Skip to main content
Log in

Highly Variable Polymorphism of the α-Amylase Gene Family in Litopenaeus vannamei (Crustacea Decapoda)

  • Published:
Journal of Molecular Evolution Aims and scope Submit manuscript

Abstract

α-Amylase from the tropical shrimp Litopenaeus vannamei presents a high degree of polymorphism and at least eight different electromorphs are detected by electrophoresis. Based on nucleotide sequences, three cDNAs have been previously characterized. In this paper we report on the organization and the evolution of corresponding α-amylase genes, determined after PCR amplification. Three AMY genes have been characterized, spanning over 3.3 kb and encoding mature proteins of 495 amino acids (aa), which are all expressed in the digestive gland. The existence of nine short introns, ranging from 86 to 454 bp, located at the same positions for each of the different genes, and presenting no similarity between them, is reported. Between 11 and 15% of changes are observed in the coding aa sequences of genes II and III compared to the gene I sequence respectively. One 5′ putative promoter sequence has been sequenced and shows no classical TATA box upstream to the coding sequence. Based on the intron size difference, a single PCR (producing the S–R fragments) allows the separation of a partial gene I (750 bp), corresponding to cDNA 20, from the others (650–680 bp). Sequencing different S–R PCR fragments from one shrimp shows at least eight different haplotypes. A complex microsatellite repeat is present in intron 6 of gene II. Using size and sequence differences in this repeated portion, it is possible to characterize two gene subfamilies (IIa and IIb) encoding previously described cDNAs 28 and 37, respectively. For the gene II family, two to four alleles are present in one shrimp corresponding to these two genes. Within the Panama natural population, 35 different alleles are shown at this locus. Regarding α-amylase gene structure in the shrimp, many recombinants are present from a set of individuals and constitute an important mechanism of evolution of α-amylase function.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Figure 6

Similar content being viewed by others

References

  1. Abukashawa S, Genest Y, Hickey DA (1993) Unpublished, direct sequence submission. EMBL U04271

  2. N Arnheim (1983) Concerted evolution of multigene family. M Nei K Koehn (Eds) Evolution of genes and proteins. Sinauer Associates Sunderland, MA 38–61

    Google Scholar 

  3. DJ Begun (1997) ArticleTitleOrigin and evolution of a new descended from alcohol deshydrogenase in Drosophila. Genetics 145 375–382 Occurrence Handle9071591

    PubMed  Google Scholar 

  4. BF Benkel T Nguyen N Ahluwalia KI Benkel DA Hickey (1997) ArticleTitleCloning and expression of a chicken alpha-amylase gene. Gene 192 261–270 Occurrence Handle10.1016/S0378-1119(97)00102-9 Occurrence Handle1:CAS:528:DyaK2sXjsVers7g%3D Occurrence Handle9224899

    Article  CAS  PubMed  Google Scholar 

  5. PM Boer DA Hickey (1986) ArticleTitleThe alpha-amylase gene in Drosophila melanogaster: Nucleotide sequence, gene structure and expression motifs. Nucleic Acids Res 14 8399–8411 Occurrence Handle1:CAS:528:DyaL2sXmt1SitA%3D%3D Occurrence Handle3024105

    CAS  PubMed  Google Scholar 

  6. ML Cariou JL Da Lage (1993) Isozymes polymorphisms. YN Tobari (Eds) Drosophila ananassae: Genetical and biological aspects. Japan Scientific Societies Press Tokyo 160–171

    Google Scholar 

  7. B Christensen (1977) ArticleTitleHabitat preference among amylase genetics in Asellus aquaticus (Isopoda). Heriditas 87 21–26 Occurrence Handle1:STN:280:CSeD28nkslM%3D

    CAS  Google Scholar 

  8. W Dall BJ Hill PC Rothlisberg DJ Sharples (1990) . JHS Blaxter . Southward (Eds) The fossil record. Adv Mar Biol 27 Academic Press New York 149–152

    Google Scholar 

  9. O Dainou M-L Cariou JR David D Hickey (1987) ArticleTitleAmylase gene duplication: An ancestral trait in the Drosophila melanogaster: species subgroup. Heredity 59 245–251 Occurrence Handle1:CAS:528:DyaL1cXnt1GhtA%3D%3D Occurrence Handle2445712

    CAS  PubMed  Google Scholar 

  10. O Dainou M-L Cariou JM Goux JR David (1993) ArticleTitleAmylase polymorphism in Drosophila melanogaster. Haplotype frequencies in tropical African and American populations. Gene Sel Evol 25 133–155 Occurrence Handle1:CAS:528:DyaK3sXkvFWksLw%3D

    CAS  Google Scholar 

  11. JL Da Lage F Lemeunier M-L Cariou JM Goux JR David (1992) ArticleTitleMultiple amylase genes in Drosophila ananassae and related species. Genet Res Cambr 59 85–92 Occurrence Handle1:CAS:528:DyaK38Xls1yjsbg%3D

    CAS  Google Scholar 

  12. JL Da Lage A Klarenberg M-L Cariou (1996) ArticleTitleVariation in sex-, stage- and tissue-specific expression of the amylase genes in Drosophila ananassae. Heredity 76 9–18 Occurrence Handle1:CAS:528:DyaK28XhtFyltbg%3D Occurrence Handle8575934

    CAS  PubMed  Google Scholar 

  13. JL Da Lage E Renard F Chartois F Lemeunier M-L Cariou (1998) ArticleTitle Amyrel, a paralogous gene of the amylase gene family in Drosophila melanogaster and Sophophora subgenus. Proc Natl Acad Sci USA 95 6848–6853 Occurrence Handle10.1073/pnas.95.12.6848 Occurrence Handle1:CAS:528:DyaK1cXjslynu78%3D Occurrence Handle9618501

    Article  CAS  PubMed  Google Scholar 

  14. JL Da Lage A Van Wormhoudt M-L Cariou (2002) ArticleTitleDiversity and evolution of the alpha-amylase genes in animals. Biol Bratislava 57 IssueIDSuppl 11 181–189 Occurrence Handle1:CAS:528:DC%2BD3sXhtVCks7c%3D

    CAS  Google Scholar 

  15. Forster PG, Abukashawa S, Hickey DA (1993) Unpublished, direct sequence submission. EMBL U04223

  16. GL Grosmann AA James (1993) ArticleTitleThe salivary gland of the vector mosquito, Aedes aegypti, expressed a novel member of the amylase gene family. Insect Mol Biol 1 223–232 Occurrence Handle1:CAS:528:DyaK2cXntVCkuw%3D%3D Occurrence Handle7505701

    CAS  PubMed  Google Scholar 

  17. GL Grossman Y Campos DW Severson AA Jams (1997) ArticleTitleEvidence for two distinct members of the amylase gene family in the yellow fever mosquito, Aedes aegypti. Insect Mol Biol 27 769–781 Occurrence Handle1:CAS:528:DyaK1cXktlWksg%3D%3D

    CAS  Google Scholar 

  18. DL Gumucio K Wiebauer RM Caldwell LC Samuelson MH Meisler (1988) ArticleTitleConcerted evolution of human amylase genes. Mol Cell Biol 8 1197–1205 Occurrence Handle1:CAS:528:DyaL1cXhsVCmurc%3D Occurrence Handle2452973

    CAS  PubMed  Google Scholar 

  19. DA Hickey BF Benkel PH Boer Y Genest S Abukashawa G Ben-David (1987) ArticleTitleEnzyme-coding genes as molecular clocks: The molecular evolution of animal alpha-amylases. J Mol Evol 26 252–256 Occurrence Handle1:CAS:528:DyaL1cXovVylsw%3D%3D Occurrence Handle3129570

    CAS  PubMed  Google Scholar 

  20. N Intomata T Yamazaki (2000) ArticleTitleEvolution of nucleotide substitutions and gene regulation In the amylase multigenes in Drosophila kikkawai and its sibling species. Mol Biol Evol 17 IssueID4 601–615 Occurrence Handle1:CAS:528:DC%2BD3cXisVSgtL8%3D Occurrence Handle10742051

    CAS  PubMed  Google Scholar 

  21. N Inomata H Shibata E Okayama T Yamazaki (1995) ArticleTitleEvolutionary relationships and sequence variation of α-amylase variants encoded by duplicated genes in the Amy locus of Drosophila melanoeaster. Genetics 141 237–244 Occurrence Handle1:CAS:528:DyaK28Xht1Cmtrc%3D Occurrence Handle8536971

    CAS  PubMed  Google Scholar 

  22. N Inomata H Tachida T Yamazaki (1997) ArticleTitleMolecular evolution of the Amy multigenes in the subgenus Sophophora of Drosophila. Mol Biol Evol 14 942–950 Occurrence Handle1:CAS:528:DyaK2sXlvVejurc%3D Occurrence Handle9287427

    CAS  PubMed  Google Scholar 

  23. S Janecek (1994) ArticleTitleSequence similarities and evolutionary relationships of microbial, plant and animal alpha-amylases. Eur J Biochem 224 IssueID2 519–524 Occurrence Handle1:CAS:528:DyaK2cXlslWqurs%3D Occurrence Handle7925367

    CAS  PubMed  Google Scholar 

  24. AS Jones (1953) ArticleTitleThe isolation of bacterial nucleic acids using cetyltrimethylammonium bromide (Cetavlon). Biochim Biophys Acta 10 607–612 Occurrence Handle10.1016/0006-3002(53)90304-7 Occurrence Handle1:CAS:528:DyaG3sXjvVSmtA%3D%3D Occurrence Handle13059024

    Article  CAS  PubMed  Google Scholar 

  25. AJ Klarenberg JWC Vermeulen PJM Jacobs W Scharloo (1988) ArticleTitleGenetic and dietary regulation of tissue-specific expression pattern of α-amylase in larvae of Drosophila melanogaster. Comp Biochem Physiol 89B 143–146 Occurrence Handle1:CAS:528:DyaL1cXnt1Giuw%3D%3D

    CAS  Google Scholar 

  26. M Laulier (1988) ArticleTitleGénétique et systématique évolutive du complexe d’espéces Sphaeroma hooker Leach, Sphaeroma levii Argano et Sphaeroma rugicauda Leach (Crustacés Isopodes Flabelliféres). I. Génétique formelle de onze locus enzymatiques. Genet Sel Evol 20 63–74 Occurrence Handle1:CAS:528:DyaK3cXkvFamt7Y%3D

    CAS  Google Scholar 

  27. C Le Boulay D Sellos A Van Wormhoudt (1998) ArticleTitleCathepsin L gene organization in crustaceans. Gene 218 77–84 Occurrence Handle10.1016/S0378-1119(98)00385-0 Occurrence Handle1:CAS:528:DyaK1cXmsFKrtb8%3D Occurrence Handle9751805

    Article  CAS  PubMed  Google Scholar 

  28. G Le Moullac B Klein D Sellos A Van Wormhoudt (1996) ArticleTitleAdaptation of trypsin, chymotrypsin and α-amylase to casein level and protein source in the shrimp P. vannamei. J. Exp Mar Biol Ecol 208 107–125 Occurrence Handle10.1016/S0022-0981(96)02671-8

    Article  Google Scholar 

  29. JN Levy RM Gemmil WW Doane (1985) ArticleTitleMolecular cloning of α-amylase in Drosophila melanogaster. II. Clone organization and verification. Genetics 11 313–324

    Google Scholar 

  30. WH Li (1997) Molecular evolution. Sinauer Associates Sunderland, MA

    Google Scholar 

  31. M Meisler TK Antonucci LO Treisman DL Gumucio LC Samuelson (1986) ArticleTitleInterstrain variation in amylase gene copy number and mRNA abundance in three mouse tissues. Genetics 113 713–722 Occurrence Handle1:CAS:528:DyaL28XkvFagt74%3D Occurrence Handle3488242

    CAS  PubMed  Google Scholar 

  32. R Nakajima J Imanaka S Aiba (1986) ArticleTitleComparison of amino acid sequences of eleven different α-amylases. Appl Microbiol Biotechnol 23 355–360 Occurrence Handle1:CAS:528:DyaL28Xhs1Chu7g%3D

    CAS  Google Scholar 

  33. Y Nakamura M Ogama T Nishida M Emi G Kosaki S Himeno K Matsubara (1984) ArticleTitleSequence of cDNAs for human salivary and pancreatic α-amylases. Gene 28 263–270 Occurrence Handle10.1016/0378-1119(84)90265-8 Occurrence Handle1:STN:280:BiuB3sjlvVQ%3D Occurrence Handle6610603

    Article  CAS  PubMed  Google Scholar 

  34. AC Pittet U Schibler (1985) ArticleTitleMouse α-amylase loci: AMY-1 and AMY-2 are closely linked. J Mol Biol 182 359–365 Occurrence Handle2989529

    PubMed  Google Scholar 

  35. JR Powell M Andjelkovic (1983) ArticleTitlePopulation genetics of Drosophila amylase IV. Selection in laboratory population maintained on different carbohydrates. Genetics 103 IssueID4 675–689 Occurrence Handle1:CAS:528:DyaL3sXktF2qtbs%3D Occurrence Handle6189764

    CAS  PubMed  Google Scholar 

  36. S Prigent M Matoub C Rouland M-L Cariou (1998) ArticleTitleMetabolic evolution in α-amylase from Drosophila virilis and Drosophila repleta; Two species with different ecological niches. Comp Biochem Physiol 119B 407–412 Occurrence Handle1:CAS:528:DyaK1cXjtFCjt74%3D

    CAS  Google Scholar 

  37. KW Rodenburg N Juge XJ Guo M Sogaard JC Chaix B Svensson (1994) ArticleTitleDomain protruding at the third β strand of the α/β barrel in barley α-amylase confers distinct isozyme-specific properties. Eur J Biochem 221 211–284 Occurrence Handle8168510

    PubMed  Google Scholar 

  38. LC Samuelson RS Philipps LJ Swanberg (1996) ArticleTitleAmylase gene structure in primates: retroposon insertions and promoter evolution. Mol Biol Evol 13 767–779 Occurrence Handle1:CAS:528:DyaK28XktFyitb4%3D Occurrence Handle8754213

    CAS  PubMed  Google Scholar 

  39. FR Schram RM Feldman MJ Copeland (1978) ArticleTitleThe late devonian Paleopalaemonidae and the earliest decapod crustaceans. J Paleontol 52 1375–1387

    Google Scholar 

  40. U Schibler AC Pittet RA Young O Hagenbuchle M Tosi S Gellman PK Wellauer (1982) ArticleTitleThe mouse alpha-amylase multigene family: Sequence organization of members expressed in the pancreas, salivary gland and liver. J Mol Evol 155 248–266

    Google Scholar 

  41. DY Sellos A Van Wormhoudt (2002) ArticleTitleStructure of the alpha-amylase genes in crustaceans and molluscs: Evolution of the exon/intron organisation. Biol Bratislava 57 IssueIDSupp 11 191–196 Occurrence Handle1:CAS:528:DC%2BD3sXhtVCksL8%3D

    CAS  Google Scholar 

  42. H Shibata T Yamazaki (1995) ArticleTitleMolecular evolution of the duplicated Amy locus in the Drosophila melanogaster species subgroup: Concerted evolution only in the coding region and an excess of nonsynonymous substitutions in speciation. Genetics 141 223–236 Occurrence Handle1:CAS:528:DyaK28Xht1CmtrY%3D Occurrence Handle8536970

    CAS  PubMed  Google Scholar 

  43. SLF Sunden SK Davis (1991) ArticleTitleEvaluation of genetic variation in a domestic population of Penaeus vannamei (Boone): A comparison with three natural populations. Aquaculture 97 131–142 Occurrence Handle10.1016/0044-8486(91)90260-E

    Article  Google Scholar 

  44. A Van Wormhoudt P Favrel (1988) ArticleTitleElectrophoretic characterization of Palaemon elegans α-amylase system: Study of amylase polymorphism during the intermolt cycle. Comp Biochem 89B 201–207 Occurrence Handle1:CAS:528:DyaL1cXhsVOms78%3D

    CAS  Google Scholar 

  45. A Van Wormhoudt D Sellos (1996) ArticleTitleCloning and sequencing analysis of three amylase cDNAs in the shrimp Penaeus vannamei (Crustacea Decapoda), evolutionary aspects. J Mol Evol 42 543–551 Occurrence Handle1:CAS:528:DyaK28XjvVajs7Y%3D Occurrence Handle8661999

    CAS  PubMed  Google Scholar 

  46. A Van Wormhoudt G Bourrreau G Le Moullac (1995) ArticleTitleAmylase polymorphism in Crustacea Decapoda: Electrophoretic and immunological studies. Biochem Syst Ecol 23 139–149 Occurrence Handle10.1016/0305-1978(94)00090-4 Occurrence Handle1:CAS:528:DyaK2MXkslSltrg%3D

    Article  CAS  Google Scholar 

  47. B Xu J-J Janson D Sellos (2001) ArticleTitleCloning and sequencing of a molluscan endo-B-1,4-glucanase gene from the blue mussel, Mytilus edulis. Eur J Biochem 268 3718–3727 Occurrence Handle11432738

    PubMed  Google Scholar 

  48. T Yamazaki Y Matsuo Y Inoue Y Matsuo (1984) ArticleTitleGenetic analysis of natural population of Drosophila melanogaster in Japan. I. Protein polymorphism, lethal genes, sterility genes, inversion polymorphism and linkage desequilibrium. Jpn J Genet 59 33–49

    Google Scholar 

Download references

Acknowledgements

This study was supported by a grant from the ECOS program (M97B04) for the collection of material.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Alain Van Wormhoudt.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Van Wormhoudt, A., Sellos, D. Highly Variable Polymorphism of the α-Amylase Gene Family in Litopenaeus vannamei (Crustacea Decapoda) . J Mol Evol 57, 659–671 (2003). https://doi.org/10.1007/s00239-003-2516-4

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00239-003-2516-4

Keywords

Navigation