Advertisement

Theoretical and Applied Genetics

, Volume 121, Issue 8, pp 1419–1430 | Cite as

iPBS: a universal method for DNA fingerprinting and retrotransposon isolation

  • Ruslan Kalendar
  • Kristiina Antonius
  • Petr Smýkal
  • Alan H. SchulmanEmail author
Original Paper

Abstract

Molecular markers are essential in plant and animal breeding and biodiversity applications, in human forensics, and for map-based cloning of genes. The long terminal repeat (LTR) retrotransposons are well suited as molecular markers. As dispersed and ubiquitous transposable elements, their “copy and paste” life cycle of replicative transposition leads to new genome insertions without excision of the original element. Both the overall structure of retrotransposons and the domains responsible for the various phases of their replication are highly conserved in all eukaryotes. Nevertheless, up to a year has been required to develop a retrotransposon marker system in a new species, involving cloning and sequencing steps as well as the development of custom primers. Here, we describe a novel PCR-based method useful both as a marker system in its own right and for the rapid isolation of retrotransposon termini and full-length elements, making it ideal for “orphan crops” and other species with underdeveloped marker systems. The method, iPBS amplification, is based on the virtually universal presence of a tRNA complement as a reverse transcriptase primer binding site (PBS) in LTR retrotransposons. The method differs from earlier retrotransposon isolation methods because it is applicable not only to endogenous retroviruses and retroviruses, but also to both Gypsy and Copia LTR retrotransposons, as well as to non-autonomous LARD and TRIM elements, throughout the plant kingdom and to animals. Furthermore, the inter-PBS amplification technique as such has proved to be a powerful DNA fingerprinting technology without the need for prior sequence knowledge.

Keywords

Long Terminal Repeat Primer Binding Site Brachypodium Long Terminal Repeat Retrotransposons Long Terminal Repeat Sequence 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Abbreviations

LTR

Long terminal repeat

PBS

Primer binding site

Notes

Acknowledgments

We thank the many collaborators listed in Online Resource 1 for gifts of plant materials. Eeva-Marja Turkki, Anne-Mari Narvanto, and Ursula Lönnqvist are thanked for their always excellent technical assistance. The work was supported by Ministry of Education of Czech Republic project MSM2678424601 and by the Academy of Finland, Grant 120810, Project Exbardiv of the ERA-NET Plant Genomics program.

Supplementary material

122_2010_1398_MOESM1_ESM.pdf (92 kb)
Online Resource 1 (PDF 91 kb)
122_2010_1398_MOESM2_ESM.pdf (1.2 mb)
Online Resource 2 (PDF 1,236 kb)

References

  1. Alix K, Heslop-Harrison JS (2004) The diversity of retroelements in diploid and allotetraploid Brassica species. Plant Mol Biol 54:895–909CrossRefPubMedGoogle Scholar
  2. Antonius-Klemola K, Kalendar R, Schulman AH (2006) TRIM retrotransposons occur in apple and are polymorphic between varieties but not sports. Theor Appl Genet 112:999–1008CrossRefPubMedGoogle Scholar
  3. Belyayev A, Kalendar R, Brodsky L, Nevo E, Schulman AH, Raskina O (2010) Transposable elements in a marginal plant population: temporal fluctuations provide new insights into genome evolution of wild diploid wheat. Mobile DNA 1:6CrossRefPubMedGoogle Scholar
  4. Boyko E, Kalendar R, Korzun V, Gill B, Schulman AH (2002) Combined mapping of Aegilops tauschii by retrotransposon, microsatellite, and gene markers. Plant Mol Biol 48:767–790CrossRefPubMedGoogle Scholar
  5. Chaparro C, Guyot R, Zuccolo A, Piegu B, Panaud O (2007) RetrOryza: a database of the rice LTR-retrotransposons. Nucleic Acids Res 35:D66–D70CrossRefPubMedGoogle Scholar
  6. Chariieu J-P, Laurent A-M, Carter DA, Bellis M, Roizeès G (1992) 3′ Alu PCR: a simple and rapid method to isolate human polymorphic markers. Nucleic Acids Res 20:1333–1337CrossRefGoogle Scholar
  7. Cheng C, Daigen M, Hirochika H (2006) Epigenetic regulation of the rice retrotransposon Tos17. Mol Genet Genomics 276:378–390CrossRefPubMedGoogle Scholar
  8. Corpet F (1988) Multiple sequence alignment with hierarchical clustering. Nucleic Acids Res 16:10881–10890CrossRefPubMedGoogle Scholar
  9. Ellis THN, Poyser SJ, Knox MR, Vershinin AV, Ambrose MJ (1998) Ty1-copia class retrotransposon insertion site polymorphism for linkage and diversity analysis in pea. Mol Gen Genet 260:9–19PubMedGoogle Scholar
  10. Feschotte C, Jiang N, Wessler S (2002) Plant transposable elements: where genetics meets genomics. Nat Rev Genet 3:329–341CrossRefPubMedGoogle Scholar
  11. Flavell AJ, Dunbar E, Anderson R, Pearce SR, Hartley R, Kumar A (1992) Ty1-copia group retrotransposons are ubiquitous and heterogeneous in higher plants. Nucleic Acids Res 20:3639–3644CrossRefPubMedGoogle Scholar
  12. Flavell AJ, Knox MR, Pearce SR, Ellis THN (1998) Retrotransposon-based insertion polymorphisms (RBIP) for high throughput marker analysis. Plant J 16:643–650CrossRefPubMedGoogle Scholar
  13. Flavell AJ, Bolshakov VN, Booth A, Jing R, Russell J, Ellis TH, Isaac P (2003) A microarray-based high throughput molecular marker genotyping method: the tagged microarray marker (TAM) approach. Nucleic Acids Res 31:e115CrossRefPubMedGoogle Scholar
  14. Hedges DJ, Batzer MA (2005) From the margins of the genome: mobile elements shape primate evolution. BioEssays 27:785–794CrossRefPubMedGoogle Scholar
  15. Hizi A (2008) The reverse transcriptase of the Tf1 retrotransposon has a specific novel activity for generating the RNA self-primer that is functional in cDNA synthesis. J Virol 82:10906–10910CrossRefPubMedGoogle Scholar
  16. Ho SYW, Larson G, Edwards CJ, Tim H, Heupink TH, Lakin KE, Holland PWH, Shapiro B (2008) Correlating Bayesian date estimates with climatic events and domestication using a bovine case study. Biol Lett 4:370–374CrossRefPubMedGoogle Scholar
  17. International Rice Genome Sequencing Project (2005) The map-based sequence of the rice genome. Nature 436:793–800CrossRefGoogle Scholar
  18. Itoh T, Tanaka T, Barrero RA et al (2007) Curated genome annotation of Oryza sativa ssp. japonica and comparative genome analysis with Arabidopsis thaliana. Genome Res 17:175–183CrossRefPubMedGoogle Scholar
  19. Jaillon O, Aury J-M, Noel B, Policriti A, Clepet C, French-Italian Public Consortium for Grapevine Genome Characterization et al (2007) The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449:463–467CrossRefPubMedGoogle Scholar
  20. Jing R, Knox MR, Lee JM, Vershinin AV, Ambrose M, Ellis TH, Flavell AJ (2005) Insertional polymorphism and antiquity of PDR1 retrotransposon insertions in Pisum species. Genetics 171:741–752CrossRefPubMedGoogle Scholar
  21. Jurka J (2004) Evolutionary impact of human Alu repetitive elements. Curr Opin Genet Dev 14:603–608CrossRefPubMedGoogle Scholar
  22. Kalendar R, Schulman AH (2006) IRAP and REMAP for retrotransposon-based genotyping and fingerprinting. Nat Protoc 1:2478–2484CrossRefPubMedGoogle Scholar
  23. Kalendar R, Grob T, Regina M, Suoniemi A, Schulman AH (1999) IRAP and REMAP: two new retrotransposon-based DNA fingerprinting techniques. Theor Appl Genet 98:704–711CrossRefGoogle Scholar
  24. Kalendar R, Tanskanen J, Immonen S, Nevo E, Schulman AH (2000) Genome evolution of wild barley (Hordeum spontaneum) by BARE-1 retrotransposon dynamics in response to sharp microclimatic divergence. Proc Natl Acad Sci USA 97:6603–6607CrossRefPubMedGoogle Scholar
  25. Kalendar R, Vicient CM, Peleg O, Anamthawat-Jonsson K, Bolshoy A, Schulman AH (2004) Large retrotransposon derivatives: abundant, conserved but nonautonomous retroelements of barley and related genomes. Genetics 166:1437–1450CrossRefPubMedGoogle Scholar
  26. Kalendar R, Tanskanen J, Chang W, Antonius K, Sela H, Peleg O, Schulman AH (2008) Cassandra retrotransposons carry independently transcribed 5S RNA. Proc Natl Acad Sci USA 105:5833–5838CrossRefPubMedGoogle Scholar
  27. Kalendar R, Flavell AJ, Ellis THN, Sjakste T, Moisy C, Schulman AH (2010) Analysis of plant diversity with retrotransposon-based molecular markers. Heredity (in press)Google Scholar
  28. Kelly NJ, Palmer MT, Morrow CD (2003) Selection of retroviral reverse transcription primer is coordinated with tRNA biogenesis. J Virol 77:8695–8701CrossRefPubMedGoogle Scholar
  29. Lebedev YB, Belonovitch OS, Zybrova NV, Khil PP, Kurdyukov SG, Vinogradova TV, Hunsmann G, Sverdlov ED (2000) Differences in HERV-K LTR insertions in orthologous loci of humans and great apes. Gene 247:265–277CrossRefPubMedGoogle Scholar
  30. LeGrice SFJ (2003) “In the beginning”: initiation of minus strand DNA synthesis in retroviruses and LTR-containing retrotransposons. Biochemistry 42:14349–14355CrossRefGoogle Scholar
  31. Leigh F, Kalendar R, Lea V, Lee D, Donini P, Schulman AH (2003) Comparison of the utility of barley retrotransposon families for genetic analysis by molecular marker techniques. Mol Genet Genomics 269:464–474CrossRefPubMedGoogle Scholar
  32. Liu R, Vitte C, Ma J, Mahama AA, Dhliwayo T, Lee M, Bennetzen JL (2007) A GeneTrek analysis of the maize genome. Proc Natl Acad Sci USA 104:11844–11849CrossRefPubMedGoogle Scholar
  33. Macas J, Neumann P, Navrátilová A (2007) Repetitive DNA in the pea (Pisum sativum L.) genome: comprehensive characterization using 454 sequencing and comparison to soybean and Medicago trunculata. BMC Genomics 8:427CrossRefPubMedGoogle Scholar
  34. Mak J, Kleiman L (1997) Primer tRNAs for reverse transcription. J Virol 71:8087–8095PubMedGoogle Scholar
  35. Marquet R, Isel C, Ehresmann C, Ehresmann B (1995) tRNAs as primer of reverse transcriptases. Biochimie 77:113–124CrossRefPubMedGoogle Scholar
  36. Pearce SR, Stuart-Rogers C, Knox MG, Kumar A, Ellis THN, Flavell AJ (1999) Rapid isolation of plant Ty1-copia group retrotransposon LTR sequences for molecular marker studies. Plant J 19:711CrossRefPubMedGoogle Scholar
  37. Pereira HS, Barao A, Delgado M, Morais-Cecilio L, Viegas W (2005) Genomic analysis of grapevine retrotransposon 1 (Gret 1) in Vitis vinifera. Theor Appl Genet 111:871–878CrossRefPubMedGoogle Scholar
  38. Schnable PS, Ware D, Fulton RS et al (2009) The B73 maize genome: complexity, diversity, and dynamics. Science 326:1112–1115CrossRefPubMedGoogle Scholar
  39. Schulman AH, Flavell AJ, Ellis THN (2004) The application of LTR retrotransposons as molecular markers in plants. Methods Mol Biol 260:145–173PubMedGoogle Scholar
  40. Shedlock AM, Okada N (2000) SINE insertions: powerful tools for molecular systematics. Bioassays 22:148–160CrossRefGoogle Scholar
  41. Shi P-Y, Maizels N, Weiner AM (1998) CCA addition by tRNA nucleotidyltransferase: polymerization without translocation? EMBO J 17:3197–3206CrossRefPubMedGoogle Scholar
  42. Shirasu K, Schulman AH, Lahaye T, Schulze-Lefert P (2000) A contiguous 66 kb barley DNA sequence provides evidence for reversible genome expansion. Genome Res 10:908–915CrossRefPubMedGoogle Scholar
  43. Syed NH, Flavell AJ (2007) Sequence specific amplification polymorphisms (SSAP)—a multi-locus approach for analysing transposon insertions. Nat Protoc 1:2746–2752CrossRefGoogle Scholar
  44. Tadege M, Wen J, He J, Tu H, Kwak Y, Eschstruth A, Cayrel A, Endre G, Zhao PX, Chabaud M, Ratet P, Mysore KS (2008) Large-scale insertional mutagenesis using the Tnt1 retrotransposon in the model legume Medicago truncatula. Plant J 54:335–347CrossRefPubMedGoogle Scholar
  45. Tang JQ, Korab-Laskowska M, Jarnik M, Cardinal G, Vanasse M, Melançon SB, Labuda D (1995) Alu-PCR combined with non-Alu primers reveals multiple polymorphic loci. Mamm Genome 6:345–349CrossRefPubMedGoogle Scholar
  46. The International Brachypodium Initiative (2010) Genome sequencing and analysis of the model grass Brachypodium distachyon. Nature 463:763–768CrossRefGoogle Scholar
  47. Vicient CM, Suoniemi A, Anamthawat-Jónsson K, Tanskanen J, Beharav A, Nevo E, Schulman AH (1999) Retrotransposon BARE-1 and its role in genome evolution in the genus Hordeum. Plant Cell 11:1769–1784CrossRefPubMedGoogle Scholar
  48. Voytas DF, Cummings MP, Konieczny A, Ausubel FM, Rodermel SR (1992) Copia-like retrotransposons are ubiquitous among plants. Proc Natl Acad Sci USA 89:7124–7128CrossRefPubMedGoogle Scholar
  49. Waugh R, McLean K, Flavell AJ, Pearce SR, Kumar A, Thomas BB, Powell W (1997) Genetic distribution of BARE-1-like retrotransposable elements in the barley genome revealed by sequence-specific amplification polymorphisms (S-SAP). Mol Gen Genet 253:687–694CrossRefPubMedGoogle Scholar
  50. Wessler SR (1996) Turned on by stress. Plant retrotransposons. Curr Biol 6:959–961CrossRefPubMedGoogle Scholar
  51. Wicker T, Zimmermann W, Perovic D, Paterson AH, Ganal M, Graner A, Stein N (2005) A detailed look at 7 million years of genome evolution in a 439 kb contiguous sequence at the barley Hv-eIF4E locus: recombination, rearrangements and repeats. Plant J 41:184–194CrossRefPubMedGoogle Scholar
  52. Wicker T, Sabot F, Hua-Van A, Bennetzen J, Capy P, Chalhoub B, Flavell AJ, Leroy P, Morgante M, Panaud O, Paux E, SanMiguel P, Schulman AH (2007) A unified classification system for eukaryotic transposable elements. Nat Rev Genet 8:973–982CrossRefPubMedGoogle Scholar
  53. Witte CP, Le QH, Bureau T, Kumar A (2001) Terminal-repeat retrotransposons in miniature (TRIM) are involved in restructuring plant genomes. Proc Natl Acad Sci USA 98:13778–13783CrossRefPubMedGoogle Scholar
  54. Xiao R, Park K, Lee H, Kim J, Park C (2008) Identification and classification of endogenous retroviruses in cattle. J Virol 82:582–587CrossRefPubMedGoogle Scholar
  55. Yu J, Wang J, Lin W, Li S, Li H, Zhou J, Ni P et al (2005) The genomes of Oryza sativa: a history of duplications. PLoS Biol 3:e38CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Ruslan Kalendar
    • 1
  • Kristiina Antonius
    • 2
  • Petr Smýkal
    • 3
  • Alan H. Schulman
    • 1
    • 2
    Email author
  1. 1.MTT/BI Plant Genomics Laboratory, Institute of Biotechnology, Viikki BiocenterUniversity of HelsinkiHelsinkiFinland
  2. 2.Biotechnology and Food ResearchMTT Agrifood Research FinlandJokioinenFinland
  3. 3.Department of Plant BiotechnologyAgritec Plant Research Ltd.ŠumperkCzech Republic

Personalised recommendations