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The Origin and Diversity of Cpt1 Genes in Vertebrate Species.

Lopes-Marques M, Delgado IL, Ruivo R, Torres Y, Sainath SB, Rocha E, Cunha I, Santos MM, Castro LF - PLoS ONE (2015)

Bottom Line: The later is considered a mammalian innovation resulting from a gene duplication event in the ancestor of mammals, after the divergence of sauropsids.In contrast, Cpt1a2 has been found exclusively in teleosts.Finally, we propose that loss of Cpt1b is the likely cause for the unusual energy metabolism of elasmobranch.

View Article: PubMed Central - PubMed

Affiliation: CIIMAR, Interdisciplinary Centre of Marine and Environmental Research, CIMAR Associate Laboratory, UPorto-University of Porto, Porto, Portugal; ICBAS, Abel Salazar Biomedical Sciences Institute, University of Porto, Porto, Portugal.

ABSTRACT
The Carnitine palmitoyltransferase I (Cpt1) gene family plays a crucial role in energy homeostasis since it is required for the occurrence of fatty acid β-oxidation in the mitochondria. The exact gene repertoire in different vertebrate lineages is variable. Presently, four genes are documented: Cpt1a, also known as Cpt1a1, Cpt1a2; Cpt1b and Cpt1c. The later is considered a mammalian innovation resulting from a gene duplication event in the ancestor of mammals, after the divergence of sauropsids. In contrast, Cpt1a2 has been found exclusively in teleosts. Here, we reassess the overall evolutionary relationships of Cpt1 genes using a combination of approaches, including the survey of the gene repertoire in basal gnathostome lineages. Through molecular phylogenetics and synteny studies, we find that Cpt1c is most likely a rapidly evolving orthologue of Cpt1a2. Thus, Cpt1c is present in other lineages such as cartilaginous fish, reptiles, amphibians and the coelacanth. We show that genome duplications (2R) and variable rates of sequence evolution contribute to the history of Cpt1 genes in vertebrates. Finally, we propose that loss of Cpt1b is the likely cause for the unusual energy metabolism of elasmobranch.

No MeSH data available.


A. Synteny maps of Cpt1b in selected vertebrate genomes. Chromosome (Chr.) and position in mega base pairs (Mb) locations are given for the gene of interest in each species. The location of the H. sapiens orthologue is also given for non-conserved neighbouring genes in the other species analysed. Red dots indicate end of the chromosome or scaffold. B. Statistical synteny analysis. Reported p-values indicate the probability of identifying non homologous chromosomal segments, and S indicates the size of the chromosomal segment identified.
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pone.0138447.g003: A. Synteny maps of Cpt1b in selected vertebrate genomes. Chromosome (Chr.) and position in mega base pairs (Mb) locations are given for the gene of interest in each species. The location of the H. sapiens orthologue is also given for non-conserved neighbouring genes in the other species analysed. Red dots indicate end of the chromosome or scaffold. B. Statistical synteny analysis. Reported p-values indicate the probability of identifying non homologous chromosomal segments, and S indicates the size of the chromosomal segment identified.

Mentions: To further clarify the orthology/paralogy relationships of the Cpt1 gene repertoire of the different lineages, we next examined the gene families adjacent to each Cpt1 gene locus in a variety of species (Figs 2 and 3). The Cpt1a locus displays a high degree of synteny conservation. For example, Mtl5 flanks Cpt1a in all of the examined Sarcopterygii species (Fig 2A), with the exception of X. tropicalis whose genome assembly at this locus is still very poor. In the paralogous Cpt1aa and Cpt1ab loci of D. rerio, the gene conservation is less evident, with the vast majority of genes having their H. sapiens orthologues mapping to chromosome 11 but at a distinct genomic region. However, adjacent to the fish Cpt1ab we found a novel gene family which although absent from mammals flanks the L. chalumnae and A. carolinensis Cpt1a orthologue (SIST-binding protein like) (Fig 2A). Comparative synteny statistical analysis was performed for H. sapiens vs A. carolinesis and H. sapiens vs D. rerio (Fig 2B). In both cases we find that the analysed chromosomal segments are orthologous to the corresponding locus in H. sapiens. In D. rerio the analysed chromosomal segment was expanded (gaps< = 100) to accommodate the highly rearranged nature of this locus in D. rerio. However the minimal number of genes was also proportionally increased, to maintain the statistical sensitivity. The analysis was not performed for X. tropicalis given that Cpt1a gene in this species is placed in an independent unplaced scaffold with no information on the neighbouring genes. Additionally, phylogenetic analysis of neighbouring genes Mtl5 and Sits-like, supports the orthology of these sequences across different species (S4 Fig) and thus the common origin of this locus.


The Origin and Diversity of Cpt1 Genes in Vertebrate Species.

Lopes-Marques M, Delgado IL, Ruivo R, Torres Y, Sainath SB, Rocha E, Cunha I, Santos MM, Castro LF - PLoS ONE (2015)

A. Synteny maps of Cpt1b in selected vertebrate genomes. Chromosome (Chr.) and position in mega base pairs (Mb) locations are given for the gene of interest in each species. The location of the H. sapiens orthologue is also given for non-conserved neighbouring genes in the other species analysed. Red dots indicate end of the chromosome or scaffold. B. Statistical synteny analysis. Reported p-values indicate the probability of identifying non homologous chromosomal segments, and S indicates the size of the chromosomal segment identified.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4589379&req=5

pone.0138447.g003: A. Synteny maps of Cpt1b in selected vertebrate genomes. Chromosome (Chr.) and position in mega base pairs (Mb) locations are given for the gene of interest in each species. The location of the H. sapiens orthologue is also given for non-conserved neighbouring genes in the other species analysed. Red dots indicate end of the chromosome or scaffold. B. Statistical synteny analysis. Reported p-values indicate the probability of identifying non homologous chromosomal segments, and S indicates the size of the chromosomal segment identified.
Mentions: To further clarify the orthology/paralogy relationships of the Cpt1 gene repertoire of the different lineages, we next examined the gene families adjacent to each Cpt1 gene locus in a variety of species (Figs 2 and 3). The Cpt1a locus displays a high degree of synteny conservation. For example, Mtl5 flanks Cpt1a in all of the examined Sarcopterygii species (Fig 2A), with the exception of X. tropicalis whose genome assembly at this locus is still very poor. In the paralogous Cpt1aa and Cpt1ab loci of D. rerio, the gene conservation is less evident, with the vast majority of genes having their H. sapiens orthologues mapping to chromosome 11 but at a distinct genomic region. However, adjacent to the fish Cpt1ab we found a novel gene family which although absent from mammals flanks the L. chalumnae and A. carolinensis Cpt1a orthologue (SIST-binding protein like) (Fig 2A). Comparative synteny statistical analysis was performed for H. sapiens vs A. carolinesis and H. sapiens vs D. rerio (Fig 2B). In both cases we find that the analysed chromosomal segments are orthologous to the corresponding locus in H. sapiens. In D. rerio the analysed chromosomal segment was expanded (gaps< = 100) to accommodate the highly rearranged nature of this locus in D. rerio. However the minimal number of genes was also proportionally increased, to maintain the statistical sensitivity. The analysis was not performed for X. tropicalis given that Cpt1a gene in this species is placed in an independent unplaced scaffold with no information on the neighbouring genes. Additionally, phylogenetic analysis of neighbouring genes Mtl5 and Sits-like, supports the orthology of these sequences across different species (S4 Fig) and thus the common origin of this locus.

Bottom Line: The later is considered a mammalian innovation resulting from a gene duplication event in the ancestor of mammals, after the divergence of sauropsids.In contrast, Cpt1a2 has been found exclusively in teleosts.Finally, we propose that loss of Cpt1b is the likely cause for the unusual energy metabolism of elasmobranch.

View Article: PubMed Central - PubMed

Affiliation: CIIMAR, Interdisciplinary Centre of Marine and Environmental Research, CIMAR Associate Laboratory, UPorto-University of Porto, Porto, Portugal; ICBAS, Abel Salazar Biomedical Sciences Institute, University of Porto, Porto, Portugal.

ABSTRACT
The Carnitine palmitoyltransferase I (Cpt1) gene family plays a crucial role in energy homeostasis since it is required for the occurrence of fatty acid β-oxidation in the mitochondria. The exact gene repertoire in different vertebrate lineages is variable. Presently, four genes are documented: Cpt1a, also known as Cpt1a1, Cpt1a2; Cpt1b and Cpt1c. The later is considered a mammalian innovation resulting from a gene duplication event in the ancestor of mammals, after the divergence of sauropsids. In contrast, Cpt1a2 has been found exclusively in teleosts. Here, we reassess the overall evolutionary relationships of Cpt1 genes using a combination of approaches, including the survey of the gene repertoire in basal gnathostome lineages. Through molecular phylogenetics and synteny studies, we find that Cpt1c is most likely a rapidly evolving orthologue of Cpt1a2. Thus, Cpt1c is present in other lineages such as cartilaginous fish, reptiles, amphibians and the coelacanth. We show that genome duplications (2R) and variable rates of sequence evolution contribute to the history of Cpt1 genes in vertebrates. Finally, we propose that loss of Cpt1b is the likely cause for the unusual energy metabolism of elasmobranch.

No MeSH data available.