Skip to main content
Log in

Genetic analysis of phenotypic variation for ectomycorrhiza formation in an interspecific F1 poplar full-sib family

  • Original Paper
  • Published:
Mycorrhiza Aims and scope Submit manuscript


A plant’s capability to develop ectomycorrhizal symbiosis is under the control of both genetic and environmental factors. In order to determine the roles played by these different factors, we have performed a quantitative genetic analysis of the ability of poplar trees to form ectomycorrhizas. Quantitative genetics were applied to an interspecific family of poplar for which the two parental genetic maps had already been described, and for which data analyses concerning fungal aggressors were obtained. Quantitative trait loci (QTL) related to ectomycorrhiza formation were identified and located in the genetic maps of the two parents. One QTL was located at a linkage group of the genetic map of Populus trichocarpa showing a high concentration of several QTL involved in the pathogenic interaction with the fungus Melampsora larici-populina, the causal agent of leaf rust.

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

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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


  • Bradshaw HD Jr, Villar M, Watson BD, Otto KG, Stewart S, Stettler RF (1994) Molecular genetics of growth and development in Populus. III. A genetic linkage map of a hybrid poplar composed of RFLP, STS, and RAPD markers. Theor Appl Genet 89:167–178

    CAS  Google Scholar 

  • Bradshaw HD Jr, Ceulemans R, Davis J, Settler RF (2000) Emerging model systems in plant biology: poplar ( Populus) as a model forest tree. J Plant Growth Regul 19:306–313

    CAS  Google Scholar 

  • Carlson JE, Tulsieram LK, Glaubitz JC, Luk VWK, Kauffeld C, Rutledge R (1991) Segregation of random amplified DNA markers in F1 progeny of conifers. Theor Appl Genet 83:194–200

    Google Scholar 

  • Cervera MT, Gusmão J, Steenackers M, Peleman J, Storme V, Vanden Broeck A, Van Montagu M, Boerjan W (1996) Identification of AFLP molecular markers for resistance against Melamspora larici-populina in Populus. Theor Appl Gen 93:733–737

    CAS  Google Scholar 

  • Cervera MT, Storme V, Ivens B, Gusmão 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 158:787 809

    CAS  PubMed  Google Scholar 

  • Cornelius J (1994) Heritabilities and additive genetic coefficients of variation in forest trees. Can J For Res 24:372–379

    Google Scholar 

  • Di Battista C, Selosse MA, Bouchard D, Stenström E, Le Tacon F (1996) Variations in symbiotic efficiency, phenotypic characters and ploidy level among different isolates of the ectomycorrhizal basidiomycete Laccaria bicolor S 238. Mycol Res 100:1315–1324

    Google Scholar 

  • Dowkiw A, Husson C, Frey P, Pinon J, Bastien C (2003) Partial resistance to Melampsora larici-populina leaf rust in hybrid poplars: genetic variability in inoculated excised leaf-disk bioassay and relationship with complete resistance. Phytopathology 93:421–427

    Google Scholar 

  • Duponnois R, Garbaye J (1991) Mycorrhization helper bacteria associated with the Douglas fir- Laccaria laccata symbiosis: effects in aseptic and in glasshouse conditions. Ann Sci For 48:239–251

    Google Scholar 

  • Faivre-Rampant P, Bastien C, Augustin S, Breton V, Delplanque A, Mourier MC, Kertadikara A, Laurans F, Lefèvre F, Lesage MC, Menard M, Pinon J, Saintagne C, Valadon A, Villar M, Prat D (1999) Locating genomic regions involved in pest resistance in poplars. Proceedings of the International Poplar Symposium II, IUFRO, Orléans, France. IUFRO, Orléans, p 31

  • Falconer DS (1989) Introduction to quantitative genetics, 3rd edn. Wiley, New York

  • Frey-Klett P, Pierrat JC, Garbaye J (1997) Location and survival of mycorrhiza helper Pseudomonas fluorescens during establishment of ectomycorrhizal symbiosis between Laccaria bicolor and Douglas fir. Appl Environ Microbiol 63:139–144

    Google Scholar 

  • Gianinazzi-Pearson V, Denarié J (1997) Red carpet genetic programmes for root endosymbioses. Trends Plant Sci 2:371–372

    Article  Google Scholar 

  • Grattapaglia G, Sederoff R (1994) Genetic-linkage maps of Eucalyptus grandis and Eucalyptus urophylla using pseudo-testcross—mapping strategy and RAPD markers. Genetics 137:1121–1137

    CAS  PubMed  Google Scholar 

  • Kistner C, Parniske M (2002) Evolution of signal transduction in intracellular symbiosis. Trends Plant Sci 7:511–518

    Article  CAS  PubMed  Google Scholar 

  • Kohler A, Delaruelle C, Martin D, Encelot N, Martin F (2003) The poplar root transcriptome: analysis of 7000 expressed sequence tags. FEBS Lett 542:37–41

    Article  PubMed  Google Scholar 

  • Lander ES, Bostein D (1989) Mapping Mendelian factors underlying quantitative traits using RFLP linkage maps. Genetics 121:185–199

    CAS  PubMed  Google Scholar 

  • Lefèvre F, Goué-Mourier MC, Faivre-Rampant P, Villar M (1998) A single gene cluster controls incompatibility and partial resistance to various Melampsora larici-populina races in hybrid poplars. Phytopathology 88:156–163

    Google Scholar 

  • Lincoln S, Daly M, Lander E (1992) Construction of genetic maps with MAPMAKER/EXP 3.0. Whitehead Institute technical report, 3rd ed. Whitehead Institute

  • Martin F (2001) Frontiers in molecular mycorrhizal research—genes, loci, dots and spins. New Phytol 150:499–507

    Article  Google Scholar 

  • Martin F, Duplessis S, Ditengou F, Lagrange H, Voiblet C, Lapeyrie F (2003) Developmental cross talking in the ectomycorrhizal symbiosis: signals and communication genes. New Phytol 151:145–154

    Article  Google Scholar 

  • Nehls U, Mikolajewski S, Magel E, Hampp R (2001) Carbohydrate metabolism in ectomycorrhizas: gene expression, monosaccharide transport and metabolic control. New Phytol 150:533–541

    Article  CAS  Google Scholar 

  • Newcombe G (1998) Association of Mmd1, a major gene for resistance to Melampsora medusae f. sp. deltoidae, with quantitative traits in poplar rust. Phytopathology 88:114–121

    CAS  Google Scholar 

  • Newcombe G, Bradshaw HD Jr (1996) Quantitative trait loci conferring resistance in hybrid poplar to Septoria populicola, the cause of leaf spot. Can J For Res 26:1943–1950

    Google Scholar 

  • Pachlewski R, Pachlewska J (1974) Studies on symbiotic properties of mycorrhizal fungi of pine ( Pinus sylvestris L.) with the aid of the method of mycorrhizal synthesis in pure cultures on agar. PhD thesis. Forest Research Institute of Warsaw, Warsaw

  • Peter M, Courty PE, Kohler A, Delaruelle C, Martin D, Tagu D, Frey-Klett P, Duplessis S, Chalot M, Podila G, Martin F (2003) Analysis of expressed sequence tags from the ectomycorrhizal basidiomycetes Laccaria bicolor and Pisolithus microcarpus. New Phytol 159:117–129

    Article  CAS  Google Scholar 

  • Peterson L, Bonfante P (1994) Comparative structure of vesicular-arbuscular mycorrhizas and ectomycorrhizas. In: Robson AD, Abbott LK, Malajczuk N (eds) Management of mycorrhizas in agriculture, horticulture and forestry. Kluwer, Dordrecht, pp 79–88

  • Podila GK, Zheng J, Balasubramanian S, Sundaram S, Hiremath S, Brand J, Hymes M (2002) Fungal gene expression in early symbiotic interactions between Laccaria bicolor and red pine. Plant Soil 244:117–128

    Article  CAS  Google Scholar 

  • Rosado SCS, Kropp BR, Piché Y (1994) Genetics of ectomycorrhizal symbiosis. I. Host plant variability and heritability of ectomycorrhizal and root traits. New Phytol 126:105–110

    Google Scholar 

  • Ruiz-Lozano JM, Gianinazzi S, Gianinazzi-Pearson V (1999) Genes involved in resistance to powdery mildew in barley differentially modulate root colonization by the mycorrhizal fungus Glomus mossae. Mycorrhiza 9:237–240

    Article  CAS  Google Scholar 

  • Smith SE, Read DJ (1997) Mycorrhizal symbiosis, 2nd edn. Academic Press, San Diego, Calif.

  • Sterky F, Regan S, Karlsson J, Hertzberg M, Rohde A, Holmberg A, Amini B, Bhalerao R, Larsson M, Villaroel R, Van Montagu M, Sandberg G, Olsson o, Teeri TT, Boerjan W, Gustafsson P, Uhlen M, Sundberg B, Lundeberg J (1998) Gene discovery on the wood-forming tissues of poplar: analysis of 5,692 expressed sequence tags. Proc Natl Acad Sci USA 95:13330–1335

    CAS  PubMed  Google Scholar 

  • Tagu D, Faivre-Rampant P, Lapeyrie F, Frey-Klettt P, Vion P, Villar M (2001) Variation in the ability to form ectomycorrhizas in the F1 progeny of an interspecific poplar ( Populus spp.) cross. Mycorrhiza 10:237–240

    CAS  Google Scholar 

  • Tagu D, Lapeyrie F, Martin F (2002) The ectomycorrhizal symbiosis: genetics and development. Plant Soil 244:97–105

    Article  CAS  Google Scholar 

  • Villar M, Lefèvre F, Bradshaw HD, Teissier du Cros E (1996) Molecular genetics of rust resistance in poplars ( Melampsora larici-populina Kleb./ Populus sp.) by bulked-segregant analysis in a 2 by 2 factorial mating design. Genetics 143:531–536

    Google Scholar 

  • Voiblet C, Duplessis S, Encelot N, Martin F (2001) Identification of symbiosis-regulated genes in Eucalyptus globulus-Pisolithus tinctorius ectomycorrhiza by differential hybridization of arrayed cDNAs. Plant J 25:181–191

    Article  CAS  PubMed  Google Scholar 

  • Wullschleger SD, Jansson S, Taylor G (2002) Genomics and forest biology: Populus emerges as the perennial favorite. Plant Cell 14:2651–2655

    Article  CAS  PubMed  Google Scholar 

  • Zhang J, Steenackers M, Storme V, Neyrinck S, Van Montagu M, Gerats T, Boerjan W (2001) Fine mapping and identification of nucleotide binding site/leucine-rich repeat sequences at the MER locus in Populus deltoides S9–2. Phytopathology 91:1069–1073

    CAS  Google Scholar 

Download references


This work could not have been completed without the technical assistance of the Unité d’Amélioration des Arbres Forestiers (INRA-Nancy): P. Legroux, B. Bertin, F. Bonne, M. Didiot, R. Herbeck and A. Nassau. B. Palin and D. Vairelles, J. L. Churin and P. Frettinger are greatly acknowledged. Drs P. Frey, J. Pinon (INRA Nancy, Pathologie Forestière), and Drs P. Frey-Klett, F. Lapeyrie and F. Le-Tacon (INRA-Nancy, UMR IaM) are thanked for encouraging discussions.

Author information

Authors and Affiliations


Corresponding author

Correspondence to D. Tagu.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Tagu, D., Bastien, C., Faivre-Rampant, P. et al. Genetic analysis of phenotypic variation for ectomycorrhiza formation in an interspecific F1 poplar full-sib family. Mycorrhiza 15, 87–91 (2005).

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: