Skip to main content
Log in

Patterns of DNA sequence variation at candidate gene loci in black poplar (Populus nigra L.) as revealed by single nucleotide polymorphisms

  • Published:
Genetica Aims and scope Submit manuscript

Abstract

Black poplar (Populus nigra L.) is an economically and ecologically important tree species and an ideal organism for studies of genetic variation. In the present work, we use a candidate gene approach to infer the patterns of DNA variation in natural populations of this species. A total of 312 single nucleotide polymorphisms (SNPs) are found among 8,056 bp sequenced from nine drought-adaptation and photosynthesis-related gene loci. The median SNP frequency is one site per 26 bp. The average nucleotide diversity is calculated to be θW = 0.01074 and πT = 0.00702, higher values than those observed in P. tremula, P. trichocarpa and most conifer species. Tests of neutrality for each gene reveal a general excess of low-frequency mutations, a greater number of haplotypes than expected and an excess of high-frequency derived variants in P. nigra, which is consistent with previous findings that genetic hitchhiking has occurred in this species. Linkage disequilibrium is low, decaying rapidly from 0.45 to 0.20 or less within a distance of 300 bp, although the declines of r 2 are variable among different loci. This is similar to the rate of decay reported in most other tree species. Our dataset is expected to enhance understanding of how evolutionary forces shape genetic variation, and it will contribute to molecular breeding in black poplar.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Andersson I, Backlund A (2008) Structure and function of Rubisco. Plant Physiol Biochem 46:275–291

    PubMed  CAS  Google Scholar 

  • Boerjan W (2005) Biotechnology and the domestication of forest trees. Curr Opin Biotechnol 16:159–166. doi:10.1016/j.copbio.2005.03.003

    Article  PubMed  CAS  Google Scholar 

  • Caicedo AL, Williamson SH, Hernandez RD, Boyko A, Fledel-Alon A, York TL, Polato NR, Olsen KM, Nielsen R, McCouch SR, Bustamante CD, Purugganan MD (2007) Genome-wide patterns of nucleotide polymorphism in domesticated rice. PLoS Genet 3:1745–1756. doi:10.1371/journal.pgen.0030163

    Article  PubMed  CAS  Google Scholar 

  • Choi I-Y, Hyten DL, Matukumalli LK, Song QJ, Chaky JM, Quigley CV, Chase K, Lark KG, Reiter RS, Yoon M-S, Hwang E-Y, Yi S-I, Young ND, Shoemaker RC, van Tassell CP, Specht JE, Cregan PB (2007) A soybean transcript map: gene distribution, haplotype and single-nucleotide polymorphism analysis. Genetics 176:685–696. doi:10.1534/genetics.107.070821

    Article  PubMed  CAS  Google Scholar 

  • Cottrell JE, Krystufek V, Tabbener HE, Milner AD, Connolly T, Sing L, Fluch S, Burg K, Lefèvre F, Achard P, Bordács S, Gebhardt K, Vornam B, Smulders MJM, Vanden Broeck AH, Van Slycken J, Storme V, Boerjan W, Castiglione S, Fossati T, Alba N, Agúndez D, Maestro C, Notivol E, Bovenschen J, van Dam BC (2005) Postglacial migration of Populus nigra L.: lessons learnt from chloroplast DNA. For Ecol Manage 219:293–312. doi:10.1016/j.foreco.2005.10.003

    Article  Google Scholar 

  • Eckenwalder JE (1996) Systematic and evolution of Populus. In: Stettler RF, Bradshaw HD Jr, Heilman PE, Hinckley TM (eds) Biology of Populus and its implications for management and conservation. NRC Research Press, National Council of Canada, Ottawa, pp 7–32

    Google Scholar 

  • Ewing B, Hillier L, Wendl MC, Green P (1998) Base-calling of automated sequencer traces using Phred. I. Accuracy assessment. Genome Res 8:175–185

    PubMed  CAS  Google Scholar 

  • Fay JC, Wu C-I (2000) Hitchhiking under positive Darwinian selection. Genetics 155:1405–1413

    PubMed  CAS  Google Scholar 

  • Flint-Garcia SA, Thornsberry JM, Buckler ESIV (2003) Structure of linkage disequilibrium in plants. Annu Rev Plant Biol 54:357–374. doi:10.1146/annurev.arplant.54.031902.134907

    Article  PubMed  CAS  Google Scholar 

  • Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925

    PubMed  CAS  Google Scholar 

  • Fu YX, Li WH (1993) Statistical tests of neutrality of mutations. Genetics 133:693–709

    PubMed  CAS  Google Scholar 

  • García MV, Ingvarsson PK (2007) An excess of nonsynonymous polymorphism and extensive haplotype structure at the PtABI1B locus in European aspen (Populus tremula): a case of balancing selection in an obligately outcrossing plant? Heredity 99:381–388

    Article  PubMed  Google Scholar 

  • Gaudet M, Fara A-G, Sabatti M, Kuzminsky E, Mugnozza GS (2007) Single-reaction for SNP genotyping on agarose gel by allele-specific PCR in black poplar (Populus nigra L.). Plant Mol Biol Rep 25:1–9. doi:10.1007/s11105-007-0003-6

    Article  CAS  Google Scholar 

  • Gaudet M, Jorge V, Paolucci I, Beritognolo I, Mugnozza GS, Sabatti M (2008) Genetic linkage maps of Populus nigra L. including AFLPs, SSRs, SNPs, and sex trait. Tree Genet Genomes 4:25–36. doi:10.1007/s11295-007-0085-1

    Article  Google Scholar 

  • Gilchrist EJ, Haughn GW, Ying CC, Otto SP, Zhuang J, Cheung D, Hamberger B, Aboutorabi F, Kalynyak T, Johnson L, Bohlmann J, Ellis BE, Douglas CJ, Cronk QC (2006) Use of ecotilling as an efficient SNP discovery tool to survey genetic variation in wild populations of Populus trichocarpa. Mol Ecol 15:1367–1378. doi:10.1111/j.1365-294X.2006.02885.x

    Article  PubMed  CAS  Google Scholar 

  • González-Martínez SC, Krutovsky KV, Neale DB (2006) Forest-tree population genomics and adaptive evolution. New Phytol 170:227–238. doi:10.1111/j.1469-8137.2006.01686.x

    Article  PubMed  Google Scholar 

  • Grossman AR, Bhaya D, Apt KE, Kehoe DM (1995) Light-harvesting complexes in oxygenic photosynthesis: diversity, control, and evolution. Annu Rev Genet 29:231–288. doi:10.1146/annurev.ge.29.120195.001311

    Article  PubMed  CAS  Google Scholar 

  • Gupta PK, Roy JK, Prasad M (2001) Single nucleotide polymorphisms: a new paradigm for molecular marker technology and DNA polymorphism detection with emphasis on their use in plants. Curr Sci 80:524–535

    CAS  Google Scholar 

  • Hedrick PW (1987) Gametic disequilibrium measures: proceed with caution. Genetics 117:331–342

    PubMed  CAS  Google Scholar 

  • Hill WG, Robertson A (1968) Linkage disequilibrium in finite populations. Theor Appl Genet 38:226–231. doi:10.1007/BF01245622

    Article  Google Scholar 

  • Hill WG, Weir BS (1988) Variances and covariances of squared linkage disequilibria in finite populations. Theor Popul Biol 33:54–78. doi:10.1016/0040-5809(88)90004-4

    Article  PubMed  CAS  Google Scholar 

  • Hudson RR, Kaplan NL (1985) Statistical properties of the number of recombination events in the history of a sample of DNA sequences. Genetics 111:147–164

    PubMed  CAS  Google Scholar 

  • Hyten DL, Choi I-Y, Song QJ, Shoemaker RC, Nelson RL, Costa JM, Specht JE, Cregan PB (2007) Highly variable patterns of linkage disequilibrium in multiple soybean populations. Genetics 175:1937–1944. doi:10.1534/genetics.106.069740

    Article  PubMed  CAS  Google Scholar 

  • Ingvarsson PK (2005) Nucleotide polymorphism and linkage disequilibrium within and among natural populations of European aspen (Populus tremula L., Salicaceae). Genetics 169:945–953. doi:10.1534/genetics.104.034959

    Article  PubMed  CAS  Google Scholar 

  • Ingvarsson PK (2008) Multilocus patterns of nucleotide polymorphism and the demographic history of Populus tremula. Genetics 180:329–340

    Article  PubMed  Google Scholar 

  • Jansson S (1994) The light-harvesting chlorophyll a/b binding proteins. Biochim Biophys Acta 1184:1–19. doi:10.1016/0005-2728(94)90148-1

    Article  PubMed  CAS  Google Scholar 

  • Jansson S (1999) A guide to the Lhc genes and their relatives in Arabidopsis. Trends Plant Sci 4:236–240. doi:10.1016/S1360-1385(99)01419-3

    Article  PubMed  Google Scholar 

  • Kelly JK (1997) A test of neutrality based on interlocus associations. Genetics 146:1197–1206

    PubMed  CAS  Google Scholar 

  • Kim S, Plagnol V, Hu TT, Toomajian C, Clark RM, Ossowski S, Ecker JR, Weigel D, Nordborg M (2007) Recombination and linkage disequilibrium in Arabidopsis thaliana. Nat Genet 39:1151–1155. doi:10.1038/ng2115

    Article  PubMed  CAS  Google Scholar 

  • Krutovsky KV, Neale DB (2005) Nucleotide diversity and linkage disequilibrium in cold-hardiness- and wood quality-related candidate genes in Douglas fir. Genetics 171:2029–2041. doi:10.1534/genetics.105.044420

    Article  PubMed  CAS  Google Scholar 

  • Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948. doi:10.1093/bioinformatics/btm404

    Article  PubMed  CAS  Google Scholar 

  • Mather KA, Caicedo AL, Polato NR, Olsen KM, McCouch S, Purugganan MD (2007) The extent of linkage disequilibrium in rice (Oryza sativa L.). Genetics 177:2223–2232. doi:10.1534/genetics.107.079616

    Article  PubMed  CAS  Google Scholar 

  • McDonald JH, Kreitman M (1991) Adaptive protein evolution at the Adh locus in Drosophila. Nature 351:652–654. doi:10.1038/351652a0

    Article  PubMed  CAS  Google Scholar 

  • Moriyama EN, Powell JR (1996) Intraspecific nuclear DNA variation in Drosophila. Mol Biol Evol 13:261–277

    PubMed  CAS  Google Scholar 

  • Morrell PL, Toleno DM, Lundy KE, Clegg MT (2005) Low levels of linkage disequilibrium in wild barley (Hordeum vulgare ssp. spontaneum) despite high rates of self-fertilization. Proc Natl Acad Sci USA 102:2442–2447. doi:10.1073/pnas.0409804102

    Article  PubMed  CAS  Google Scholar 

  • Neale DB (2007) Genomics to tree breeding and forest health. Curr Opin Genet Dev 17:539–544. doi:10.1016/j.gde.2007.10.002

    Article  PubMed  CAS  Google Scholar 

  • Neale DB, Ingvarsson PK (2008) Population, quantitative and comparative genomics of adaptation in forest trees. Curr Opin Plant Biol 11:149–155

    PubMed  CAS  Google Scholar 

  • Neale DB, Savolainen O (2004) Association genetics of complex traits in conifers. Trends Plant Sci 9:325–330. doi:10.1016/j.tplants.2004.05.006

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Nei M, Li WH (1979) Mathematical model for studying genetic variation in terms of restriction endonucleases. Proc Natl Acad Sci USA 76:5269–5273. doi:10.1073/pnas.76.10.5269

    Article  PubMed  CAS  Google Scholar 

  • Nordborg M, Hu TT, Ishino Y, Jhaveri J, Toomajian C, Zheng H, Bakker E, Calabrese P, Gladstone J, Goyal R, Jakobsson M, Kim S, Morozov Y, Padhukasahasram B, Plagnol V, Rosenberg NA, Shah C, Wall JD, Wang J, Zhao K, Kalbfleisch T, Schulz V, Kreitman M, Bergelson J (2005) The pattern of polymorphism in Arabidopsis thaliana. PLoS Biol 3:e196. doi:10.1371/journal.pbio.0030196

    Article  PubMed  Google Scholar 

  • Przeworski M (2002) The signature of positive selection at randomly chosen loci. Genetics 160:1179–1189

    PubMed  Google Scholar 

  • Rafalski A (2002) Applications of single nucleotide polymorphisms in crop genetics. Curr Opin Plant Biol 5:94–100. doi:10.1016/S1369-5266(02)00240-6

    Article  PubMed  CAS  Google Scholar 

  • Remington DL, Thornsberry JM, Matsuoka Y, Wilson LM, Whitt SR, Doebley J, Kresovich S, Goodman MM, Buckler ESIV (2001) Structure of linkage disequilibrium and phenotypic associations in the maize genome. Proc Natl Acad Sci USA 98:11479–11484. doi:10.1073/pnas.201394398

    Article  PubMed  CAS  Google Scholar 

  • Rorat T (2006) Plant dehydrins-tissue location, structure and function. Cell Mol Biol Lett 11:536–556. doi:10.2478/s11658-006-0044-0

    Article  PubMed  CAS  Google Scholar 

  • Ross-Ibarra J, Wright SI, Foxe JP, Kawabe A, DeRose-Wilson L, Gos G, Charlesworth D, Gaut BS (2008) Patterns of polymorphism and demographic history in natural populations of Arabidopsis lyrata. PLoS One 3:e2411. doi:10.1371/journal.pone.0002411

    Article  PubMed  Google Scholar 

  • Rozas J, Sánchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497. doi:10.1093/bioinformatics/btg359

    Article  PubMed  CAS  Google Scholar 

  • Rozen S, Skaletsky HJ (2000) Primer 3 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 365–386

    Google Scholar 

  • Savolainen O, Pyhäjärvi T (2007) Genomic diversity in forest trees. Curr Opin Plant Biol 10:162–167. doi:10.1016/j.pbi.2007.01.011

    Article  PubMed  CAS  Google Scholar 

  • Smulders MJM, Cottrell JE, Lefèvre F, van der Schoot J, Arens P, Vosman B, Tabbener HE, Grassi F, Fossati T, Castiglione S, Krystufek V, Fluch S, Burg K, Vornam B, Pohl A, Gebhardt K, Alba N, Agúndez D, Maestro C, Notivol E, Volosyanchuk R, Pospíšková M, Bordács S, Bovenschen J, van Dam BC, Koelewijn HP, Halfmaerten D, Ivens B, van Slycken J, Vanden Broeck A, Storme V, Boerjan W (2008) Structure of the genetic diversity in black poplar (Populus nigra L) populations across European river systems: consequences for conservation and restoration. For Ecol Manage 255:1388–1399. doi:10.1016/j.foreco.2007.10.063

    Article  Google Scholar 

  • Storme V, Vanden Broeck A, Ivens B, Halfmaerten D, Van Slycken J, Castiglione S, Grassi F, Fossati T, Cottrell JE, Tabbener HE, Lefèvre F, Saintagne C, Fluch S, Krystufek V, Burg K, Bordács S, Borovics A, Gebhardt K, Vornam B, Pohl A, Alba N, Agúndez D, Maestro C, Notivol E, Bovenschen J, van Dam BC, van der Schoot J, Vosman B, Boerjan W, Smulders MJ (2004) Ex-situ conservation of black poplar in Europe: genetic diversity in nine gene bank collections and their value for nature development. Theor Appl Genet 108:969–981. doi:10.1007/s00122-003-1523-6

    Article  PubMed  CAS  Google Scholar 

  • Street NR, Skogström O, Sjödin A, Tucker J, Rodríguez-Acosta M, Nilsson P, Jansson S, Taylor G (2006) The genetics and genomics of the drought response in Populus. Plant J 48:321–341. doi:10.1111/j.1365-313X.2006.02864.x

    Article  PubMed  CAS  Google Scholar 

  • Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595

    PubMed  CAS  Google Scholar 

  • Tuskan GA, Difazio S, Jansson S, Bohlmann J, Grigoriev I, Hellsten U, Putnam N, Ralph S, Rombauts S, Salamov A, Schein J, Sterck L, Aerts A, Bhalerao RR, Bhalerao RP, Blaudez D, Boerjan W, Brun A, Brunner A, Busov V, Campbell M, Carlson J, Chalot M, Chapman J, Chen GL, Cooper D, Coutinho PM, Couturier J, Covert S, Cronk Q, Cunningham R, Davis J, Degroeve S, Déjardin A, Depamphilis C, Detter J, Dirks B, Dubchak I, Duplessis S, Ehlting J, Ellis B, Gendler K, Goodstein D, Gribskov M, Grimwood J, Groover A, Gunter L, Hamberger B, Heinze B, Helariutta Y, Henrissat B, Holligan D, Holt R, Huang W, Islam-Faridi N, Jones S, Jones-Rhoades M, Jorgensen R, Joshi C, Kangasjärvi J, Karlsson J, Kelleher C, Kirkpatrick R, Kirst M, Kohler A, Kalluri U, Larimer F, Leebens-Mack J, Leplé JC, Locascio P, Lou Y, Lucas S, Martin F, Montanini B, Napoli C, Nelson DR, Nelson C, Nieminen K, Nilsson O, Pereda V, Peter G, Philippe R, Pilate G, Poliakov A, Razumovskaya J, Richardson P, Rinaldi C, Ritland K, Rouzé P, Ryaboy D, Schmutz J, Schrader J, Segerman B, Shin H, Siddiqui A, Sterky F, Terry A, Tsai CJ, Uberbacher E, Unneberg P, Vahala J, Wall K, Wessler S, Yang G, Yin T, Douglas C, Marra M, Sandberg G, Van de Peer Y, Rokhsar D (2006) The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313:1596–1604. doi:10.1126/science.1128691

    Article  PubMed  CAS  Google Scholar 

  • van der Schoot J, Pospíšková M, Vosman B, Smulders MJM (2000) Development and characterization of microsatellite markers in black poplar (Populus nigra L.). Theor Appl Genet 101:317–322. doi:10.1007/s001220051485

    Article  Google Scholar 

  • Vanden BA (2003) EUFORGEN technical guidelines for genetic conservation and use for European black poplar (Populus nigra L.). International Plant Genetic Resources Institute, Rome, pp 1–6

    Google Scholar 

  • Watterson GA (1975) On the number of segregating sites in genetical models without recombination. Theor Popul Biol 7:256–276. doi:10.1016/0040-5809(75)90020-9

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank Bronwyn Matheson (CSIRO Plant Industry, Australia) for her critical reading of the manuscript. This work was financially supported by the National Key Technology R&D Program for the Eleventh Five-Year-Plan of China (Grant No. 2006BAD01A15 and 2006BAD24B0403) and National Basic Research Program of China (973 program) (Grant No. 2009CB119107).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Xiaohua Su.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 22 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Chu, Y., Su, X., Huang, Q. et al. Patterns of DNA sequence variation at candidate gene loci in black poplar (Populus nigra L.) as revealed by single nucleotide polymorphisms. Genetica 137, 141–150 (2009). https://doi.org/10.1007/s10709-009-9371-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10709-009-9371-1

Keywords

Navigation