Skip to main content
SpringerLink
Log in

Molecular Evolution of a Plastid Tandem Repeat Locus in an Orchid Lineage

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

Abstract

The molecular evolution of a chloroplast minisatellite locus in the Anacamptis palustris (Orchidaceae) lineage and haplotype variation in two Italian A. palustris populations were investigated. A phylogenetic analyses of the chloroplast tRNALEU intron, where the minisatellite locus is located, revealed that a deletion in the ancestor of the A. palustris lineage led to the formation of two noncontiguous, complementary sequence motifs. We propose a model to explain the initial formation of the minisatellite repeat motif, starting with the two noncontiguous, complementary sequence motifs. A survey of minisatellite variation in four species of the A. palustris lineage revealed several haplotypes that differed not only in repeat number, but also in repeat organization. A haplotype network suggests that three different minisatellite loci evolved independently at the same position in the tRNALEU intron. A secondary structure model revealed that the A. palustris minisatellite repeat forms a stem region of the tRNALEU intron, which allows its notable expansion without negatively affecting splicing. Minisatellite variation was high in the two examined A. palustris populations where 20 haplotypes were detected, whereas no length variation was detected in a neighboring poly (A) microsatellite locus. We estimated a chloroplast minisatellite mutation rate of 3.2 × 10−3 mutations per generation. Southern blot analyses did not find evidence for chloroplast heteroplasmy. Based on the analysis of the largest known, extant A. palustris population, a stepwise mutation model (SMM) was inferred.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. S Aceto S Cozzolino L Gaudio R Nazzaro P De Luca (1999a) ArticleTitlePollination flow between Orchis morio and O. papilionacea in hybrid formation in different habitats. Int J Plant Sci 160 1153–1156

    Google Scholar 

  2. S Aceto P Caputo S Cozzolino L Gaudio A Moretti (1999b) ArticleTitlePhylogeny and evolution of Orchis and allied genera based on ITS DNA variation: Morphological gaps and molecular continuity. Mol Phylogenet Evol 13 67–76 Occurrence Handle1:CAS:528:DyaK1MXmt1OmsLs%3D

    CAS  Google Scholar 

  3. CW Birky P Fuerst T Maruyama (1989) ArticleTitleOrganelle gene diversity under migration, mutation, and drift: Equilibrium expectations, approach to equilibrium, effects of heteroplasmic cells, and comparison to nuclear genes. Genetics 121 613–627 Occurrence Handle2714640

    PubMed  Google Scholar 

  4. K Blasko SA Kaplan KG Higgins R Wolfson B Sears (1988) ArticleTitleVariation in copy number of a 24-base pair tandem repeat in the chloroplast DNA of Oenothera hookeri strain Johansen. Curr Genet 14 287–292 Occurrence Handle1:CAS:528:DyaL1cXmtVKisbk%3D Occurrence Handle3197136

    CAS  PubMed  Google Scholar 

  5. D Cafasso G Pellegrino A Musacchio A Widmer S Cozzolino (2001) ArticleTitleCharacterization of a minisatellite repeat locus in the chloroplast genome of Orchis palustris (Orchidaceae). Curr Genet 39 394–398

    Google Scholar 

  6. JM Cornuet G Luikart (1996) ArticleTitleDescription and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144 2001–2014 Occurrence Handle1:STN:280:ByiC3s3mtlU%3D Occurrence Handle8978083

    CAS  PubMed  Google Scholar 

  7. S Cozzolino S Aceto P Caputo A Widmer A Dafni (2001) ArticleTitleSpeciation processes in Eastern Mediterranean Orchis s.1. species: Molecular evidence and the role of pollination biology. Isr J Plant Sci 49 91–103 Occurrence Handle10.1092/QV6M-E7A0-QFC7-G6BL Occurrence Handle1:CAS:528:DC%2BD3MXnsVKms7c%3D

    Article  CAS  Google Scholar 

  8. P Delforge (1994) Guide des Orchidées d’Europe, d’Afrique du Nord et du Proche-Orient. Delachaux et Niestlé Lausanne

    Google Scholar 

  9. A Di Rienzo AC Peterson JC Garza AM Valdes M Slatkin NB Freimer (1994) ArticleTitleMutational processes of simple-sequence repeat loci in human populations. Proc Natl Acad Sci USA 91 3166–3170 Occurrence Handle8159720

    PubMed  Google Scholar 

  10. JJ Doyle JL Doyle (1987) ArticleTitleA rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19 11–15

    Google Scholar 

  11. H Ellegren (2000) ArticleTitleHeterogeneous mutation processes in human microsatellite DNA sequences. Nature Genet 24 400–402 Occurrence Handle10.1038/74249 Occurrence Handle1:CAS:528:DC%2BD3cXisVCjtr4%3D Occurrence Handle10742106

    Article  CAS  PubMed  Google Scholar 

  12. L Fumagalli P Taberlet L Favre J Hausser (1996) ArticleTitleOrigin and evolution of homologous repeated sequences in the mitochondrial DNA control region of shrews. Mol Biol Evol 13 IssueID1 31–46 Occurrence Handle1:CAS:528:DyaK28XhtVyltbk%3D Occurrence Handle8583904

    CAS  PubMed  Google Scholar 

  13. T Giraud D Fortini C Levis Y Brygoo (1998) ArticleTitleThe minisatellite MSB1, in the fungus Botrytis cinerea, probably mutates by slippage. Mol Biol Evol 15 IssueID11 1524–1531 Occurrence Handle1:CAS:528:DyaK1cXntlOgs7o%3D

    CAS  Google Scholar 

  14. F Gugerli C Sperisen U Büchler F Magni T Geburek S Jeandroz J Senn (2001) ArticleTitleHaplotype variation in a mitochondrial tandem repeat of Norway spruce (Picea abies) populations suggests a serious founder effect during postglacial re-colonization of the western Alps. Mol Ecol 10 1255–1263 Occurrence Handle1:CAS:528:DC%2BD3MXktFKiuro%3D Occurrence Handle11380882

    CAS  PubMed  Google Scholar 

  15. DG Higgins AJ Bleasby R Fuchs (1992) ArticleTitleCLUSTAL V: Improved software for multiple sequence alignment. Comput Appl Biosci 8 189–191 Occurrence Handle1591615

    PubMed  Google Scholar 

  16. VD Hipkins KA Marshall DB Neale WH Rottmann SH Strauss (1995) ArticleTitleA mutation hotspot in the chloroplast genome of a conifer (Douglas-fir: Pseudotsuga) is caused by variability in the number of direct repeats derived from a partially duplicated tRNA gene. Curr Genet 27 572–579 Occurrence Handle1:CAS:528:DyaK2MXmslegtL8%3D Occurrence Handle7553944

    CAS  PubMed  Google Scholar 

  17. K Isoda S Shiraishi H Kisanuki (2000) ArticleTitleClassifying Abies species (Pinaceae) based on the sequence variation of a tandemly repeated array found in the chloroplast DNA trnL and trnF intergenic spacer. Silvae Genet 49 IssueID3 161–l65

    Google Scholar 

  18. P Jarne PJL Lagoda (1996) ArticleTitleMicrosatellites, from molecules to populations and back. Trends Ecol Evol 11 IssueID10 424–429 Occurrence Handle10.1016/0169-5347(96)10049-5

    Article  Google Scholar 

  19. AJ Jeffreys V Wilson SL Thein (1985) ArticleTitleHypervariable ‘minisatellite’ regions in human DNA. Nature 314 767–73

    Google Scholar 

  20. RA King C Ferris (2002) ArticleTitleA variable minisatellite sequence in the chloroplast genome of Sorbus L. (Rosaceae: Maloideae). Genome 45 570–576 Occurrence Handle10.1139/g02-018 Occurrence Handle1:CAS:528:DC%2BD38Xks1yju78%3D Occurrence Handle12033626

    Article  CAS  PubMed  Google Scholar 

  21. G Levinson GA Gutman (1987) ArticleTitleSlipped-strand mispairing: A major mechanism for DNA sequence evolution. Mol Biol Evol 4 IssueID3 203–221 Occurrence Handle1:CAS:528:DyaL2sXksFejsLw%3D Occurrence Handle3328815

    CAS  PubMed  Google Scholar 

  22. DH Lunt LE Whipple BC Hyman (1998) ArticleTitleMitochondrial DNA variable number tandem repeat (VNTRs): Utility and problems in molecular ecology. Mol Ecol 7 1441–1455 Occurrence Handle10.1046/j.1365-294x.1998.00495.x Occurrence Handle1:CAS:528:DyaK1cXnsFSgt7g%3D Occurrence Handle9819900

    Article  CAS  PubMed  Google Scholar 

  23. M Nei (1987) Molecular evolutionary genetics. Columbia University Press New York

    Google Scholar 

  24. G Platas J Acero JA Borkowski V Gonzàlez MA Portal V Rubio J Sànchez-Ballesteros O Salazar F Pelàez (2001) ArticleTitlePresence of a simple tandem repeat in the ITS1 region of the Xylariales. Curr Microbiol 43 43–50 Occurrence Handle10.1007/s002840010258 Occurrence Handle1:CAS:528:DC%2BD3MXjslKgsLo%3D Occurrence Handle11375663

    Article  CAS  PubMed  Google Scholar 

  25. J Provan N Soranzo NJ Wilson DB Goldstein W Powell (1999) ArticleTitleA low mutation rate for chloroplast microsatellites. Genetics 153 943–947 Occurrence Handle1:CAS:528:DyaK1MXmvFGmsbc%3D Occurrence Handle10511569

    CAS  PubMed  Google Scholar 

  26. DM Rand RG Harrison (1989) ArticleTitleMolecular population genetics of mtDNA size variation in crickets. Genetics 121 551–569 Occurrence Handle1:CAS:528:DyaL1MXhvVOjur4%3D Occurrence Handle2565855

    CAS  PubMed  Google Scholar 

  27. GF Richard F Pâques (2000) ArticleTitleMini- and microsatellite expansions: the recombination connection. EMBO Rep 1 IssueID2 122–126 Occurrence Handle1:CAS:528:DC%2BD3cXnt1yrs7c%3D Occurrence Handle11265750

    CAS  PubMed  Google Scholar 

  28. J Sambrook EF Fritsch T Maniatis (1989) Molecular cloning: A laboratory manual. Cold Spring Harbor Laboratory Press Cold Spring Harbor, NY

    Google Scholar 

  29. EA Sia RJ Kokoska M Dominska (1997) ArticleTitleMicrosatellite instability in yeast: Dependence on repeat unit size and DNA mismatch repair genes. Mol Cell Biol 17 IssueID5 2851–2858 Occurrence Handle1:CAS:528:DyaK2sXislCms78%3D Occurrence Handle9111357

    CAS  PubMed  Google Scholar 

  30. M Soliva A Kocyan A Widmer (2001) ArticleTitleMolecular phylogenetics of the sexually deceptive orchid genus Ophrys (Orchidaceae) based on nuclear and chloroplast DNA sequences. Mol Phylogenet Evol 20 IssueID1 78–88 Occurrence Handle10.1006/mpev.2001.0953 Occurrence Handle1:CAS:528:DC%2BD3MXksF2mu70%3D Occurrence Handle11421649

    Article  CAS  PubMed  Google Scholar 

  31. DL Swofford (1998) Paup*. Phylogenetic analysis using parsimony (*and other methods). Version 4. Sinauer Associates Sunderland, MA

    Google Scholar 

  32. P Taberlet L Gielly G Pautou J Bouvet (1991) ArticleTitleUniversal primers for amplification of three non-coding regions of chloroplast DNA. Plant Mol Biol 17 1105–1109 Occurrence Handle1:CAS:528:DyaK38Xhslel Occurrence Handle1932684

    CAS  PubMed  Google Scholar 

  33. D Tautz C Schlötterer (1994) ArticleTitleSimple sequences. Curr Opin Genet Dev 4 832–837 Occurrence Handle1:CAS:528:DyaK2MXivFKmsro%3D Occurrence Handle7888752

    CAS  PubMed  Google Scholar 

  34. JS Taylor F Breden (2000) ArticleTitleSlipped-strand mispairing at noncontiguous repeats in Poecilia reticulata: A model for minisatellite birth. Genetics 155 1313–1320 Occurrence Handle1:CAS:528:DC%2BD3cXlsFSku7g%3D Occurrence Handle10880490

    CAS  PubMed  Google Scholar 

  35. IJ Wilson DJ Balding (1998) ArticleTitleGenealogical inference from microsatellite data. Genetics 150 IssueID1 499–510 Occurrence Handle1:STN:280:DyaK1czptlKjtg%3D%3D Occurrence Handle9725864

    CAS  PubMed  Google Scholar 

  36. M Zuker DH Mathews DH Turner (1999) Algorithms and thermodynamics for RNA secondary structure prediction: A practical guide. . Barciszewski . Clark (Eds) RNA biochemistry and biotechnology, NATO ASI Series. Kluwer Academic New York

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Dipartimento di Biologia Vegetale, Università degli Studi di Napoli Federico II, via Foria 223, I-80139 Naples, Italy

    Salvatore Cozzolino & Donata Cafasso

  2. Dipartimento di Ecologia, Università della Calabria, Arcavacata di Rende, I-87036 Cosenza, Italy

    Giuseppe Pellegrino & Aldo Musacchio

  3. Department of Biology, Indiana University, Bloomington, IN 47405-3700, USA

    Alex Widmer

  4. Laboratoire d’Écologie, Systématique et Évolution, Université de Paris-Sud (XI), Bâtiment 362, 91405 Orsay Cedex, France

    Alex Widmer

Authors
  1. Salvatore Cozzolino
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Donata Cafasso
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Giuseppe Pellegrino
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Aldo Musacchio
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Alex Widmer
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Salvatore Cozzolino.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cozzolino, S., Cafasso, D., Pellegrino, G. et al. Molecular Evolution of a Plastid Tandem Repeat Locus in an Orchid Lineage . J Mol Evol 57 (Suppl 1), S41–S49 (2003). https://doi.org/10.1007/s00239-003-0006-3

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00239-003-0006-3

Keywords

Search

Navigation