Genetica

, Volume 131, Issue 3, pp 315–324 | Cite as

The use of a non-LTR element to date the formation of the Sdic gene cluster

Article

Abstract

Transposable elements comprise a considerable part of eukaryotic genomes, and there is increasing evidence for their role in the evolution of genomes. The number of active transposable elements present in the host genome at any given time is probably small relative to the number of elements that no longer transpose. The elements that have lost the ability to transpose tend to evolve neutrally. For example, non-LTR retrotransposons often become 5′ truncated due to their own transposition mechanism and hence lose their ability to transpose. The resulting transposons can be characterized as “dead-on-arrival” (DOA) elements. Because they are abundant and ubiquitous, and evolve neutrally in the location where they were inserted, these DOA non-LTR elements make a useful tool to date molecular events. There are four copies of a “dead-on-arrival” RT1C element on the recently formed Sdic gene cluster of Drosophila melanogaster, that are not present in the equivalent region of the other species of the melanogaster subgroup. The life history of the RT1C elements in the genome of D. melanogaster was used to determine the insertion chronology of the elements in the cluster and to date the duplication events that originated this cluster.

Keywords

Gene duplication Gene cluster Retrotransposon RT1C Sdic Transposon evolution 

Abbreviations

TE

Transposable element

non-LTR

Non-long terminal repeat

DOA

Dead-on-arrival

AnnX

Gene encoding annexin X

Cdic

Gene encoding cytoplasmic dynein intermediate polypeptide chain

Sdic

Gene encoding sperm-specific dynein intermediate polypeptide chain

bp

Base pair(s)

A

Adenosine

C

Cytidine

G

Guanosine

T

Thymidine

ORF

Open reading frame

MY

Million years

Notes

Acknowledgements

I thank Daniel Hartl and Margarida Matos for their valuable comments and reviews, Justin Blumenstiel for advice on TE analysis, and Daniel Muller for the illustrations. This work was supported by a fellowship PRAXIS XXI/BD/15886/98 from Fundação para a Ciência e Tecnologia, Portugal.

References

  1. Bowen NJ, McDonald JF (2001) Drosophila euchromatic LTR retrotransposons are much younger than the host species in which they reside. Genome Res 11:1527–1540PubMedCrossRefGoogle Scholar
  2. Blumenstiel JP, Hartl DL, Lozovsky ER (2002) Patterns of insertion and deletion in contrasting chromatin domains. Mol Biol Evol 19:2211–2225PubMedGoogle Scholar
  3. Caccone A, Amato GD, Powell JR (1988) Rates and patterns of scnDNA and mtDNA divergence within the Drosophila melanogaster subgroup. Genetics 118:671–683PubMedGoogle Scholar
  4. Celniker SE, Wheeler DA, Kronmiller B, Carlson JW, Halpern A, Patel S, Adams M, Champe M, Dugan SP, Frise E, Hodgson A, George RA, Hoskins RA, Laverty T, Muzny DM, Nelson CR, Pacleb JM, Park S, Pfeiffer BD, Richards S, Sodergren EJ, Svirskas R, Tabor PE, Wan K, Stapleton M, Sutton GG, Venter C, Weinstock G, Scherer SE, Myers EW, Gibbs RA, Rubin GM (2002) Finishing a whole genome shotgun: release 3 of the Drosophila melanogaster euchromatic genome sequence, Genome Biol 3: Research0079.1-0079.14Google Scholar
  5. Charlesworth B, Sniegowski P, Stephan W (1994) The evolutionary dynamics of repetitive DNA in eukaryotes. Nature 371:215–220PubMedCrossRefGoogle Scholar
  6. Felsenstein J (1978) Cases in which parsimony or compatibility methods will be positively misleading. Syst Zool 27:401–410CrossRefGoogle Scholar
  7. Felsenstein J (1988) Phylogenies from molecular sequences: inferences and reliability. Annu Rev Genet 22:521–565PubMedCrossRefGoogle Scholar
  8. Hall BG (1999) Transposable elements as activators of cryptic genes in E coli Genetica 107:181–187PubMedCrossRefGoogle Scholar
  9. Kamimker JS, Bergman CM, Kronmiller B, Carlson J, Svirskas R, Patel S, Frise E, Wheeler DA, Lewis SE, Rubin GM, Ashburner M, Celniker SM (2002) The transposable elements of Drosophila melanogaster euchromatin: a genomics perspective. Genome Biol 3: Research0084.01-0084-20Google Scholar
  10. Kapitonov VV, Jurka J (2000) Direct submission (June, 2000), http://www.girinst.org/server/RepBase/RepBase6.6.embl/drorep.refGoogle Scholar
  11. Kapitonov VV, Jurka J (2003) Molecular paleontology of transposable elements in the Drosophila melanogaster genome. Proc Natl Acad Sci U S A 100:6569–6574PubMedCrossRefGoogle Scholar
  12. Kulathinal RJ, Sawyer SA, Bustamante CD, Nurminsky DI, Ponce R, Ranz JM, Hartl DL (2004) Selective sweep in the evolution of a new sperm-specific gene in Drosophila. In: Nurminsky D (ed) Selective sweep. Landes Company, Austin, TXGoogle Scholar
  13. Lander ES, Linton LM, Birren B et al (2001) Initial sequencing and analysis of the human genome. Nature 409:860–921PubMedCrossRefGoogle Scholar
  14. Lerat E, Rizzon C, Biemont C (2003) Sequence divergence within transposable element families in the Drosophila melanogaster genome. Genome Res 13:1889–1896PubMedGoogle Scholar
  15. Li W (1997) Molecular evolution. Sinauer, Sunderland, MAGoogle Scholar
  16. Lozovskaya ER, Nurminsky DI, Petrov DA, Hartl DL (1999) Genome size as a mutation–selection–drift process. Genes Genet Syst 74:201–207PubMedCrossRefGoogle Scholar
  17. Luan DD, Korman MH, Jakubczak JL, Eickbush TH (1993) Reverse transcription of R2Bm RNA is primed by a nick at the chromosomal target site: a mechanism for non-LTR retrotransposition. Cell 72:595–605PubMedCrossRefGoogle Scholar
  18. Malik HS, Burke WD, Eickbush TH (1999) The age and evolution of non-LTR retrotransposable elements. Mol Biol Evol 16:793–805PubMedGoogle Scholar
  19. Malik HS, Eickbush TH (2001) Phylogenetic analysis of ribonuclease H domains suggest a late, chimeric origin of LTR retrotransposable elements and retroviruses. Genome Res 11:1187–1197PubMedCrossRefGoogle Scholar
  20. Maside X, Bartolomé C, Charlesworth B (2002) S-elements insertions are associated with the evolution of Hsp70 genes in Drosophila melanogaster. Curr Biol 12:1686–1691PubMedCrossRefGoogle Scholar
  21. Maside X, Bartolomé C, Charlesworth B (2003) Inferences on the evolutionary history of the S-element family of Drosophila melanogaster. Mol Biol Evol 20:1183–1187PubMedCrossRefGoogle Scholar
  22. Nurminsky DI, Nurminskaya MV, De Aguiar D, Hartl DL (1998) Selective sweep of a newly evolved sperm-specific gene in Drosophila. Nature 396:572–575PubMedCrossRefGoogle Scholar
  23. Nurminsky D, De Aguiar D, Bustamante CD, Hartl DL (2001) Chromosomal effect of rapid gene evolution in Drosophila melanogaster. Science 291:128–130PubMedCrossRefGoogle Scholar
  24. Page R (2002) Modified DM mincut supertrees. In: Guigó R, Gusfield D (eds) WABI 2002, pp 537–551. LNCS 2452Google Scholar
  25. Petrov DA, Lozovskaya ER, Hartl DL (1996) High intrinsic rate of DNA loss in Drosophila. Nature 384:346–349PubMedCrossRefGoogle Scholar
  26. Petrov DA, Hartl DL (1998) High rate of DNA loss in the Drosophila melanogaster and Drosophila virilis species groups. Mol Biol Evol 15:293–302PubMedGoogle Scholar
  27. Ponce R, Hartl DL (2006) The evolution of the novel Sdic gene cluster in Drosophila melanogaster. Gene 376:174–183PubMedCrossRefGoogle Scholar
  28. Ranz JM, Ponce AR, Hartl DL, Nurminsky D (2003) Origin and evolution of a new gene expressed in Drosophila sperm axoneme. Genetica 118:233–244PubMedCrossRefGoogle Scholar
  29. Rowan RG, Hunt JA (1991) Rates of DNA change and phylogeny from the DNA sequences of the alcohol dehydrogenase gene for five closely related species of Hawaiian Drosophila. Mol Biol Evol 8:49–70PubMedGoogle Scholar
  30. SanMiguel P, Tikhonov A, Jin YK, Motchoulskaia N, Zakharov D, Melake-Berhan A, Springer PS, Edwards KJ, Lee M, Avramova Z, Bennetzen JL (1996) Nested retrotransposons in the intergenic regions of the maize genome. Science 274:765–768PubMedCrossRefGoogle Scholar
  31. SanMiguel P, Brandon SG, Tikhonov A, Nakajima Y, Bennetzen J (1998) The paleontology of intergene retrotransposons of maize. Nat Genet 20:43–45PubMedCrossRefGoogle Scholar
  32. Schlenke TA, Begun DJ (2004) Strong selective sweep associated with a transposon insertion in Drosophila simulans. Proc Natl Acad Sci U S A 101:1626–1631PubMedCrossRefGoogle Scholar
  33. Schenkel H, Hanke S, De Lorenzo C, Schmitt R, Mechler BM (2002) P elements inserted in the vicinity of or within the Drosophila snRNP SmD3 gene nested in the first intron of the ornithine decarboxylase antizyme gene affect only the expression of SmD3. Genetics 161:763–772PubMedGoogle Scholar
  34. Swofford DL (2003) PAUP*. Phylogenetic analysis using parsimony (*and Other Methods). Version 4. Sinauer Associates, Sunderland, MassachusettsGoogle Scholar
  35. Tamura K, Subramanian S, Kumar S (2004) Temporal patterns of fruit fly (Drosophila) evolution revealed by mutation clocks. Mol Biol Evol 21:36–44PubMedCrossRefGoogle Scholar
  36. Tatusova TA, Madden TL (1999) BLAST 2 sequences, a new tool for comparing protein and nucleotide sequences. FEMS Microbiol Lett 174:247–250PubMedCrossRefGoogle Scholar
  37. Zatsepina OG, Velikodvorskaia VV, Molodtsov VB, Garbuz D, Lerman DN, Bettencourt BR, Feder ME, Evgenev MB (2001) A Drosophila melanogaster strain fom sub-equatorial Africa has exceptional thermotolerance but decreased Hsp70 expression. J Exp Biol 204:1869–1881PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, Inc. 2007

Authors and Affiliations

  1. 1.Department of Organismic and Evolutionary BiologyHarvard UniversityCambridgeUSA

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