Tree Genetics & Genomes

, Volume 4, Issue 1, pp 25–36 | Cite as

Genetic linkage maps of Populus nigra L. including AFLPs, SSRs, SNPs, and sex trait

  • M. Gaudet
  • V. Jorge
  • I. Paolucci
  • I. Beritognolo
  • G. Scarascia Mugnozza
  • M. Sabatti
Original Paper


Black poplar (Populus nigra L.) is a tree of ecological and economic interest. A better knowledge of P. nigra genome is needed for an effective protection and use of its genetic resources. The main objective of this study is the construction of a highly informative genetic map of P. nigra species including genes of adaptive and economic interest. Two genotypes originated from contrasted natural Italian populations were crossed to generate a F1 mapping pedigree of 165 individuals. Amplification fragment length polymorphism (AFLP), simple sequence repeat (SSR), and single nucleotide polymorphism (SNP) markers were used to genotype 92 F1 individuals, and the pseudo-test-cross strategy was applied for linkage analysis. The female parent map included 368 markers (274 AFLPs, 91 SSRs, and 3 SNPs) and spanned 2,104 cM with 20 linkage groups, and the male parent map, including 317 markers (205 AFLPs, 106 SSRs, 5 SNPs, and sex trait), spanned 2,453 cM with 23 main linkage groups. The sex, as morphological trait, was mapped on the linkage group XIX of the male parent map. The generated maps are among the most informative in SSRs when compared to the Populus maps published so far and allow a complete alignment with the 19 haploid chromosomes of Populus sequence genome. These genetic maps provide informative tools for a better understanding of P. nigra genome structure and genetic improvement of this ecologically and economically important European tree species.


Populus nigra Genetic map Sex trait 



The authors thank G. Zaina and M. Morgante for providing the sequence of the SNPs and A. G. Fara for the laboratory analysis of the SNP markers. This work was supported by grants from the European Project QLK5-CT-2002-00953 (POPYOMICS).

Supplementary material

11295_2007_85_MOESM1_ESM.doc (46 kb)
ESM S1 AFLP primer combination code with selective nucleotides at the 3’ end of the E (EcoRI) primer (2 nucleotides) and the M (MseI) primer (3 nucleotides) respectively. (DOC 47 Kb)
11295_2007_85_MOESM2_ESM.doc (62 kb)
ESM S2 Marker description of each linkage group of the female (♀) and male (♂)map. The number of total markers mapped (N i ), the number of each sort of markers (AFLP, SSR, SNP, sex trait (S)), framework markers, and distorted markers (p ≤ 0.05) are presented. The number (∑N.j ) of significant (α ≤ 0.05) clustered and dispersed markers with the proportion (L i %) of the corresponding region relative to the linkage group length (L i ) are also reported (see “Materials and methods” and Electronic Supplementary Materials S3 for details). (DOC 63 Kb)
11295_2007_85_MOESM3_ESM.doc (80 kb)
ESM S3 Significant clustered and dispersed region on each linkage group in the female and male map. (DOC 82 Kb)


  1. Alstrom-Rapaport C, Lascoux M, Wang YC, Roberts G, Tuskan GA (1998) Identification of a RAPD marker linked to sex determination in the basket willow (Salix viminalis L.). J Hered 89:44–49CrossRefGoogle Scholar
  2. Arens P, Coops H, Jansen J, Vosman B (1998) Molecular genetic analysis of black poplar (Populus nigra L.) along Dutch rivers. Mol Ecol 7:11–18CrossRefGoogle Scholar
  3. Bert PF, Charmet G, Sourdille P, Balfourier F, Hayward MD (1999) A high-density molecular map for ryegrass (Lolium perenne) using AFLP markers. Theor Appl Genet 99:445–452CrossRefGoogle Scholar
  4. Binelli G, Bucci G (1994) A genetic linkage map of Picea abies Karst, based on RAPD markers, as a tool in population genetics. Theor Appl Genet 88:283–288CrossRefGoogle Scholar
  5. Boutin-Ganache I, Raposo M, Raymond M, Deschepper CF (2001) M13-tailed primers improve the readability and usability of microsatellite analyses performed with two different allele-sizing methods. BioTechniques 31:24–28PubMedGoogle Scholar
  6. Bradshaw HD Jr, Ceulemans R, Davis J, Stettler R (2000) Emerging model systems in plant biology: poplar (Populus) as a model forest tree. J Plant Growth Regul 19:306–313CrossRefGoogle Scholar
  7. Brunner AM, Rottmann WH, Sheppard LA, Krutovskii K, DiFazio SP, Leonardi S, Strauss SH (2000) Structure and expression of duplicate AGAMOUS orthologues in poplar. Plant Mol Biol 44:619–634PubMedCrossRefGoogle Scholar
  8. Cervera MT, Storme V, Ivens B, Gusmao J, Liu BH, Hostyn V, Van Slycken J, Van Montagu M, Boerjan W (2001) Dense genetic linkage maps of three Populus species (Populus deltoides, P. nigra and P. trichocarpa) based on AFLP and microsatellite markers. Genetics 158:787–809PubMedGoogle Scholar
  9. Cervera MT, Sewell MM, Faivre-Rampant P, Storme V, Boerjan W (2004) Genome mapping in Populus. In: Kumar S and Fladung M (eds) Molecular genetics and breeding of forest trees. Food Product, New York, pp 387–410Google Scholar
  10. Chakravarti A, Lasher LK, Reefer JE (1991) A maximum likelihood method for estimating genome length using genetic linkage data. Genetics 128:175–182PubMedGoogle Scholar
  11. Charlesworth D (2002) Plant sex determination and sex chromosomes. Heredity 88:94–101PubMedCrossRefGoogle Scholar
  12. Chen THH, Howe GT, Bradshaw HD (2002) Molecular genetic analysis of dormancy-related traits in poplars. Weed Sci 50:232–240CrossRefGoogle Scholar
  13. Collard BCY, Pang ECK, Jahufer MZZ, Brouwer JB (2005) An introduction to markers, quantitative trait loci (QTL) mapping and marker-assisted selection for crop improvement: The basic concepts. Euphytica 142:169–196CrossRefGoogle Scholar
  14. Dayanandan S, Rajora OP, Bawa KS (1998) Isolation and characterization of microsatellites in trembling aspen (Populus tremuloides). Theor Appl Genet 96:950–956CrossRefGoogle Scholar
  15. De Vries SMG, Turok J (2001) Introduction. In: Lefevre F, Barsoum N, Heinze B, Kajba D, Rotach P, De Vries SMG, Turok J (eds) In situ conservation of Populus nigra. International Plant Genetic Resources Institute, Rome, pp 5–7Google Scholar
  16. Dorken ME, Barrett SCH (2004) Sex determination and the evolution of dioecy from monoecy in Sagittaria latifolia (Alismataceae). Proc R Soc Lond B 271:213–219CrossRefGoogle Scholar
  17. 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 7–32Google Scholar
  18. Frewen BE, Chen TH, Howe GT, Davis J, Rohde A, Boerjan W, Bradshaw HD Jr (2000) Quantitative trait loci and candidate gene mapping of bud set and bud flush in Populus. Genetics 154:837–845Google Scholar
  19. Fu H, Zheng Z, Dooner HK (2002) Recombination rates between adjacent genic and retrotransposon regions in maize vary by 2 orders of magnitude. Proc Natl Acad Sci U S A 99:1082–1087PubMedGoogle Scholar
  20. Grant MC, Mitton JB (1979) Elevational gradient in adult sex ratios and sexual differentiation in vegetative growth rates of Populus tremuloides Michx. Evolution 33:914–918CrossRefGoogle Scholar
  21. Grattapaglia D, Sederoff R (1994) Genetic linkage maps of Eucalyptus grandis and Eucalyptus urophylla using a pseudo-testcross: mapping strategy and RAPD markers. Genetics 137:1121–1137PubMedGoogle Scholar
  22. Hulbert SH, Ilott TW, Legg EJ, Lincoln SE, Lander ES, Michelmore RW (1988) Genetic analysis of the fungus, Bremia lactucae, using restriction fragment length polymorphisms. Genetics 120:947–958PubMedGoogle Scholar
  23. Imbert E, Lefèvre F (2003) Dispersal and gene flow of Populus nigra (Salicaceae) along a dynamic river system. J Ecol 91:447–456CrossRefGoogle Scholar
  24. Ingvarsson PK, Garcia MV, Hall D, Luquez V, Jansson S (2006) Clinal variation in phyB2, a candidate gene for day-lengh induced growth cessation and bud set, across a latitudinal gradient in European aspen (Populus tremula). Genetics 172:1845–1853PubMedCrossRefGoogle Scholar
  25. Jenczewski E, Bonnin I, Prosperi JM, Gherardi M, Huguet T, Olivieri I (1997) Insight on segregation distortions in two intraspecific crosses between annual species of Medicago (Leguminosae). Theor Appl Genet 94:682–691CrossRefGoogle Scholar
  26. Kuang H, Bongarten B, Richardson T, Carson S, Wilcox P (1999) Genetic analysis of inbreeding depression in plus tree 850.55 of Pinus radiata D. Don. I. Genetic map with distorted markers. Theor Appl Genet 98:697–703CrossRefGoogle Scholar
  27. Lander ES, Green P, Abrahamson J, Barlow A, Daly MJ, Lincoln SE, Newburg L (1987) MAPMAKER: An interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1:174–181PubMedCrossRefGoogle Scholar
  28. Lange K, Boehnke M (1982) How many polymorphic genes will it take to span the human genome? Am J Hum Genet 34:842–845PubMedGoogle Scholar
  29. Lashermes P, Combes MC, Prakash NS, Trouslot P, Lorieux M, Charrier A (2001) Genetic linkage map of Coffea canephora: Effect of segregation distortion and analysis of recombination rate in male and female meioses. Genome 44:589–596PubMedCrossRefGoogle Scholar
  30. Lebel-Hardenack S, Grant SR (1997) Genetics of sex determination in flowering plants. Trends Plant Sci 2:130–137CrossRefGoogle Scholar
  31. Lincoln SE, Lander ES (1992) Systematic detection of errors in genetic linkage data. Genomics 14:604–610PubMedCrossRefGoogle Scholar
  32. Marques CM, Whetten R, O’Malley DM, Liu BH, Sederoff R, Araújo JA, Ferreira JG (1998) AFLP genetic maps of Eucalyptus globulus and E. tereticornis. Theor Appl Genet 96:727–737CrossRefGoogle Scholar
  33. McLetchie DN, Tuskan GA, Dietrichson J (1994) Gender determination in Populus. J Agric Sci 18:57–66Google Scholar
  34. Meyers BC, Kozik A, Griego A, Kuang H, Michelmore RW (2003) Genome-wide analysis of NBS-LRR-encoding genes in Arabidopsis. Plant Cell 15:809–834CrossRefGoogle Scholar
  35. Mohan M, Nair S, Bhagwat A, Krishna TG, Bhatia CR, Yano M, Sasaki T (1997) Genome mapping, molecular markers and marker-assisted selection in crop plants. Mol Breed 3:87–103CrossRefGoogle Scholar
  36. Neff MM, Neff JD, Chory J, Pepper AE (1998) dCAPS, a simple technique for the genetic analysis of single nucleotide polymorphisms: experimental applications in Arabidopsis thaliana genetics. Plant J 14:387–392PubMedCrossRefGoogle Scholar
  37. Neff MM, Turk E, Kalishman M (2002) Web-based primer design for single nucleotide polymorphism analysis. Trends Genet 18:613–615PubMedCrossRefGoogle Scholar
  38. Oetting WS, Lee HK, Flanders DJ, Wiesner GL, Sellers TA, King RA (1995) Linkage analysis with multiplexed short tandem repeat polymorphisms using infrared fluorescence and M13 tailed primers. Genomics 30:450–458PubMedCrossRefGoogle Scholar
  39. Rahman MH, Dayanandan S, Rajora OP (2000) Microsatellite DNA markers in Populus tremuloides. Genome 43:293–297PubMedCrossRefGoogle Scholar
  40. Remington DL, Whetten RW, Liu BH, O’Malley DM (1999) Construction of an AFLP genetic map with nearly complete genome coverage in Pinus taeda. Theor Appl Genet 98:1279–1292PubMedCrossRefGoogle Scholar
  41. Ritter E, Gebhardt C, Salamini F (1990) Estimation of recombination frequencies and construction of RFLP linkage maps in plants from crosses between heterozygous parents. Genetics 125:645–654PubMedGoogle Scholar
  42. Semerikov V, Alström-Rapaport C, Lascoux M, Lagercrantz U, Tsarouhas V, Rönnberg W (2003) Genetic mapping of sex-linked markers in Salix viminalis L. Heredity 91:293–299PubMedCrossRefGoogle Scholar
  43. Smulders MJM, van der Schoot J, Arens P, Vosman B (2001) Trinucleotide repeat microsatellite markers for black poplar (Populus nigra L.). Mol Ecol Notes 1:188–190CrossRefGoogle Scholar
  44. Sterck L, Rombauts S, Jansson S, Sterky F, Rouze P, Van de Peer Y (2005) EST data suggest that poplar is an ancient polyploid. New Phytol 167:165–170PubMedCrossRefGoogle Scholar
  45. Storme V, Vanden Broeck A, Ivens B, Halfmaerten D, Van Slycken J, Castiglione S, Grassi F, Fossati T, Cottrell JE, Tabbener HE, Lefevre F, Saintagne C, Fluch S, Krystufek V, Burg K, Bordacs S, Borovics A, Gebhardt K, Vornam B, Pohl A, Alba N, Agundez D, Maestro C, Notivol E, Bovenschen J, Van Dam BC, Van Der SJ, Vosman B, Boerjan W, Smulders MJ (2003) Ex-situ conservation of Black poplar in Europe: genetic diversity in nine gene bank collections and their value for nature development. Theor Appl Genet 108:969–981PubMedCrossRefGoogle Scholar
  46. Tanksley SD, Ganal MW, Prince JP, De Vicente MC, Bonierbale MW, Broun P, Fulton TM, Giovannoni JJ, Grandillo S, Martin GB, Messeguer R, Miller JC, Miller L, Paterson AH, Pineda O, Roder MS, Wing RA, Wu W, Young ND (1992) High density molecular linkage maps of the tomato and potato genomes. Genetics 132:1141–1160PubMedGoogle Scholar
  47. Taylor G (2002) Populus: Arabidopsis for forestry. Do we need a model tree? Ann Bot 90:681–689PubMedCrossRefGoogle Scholar
  48. Testolin R, Huang WG, Lain O, Messina R, Vecchione A, Cipriani G (2001) A kiwifruit (Actinidia spp.) linkage map based on microsatellites and integrated with AFLP markers. Theor Appl Genet 103:30–36CrossRefGoogle Scholar
  49. Tschaplinski TJ, Tuskan GA, Gunderson CA (1994) Water-stress tolerance of black and eastern cottonwood clones and four hybrid progeny. I. Growth, water relations, and gas exchange. Can J For Res 24:364–371CrossRefGoogle Scholar
  50. Tuskan GA, Gunter LE, Yang ZK, Yin T, Sewell MM, DiFazio SP (2004) Characterization of microsatellites revealed by genomic sequencing of Populus trichocarpa. Can J For Res 34:85–93CrossRefGoogle Scholar
  51. Tuskan GA, DiFazio S, Jansson S, Bohlmann J, Grigoriev I, Hellsten U, Putnam M, 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, jardin 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, rvi J, Karlsson J, Kelleher C, Kirkpatrick R, Kirst M, Kohler A, Kalluri U, Larimer F, Leebens-Mack J, Leple? J-C, 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, Rouze? 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 313:1596–1604PubMedCrossRefGoogle Scholar
  52. van der Schoot J, Pospiskova M, Vosman B, Smulders MJM (2000) Development and characterization of microsatelite markers in black poplar (Populus nigra L.). Theor Appl Genet 101:317–322CrossRefGoogle Scholar
  53. Vanden Broeck A (2003) EURFORGEN Technical Guidelines for genetic conservation and use for European black poplar (Populus nigra L.). International Plant Genetic Resources Institute, Rome, pp 1–6Google Scholar
  54. Vanden Broeck A, Villar M, Van Bockstaele E, Van Slycken J (2005) Natural hybridization between cultivated poplars and their wild relatives: Evidence and consequences for native poplar populations. Ann For Sci 62:601–613CrossRefGoogle Scholar
  55. Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78PubMedCrossRefGoogle Scholar
  56. Winfield MO, Arnold GM, Cooper F, Le Ray M, White J, Karp A, Edwards KJ (1998) A study of genetic diversity in Populus nigra subsp. Populus nigra betulifolia in the Upper Severn area of the UK using AFLP markers. Mol Ecol 7:3–10CrossRefGoogle Scholar
  57. Wullschleger SD, Jansson S, Taylor G (2002) Genomics and forest biology: Populus emerges as the perennial favorite. Plant Cell 14:2651–2655PubMedCrossRefGoogle Scholar
  58. Yin TM, DiFazio SP, Gunter LE, Riemenschneider D, Tuskan GA (2004) Large-scale heterospecific segregation distortion in Populus revealed by a dense genetic map. Theor Appl Genet 109:451–463PubMedCrossRefGoogle Scholar
  59. Yin TM, DiFazio SP, Tuskan GA, Gunter LE, Zhang XY, Sewell MM (2006) A high-density consensus map established for comparative mapping and genome assembly in Populus by SSR markers. Proceeding of “The IV International poplar symposium”, Nanjing, China, 5–9 June, p 7Google Scholar
  60. Young ND (2000) The genetic architecture of resistance. Curr Opin Plant Biol 3:285–290PubMedCrossRefGoogle Scholar
  61. Zhang D, Zhang Z, Yang K, Li B (2004) Genetic mapping in (Populus tomentosa × Populus bolleana) and P. tomentosa Carr. using AFLP markers. Theor Appl Genet 108:657–662PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • M. Gaudet
    • 1
  • V. Jorge
    • 2
  • I. Paolucci
    • 1
  • I. Beritognolo
    • 1
  • G. Scarascia Mugnozza
    • 1
  • M. Sabatti
    • 1
  1. 1.Dip. di Scienze dell’Ambiente Forestale e delle sue Risorse (DISAFRI)Università della TusciaViterboItaly
  2. 2.Unité Amélioration Génétique et Physiologie ForestièresINRA Centre d’OrléansOlivet cedexFrance

Personalised recommendations