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Characterization of Maltase Clusters in the Genus Drosophila

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Abstract

To reveal evolutionary history of maltase gene family in the genus Drosophila, we undertook a bioinformatics study of maltase genes from available genomes of 12 Drosophila species. Molecular evolution of a closely related glycoside hydrolase, the α-amylase, in Drosophila has been extensively studied for a long time. The α-amylases were even used as a model of evolution of multigene families. On the other hand, maltase, i.e., the α-glucosidase, got only scarce attention. In this study, we, therefore, investigated spatial organization of the maltase genes in Drosophila genomes, compared the amino acid sequences of the encoded enzymes and analyzed the intron/exon composition of orthologous genes. We found that the Drosophila maltases are more numerous than previously thought (ten instead of three genes) and are localized in two clusters on two chromosomes (2L and 2R). To elucidate the approximate time line of evolution of the clusters, we estimated the order and dated duplication of all the 10 genes. Both clusters are the result of ancient series of subsequent duplication events, which took place from 352 to 61 million years ago, i.e., well before speciation to extant Drosophila species. Also observed was a remarkable intron/exon composition diversity of particular maltase genes of these clusters, probably a result of independent intron loss after duplication of intron-rich gene ancestor, which emerged well before speciation in a common ancestor of all extant Drosophila species.

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Abbreviations

CAZy:

Carbohydrate-Active enZymes

CSR:

Conserved sequence region

EST:

Expressed sequence tags

GH:

Glycoside hydrolase

kb:

Kilo base

LRT:

Likelihood-ratio test

ML:

Maximum likelihood

MP:

Maximum parsimony

MYA:

Million years ago

NJ:

Neighbor-joining

S.E.:

Standard error

References

  • Adams MD, Celniker SE, Holt RA, Evans CA, Venter JC et al (2000) The genome sequence of Drosophila melanogaster. Science 287:2185–2195

    Article  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Benson DA, Karsch-Mizrachi I, Lipman DJ, Ostell J, Sayers EW (2009) GenBank. Nucleic Acids Res 37(Database issue):D26–D31

    Article  CAS  PubMed  Google Scholar 

  • Beverley SM, Wilson AC (1984) Molecular evolution in Drosophila and the higher Diptera II. A time scale for fly evolution. J Mol Evol 21:1–13

    Article  CAS  PubMed  Google Scholar 

  • Birney E, Clamp M, Durbin R (2004) GeneWise and Genomewise. Genome Res 14:988–995

    Article  CAS  PubMed  Google Scholar 

  • Brown CJ, Aquadro CF, Anderson WW (1990) DNA sequence evolution of the amylase multigene family in Drosophila pseudoobscura. Genetics 126:131–138

    CAS  PubMed  Google Scholar 

  • Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, Henrissat B (2009) The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics. Nucleic Acids Res 37(Database issue):D233–D238

    Article  CAS  PubMed  Google Scholar 

  • Chiba S (1997) Molecular mechanism in α-glucosidase and glucoamylase. Biosci Biotechnol Biochem 61:1233–1239

    Article  CAS  PubMed  Google Scholar 

  • Da Lage JL, Wegnez M, Cariou ML (1996) Distribution and evolution of introns in Drosophila amylase genes. J Mol Evol 43:334–347

    Article  CAS  PubMed  Google Scholar 

  • Da Lage JL, Renard E, Chartois F, Lemeunier F, Cariou ML (1998) Amyrel, a paralogous gene of the amylase gene family in Drosophila melanogaster and the Sophophora subgenus. Proc Natl Acad Sci USA 95:6848–6853

    Article  CAS  PubMed  Google Scholar 

  • Da Lage JL, Maczkowiak F, Cariou ML (2000) Molecular characterization and evolution of the amylase multigene family of Drosophila ananassae. J Mol Evol 51:391–403

    CAS  PubMed  Google Scholar 

  • Drosophila 12 Genomes Consortium (2007) Evolution of genes and genomes on the Drosophila phylogeny. Nature 450:184–185

    Article  Google Scholar 

  • Eck RV, Dayhoff MO (1966) Atlas of protein sequence and structure. National Biomedical Research Foundation, Silver Springs, MD

    Google Scholar 

  • Ernst HA, Lo Leggio L, Willemoes M, Leonard G, Blum P, Larsen S (2006) Structure of the Sulfolobus solfataricus α-glucosidase: implicationsfor domain conservation and substrate recognition in GH31. J Mol Biol 358:1106–1124

    Article  CAS  PubMed  Google Scholar 

  • Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–376

    Article  CAS  PubMed  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Article  Google Scholar 

  • Gabrisko M, Janecek S (2009) Looking for the ancestry of the heavy-chain subunits of heteromeric amino acid transporters rBAT and 4F2hc within the GH13 α-amylase family. FEBS J 276:7265–7278

    Article  CAS  PubMed  Google Scholar 

  • Gaunt MW, Miles MA (2002) An insect molecular clock dates the origin of the insects and accords with palaeontological and biogeographic landmarks. Mol Biol Evol 19:748–761

    CAS  PubMed  Google Scholar 

  • Gilbert DG (2007) DroSpeGe: rapid access database for new Drosophila species genomes. Nucleic Acids Res 35(Database issue):D480–D485

    Article  CAS  PubMed  Google Scholar 

  • Gloster TM, Turkenburg JP, Potts JR, Henrissat B, Davies GJ (2008) Divergence of catalytic mechanism within a glycosidase family provides insight into evolution of carbohydrate metabolism by human gut flora. Chem Biol 15:1058–1067

    Article  CAS  PubMed  Google Scholar 

  • Godany A, Majzlova K, Horvathova V, Vidova B, Janecek S (2010) Tyrosine 39 of GH13 α-amylase from Thermococcus hydrothermalis contributes to its thermostability. Biologia 65:408–415

    Article  CAS  Google Scholar 

  • Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704

    Article  PubMed  Google Scholar 

  • Hartl DL, Lozovskaya ER (1994) Genome evolution: between the nucleosome and the chromosome. In: Schierwater B, Streit B, Wagner GP, DeSalle R (eds) Molecular ecology and evolution: approaches and applications. Birkhäuser Verlag, Basel, pp 579–592

    Google Scholar 

  • Henikoff S, Wallace JC (1988) Detection of protein similarities using nucleotide sequence databases. Nucleic Acids Res 16:6191–6204

    Article  CAS  PubMed  Google Scholar 

  • Huber RE, Thompson DJ (1973) Studies on a honey bee sucrase exhibiting unusual kinetics and transglucolytic activity. Biochemistry 12:4011–4020

    Article  CAS  PubMed  Google Scholar 

  • Inomata N, Yamazaki T (2000) Evolution of nucleotide substitutions and gene regulation in the amylase multigenes in Drosophila kikkawai and its sibling species. Mol Biol Evol 17:601–615

    CAS  PubMed  Google Scholar 

  • James AA, Blackmer K, Racioppi JV (1989) A salivary gland-specific, maltase-like gene of the vector mosquito, Aedes aegypti. Gene 75:73–83

    Article  CAS  PubMed  Google Scholar 

  • Janecek S (1992) New conserved amino acid region of α-amylases in the third loop of their (β/α)8-barrel domains. Biochem J 288:1069–1070

    CAS  PubMed  Google Scholar 

  • Janecek S (1994a) Sequence similarities and evolutionary relationships of microbial, plant and animal α-amylases. Eur J Biochem 224:519–524

    Article  CAS  PubMed  Google Scholar 

  • Janecek S (1994b) Parallel β/α-barrels of α-amylase, cyclodextrin glycosyltransferase and oligo-1,6-glucosidase versus the barrel of β-amylase: evolutionary distance is a reflection of unrelated sequences. FEBS Lett 353:119–123

    Article  CAS  PubMed  Google Scholar 

  • Janecek S (1995) Close evolutionary relatedness among functionally distantly related members of the (α/β)8-barrel glycosyl hydrolases suggested by the similarity of their fifth conserved sequence region. FEBS Lett 377:6–8

    Article  CAS  PubMed  Google Scholar 

  • Janecek S (2002) How many conserved sequence regions are there in the α-amylase family? Biologia 57(Suppl. 11):29–41

    CAS  Google Scholar 

  • Janecek S, Svensson B, Henrissat B (1997) Domain evolution in the α-amylase family. J Mol Evol 45:322–331

    Article  CAS  PubMed  Google Scholar 

  • Janecek S, Svensson B, MacGregor EA (2003) Relation between domain evolution, specificity, and taxonomy of the α-amylase family members containing a C-terminal starch-binding domain. Eur J Biochem 270:635–645

    Article  CAS  PubMed  Google Scholar 

  • Janecek S, Svensson B, MacGregor EA (2007) A remote but significant sequence homology between glycoside hydrolase clan GH-H and family GH31. FEBS Lett 581:1261–1268

    Article  CAS  PubMed  Google Scholar 

  • Jeanmougin F, Thompson JD, Gouy M, Higgins DG, Gibson TJ (1998) Multiple sequence alignment with Clustal X. Trends Biochem Sci 23:403–405

    Article  CAS  PubMed  Google Scholar 

  • Jeffs PS, Holmes EC, Ashburner M (1994) The molecular evolution of the alcohol dehydrogenase and alcohol dehydrogenase-related genes in the Drosophila melanogaster species subgroup. Mol Biol Evol 11:287–304

    CAS  PubMed  Google Scholar 

  • Jobb G, von Haeseler A, Strimmer K (2004) TREEFINDER: a powerful graphical analysis environment for molecular phylogenetics. BMC Evol Biol 4:18

    Article  PubMed  Google Scholar 

  • Jones DT, Taylor WR, Thornton JM (1992) The rapid generation of mutation data matrices from protein sequences. Comput Applic Biosci 8:275–282

    CAS  Google Scholar 

  • Kimura A, Takewaki S, Matsui H, Kubota M, Chiba S (1990) Allosteric properties, substrate specificity, and subsite affinities of honeybee α-glucosidase I. J Biochem 107:762–768

    CAS  PubMed  Google Scholar 

  • Kitamura M, Okuyama M, Tanzawa F, Mori H, Kitago Y, Watanabe N, Kimura A, Tanaka I, Yao M (2008) Structural and functional analysis of a glycoside hydrolase family 97 enzyme from Bacteroides thetaiotaomicron. J Biol Chem 283:36328–36337

    Article  CAS  PubMed  Google Scholar 

  • Kubota M, Tsuji M, Nishimoto M, Wongchawalit J, Okuyama M, Mori H, Matsui H, Surarit R, Svasti J, Kimura A, Chiba S (2004) Localization of α-glucosidases I, II and III in organs of European honeybee. Apis mellifera L., and origin of α-glucosidase in honey. Biosci Biotechnol Biochem 68:2346–2352

    Article  CAS  PubMed  Google Scholar 

  • Kuriki T, Imanaka T (1999) The concept of the α-amylase family: structural similarity and common catalytic mechanism. J Biosci Bioeng 87:557–565

    Article  CAS  PubMed  Google Scholar 

  • Lajoie M, Bertrand D, El-Mabrouk N (2010) Inferring the evolutionary history of gene clusters from phylogenetic and gene order data. Mol Biol Evol 27:761–772

    Article  CAS  PubMed  Google Scholar 

  • Le SQ, Gascuel O (2008) An improved general amino acid replacement matrix. Mol Biol Evol 25:132–1307

    Article  Google Scholar 

  • Lehmann J, Eisenhardt C, Stadler PF, Krauss V (2010) Some novel intron positions in conserved Drosophila genes are caused by intron sliding or tandem duplication. BMC Evol Biol 10:156

    Article  PubMed  Google Scholar 

  • Lin K, Zhang DY (2005) The excess of 5′ introns in eukaryotic genomes. Nucleic Acids Res 33:6522–6527

    Article  CAS  PubMed  Google Scholar 

  • Lodge JA, Maier T, Liebl W, Hoffmann V, Sträter N (2003) Crystal structure of Thermotoga maritima α-glucosidase AglA defines a new clan of NAD+-dependent glycosidases. J Biol Chem 278:19151–19158

    Article  CAS  PubMed  Google Scholar 

  • MacGregor EA, Janecek S, Svensson B (2001) Relationship of sequence and structure to specificity in the α-amylase family of enzymes. Biochim Biophys Acta 1546:1–20

    Article  CAS  PubMed  Google Scholar 

  • Machovic M, Janecek S (2006a) The evolution of putative starch-binding domains. FEBS Lett 580:6349–6356

    Article  CAS  PubMed  Google Scholar 

  • Machovic M, Janecek S (2006b) Starch-binding domains in the post-genome era. Cell Mol Life Sci 63:2710–2724

    Article  CAS  PubMed  Google Scholar 

  • Machovic M, Janecek S (2008) Domain evolution in the GH13 pullulanase subfamily with focus on the carbohydrate-binding module family 48. Biologia 63:1053–1064

    Article  Google Scholar 

  • Maczkowiak F, Da Lage JL (2006) Origin and evolution of the Amyrel gene in the α-amylase multigene family of Diptera. Genetica 128:145–158

    Article  CAS  PubMed  Google Scholar 

  • Matsuura Y, Kusunoki M, Harada W, Kakudo M (1984) Structure and possible catalytic residues of Taka-amylase A. J Biochem 95:697–702

    CAS  PubMed  Google Scholar 

  • Mitri C, Parmentier ML, Pin JP, Bockaert J, Grau Y (2004) Divergent evolution in metabotropic glutamate receptors. A new receptor activated by an endogenous ligand different from glutamate in insects. J Biol Chem 279:9313–9320

    Article  CAS  PubMed  Google Scholar 

  • Mitri C, Soustelle L, Framery B, Bockaert J, Parmentier ML, Grau Y (2009) Plant insecticide L-canavanine repels Drosophila via the insect orphan GPCR DmX. PLoS Biol 7:e1000147

    Article  PubMed  Google Scholar 

  • Nakajima R, Imanaka T, Aiba S (1986) Comparison of amino acid sequences of eleven different α-amylases. Appl Microbiol Biotechnol 23:355–360

    Article  CAS  Google Scholar 

  • Nishimoto M, Kubota M, Tsuji M, Mori H, Kimura A, Matsui H, Chiba S (2001) Purification and substrate specificity of honeybee. Apis mellifera L., α-glucosidase III. Biosci Biotechnol Biochem 65:1610–1616

    Article  CAS  PubMed  Google Scholar 

  • Oslancova A, Janecek S (2002) Oligo-1,6-glucosidase and neopullulanase enzyme subfamilies from the α-amylase family defined by the fifth conserved sequence region. Cell Mol Life Sci 59:1945–1959

    Article  CAS  PubMed  Google Scholar 

  • Popadic A, Anderson WW (1995) Evidence for gene conversion in the amylase multigene family of Drosophila pseudoobscura. Mol Biol Evol 12:564–572

    CAS  PubMed  Google Scholar 

  • Rigden DJ (2002) Iterative database searches demonstrate that glycoside hydrolase families 27, 31, 36 and 66 share a common evolutionary origin with family 13. FEBS Lett 523:17–22

    Article  CAS  PubMed  Google Scholar 

  • Russo CA, Takezaki N, Nei M (1995) Molecular phylogeny and divergence times of drosophilid species. Mol Biol Evol 12:391–404

    CAS  PubMed  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  PubMed  Google Scholar 

  • Shirai T, Hung VS, Morinaka K, Kobayashi T, Ito S (2008) Crystal structure of GH13 α-glucosidase GSJ from one of the deepest sea bacteria. Proteins 73:126–133

    Article  CAS  PubMed  Google Scholar 

  • Snyder M, Davidson N (1983) Two gene families clustered in a small region of the Drosophila genome. J Mol Biol 166:101–118

    Article  CAS  PubMed  Google Scholar 

  • Stam MR, Danchin EG, Rancurel C, Coutinho PM, Henrissat B (2006) Dividing the large glycoside hydrolase family 13 into subfamilies: towards improved functional annotations of α-amylase-related proteins. Protein Eng Des Sel 19:555–562

    Article  CAS  PubMed  Google Scholar 

  • Stoltzfus A, Logsdon JM Jr, Palmer JD, Doolittle WF (1997) Intron “sliding” and the diversity of intron positions. Proc Natl Acad Sci USA 94:10739–10744

    Article  CAS  PubMed  Google Scholar 

  • Takewaki S, Chiba S, Kimura A, Matsui H, Koike Y (1980) Purification and properties of α-glucosidases of the honey bee Apis mellifera L. Agric Biol Chem 44:731–740

    CAS  Google Scholar 

  • Takewaki S, Kimura A, Kubota M, Chiba S (1993) Substrate specificity and subsite affinities of honeybee α-glucosidase II. Biosci Biotechnol Biochem 57:1508–1513

    Article  CAS  Google Scholar 

  • Tamura K, Subramanian S, Kumar S (2004) Temporal patterns of fruit fly (Drosophila) evolution revealed by mutation clocks. Mol Biol Evol 21:36–44

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  CAS  PubMed  Google Scholar 

  • Throckmorton LH (1975) The phylogeny, ecology and geography of Drosophila. In: King RC (ed) Handbook of genetics, volume 3, invertebrates of genetic interest. Plenum Publishing, New York, pp 421–470

    Google Scholar 

  • Tweedie S, Ashburner M, Falls K, Leyland P, McQuilton P, Marygold S, Millburn G, Osumi-Sutherland D, Schroeder A, Seal R, Zhang H, The FlyBase Consortium (2009) FlyBase: enhancing Drosophila Gene Ontology annotations. Nucleic Acids Res 37(Database issue):D555–D559

    Article  CAS  PubMed  Google Scholar 

  • Vieira CP, Vieira J, Hartl DL (1997) The evolution of small gene clusters: evidence for an independent origin of the maltase gene cluster in Drosophila virilis and Drosophila melanogaster. Mol Biol Evol 14:985–993

    CAS  PubMed  Google Scholar 

  • Zhang Z, Inomata N, Cariou ML, Da Lage JL, Yamazaki T (2003a) Phylogeny and the evolution of the amylase multigenes in the Drosophila montium species subgroup. J Mol Evol 56:121–130

    Article  CAS  PubMed  Google Scholar 

  • Zhang Z, Inomata N, Yamazaki T, Kishino H (2003b) Evolutionary history and mode of the amylase multigene family in Drosophila. J Mol Evol 57:702–709

    Article  CAS  PubMed  Google Scholar 

  • Zheng L, Whang LH, Kumar V, Kafatos FC (1995) Two genes encoding midgut-specific maltase-like polypeptides from Anopheles gambiae. Exp Parasitol 81:272–283

    Article  CAS  PubMed  Google Scholar 

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Acknowledgment

This study was supported by the grant No. 2/0114/08 from the Slovak Grant Agency VEGA.

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  1. Institute of Molecular Biology, Slovak Academy of Sciences, Dúbravská cesta 21, 84551, Bratislava, Slovakia

    Marek Gabriško & Štefan Janeček

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  1. Marek Gabriško
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Correspondence to Marek Gabriško.

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Gabriško, M., Janeček, Š. Characterization of Maltase Clusters in the Genus Drosophila . J Mol Evol 72, 104–118 (2011). https://doi.org/10.1007/s00239-010-9406-3

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