin, while nine PS sites located within the functionally significant segment 85-119 of leptin and one unique motif appeared only in pika lineages-the ATP synthase alpha and beta subunit signature site.Our findings support the viewpoint that adaptive evolution may occur in pika leptin, which may play important roles in pikas' ecological adaptation to extreme environmental stress.We speculate that cold, and probably not hypoxia, may be the primary environmental factor for driving adaptive evolution of pika leptin.

View Article: PubMed Central - PubMed

Affiliation: Key Laboratory of Qinghai-Tibetan Plateau Biological Evolution and Adaptation, Northwest Institute of Plateau Biology, The Chinese Academy of Sciences, Xining, Qinghai, China.

ABSTRACT

Background: Environmental stress can accelerate the evolutionary rate of specific stress-response proteins and create new functions specialized for different environments, enhancing an organism's fitness to stressful environments. Pikas (order Lagomorpha), endemic, non-hibernating mammals in the modern Holarctic Region, live in cold regions at either high altitudes or high latitudes and have a maximum distribution of species diversification confined to the Qinghai-Tibet Plateau. Variations in energy metabolism are remarkable for them living in cold environments. Leptin, an adipocyte-derived hormone, plays important roles in energy homeostasis.

Methodology/principal findings: To examine the extent of leptin variations within the Ochotona family, we cloned the entire coding sequence of pika leptin from 6 species in two regions (Qinghai-Tibet Plateau and Inner Mongolia steppe in China) and the leptin sequences of plateau pikas (O. curzonia) from different altitudes on Qinghai-Tibet Plateau. We carried out both DNA and amino acid sequence analyses in molecular evolution and compared modeled spatial structures. Our results show that positive selection (PS) acts on pika leptin, while nine PS sites located within the functionally significant segment 85-119 of leptin and one unique motif appeared only in pika lineages-the ATP synthase alpha and beta subunit signature site. To reveal the environmental factors affecting sequence evolution of pika leptin, relative rate test was performed in pikas from different altitudes. Stepwise multiple regression shows that temperature is significantly and negatively correlated with the rates of non-synonymous substitution (Ka) and amino acid substitution (Aa), whereas altitude does not significantly affect synonymous substitution (Ks), Ka and Aa.

Conclusions/significance: Our findings support the viewpoint that adaptive evolution may occur in pika leptin, which may play important roles in pikas' ecological adaptation to extreme environmental stress. We speculate that cold, and probably not hypoxia, may be the primary environmental factor for driving adaptive evolution of pika leptin.

Show MeSH
Related in: MedlinePlus