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Cross-amplification and sequence variation of microsatellite loci in Eurasian hard pines

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Abstract

Microsatellite transfer across coniferous species is a valued methodology because de novo development for each species is costly and there are many species with only a limited commodity value. Cross-species amplification of orthologous microsatellite regions provides valuable information on mutational and evolutionary processes affecting these loci. We tested 19 nuclear microsatellite markers from Pinus taeda L. (subsection Australes) and three from P. sylvestris L. (subsection Pinus) on seven Eurasian hard pine species (P. uncinata Ram., P. sylvestris L., P. nigra Arn., P. pinaster Ait., P. halepensis Mill., P. pinea L. and P. canariensis Sm.). Transfer rates to species in subsection Pinus (36–59%) were slightly higher than those to subsections Pineae and Pinaster (32–45%). Half of the trans-specific microsatellites were found to be polymorphic over evolutionary times of approximately 100 million years (ten million generations). Sequencing of three trans-specific microsatellites showed conserved repeat and flanking regions. Both a decrease in the number of perfect repeats in the non-focal species and a polarity for mutation, the latter defined as a higher substitution rate in the flanking sequence regions close to the repeat motifs, were observed in the trans-specific microsatellites. The transfer of microsatellites among hard pine species proved to be useful for obtaining highly polymorphic markers in a wide range of species, thereby providing new tools for population and quantitative genetic studies.

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References

  • Al-Rababah M, Williams CG (2002) Population dynamics of Pinus taeda L. based on nuclear microsatellites. For Ecol Manage 163:263–271

    Google Scholar 

  • Auckland LD, Bui T, Zhou Y, Shepherd M, Williams CG (2002) Conifer microsatellite handbook. Corporate Press, Raleigh, N.C.

  • Barbéro M, Loisel R, Quézel P, Richardson DM, Romane F (1998) Pines of the Mediterranean basin. In: Richardson DM (ed) Ecology and biogeography of Pinus. Cambridge University Press, Cambridge, pp 153–170

  • Brohede J, Ellegren H (1999) Microsatellite evolution: polarity of substitutions within repeats and neutrality of flanking sequences. Proc R Soc London Ser B 266:825–833

    CAS  Google Scholar 

  • Cooper G, Rubinsztein DC, Amos W (1998) Ascertainment bias cannot entirely account for human microsatellites being longer than their chimpanzee homologues. Hum Mol Genet 7:1425–1429

    CAS  PubMed  Google Scholar 

  • Crawford AM, Kappes SM, Paterson KA, deGotari MJ, Dodds KG, Freking BA, Stone RT, Beattie CW (1998) Microsatellite evolution: testing the ascertainment bias hypothesis. J Mol Evol 46:256–260

    CAS  PubMed  Google Scholar 

  • Dellaporta SL, Wood J, Hicks JB (1983) A plant DNA minipreparation: Version II. Plant Mol Biol Rep 1:19–21

    CAS  Google Scholar 

  • Devey ME, Jermstad KD, Tauer CG, Neale DB (1991) Inheritance of RFLP loci in a loblolly pine three-generation pedigree. Theor Appl Genet 83:238–242

    Google Scholar 

  • Devey ME, Sewell MM, Uren TL, Neale DB (1999) Comparative mapping in loblolly and radiata pine using RFLP and microsatellite markers. Theor Appl Genet 99:656–662

    CAS  Google Scholar 

  • Echt CS, Deverno LL, Anzidei M, Vendramin GG (1998) Chloroplast microsatellites reveal population genetic diversity in red pine, Pinus resinosa Ait. Mol Ecol 7:307–316

    Article  Google Scholar 

  • Echt CS, Vendramin GG, Nelson CD, Marquardt P (1999) Microsatellite DNA as shared genetic markers among conifer species. Can J For Res 29:365–371

    Article  CAS  Google Scholar 

  • Ellegren H (2000) Microsatellite mutations in the germline: implications for evolutionary inference. Trends Genet 16:551–558

    Article  CAS  PubMed  Google Scholar 

  • Ellegren H, Primmer CR, Sheldon BC (1995) Microsatellite evolution: directionality or bias in locus selection. Nat Genet 11:360–362

    CAS  PubMed  Google Scholar 

  • Elsik CG, Williams CG (2001) Families of clustered microsatellites in a conifer genome. Mol Genet Genomics 265:535–542

    CAS  PubMed  Google Scholar 

  • Fallour D, Fady B, Lefevre F (1997) Study on isozyme variation in Pinus pinea L.: Evidence for low polymorphism. Silvae Genet 46:201–207

    Google Scholar 

  • Frankis MP (1993) Morphology and affinities of Pinus brutia. In: Ministry of Forestry (ed) Int Symp Pinus brutia Ten. Ministry of Forestry, Ankara, pp 11–18

  • Geada-López G, Kamiya K, Harada K (2002) Phylogenetic relationships of Diploxylon pines (subgenus Pinus) based on plastid sequence data. Int J Plant Sci 163:737–747

    Article  Google Scholar 

  • Gómez A, Aguiriano E, Alía R, Bueno MA (2002) Análisis de los recursos genéticos de Pinus pinea L. en España mediante microsatélites del cloroplasto. Invest Agrar Sist Recur For 11:145–154

    Google Scholar 

  • Hurlbert SH (1971) The nonconcept of species diversity: a critique and alternative parameters. Ecology 52:577–586

    Google Scholar 

  • Joyner KL, Wang X-R, Johnston JS, Price HJ, Williams CG (2001) DNA content for Asian pines parallels New World relatives. Can J Bot 79:179–191

    Article  Google Scholar 

  • Karhu A (2001) Evolution and applications of pine microsatellites. University of Oulu, Oulu, Finland

  • Karhu A, Dieterich JH, Savolainen O (2000) Rapid expansion of microsatellite sequences in pines. Mol Biol Evol 17:259–265

    CAS  PubMed  Google Scholar 

  • Keys RN, Autino A, Edwards KJ, Fady B, Pichot C, Vendramin GG (2000) Characterization of nuclear microsatellites in Pinus halepensis Mill. and their inheritance in Pinus halepensis and Pinus brutia Ten. Mol Ecol 9:2157–2159

    CAS  PubMed  Google Scholar 

  • Klaus W (1989) Mediterranean pines and their history. Plant Syst Evol 162:133–163

    Google Scholar 

  • Kostia S, Varvio SL, Vakkari P, Pulkkinen P (1995) Microsatellite sequences in a conifer, Pinus sylvestris. Genome 38:1244–1248

    CAS  PubMed  Google Scholar 

  • Krupkin AB, Liston A, Strauss SH (1996) Phylogenetic analysis of the hard pines (subgenus Pinus, Pinaceae) from chloroplast DNA restriction site analysis. Am J Bot 83:489–498

    Google Scholar 

  • Kutil B, Williams CG (2001) Triplet-repeat microsatellites shared among hard and soft pines. J Hered 92:327–332

    CAS  PubMed  Google Scholar 

  • Liston A, Robinson WA, Piñero D, Álvarez-Buylla ER (1999) Phylogenetics of Pinus (Pinaceae) based on nuclear ribosomal DNA internal transcribed spacer region sequences. Mol Phylogenet Evol 11:95–109

    Article  PubMed  Google Scholar 

  • Mariette S, Chagne D, Decroocq S, Vendramin GG, Lalanne C, Madur D, Plomion C (2001) Microsatellite markers for Pinus pinaster Ait. Ann For Sci 58:203–206

    Article  Google Scholar 

  • Meksem K, Njiti VN, Banz WJ, Iqbal MJ, Kassem MyM, Hyten DL, Yuang J, Winters TA, Lightfoot DA (2001) Genomic regions that underlie soybean seed isoflavone content. J Biomed Biotechnol 1:38–44

    Article  PubMed  Google Scholar 

  • Miller C (1977) Mesozoic conifers. Bot Rev 43:217–280

    Google Scholar 

  • Nei M (1973) Analysis of gene diversity in subdivided populations. Proc Natl Acad Sci USA 70:3321–3323

    CAS  PubMed  Google Scholar 

  • Orti G, Pearse DE, Avise JC (1997) Phylogenetic assessment of length variation at a microsatellite locus. Proc Natl Acad Sci USA 94:10745–10749

    CAS  PubMed  Google Scholar 

  • Price RA, Liston A, Strauss SH (1998) Phylogeny and systematics of Pinus. In: Richardson DM (ed) Ecology and biogeography of Pinus. Cambridge University Press, Cambridge, pp 49–68

  • Primmer CR, Ellegren H (1998) Patterns of molecular evolution in avian microsatellites. Mol Biol Evol 15:997–1008

    Google Scholar 

  • Prus-Glowacki W, Stephan BR (1994) Genetic variation of Pinus sylvestris from Spain in relation to other European populations. Silvae Genet 43:7–14

    Google Scholar 

  • Raymond M, Rousset F (1995a) An exact test for population differentiation. Evolution 49:1280–1283.

    Google Scholar 

  • Raymond M, Rousset F (1995b) genepop (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249

    Google Scholar 

  • Shepherd M, Cross M, Maguire TL, Dieters MJ, Williams CG, Henry RJ (2002) Transpecific microsatellites for hard pines. Theor Appl Genet 104:819–827

    CAS  Google Scholar 

  • Soranzo N, Provan J, Powell W (1998) Characterization of microsatellite loci in Pinus sylvestris L. Mol Ecol 7:1260–1261

    CAS  PubMed  Google Scholar 

  • Soranzo N, Alía R, Provan J, Powell W (2000) Patterns of variation at mitochondrial sequence-tagged-site locus provides new insights into the postglacial history of European Pinus sylvestris populations. Mol Ecol 9:1205–1211

    Article  CAS  PubMed  Google Scholar 

  • Taylor JS, Durkin JM, Breden F (1999) The death of a microsatellite: a phylogenetic perspective on microsatellite interruptions. Mol Biol Evol 16:567–572

    CAS  PubMed  Google Scholar 

  • Zhou Y, Bui T, Auckland LD, Williams CG (2002) Undermethylated DNA as a source of microsatellites from a conifer genome. Genome 45:91–99

    Article  PubMed  Google Scholar 

  • Zhu Y, Queller DC, Strassmann JE (2000) A phylogenetic perspective of sequence evolution in microsatellite loci. J Mol Evol 50:324–338

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank G. Geada-López, who provided unpublished data on the phylogenetic classification of hard pines, and A. Gómez for her technical assistance. JJR was supported by a PhD scholarship from the UPM (Universidad Politécnica de Madrid). AD was supported by a PhD scholarship from the Ministerio de Educación, Cultura y Deporte (Spain). The study was funded by the Cooperation project DGCN (Dirección General de Conservación de la Naturaleza)-INIA (Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria) CC00-0035 and the Ramón y Cajal project (Ministerio de Ciencia y Tecnología) RC01-0611.

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Authors and Affiliations

  1. Unidad de Genética Forestal, CIFOR-INIA, P.O. Box 8111, 28080, Madrid, Spain

    S. C. González-Martínez, J. J. Robledo-Arnuncio, R. Alía & M. T. Cervera

  2. Departamento de Biotecnología, ETSIM, Ciudad Universitaria s/n, 28040, Madrid, Spain

    C. Collada & A. Díaz

  3. Graduate Genetics Program, TAMU 2135, Texas A & M University, College Station, TX 77843-2125, USA

    C. G. Williams

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  1. S. C. González-Martínez
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  2. J. J. Robledo-Arnuncio
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  3. C. Collada
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  4. A. Díaz
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  5. C. G. Williams
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  6. R. Alía
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  7. M. T. Cervera
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Correspondence to M. T. Cervera.

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Communicated by D.B. Neale

S.C. González-Martínez and J.J. Robledo-Arnuncio have contributed equally to this work and are to be considered as joint first authors

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González-Martínez, S.C., Robledo-Arnuncio, J.J., Collada, C. et al. Cross-amplification and sequence variation of microsatellite loci in Eurasian hard pines. Theor Appl Genet 109, 103–111 (2004). https://doi.org/10.1007/s00122-004-1596-x

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  • DOI: https://doi.org/10.1007/s00122-004-1596-x

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