The evolutionary history of the stearoyl-CoA desaturase gene family in vertebrates

BackgroundStearoyl-CoA desaturases (SCDs) are key enzymes involved in de novo monounsaturated fatty acid synthesis. They catalyze the desaturation of saturated fatty acyl-CoA substrates at the delta-9 position, generating essential components of phospholipids, triglycerides, cholesterol esters and wax esters. Despite being crucial for interpreting SCDs roles across species, the evolutionary history of the SCD gene family in vertebrates has yet to be elucidated, in particular their isoform diversity, origin and function. This work aims to contribute to this fundamental effort.ResultsWe show here, through comparative genomics and phylogenetics that the SCD gene family underwent an unexpectedly complex history of duplication and loss events. Paralogy analysis hints that SCD1 and SCD5 genes emerged as part of the whole genome duplications (2R) that occurred at the stem of the vertebrate lineage. The SCD1 gene family expanded in rodents with the parallel loss of SCD5 in the Muridae family. The SCD1 gene expansion is also observed in the Lagomorpha although without the SCD5 loss. In the amphibian Xenopus tropicalis we find a single SCD1 gene but not SCD5, though this could be due to genome incompleteness. In the analysed teleost species no SCD5 is found, while the surrounding SCD5-less locus is conserved in comparison to tetrapods. In addition, the teleost SCD1 gene repertoire expanded to two copies as a result of the teleost specific genome duplication (3R). Finally, we describe clear orthologues of SCD1 and SCD5 in the chondrichthian, Scyliorhinus canicula, a representative of the oldest extant jawed vertebrate clade. Expression analysis in S. canicula shows that whilst SCD1 is ubiquitous, SCD5 is mainly expressed in the brain, a pattern which might indicate an evolutionary conserved function.ConclusionWe conclude that the SCD1 and SCD5 genes emerged as part of the 2R genome duplications. We propose that the evolutionary conserved gene expression between distinct lineages underpins the importance of SCD activity in the brain (and probably the pancreas), in a yet to be defined role. We argue that an expression independent of an external stimulus, such as diet induced activity, emerged as a novel function in vertebrate ancestry allocated to the SCD5 isoform in various tissues (e.g. brain and pancreas), and it was selectively maintained throughout vertebrate evolution.

[1]  H. Enoch,et al.  Mechanism of rat liver microsomal stearyl-CoA desaturase. Studies of the substrate specificity, enzyme-substrate interactions, and the function of lipid. , 1976, The Journal of biological chemistry.

[2]  A. T. James,et al.  The control of stearoyl‐CoA desaturase by dietary linoleic acid , 1978, FEBS letters.

[3]  K. Kaestner,et al.  Differentiation-induced gene expression in 3T3-L1 preadipocytes. Characterization of a differentially expressed gene encoding stearoyl-CoA desaturase. , 1988, The Journal of biological chemistry.

[4]  J. Ntambi,et al.  The regulation of stearoyl-CoA desaturase (SCD). , 1995, Progress in lipid research.

[5]  Roderic D. M. Page,et al.  TreeView: an application to display phylogenetic trees on personal computers , 1996, Comput. Appl. Biosci..

[6]  G. Durand,et al.  Endogenous synthesis cannot compensate for absence of dietary oleic acid in rats. , 1997, The Journal of nutrition.

[7]  John Shanklin,et al.  DESATURATION AND RELATED MODIFICATIONS OF FATTY ACIDS1. , 1998, Annual review of plant physiology and plant molecular biology.

[8]  W. Lee,et al.  Fatty Acid Transport and Utilization for the Developing Brain , 1998, Journal of neurochemistry.

[9]  S. Henikoff,et al.  Consensus-degenerate hybrid oligonucleotide primers for amplification of distantly related sequences. , 1998, Nucleic acids research.

[10]  J. Kamholz,et al.  Regulation of Oleoyl‐CoA Synthesis in the Peripheral Nervous System: Demonstration of a Link with Myelin Synthesis , 1998, Journal of neurochemistry.

[11]  S. Clarke,et al.  Omega-3 polyunsaturated fatty acid regulation of gene expression. , 2000, Current opinion in lipidology.

[12]  M. Miyazaki,et al.  The Biosynthesis of Hepatic Cholesterol Esters and Triglycerides Is Impaired in Mice with a Disruption of the Gene for Stearoyl-CoA Desaturase 1* , 2000, The Journal of Biological Chemistry.

[13]  P. Holland,et al.  Evidence for 14 homeobox gene clusters in human genome ancestry , 2000, Current Biology.

[14]  S Rozen,et al.  Primer3 on the WWW for general users and for biologist programmers. , 2000, Methods in molecular biology.

[15]  C. Kuo,et al.  Molecular cloning of full‐length cDNA encoding delta‐9 desaturase through PCR strategies and its genomic organization and expression in grass carp (Ctenopharyngodon idella) * , 2001, Molecular reproduction and development.

[16]  J. Sundberg,et al.  Scd3--a novel gene of the stearoyl-CoA desaturase family with restricted expression in skin. , 2001, Genomics.

[17]  B. Yandell,et al.  Loss of stearoyl–CoA desaturase-1 function protects mice against adiposity , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[18]  J. Friedman,et al.  Identification and Characterization of Murine SCD4, a Novel Heart-specific Stearoyl-CoA Desaturase Isoform Regulated by Leptin and Dietary Factors* , 2003, Journal of Biological Chemistry.

[19]  A. Cossins,et al.  Differential expression of cold- and diet-specific genes encoding two carp liver delta 9-acyl-CoA desaturase isoforms. , 2003, American journal of physiology. Regulatory, integrative and comparative physiology.

[20]  M. Miyazaki,et al.  Role of stearoyl-coenzyme A desaturase in lipid metabolism. , 2003, Prostaglandins, leukotrienes, and essential fatty acids.

[21]  A. Coulson,et al.  Dispersal of NK homeobox gene clusters in amphioxus and humans , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[22]  S. O’Brien,et al.  Placental mammal diversification and the Cretaceous–Tertiary boundary , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[23]  O. Gascuel,et al.  A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. , 2003, Systematic biology.

[24]  Charles E. Chapple,et al.  Genome duplication in the teleost fish Tetraodon nigroviridis reveals the early vertebrate proto-karyotype , 2004, Nature.

[25]  H. Sampath,et al.  Polyunsaturated fatty acid regulation of gene expression. , 1998, The Journal of nutrition.

[26]  David Posada,et al.  ProtTest: selection of best-fit models of protein evolution , 2005, Bioinform..

[27]  R. Schmidt,et al.  Characterization of HSCD5, a novel human stearoyl-CoA desaturase unique to primates. , 2005, Biochemical and biophysical research communications.

[28]  A. Graham,et al.  Vertebrate neurogenin evolution: long-term maintenance of redundant duplicates , 2005, Development Genes and Evolution.

[29]  P. Holland,et al.  Breakup of a homeobox cluster after genome duplication in teleosts , 2006, Proceedings of the National Academy of Sciences.

[30]  James M. Ntambi,et al.  Polyunsaturated fatty acid regulation of gene expression , 2001, Journal of Molecular Neuroscience.

[31]  M. Nei,et al.  MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. , 2007, Molecular biology and evolution.

[32]  T. Hsieh,et al.  Influence of dietary lipids on the fatty acid composition and stearoyl-CoA desaturase expression in hybrid tilapia (Oreochromis niloticusxO. aureus) under cold shock. , 2007, Comparative biochemistry and physiology. Part B, Biochemistry & molecular biology.

[33]  Justin Johnson,et al.  Survey Sequencing and Comparative Analysis of the Elephant Shark (Callorhinchus milii) Genome , 2007, PLoS biology.

[34]  B. Corl,et al.  Identification and Characterization of a Novel Bovine Stearoyl-CoA Desaturase Isoform with Homology to Human SCD5 , 2007, Lipids.

[35]  Y. Qian,et al.  Identification and Characterization of Hamster Stearoyl-CoA Desaturase Isoforms , 2008, Lipids.

[36]  B. Corl,et al.  Comparison of pig, sheep and chicken SCD5 homologs: Evidence for an early gene duplication event. , 2008, Comparative biochemistry and physiology. Part B, Biochemistry & molecular biology.

[37]  J. Rogers,et al.  Ancient and modern duplication events and the evolution of stearoyl-CoA desaturases in teleost fishes. , 2008, Physiological genomics.

[38]  Nicholas H. Putnam,et al.  The amphioxus genome and the evolution of the chordate karyotype , 2008, Nature.

[39]  M. Cnop Fatty acids and glucolipotoxicity in the pathogenesis of Type 2 diabetes. , 2008, Biochemical Society transactions.

[40]  Kathryn E Crosier,et al.  Intestinal differentiation in zebrafish requires Cdx1b, a functional equivalent of mammalian Cdx2. , 2008, Gastroenterology.

[41]  J. Ntambi,et al.  Role of stearoyl-coenzyme A desaturase in regulating lipid metabolism , 2008, Current opinion in lipidology.

[42]  S. Aizawa,et al.  The genus Polypterus (bichirs): a fish group diverged at the stem of ray-finned fishes (Actinopterygii). , 2009, Cold Spring Harbor protocols.

[43]  J. Gustafsson,et al.  Susceptibility of Pancreatic Beta Cells to Fatty Acids Is Regulated by LXR/PPARα-Dependent Stearoyl-Coenzyme A Desaturase , 2009, PloS one.

[44]  Ó. Monroig,et al.  Highly Unsaturated Fatty Acid Synthesis in Atlantic Salmon: Characterization of ELOVL5- and ELOVL2-like Elongases , 2009, Marine Biotechnology.

[45]  P. Holland,et al.  Parallel Retention of Pdx2 Genes in Cartilaginous Fish and Coelacanths , 2010, Molecular biology and evolution.

[46]  C. Mounier,et al.  Hormonal and nutritional regulation of SCD1 gene expression. , 2011, Biochimie.