Relaxed functional constraints on triplicate α-globin gene in the bank vole suggest a different evolutionary history from other rodents

. 2014 Jul ; 113 (1) : 64-73. [epub] 20140305

Jazyk angličtina Země Velká Británie, Anglie Médium print-electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid24595364

Gene duplication plays an important role in the origin of evolutionary novelties, but the mechanisms responsible for the retention and functional divergence of the duplicated copy are not fully understood. The α-globin genes provide an example of a gene family with different numbers of gene duplicates among rodents. Whereas Rattus and Peromyscus each have three adult α-globin genes (HBA-T1, HBA-T2 and HBA-T3), Mus has only two copies. High rates of amino acid evolution in the independently derived HBA-T3 genes of Peromyscus and Rattus have been attributed to positive selection. Using RACE PCR, reverse transcription-PCR (RT-PCR) and RNA-seq, we show that another rodent, the bank vole Clethrionomys glareolus, possesses three transcriptionally active α-globin genes. The bank vole HBA-T3 gene is distinguished from each HBA-T1 and HBA-T2 by 20 amino acids and is transcribed 23- and 4-fold lower than HBA-T1 and HBA-T2, respectively. Polypeptides corresponding to all three genes are detected by electrophoresis, demonstrating that the translated products of HBA-T3 are present in adult erythrocytes. Patterns of codon substitution and the presence of low-frequency null alleles suggest a postduplication relaxation of purifying selection on bank vole HBA-T3.

Zobrazit více v PubMed

Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. (1990). Basic local alignment search tool. J Mol Biol 215: 403–410. PubMed

Arnold K, Bordoli L, Kopp J, Schwede T. (2006). The SWISS-MODEL Workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22: 195–201. PubMed

Ashkenazy H, Erez E, Martz E, Pupko T, Ben-Tal N. (2010). ConSurf 2010: calculating evolutionary conservation in sequence and structure of proteins and nucleic acids. Nucleic Acids Res 38: W529–W533. PubMed PMC

Baker KE, Parker R. (2004). Nonsense-mediated mRNA decay: terminating erroneous gene expression. Curr Opin Cell Biol 16: 293. PubMed

Betrán E, Long M. (2002). Expansion of genome coding regions by acquisition of new genes. Genetica 115: 65–80. PubMed

Betrán E, Rozas J, Navarro A, Barbadilla A. (1997). The estimation of the number and the length distribution of gene conversion tracts from population DNA sequence data. Genetics 146: 89–99. PubMed PMC

Bielawski JP, Yang Z. (2004). A maximum likelihood method for detecting functional divergence at individual codon sites, with application to gene family evolution. J Mol Evol 59: 121–132. PubMed

Brodsky I, Dennis LH, Kahn SB, Brady LW. (1966). Normal mouse erythropoiesis. I. The role of the spleen in mouse erythropoiesis. Cancer Res 26: 198–201. PubMed

Campos R, Storz JF, Ferrand N. (2012). Copy number polymorphism in the α-globin gene cluster of European rabbit (Oryctolagus cuniculus). Heredity 108: 531–536. PubMed PMC

Cheng TC, Polmar SK, Kazazian HH. (1974). Isolation and characterization of modified globin messenger ribonucleic acid from erythropoietic mouse spleen. J Biol Chem 249: 1781–1788. PubMed

Colangelo P, Aloise G, Franchini P, Amori G. (2012). Mitochondrial DNA reveals hidden diversity and an ancestral lineage of the bank vole in the Italian peninsula. J Zool 287: 41–52.

Colbourne JK, Pfrender ME, Gilbert D, Thomas WK, Tucker A, Oakley TH et al. (2011). The ecoresponsive genome of Daphnia pulex. Science 331: 555–561. PubMed PMC

Cook JA, Runck AM, Conroy CJ. (2004). Historical biogeography at the crossroads of the northern continents: molecular phylogenetics of red-backed voles (Rodentia: Arvicolinae). Mol Phylogenet Evol 30: 767–777. PubMed

Darriba D, Taboada GL, Doallo R, Posada D. (2012). jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9: 772. PubMed PMC

Ding Y, Zhou Q, Wang W. (2012). Origins of new genes and evolution of their novel functions. Annu Rev Ecol Evol Syst 43: 345–363.

Duffy LK, Genaux CT, Stratton LP. (1976). Amino acid differences between the α-chains from two hemoglobins of the yellow-cheeked vole (family Cricetidae). Biochem Genet 14: 809–821. PubMed

Fabre P-H, Hautier L, Dimitrov D, Douzery EJP. (2012). A glimpse on the pattern of rodent diversification: a phylogenetic approach. BMC Evol Biol 12: 88. PubMed PMC

Ferrand N. (1989). Biochemical and genetic studies on rabbit hemoglobin. I. Electrophoretic polymorphism of the beta chain. Biochem Genet 27: 673–678. PubMed

Fontanillas P, Landry CR, Wittkopp PJ, Russ C, Gruber JD, Nusbaum C et al. (2010). Key considerations for measuring allelic expression on a genomic scale using high-throughput sequencing. Mol Ecol 19: 212–227. PubMed PMC

Force A, Lynch M, Pickett FB, Amores A, Yan YL, Postlethwait J. (1999). Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151: 1531–1545. PubMed PMC

Friedman R, Austin LH. (2001). Pattern and timing of gene duplication in animal genomes. Genome Res 11: 1842–1847. PubMed PMC

Hahn MW. (2009). Distinguishing among evolutionary models for the maintenance of gene duplicates. J Hered 100: 605–617. PubMed

Hoffmann FG, Opazo JC, Storz JF. (2008). Rapid rates of lineage specific gene duplication and deletion in the α-globin gene family. Mol Biol Evol 25: 591–602. PubMed

Hoffmann FG, Storz JF. (2007). The αD-globin gene originated via duplication of an embryonic α-like globin gene in the ancestor of tetrapod vertebrates. Mol Biol Evol 24: 1982–1990. PubMed

Hoffmann FG, Storz JF, Gorr TA, Opazo JC. (2010). Lineage-specific patterns of functional diversification in the α- and β-globin gene families of tetrapod vertebrates. Mol Biol Evol 27: 1126–1138. PubMed PMC

Huelsenbeck JP, Ronquist F. (2001). MRBAYES: Bayesian inference of phylogeny. Bioinformatics 17: 754–755. PubMed

Hughes AL. (1994). The evolution of functionally novel proteins after gene duplication. Proc Biol Sci 256: 119–124. PubMed

Innan H, Kondrashov F. (2010). The evolution of gene duplications: classifying and distinguishing between models. Nat Rev Genet 11: 97–108. PubMed

Kaessmann H. (2010). Origins, evolution, and phenotypic impact of new genes. Genome Res 20: 1313–1326. PubMed PMC

Kosakovsky Pond SL, Frost SDW. (2005). Datamonkey: rapid detection of selective pressure on individual sites of codon alignments. Bioinformatics 21: 2531–2533. PubMed

Kosakovsky Pond SL, Frost SDW, Muse SV. (2005). HyPhy: hypothesis testing using phylogenies. Bioinformatics 21: 676–679. PubMed

Librado P, Rozas J. (2009). DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25: 1451–1452. PubMed

Lynch M, Conery JS. (2003). The evolutionary demography of duplicate genes. J Struct Funct Genomics 3: 35–44. PubMed

Lynch M, Conery JS. (2000). The evolutionary fate and consequences of duplicate genes. Science 290: 1151–1155. PubMed

Maquat LE. (2004). Nonsense-mediated mRNA decay: splicing, translation and mRNP dynamics. Nat Rev Mol Cell Biol 5: 89–99. PubMed

Maquat LE. (2005). Nonsense-mediated mRNA decay in mammals. J Cell Sci 118: 1773–1776. PubMed

Nielsen R, Yang Z. (1998). Likelihood models for detecting positively selected amino acid sites and applications to the HIV-1 envelope gene. Genetics 148: 929–936. PubMed PMC

Ohno S. (1970) Evolution by Gene Duplication. Springer Verlag: New York.

Pegueroles C, Laurie S, Alba MM. (2013). Accelerated evolution after gene duplication: a time-dependent process affecting just one copy. Mol Biol Evol 30: 1830–1842. PubMed

Robin GC, Russell RJ, Cutler DJ, Oakeshott JG. (2000). The evolution of an alpha-esterase pseudogene inactivated in the Drosophila melanogaster lineage. Mol Biol Evol 17: 563–575. PubMed

Ronquist F, Huelsenbeck JP. (2003). MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572–1574. PubMed

Sawyer SA. (1989). Statistical tests for detecting gene conversion. Mol Biol Evol 6: 526–538. PubMed

Sawyer SA. (1999). GENECONV: A computer package for the statistical detection of gene conversion. Distributed by the author, Department of Mathematics, Washington University in St. Louis, available at http://www.math.wustl.edu/~sawyer.

Storz JF. (2007). Hemoglobin function and physiological adaptation to hypoxia in high-altitude mammals. J Mammal 88: 24–31.

Storz JF. (2009). Genome evolution: gene duplication and the resolution of adaptive conflict. Heredity 102: 99–100. PubMed PMC

Storz JF, Baze M, Waite JL, Hoffmann FG, Opazo JC, Hayes JP. (2007. b). Complex signatures of selection and gene conversion in the duplicated globin genes of house mice. Genetics 177: 481–500. PubMed PMC

Storz JF, Hoffmann FG, Opazo JC, Moriyama H. (2008). Adaptive functional divergence among triplicated α-globin genes in rodents. Genetics 178: 1623–1638. PubMed PMC

Storz JF, Opazo JC, Hoffmann FG. (2011). Phylogenetic diversification of the globin gene superfamily in chordates. IUBMB Life 63: 313–322. PubMed PMC

Storz JF, Opazo JC, Hoffmann FG. (2013). Gene duplication, genome duplication, and the functional diversification of vertebrate globins. Mol Phylogenet Evol 66: 469–478. PubMed PMC

Storz JF, Runck AM, Moriyama H, Weber RE, Fago A. (2010). Genetic differences in hemoglobin function between highland and lowland deer mice. J Exp Biol 213: 565–2574. PubMed PMC

Storz JF, Sabatino SJ, Hoffmann FG, Gering EJ, Moriyama H, Ferrand N et al. (2007. a). The molecular basis of high-altitude adaptation in deer mice. PLoS Genet 3: 448–459. PubMed PMC

Swofford DL. (2003) PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods) Version 4.0b10 Sinauer Associates: Sunderland, Massachusetts.

Tautz D, Domazet-Lošo T. (2011). The evolutionary origin of orphan genes. Nat Rev Genet 12: 692–702. PubMed

Tesakov AS, Lebedev VS, Bannikova AA, Abramson NI. (2010). Clethrionomys Tilesius, 1850 is the valid generic name for red-backed voles and Myodes Pallas, 1811 is a junior synonym of Lemmus Link, 1795. Russian J Theriol 9: 83–86.

Thein SL. (2004). Genetic insights into the clinical diversity of beta thalassaemia. Br J Haematol 124: 264–274. PubMed

Tufarelli C, Hardison R, Miller W, Hughes J, Clark K, Ventress N et al. (2004). Comparative analysis of the alpha-like globin clusters in mouse, rat, and human chromosomes indicates a mechanism underlying breaks in conserved synteny. Genome Res 14: 623–630. PubMed PMC

Wołk E. (1983). Ontogenetic changes in the hemoglobin of the bank vole. Acta Theriol 28: 387–396.

Yang Z. (1997). PAML: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci 13: 555–556. PubMed

Yang Z. (1998). Likelihood ratio tests for detecting positive selection and application to primate lysozyme evolution. Mol Biol Evol 15: 568–573. PubMed

Yang Z. (2007). PAML 4: Phylogenetic analysis by maximum likelihood. Mol Biol Evol 24: 1586–1591. PubMed

Yang Z, Wong WSW, Nielsen R. (2005). Bayes empirical Bayes inference of amino acid sites under positive selection. Mol Biol Evol 22: 1107–1118. PubMed

Yingzhong Y, Yue C, Guoen J, Zhenzhong B, Lan M, Haixia Y et al. (2007). Molecular cloning and characterization of hemoglobin alpha and beta chains from plateau pika (Ochotona curzoniae) living at high altitude. J Biochem Mol Biol 40: 426–431. PubMed

Zhang J. (2003). Evolution by gene duplication: an update. Trends Ecol Evol 18: 292–298.

Zhang J, Nielsen R, Yang Z. (2005). Evaluation of an improved branch-site likelihood method for detecting positive selection at the molecular level. Mol Biol Evol 22: 2472–2479. PubMed

Zwickl D. (2006) Genetic Algorithm Approaches for the Phylogenetic Analysis of Large Biological Sequence Datasets Under the Maximum Likelihood Criterion PhD Thesis. University of Texas at Austin, Austin, TX.

Zobrazit více v PubMed

GENBANK
KF958827, KF958828, KF958829, KF958830, KF958831, KF958832, KF958833, KF958834, KF958835, KF958836, KF958837

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...