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Functional desaturase Fads1 (Δ5) and Fads2 (Δ6) orthologues evolved before the origin of jawed vertebrates.

Castro LF, Monroig Ó, Leaver MJ, Wilson J, Cunha I, Tocher DR - PLoS ONE (2012)

Bottom Line: With respect to desaturation activities some noteworthy differences have been noted in vertebrate classes.To determine the timing of Fads1-Δ5 and Fads2-Δ6 evolution in vertebrates we used a combination of comparative and functional genomics with the analysis of key phylogenetic species.Our findings enlighten the history of a crucially important gene family in vertebrate fatty acid metabolism and physiology and provide an explanation of how observed lineage-specific gene duplications, losses and diversifications might be linked to habitat-specific food web structures in different environments and over geological timescales.

View Article: PubMed Central - PubMed

Affiliation: CIIMAR - Interdisciplinary Centre of Marine and Environmental Research, CIMAR Associate Laboratory, University of Porto, Porto, Portugal. filipe.castro@ciimar.up.pt

ABSTRACT
Long-chain polyunsaturated fatty acids (LC-PUFAs) such as arachidonic (ARA), eicosapentaenoic (EPA) and docosahexaenoic (DHA) acids are essential components of biomembranes, particularly in neural tissues. Endogenous synthesis of ARA, EPA and DHA occurs from precursor dietary essential fatty acids such as linoleic and α-linolenic acid through elongation and Δ5 and Δ6 desaturations. With respect to desaturation activities some noteworthy differences have been noted in vertebrate classes. In mammals, the Δ5 activity is allocated to the Fads1 gene, while Fads2 is a Δ6 desaturase. In contrast, teleosts show distinct combinations of desaturase activities (e.g. bifunctional or separate Δ5 and Δ6 desaturases) apparently allocated to Fads2-type genes. To determine the timing of Fads1-Δ5 and Fads2-Δ6 evolution in vertebrates we used a combination of comparative and functional genomics with the analysis of key phylogenetic species. Our data show that Fads1 and Fads2 genes with Δ5 and Δ6 activities respectively, evolved before gnathostome radiation, since the catshark Scyliorhinus canicula has functional orthologues of both gene families. Consequently, the loss of Fads1 in teleosts is a secondary episode, while the existence of Δ5 activities in the same group most likely occurred through independent mutations into Fads2 type genes. Unexpectedly, we also establish that events of Fads1 gene expansion have taken place in birds and reptiles. Finally, a fourth Fads gene (Fads4) was found with an exclusive occurrence in mammalian genomes. Our findings enlighten the history of a crucially important gene family in vertebrate fatty acid metabolism and physiology and provide an explanation of how observed lineage-specific gene duplications, losses and diversifications might be linked to habitat-specific food web structures in different environments and over geological timescales.

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Maximum likelihood tree for the Fads gene family based on protein sequences. aLRT values are shown on each node.Accession numbers of the sequences are given in table S1.
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pone-0031950-g002: Maximum likelihood tree for the Fads gene family based on protein sequences. aLRT values are shown on each node.Accession numbers of the sequences are given in table S1.

Mentions: The search of Fads front-end desaturases in vertebrate genomes uncovered an unexpected diversity of genes. To model the relative timing of duplication and evolutionary histories, we next examined their phylogenetic relationships (Figure 2). Apart from the desaturases identified above, we also included other reported Fads sequences in particular from teleosts. Two well-supported clades can be observed, one including Fads1-like sequences (aLRT 0.958) and a second with Fads2, Fads3 and the novel mammal-specific gene family which we name Fads4 (aLRT 0.990). The Fads1 clade includes sequences from tetrapod species but not teleosts. Furthermore, the unexpected high number of Fads sequences found in reptiles and birds can now be unequivocally attributed to a lineage-specific expansion of the Fads1 gene group. We labelled each bird and reptile species gene (a to e) according to their position in the cluster (see below). In the Fads2/3/4 clade we find that mammalian species have single copy genes of Fads2, Fads3 and Fads4, though the entire group does not form an independent well supported clade. Fads3 and Fads4 are outgrouped by the chicken and anolis Fads2 but this is a poorly supported clade. This larger collection is outgrouped by the amphibian and teleost FADS2 genes. We opted to maintain the gene nomenclature, although the mammalian Fads2, Fads3 and Fads4 are probably co-orthologues of the remaining Fads2 sequences. Though some teleost species have more than one Fads gene these have clearly resulted from species-specific expansions as well (e.g. Atlantic salmon). Thus, the present phylogenetic tree suggests that teleosts have probably lost a Fads1 orthologue; an expansion of a Fads1-like gene took place in the ancestor of birds and reptiles; and the Fads2/3/4 duplications are specific to mammals.


Functional desaturase Fads1 (Δ5) and Fads2 (Δ6) orthologues evolved before the origin of jawed vertebrates.

Castro LF, Monroig Ó, Leaver MJ, Wilson J, Cunha I, Tocher DR - PLoS ONE (2012)

Maximum likelihood tree for the Fads gene family based on protein sequences. aLRT values are shown on each node.Accession numbers of the sequences are given in table S1.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3285190&req=5

pone-0031950-g002: Maximum likelihood tree for the Fads gene family based on protein sequences. aLRT values are shown on each node.Accession numbers of the sequences are given in table S1.
Mentions: The search of Fads front-end desaturases in vertebrate genomes uncovered an unexpected diversity of genes. To model the relative timing of duplication and evolutionary histories, we next examined their phylogenetic relationships (Figure 2). Apart from the desaturases identified above, we also included other reported Fads sequences in particular from teleosts. Two well-supported clades can be observed, one including Fads1-like sequences (aLRT 0.958) and a second with Fads2, Fads3 and the novel mammal-specific gene family which we name Fads4 (aLRT 0.990). The Fads1 clade includes sequences from tetrapod species but not teleosts. Furthermore, the unexpected high number of Fads sequences found in reptiles and birds can now be unequivocally attributed to a lineage-specific expansion of the Fads1 gene group. We labelled each bird and reptile species gene (a to e) according to their position in the cluster (see below). In the Fads2/3/4 clade we find that mammalian species have single copy genes of Fads2, Fads3 and Fads4, though the entire group does not form an independent well supported clade. Fads3 and Fads4 are outgrouped by the chicken and anolis Fads2 but this is a poorly supported clade. This larger collection is outgrouped by the amphibian and teleost FADS2 genes. We opted to maintain the gene nomenclature, although the mammalian Fads2, Fads3 and Fads4 are probably co-orthologues of the remaining Fads2 sequences. Though some teleost species have more than one Fads gene these have clearly resulted from species-specific expansions as well (e.g. Atlantic salmon). Thus, the present phylogenetic tree suggests that teleosts have probably lost a Fads1 orthologue; an expansion of a Fads1-like gene took place in the ancestor of birds and reptiles; and the Fads2/3/4 duplications are specific to mammals.

Bottom Line: With respect to desaturation activities some noteworthy differences have been noted in vertebrate classes.To determine the timing of Fads1-Δ5 and Fads2-Δ6 evolution in vertebrates we used a combination of comparative and functional genomics with the analysis of key phylogenetic species.Our findings enlighten the history of a crucially important gene family in vertebrate fatty acid metabolism and physiology and provide an explanation of how observed lineage-specific gene duplications, losses and diversifications might be linked to habitat-specific food web structures in different environments and over geological timescales.

View Article: PubMed Central - PubMed

Affiliation: CIIMAR - Interdisciplinary Centre of Marine and Environmental Research, CIMAR Associate Laboratory, University of Porto, Porto, Portugal. filipe.castro@ciimar.up.pt

ABSTRACT
Long-chain polyunsaturated fatty acids (LC-PUFAs) such as arachidonic (ARA), eicosapentaenoic (EPA) and docosahexaenoic (DHA) acids are essential components of biomembranes, particularly in neural tissues. Endogenous synthesis of ARA, EPA and DHA occurs from precursor dietary essential fatty acids such as linoleic and α-linolenic acid through elongation and Δ5 and Δ6 desaturations. With respect to desaturation activities some noteworthy differences have been noted in vertebrate classes. In mammals, the Δ5 activity is allocated to the Fads1 gene, while Fads2 is a Δ6 desaturase. In contrast, teleosts show distinct combinations of desaturase activities (e.g. bifunctional or separate Δ5 and Δ6 desaturases) apparently allocated to Fads2-type genes. To determine the timing of Fads1-Δ5 and Fads2-Δ6 evolution in vertebrates we used a combination of comparative and functional genomics with the analysis of key phylogenetic species. Our data show that Fads1 and Fads2 genes with Δ5 and Δ6 activities respectively, evolved before gnathostome radiation, since the catshark Scyliorhinus canicula has functional orthologues of both gene families. Consequently, the loss of Fads1 in teleosts is a secondary episode, while the existence of Δ5 activities in the same group most likely occurred through independent mutations into Fads2 type genes. Unexpectedly, we also establish that events of Fads1 gene expansion have taken place in birds and reptiles. Finally, a fourth Fads gene (Fads4) was found with an exclusive occurrence in mammalian genomes. Our findings enlighten the history of a crucially important gene family in vertebrate fatty acid metabolism and physiology and provide an explanation of how observed lineage-specific gene duplications, losses and diversifications might be linked to habitat-specific food web structures in different environments and over geological timescales.

Show MeSH
Related in: MedlinePlus