Mycorrhiza

, Volume 15, Issue 2, pp 87–91 | Cite as

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

  • D. Tagu
  • C. Bastien
  • P. Faivre-Rampant
  • J. Garbaye
  • P. Vion
  • M. Villar
  • F. Martin
Original Paper

Abstract

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.

Keywords

Mycorrhiza Poplar Quantitative trait loci Rust Symbiosis 

References

  1. 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 89:167–178Google Scholar
  2. 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 19:306–313Google Scholar
  3. 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 83:194–200Google Scholar
  4. 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 93:733–737Google Scholar
  5. 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 809PubMedGoogle Scholar
  6. Cornelius J (1994) Heritabilities and additive genetic coefficients of variation in forest trees. Can J For Res 24:372–379Google Scholar
  7. 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 100:1315–1324Google Scholar
  8. 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 93:421–427Google Scholar
  9. 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 48:239–251Google Scholar
  10. 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 31Google Scholar
  11. Falconer DS (1989) Introduction to quantitative genetics, 3rd edn. Wiley, New YorkGoogle Scholar
  12. 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 63:139–144Google Scholar
  13. Gianinazzi-Pearson V, Denarié J (1997) Red carpet genetic programmes for root endosymbioses. Trends Plant Sci 2:371–372CrossRefGoogle Scholar
  14. Grattapaglia G, Sederoff R (1994) Genetic-linkage maps of Eucalyptus grandis and Eucalyptus urophylla using pseudo-testcross—mapping strategy and RAPD markers. Genetics 137:1121–1137PubMedGoogle Scholar
  15. Kistner C, Parniske M (2002) Evolution of signal transduction in intracellular symbiosis. Trends Plant Sci 7:511–518CrossRefPubMedGoogle Scholar
  16. Kohler A, Delaruelle C, Martin D, Encelot N, Martin F (2003) The poplar root transcriptome: analysis of 7000 expressed sequence tags. FEBS Lett 542:37–41CrossRefPubMedGoogle Scholar
  17. Lander ES, Bostein D (1989) Mapping Mendelian factors underlying quantitative traits using RFLP linkage maps. Genetics 121:185–199PubMedGoogle Scholar
  18. 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 88:156–163Google Scholar
  19. Lincoln S, Daly M, Lander E (1992) Construction of genetic maps with MAPMAKER/EXP 3.0. Whitehead Institute technical report, 3rd ed. Whitehead InstituteGoogle Scholar
  20. Martin F (2001) Frontiers in molecular mycorrhizal research—genes, loci, dots and spins. New Phytol 150:499–507CrossRefGoogle Scholar
  21. 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 151:145–154CrossRefGoogle Scholar
  22. Nehls U, Mikolajewski S, Magel E, Hampp R (2001) Carbohydrate metabolism in ectomycorrhizas: gene expression, monosaccharide transport and metabolic control. New Phytol 150:533–541CrossRefGoogle Scholar
  23. Newcombe G (1998) Association of Mmd1, a major gene for resistance to Melampsora medusae f. sp. deltoidae, with quantitative traits in poplar rust. Phytopathology 88:114–121Google Scholar
  24. 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 26:1943–1950Google Scholar
  25. 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, WarsawGoogle Scholar
  26. 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 159:117–129CrossRefGoogle Scholar
  27. 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 79–88Google Scholar
  28. 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 244:117–128CrossRefGoogle Scholar
  29. Rosado SCS, Kropp BR, Piché Y (1994) Genetics of ectomycorrhizal symbiosis. I. Host plant variability and heritability of ectomycorrhizal and root traits. New Phytol 126:105–110Google Scholar
  30. 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 9:237–240CrossRefGoogle Scholar
  31. Smith SE, Read DJ (1997) Mycorrhizal symbiosis, 2nd edn. Academic Press, San Diego, Calif.Google Scholar
  32. 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 95:13330–1335PubMedGoogle Scholar
  33. 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 10:237–240Google Scholar
  34. Tagu D, Lapeyrie F, Martin F (2002) The ectomycorrhizal symbiosis: genetics and development. Plant Soil 244:97–105CrossRefGoogle Scholar
  35. 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 143:531–536Google Scholar
  36. 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 25:181–191CrossRefPubMedGoogle Scholar
  37. Wullschleger SD, Jansson S, Taylor G (2002) Genomics and forest biology: Populus emerges as the perennial favorite. Plant Cell 14:2651–2655CrossRefPubMedGoogle Scholar
  38. 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 91:1069–1073Google Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  • D. Tagu
    • 1
    • 3
  • C. Bastien
    • 2
  • P. Faivre-Rampant
    • 1
    • 4
  • J. Garbaye
    • 1
  • P. Vion
    • 1
  • M. Villar
    • 2
  • F. Martin
    • 1
  1. 1.UMR INRA-UHP 1136 IaM Interactions Arbres/Micro-OrganismesINRAChampenouxFrance
  2. 2.Unité Amélioration Génétique et Physiologie ForestièresINRAOlivetFrance
  3. 3.UMR BiO3PINRA-RennesLe Rheu France
  4. 4.Unité de Recherches en Génomique Végétale (URGV-INRA)ÉvryFrance

Personalised recommendations