Advertisement

Tree Genetics & Genomes

, Volume 10, Issue 4, pp 885–893 | Cite as

Primers for 52 polymorphic regions in the Quercus rubra chloroplast, 47 of which amplify across 11 tracheophyte clades

  • Daniel S. Borkowski
  • Tim McCleary
  • Mary McAllister
  • Jeanne Romero-SeversonEmail author
Original Paper

Abstract

Postglacial migration studies in Quercus rubra L. (northern red oak) are hampered by low levels of population differentiation in the widely used universal chloroplast primers. We sequenced the large single copy (LSC) regions of the Q. rubra and Quercus ellipsoidalis chloroplasts to enable us to query additional regions for future studies on migration and speciation. Using 454 sequencing of long-range PCR amplicons and Sanger sequencing for gap closure, we report 65 coding sequences from Q. rubra and 59 from Q. ellipsoidalis. Comparison of our de novo assembly of the LSC region sequence for Q. rubra to Q. rubra chloroplast sequence (NCBI Reference Sequence: NC_020152.1) from a different tree revealed 106 polymorphisms, all within intergenic regions, that can serve as tools for postglacial migration studies and taxonomic studies within the Lobatae. Sequence alignment for the 59 complete coding regions in common for theQ. rubrachloroplast reference sequence, our Q. rubra sequence and our Q. ellipsoidalis sequence revealed no sequence polymorphisms and no indels. We also report the 52 primer pairs we used for gap closure, including 53 new primer pairs not previously reported. We tested these 52 primer pairs against 11 species representing the Tracheophyta and detected 47 that produced amplicons in all 11 species. The new universal primers we have identified provide additional tools for resolving the taxonomic relationships among the congeneric taxa of forest trees in the temperate and subtropical forests of the Northern Hemisphere.

Keywords

Quercus rubra Chloroplast genome Universal primers Long-range PCR 

Notes

Acknowledgments

We thank Meg Staton (Clemson University Genomics Institute) for bioinformatics assistance; John Tan, Brent Harker, and Rory Carmichael (Notre Dame Genomics and Bioinformatics Core Facilities) for DNA sequencing and genome assembly; and Amy Fernow for assistance with PCR reactions. Funding for Daniel Borkowski was provided in part by the National Science Foundation (NSF IOS-1025974). The University of Notre Dame Core Genomics Facility provided funding for the 454 sequencing.

Data archiving statement

We have submitted chloroplast genome contigs to GenBank at NCBI, and the accession numbers will be provided as soon as they are available.

Supplementary material

11295_2014_729_MOESM1_ESM.docx (16 kb)
Supplemental Table 1 (DOCX 15 kb)

References

  1. Aziz R, Bartels D, Best A, DeJongh M, Disz T, Edwards R, Formsma K, Gerdes S, Glass E, Kubal M, Meyer F, Olsen G, Olson R, Osterman A, Overbeek R, McNeil L, Paarmann D, Paczian T, Parrello B, Pusch G, Reich C, Stevens R, Vassieva O, Vonstein V, Wilke A, Zagnitko O (2008) The RAST server: rapid annotations using subsystems technology. BMC Genomics 9(1):75PubMedCentralPubMedCrossRefGoogle Scholar
  2. Birchenko I, Feng Y, Romero-Severson J (2009) Biogeographical distribution of chloroplast diversity in northern red oak (Quercus rubra L.). Am Midl Nat 161(1):134–145CrossRefGoogle Scholar
  3. Conant GC, Wolfe KH (2008) GenomeVx: simple web-based creation of editable circular chromosome maps. Bioinformatics 24(6):861–862. doi: 10.1093/bioinformatics/btm598 PubMedCrossRefGoogle Scholar
  4. Deguilloux MF, Dumolin-Lapegue S, Gielly L, Grivet D, Petit RJ (2003) A set of primers for the amplification of chloroplast microsatellites in Quercus. Mol Ecol Notes 3(1):24–27CrossRefGoogle Scholar
  5. Demesure B (1995) A set of universal primers for amplification of polymorphic noncoding regions of mitochondrial and chloroplast DNA in plants. Mol Ecol 4(1):129–131PubMedCrossRefGoogle Scholar
  6. Dumolin-Lapegue S, Demesure B, Fineschi S, LeCorre V, Petit RJ (1997) Phylogeographic structure of white oaks throughout the European continent. Genetics 146(4):1475–1487PubMedCentralPubMedGoogle Scholar
  7. Dumolin-Lapegue S, Kremer A, Petit RJ (1999) Are chloroplast and mitochondrial DNA variation species independent in oaks? Evolution 53(5):1406–1413CrossRefGoogle Scholar
  8. Ferris C, Oliver RP, Davy AJ, Hewitt GM (1995) Using chloroplast DNA to trace postglacial migration routes of oaks into Britain. Mol Ecol 4(6):731–738. doi: 10.1111/j.1365-294X.1995.tb00273.x PubMedCrossRefGoogle Scholar
  9. Grivet D, Heinze B, Vendramin GG, Petit RJ (2001) Genome walking with consensus primers: application to the large single copy region of chloroplast DNA. Mol Ecol Notes 1(4):345–349CrossRefGoogle Scholar
  10. Haider N, Wilkinson MJ (2011) A set of plastid DNA-specific universal primers for flowering plants. Russ J Genet 47(9):1066–1077. doi: 10.1134/s1022795411090079 CrossRefGoogle Scholar
  11. Hipp AL, Weber JA (2008) Taxonomy of Hill’s Oak (Quercus ellipsoidalis: Fagaceae): Evidence from AFLP Data. Syst Bot 33(1):148–158. doi: 10.1600/036364408783887320 CrossRefGoogle Scholar
  12. Hokanson SC, Isebrands JG, Jensen RJ, Hancock JF (1993) Isozyme variation in oaks of the Apostle Islands in Wisconsin - Genetic-structure and levels of inbreeding in Quercus-rubra and Q. ellipsoidalis (Fagaceae). Am J Bot 80(11):1349–1357CrossRefGoogle Scholar
  13. Jansen R, Kaittanis C, Saski C, Lee S-B, Tomkins J, Alverson A, Daniell H (2006) Phylogenetic analyses of Vitis (Vitaceae) based on complete chloroplast genome sequences: effects of taxon sampling and phylogenetic methods on resolving relationships among rosids. BMC Evol Biol 6(1):32PubMedCentralPubMedCrossRefGoogle Scholar
  14. Jansen RK, Saski C, Lee S-B, Hansen AK, Daniell H (2011) Complete plastid genome sequences of three rosids (Castanea, Prunus, Theobroma): evidence for at least two independent transfers of rpl22 to the nucleus. Mol Biol Evol 28(1):835–847. doi: 10.1093/molbev/msq261 PubMedCentralPubMedCrossRefGoogle Scholar
  15. LeCorre V, Kremer A (1998) Cumulative effects of founding events during colonisation on genetic diversity and differentiation in an island and stepping-stone model. J Evol Biol 11(4):195–512Google Scholar
  16. Lind J, Gailing O (2013) Genetic structure of Quercus rubra L. and Quercus ellipsoidalis E. J. Hill populations at gene-based EST-SSR and nuclear SSR markers. Tree Genet Genomes 9(3):707–722. doi: 10.1007/s11295-012-0586-4 CrossRefGoogle Scholar
  17. Little ELJ (1979) Atlas of United States trees. J For 77(3):188Google Scholar
  18. Magni CR, Ducousso A, Caron H, Petit RJ, Kremer A (2005) Chloroplast DNA variation of Quercus rubra L. in North America and comparison with other Fagaceae. Mol Ecol 14(2):513–524PubMedCrossRefGoogle Scholar
  19. McCleary TS, Robichaud RL, Nuanes S, Anagnostakis SL, Schlarbaum SE, Romero-Severson J (2009) Four cleaved amplified polymorphic sequence (CAPS) markers for the detection of the Juglans ailantifolia chloroplast in putatively native J. cinerea populations. Mol Ecol Resour 9(2):525–527. doi: 10.1111/j.1755-0998.2008.02465.x PubMedCrossRefGoogle Scholar
  20. McCleary T, McAllister M, Coggeshall M, Romero-Severson J (2013) EST-SSR markers reveal synonymies, homonymies and relationships inconsistent with putative pedigrees in chestnut cultivars. Genet Resour Crop Evol 60(4):1209–1222. doi: 10.1007/s10722-012-9912-9 CrossRefGoogle Scholar
  21. Petit R, Wagner D, Kremer A (1993a) Ribosomal DNA and chloroplast DNA polymorphisms in a mixed stand of Quercus robur and Q. petraea. Ann For Sci 50(Supplement):41s–47sCrossRefGoogle Scholar
  22. Petit RJ, Kremer A, Wagner DB (1993b) Geographic structure of chloroplast DNA polymorphisms in European oaks. Theor Appl Genet 87(1–2):122–128. doi: 10.1007/bf00223755 PubMedGoogle Scholar
  23. Petit RJ, Pineau E, Demesure B, Bacilieri R, Ducousso A, Kremer A (1997) Chloroplast DNA footprints of postglacial recolonization by oaks. Proc Natl Acad Sci U S A 94(18):9996–10001PubMedCentralPubMedCrossRefGoogle Scholar
  24. Petit R, Csaikl U, Bordacs S, Burg K, Coart E, Cottrell J et al (2002) Chloroplast DNA variation in European white oaks—phylogeography and patterns of diversity based on data from over 2600 populations. For Ecol Manag 156(1–3):5–26CrossRefGoogle Scholar
  25. Petit RJ, Aguinagalde I, de Beaulieu JL, Bittkau C, Brewer S, Cheddadi R, Ennos R, Fineschi S, Grivet D, Lascoux M, Mohanty A, Muller-Starck GM, Demesure-Musch B, Palme A, Martin JP, Rendell S, Vendramin GG (2003) Glacial refugia: hotspots but not melting pots of genetic diversity. Science 300(5625):1563–1565PubMedCrossRefGoogle Scholar
  26. Romero-Severson J, Aldrich P, Feng Y, Sun WL, Michler A (2003) Chloroplast DNA variation of northern red oak (Quercus rubra L.) in Indiana. New For 26(1):43–49CrossRefGoogle Scholar
  27. Rozen S, Skaletsky HJ (2000) Primer3 on the WWW for general users and for biologist programmers. In: Krawetz S, Misener S (eds) Bioinformatics methods and protocols: methods in molecular biology. Humana Press, Totowa, pp 365–386Google Scholar
  28. Shaw J, Lickey EB, Beck JT, Farmer SB, Liu W, Miller J, Siripun KC, Winder CT, Schilling EE, Small RL (2005) The tortoise and the hare II: relative utility of 21 noncoding chloroplast DNA sequences for phylogenetic analysis. Am J Bot 92(1):142–166. doi: 10.3732/ajb.92.1.142 PubMedCrossRefGoogle Scholar
  29. Shaw J, Lickey EB, Schilling EE, Small RL (2007) Comparison of whole chloroplast genome sequences to choose noncoding regions for phylogenetic studies in angiosperms: the tortoise and the hare III. Am J Bot 94(3):275–288. doi: 10.3732/ajb.94.3.275 PubMedCrossRefGoogle Scholar
  30. Taberlet P, Gielly L, Pautou G, Bouvet J (1991) Universal primers for amplification of three non-coding regions of chloroplast DNA. Plant Mol Biol 17(5):1105–1109. doi: 10.1007/bf00037152 PubMedCrossRefGoogle Scholar
  31. Tomlinson PT, Jensen RJ, Hancock JF (2000) Do whole tree silvic characters indicate hybridization in red oak (Quercus Section Lobatae)? Am Midl Nat 143(1):154–168. doi: 10.1674/0003-0031(2000)143[0154:dwtsci]2.0.co;2 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Daniel S. Borkowski
    • 1
  • Tim McCleary
    • 1
  • Mary McAllister
    • 1
  • Jeanne Romero-Severson
    • 1
    Email author
  1. 1.Department of Biological SciencesUniversity of Notre DameNotre DameUSA

Personalised recommendations