Skip to main content
SpringerLink
Log in

The ectomycorrhizal symbiosis: genetics and development

  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Ectomycorrhiza represents a symbiotic structure made between tree roots and filamentous hyphae. This new organ results from a favourable interaction between plant and microbes, taking place in the soil at the vicinity of the root. Diversity is extremely important in the rhizosphere, with large numbers of bacterial, fungal, nematode and invertebrate species. Therefore, partners of the mycorrhiza have to recognize each other and they do it by using diffusible rhizospheric molecules. This recognition leads to cellular interactions between root and fungal cells, driven by changes in gene and protein expression. The aim of this review is to describe the cellular, genetic and molecular events leading to the formation of the ectomycorrhizal tissues with an emphasis on gene expression and cell-to-cell communication.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Barker S J and Tagu D 2000 The roles of auxins and cytokinins in mycorrhizal symbioses. J. Plant Growth Regul. 19, 144-154.

    Google Scholar 

  • Béguiristain T, Côté R, Rubini, P, Jay-Allemand C and Lapeyrie F 1995 Hypaphorine accumulation in hyphae of the ectomycorrhizal fungus, Pisolithus tinctorius. Phytochemistry 40, 1089-1091.

    Google Scholar 

  • Bilewicz R, Witomski J, Van der Heyden A, Tagu D, Palin B and Rogalska E 2001 Modification of electrodes with self-assembled hydrophobin layers. J. Phys. Chem. B 105, 9772-9777.

    Google Scholar 

  • Bonfante P 2001 At the interface between mycorrhizal fungi and plants: The structural organization of cell wall, plasma membrane and cytoskeleton. In The Mycota IX Fungal Associations. Ed. B Hock. pp 45-61. Springer Verlag, Berlin, Germany.

    Google Scholar 

  • Boulianne R P, Liu Y, Aebi M, Lu B C and Kües U 2000 Fruiting body development in Coprinus cinereus: Regulated expression of two galectins secreted by a non-classical pathway. Microbiology 146, 1841-1853.

    Google Scholar 

  • Broughton W J, Jabbouri S and Perret X 2000 Keys to symbiotic harmony. J. Bacteriol. 182, 5641-5652.

    Google Scholar 

  • Cairney J W G 1992 Translocation of solutes in ectomycorrhizal and saprotrophic rhizomorphs. Mycol. Res. 96, 135-141.

    Google Scholar 

  • Carnero Diaz E, Martin F and Tagu D 1996 Eucalypt ?-tubulin: cDNA cloning and increased level of transcripts in ectomycorrhizal root system. Plant Mol. Biol. 31, 905-910.

    Google Scholar 

  • Cole L, Orlovich D A and Ashford AE 1998 Structure, function, and motility of vacuoles in filamentous fungi. Fungal Genet. Biol. 24, 86-100.

    Google Scholar 

  • Corrêa A, Staples R C and Hoch H C 1996 Inhibition of thigmostimulated cell differentiation with RGD-peptides in Uromyces germlings. Protoplasma 194, 91-102.

    Google Scholar 

  • Debaud J C, Gay G, Prevost A, Lei J and Dexheimer J 1988 Ectomycorrhizal ability of genetically different homokaryotic and dikaryotic mycelia of Hebeloma cylindrosporum. New Phytol. 108, 323-328.

    Google Scholar 

  • Ditengou F A and Lapeyrie F 2000 Hypaphorine from the ectomycorrhizal fungus Pisolithus tinctorius counteracts activities of indole-3-acetic acid and ethylene but not synthetic auxins in eucalypt seedlings. Mol. Plant-Microbe Interact. 13, 151-158.

    Google Scholar 

  • Ditengou F A, Béguiristain T and Lapeyrie F 2000 Root hair elongation is inhibited by hypaphorine, the indole alkaloid from the ectomycorrhizal fungus Pisolithus tinctorius, and restored by IAA. Planta 211, 722-728.

    Google Scholar 

  • Doudrick R L, Raffle V L, Nelson C D and Furnier G R 1995 Genetic analysis of homokaryons from a basidiome of Laccaria bicolor using random amplified polymorphic DNA (RAPD) markers. Mycol. Res. 99, 1361-1366.

    Google Scholar 

  • Duplessis S, Sorin C, Voiblet C, Palin B, Martin F and Tagu D 2001a Cloning and expression analysis of a new hydrophobin cDNA from the ectomycorrhizal basidiomycete Pisolithus. Curr. Genet. 39, 335-339.

    Google Scholar 

  • Duplessis S, Tagu D and Martin F 2001b Living together underground: A molecular glimpse of the ectomycorrhizal symbiosis. In Molecular Biology of Fungal Development: Mycological Series. Ed. H Osiewacz. Dekker &; Dekker, New York, USA. In press.

    Google Scholar 

  • Gay G, Normand L, Marmeisse R, Sotta B and Debaud J C 1994 Auxin overproducer mutants of Hebeloma cylindrosporum Romagnési have increased mycorrhizal activity. New Phytol. 128, 645-657.

    Google Scholar 

  • Gorfer M, Tarkka M T, Hanif M, Pardo A G, Laitiainen E and Raudaskoski M 2001 Characterization of small GTPases Cdc42 and Rac and the relationship between Cdc42 and actin cytoskeleton in vegetative and ectomycorrhizal hyphae of Suillus bovinus. Mol. Plant-Microbe Interact. 14, 135-144.

    Google Scholar 

  • Hebe G, Hager A and Salzer P 1999 Initial signalling processes induced by elicitors of ectomycorrhiza-forming fungi in spruce cells can also be triggered by G-protein-activating mastoparan and protein phosphatase-inhibiting cantharidin. Planta 207, 418-425.

    Google Scholar 

  • Hibbett D S, Gilbert L B and Donoghue M J 2000 Evolutionary instability of ectomycorrhizal symbioses in basidiomycetes. Nature 407, 506-508.

    Google Scholar 

  • Hilbert J L, Costa G and Martin F 1991 Ectomycorrhizin synthesis and polypeptide changes during the early stage of eucalypt mycorrhiza development. Plant Physiol. 97, 977-984.

    Google Scholar 

  • Hynes R O 1992 Integrins: Versatility, modulation, and signaling in cell adhesion. Cell 69, 11-25.

    Google Scholar 

  • International Human Genome Sequencing Consortium 2001 Initial sequencing and analysis of the human genome. Nature 409, 860-921.

    Google Scholar 

  • Karabaghli-Degron C, Sotta B, Bonnet M, Gay G and Le Tacon F 1998 The auxin transport inhibitor 2,3,5-triiodobenzoic acid (TIBA) inhibits the stimulation of in vitro lateral root formation and the colonization of the tap-root cortex of Norway spruce (Picea abies) seedlings by the ectomycorrhizal fungus Laccaria bicolor. New Phytol. 140, 723-733.

    Google Scholar 

  • Kaska D D, Myllylä R and Cooper J B 1999 Auxin transport inhibitors act through ethylene to regulate dichotomous branching of lateral root meristems in pine. New Phytol. 142, 49-58.

    Google Scholar 

  • Kawano T, Kawano N and Lapeyrie F 2001 Fungal auxin antagonist hypaphorine competitively inhibits indole-3-acetic aciddependent superoxide generation by horseradish peroxidase. Biochem. Biophys. Res. Com. 288, 546-551.

    Google Scholar 

  • Kershaw K J and Talbot N J 1998 Hydrophobins and repellents: Proteins with fundamental roles in fungal morphogenesis. Fungal Genet. Biol. 23, 18-33.

    Google Scholar 

  • Kiba A, Sugimoto M, Toyoda K, Ichinose Y, Yamada T and Shiraishi T 1998 Interaction between cell wall and plasma membrane via RGD motif is implicated in plant defense responses. Plant Cell Physiol. 39, 1245-1249.

    Google Scholar 

  • Kim S J, Bernreuther D, Thumm M and Podila G K 1999 LBAUT7, a novel symbiosis-regulated gene from an ectomycorrhizal fungus, Laccaria bicolor, is functionally related to vesicular transport and autophagocytosis. J. Bacteriol. 181, 1963-1967.

    Google Scholar 

  • Kottke I, Pargney J C, Qian X M and Le Disquet I 1995 Passage and deposition of solutes in the hyphal sheath of ectomycorrhizas-The soil-root interface. In EUROSILVA-Contribution to Forest Tree Physiology. Eds. H Sandermann and M Bonnet-Masimbert. pp 255-271. INRA Editions, Paris, France.

    Google Scholar 

  • Kropp B R and Anderson A J 1994 Molecular and genetic approaches to understanding variability in mycorrhizal formation and functioning. In Mycorrhizae and Plant Health. Eds. F L Pfleger and R G Linderman. pp 309-336. APS Press, St. Paul, Minnesota, USA.

    Google Scholar 

  • Lagrange H and Lapeyrie F 2001 Zeatin, a cytokinin from Eucalyptus seedling root exudates, controls hyphal branching and hypaphorine accumulation by the ectomycorrhizal fungus Pisolitus sp. Submitted.

  • Lagrange H, Jay-Allemand C and Lapeyrie F 2001 Rutin, the phenolglycoside from eucalyptus root exudates, stimulates Pisolithus hyphal growth at picomolar concentrations. New Phytol. 149, 349-355.

    Google Scholar 

  • Lamhamedi MS, Fortin A J, Kope H H and Kropp B R 1990 Genetic variation in ectomycorrhiza formation by Pisolithus arhizus on Pinus pinaster and Pinus banksiana. New Phytol. 115, 689-697.

    Google Scholar 

  • Laurent P, Voiblet C, Tagu D, de Carvalho D, Nehls U, De Bellis R, Balestrini R, Bauw G, Bonfante P and Martin F 1999 A novel class of ectomycorrhiza-regulated cell wall polypeptides in Pisolithus tinctorius. Mol. Plant-Microbe Interact. 12, 862-871.

    Google Scholar 

  • Lei J, Lapeyrie F, Malajczuk N and Dexheimer J 1990 Infectivity of pine and eucalypt isolates of Pisolithus tinctorius (Pers.) Coker &; Couch on roots of Eucalyptus urophylla S. T. Blake in vitro. II. Ultrastructural and biochemical changes at the early stage of mycorrhiza formation. New Phytol. 116, 115-122.

    Google Scholar 

  • Martin F, Laurent P, de Carvalho D, Voiblet C, Balestrini R, Bonfante P and Tagu D 1999 Cell wall proteins of the ectomycorrhizal basidiomycete Pisolithus tinctorius: Identification, function, and expression in symbiosis. Fungal Genet. Biol. 27, 161-174.

    Google Scholar 

  • Mellersh D G and Heath M C 2001 Plasma membrane-cell wall adhesion is required for expression of plant defense responses during fungal penetration. Plant Cell 13, 413-124.

    Google Scholar 

  • Mitchell T K and Dean R A 1995 The cAMP-dependent protein kinase catalytic subunit is required for appressorium formation and pathogenesis by the rice blast pathogen Magnaporthe grisea. Plant Cell 7, 1869-1878.

    Google Scholar 

  • Nehls U, Béguiristain T, Ditengou F, Lapeyrie F and Martin F 1998 The expression of a symbiosis-regulated gene in eucalypt roots is regulated by auxins and hypaphorine, the tryptophan betaine of the ectomycorrhizal basidiomycete Pisolithus tinctorius. Planta 207, 296-302.

    Google Scholar 

  • Niini S S, Tarkka T and Raudaskoski M 1996 Tubulin and actin protein patterns in Scots pine (Pinus sylvestris) roots and developing ectomycorrhiza with Suillus bovinus. Physiol. Plant. 96, 186-192.

    Google Scholar 

  • Paiva N L 2000 An introduction to the biosynthesis of chemicals used in plant-microbe communication. J. Plant Growth Regul. 19, 131-143.

    Google Scholar 

  • Pandey A and Mann M 2000 Proteomics to study genes and genomes. Nature 405, 837-846.

    Google Scholar 

  • Paris F, Dexheimer J and Lapeyrie F 1993 Cytochemical evidence of a fungal cell wall alteration during infection of Eucalyptus roots by the ectomycorrhizal fungus Cenococcum geophilum. Arch. Microbiol. 159, 526-529.

    Google Scholar 

  • Pérez-García A, Snoeijers S S, Joosten M H A J, Goosen T and de Wit P J G M 2001 Expression of the avirulence gene Avr9 of the fungal tomato pathogen Cladosporium fulvum is regulated by the global nitrogen response factor NRF1. Mol. Plant-Microbe Interact. 14 316-325.

    Google Scholar 

  • Raamsdonk L M, Teusink B, Broadhurst D, Zhang N, Hayes A, Walsh M C, Berden J A, Brindle K M, Kell D B, Rowland J J, Westerhoff H V, Van Dam K and Oliver S G 2001 A functional genomics strategy that uses metabolome data to reveal the phenotype of silent mutations. Nature Biotech. 19, 45-50.

    Google Scholar 

  • Regenfelder E, Spellig T, Hartmann A, Lauenstein S, Bolker M and Kahmann R 1997 G proteins in Ustilago maydis: Transmission of multiple signals? EMBO J. 16, 1934-1942.

    Google Scholar 

  • Salzer P and Boller T 2000 Elicitor induced reactions in mycorrhizae and their suppression. In Current Advances in Mycorrhizae Research. Eds. G K Podila and D D Douds Jr. pp 1-10.APS Press, St Paul, Minesota, USA.

    Google Scholar 

  • Simoneau P, Viemont J D, Moreau J C and Strullu D G 1993 Symbiosis-related polypeptides associated with the early stages of ectomycorrhiza organogenesis in birch (Betula pendula Roth). New Phytol. 124, 495-504.

    Google Scholar 

  • Smith S E and Read D J 1997 Mycorrhizal Symbiosis, 2nd edn. Academic Press, San Diego, California.

    Google Scholar 

  • Sundaram S, Kim S J, Suzuki H, Mcquattie C J, Hiremath S T and Podila G K 2001 Isolation and characterization of a symbiosisregulated ras from the ectomycorrhizal fungus Laccaria bicolor. Mol. Plant-Microbe Interact. 14, 618-628.

    Google Scholar 

  • Tagu D and Martin F 1996 Molecular analysis of cell wall proteins expressed during the early steps of ectomycorrhizal development. New Phytol. 133, 73-85.

    Google Scholar 

  • Tagu D, De Bellis R, Balestrini R, de Vries O M H, Piccoli G, Stocchi V, Bonfante P and Martin F 2001a Immunolocalization of hydrophobin HYDPt-1 from the ectomycorrhizal basidiomycete Pisolithus tinctorius during colonization of Eucalyptus globulus roots. New Phytol. 149, 127-135.

    Google Scholar 

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

    Google Scholar 

  • Tagu D, Nasse B and Martin F 1996 Cloning and characterization of hydrophobin-encoding cDNAs from the ectomycorrhizal basidiomycete Pisolithus tinctorius. Gene 168, 93-97.

    Google Scholar 

  • Tagu D, Python M, Crétin C and Martin F 1993 Cloning symbiosisrelated cDNAs from eucalypt ectomycorrhiza by PCR-assisted differential screening. New Phytol. 125, 339-343.

    Google Scholar 

  • Tarkka M, Niini S S and Raudaskoski M 1998 Developmentally regulated proteins during differentiation of root system and ectomycorrhiza in Scots pine (Pinus sylvestris) with Suillus bovinus. Physiol. Plant. 104, 449-455.

    Google Scholar 

  • Tarkka M T, Vasara R, Gorfer M and Raudaskoski M 2000 Molecular characterization of actin genes from homobasidiomycetes: two different actin genes from Schizophyllum commune and Suillus bovinus. Gene 251, 27-35.

    Google Scholar 

  • Tranvan H, Habricot Y, Jeannette E, Gay G and Sotta B 2000 Dynamics of symbiotic establishment between an IAAoverproducing mutant of the ectomycorrhizal fungus Hebeloma cylindrosporum and Pinus pinaster. Tree Physiol. 20, 123-129.

    Google Scholar 

  • Velculescu V E, Madden S L, Zhang L, Lash A E, Yu J, Rago C, Lal A, Wang C J, Beaudry G A, Ciriello K M, Cook B P, Dufault M R, Ferguson A T, Gao Y H, He T C, Hermeking H, Hiraldo S K, Hwang P M, Lopez M A, Luderer H F, Mathews B, Petroziello J M, Polyak K, Zawel L, Zhang W, Zhang X M, Zhou W, Haluska F G, Jen J, Sukumar S, Landes G M, Riggins G J, Vogelstein B and Kinzler KW 1999 Analysis of human transcriptomes. Nature Genet. 23, 387-388.

    Google Scholar 

  • Vesk P A, Ashford A E, Markovina A L and Allaway W G 2000 Apoplasmic barriers and their significance in the exodermis and sheath of Eucalyptus pilularis-Pisolithus tinctorius ectomycorrhizas. New Phytol. 145, 333-346.

    Google Scholar 

  • Voiblet C, Duplessis S, Encelot N and Martin F 2001 Identification of symbiosis-regulated genes in Eucalyptus globulus-Pisolithus tinctorius ectomycorrhiza by differential hybridization of arrayed cDNAs. Plant J. 25, 181-192.

    Google Scholar 

  • Wessels J G H 1997 Hydrophobins: Proteins that change the nature of the fungal surface. Adv. Microbial Physiol. 38, 1-45.

    Google Scholar 

  • Wösten H A B, van Wetter M A, Lugones L G, van der Mei H C, Busscher H J and Wessels J G H 1999 How a fungus escapes the water to grow into air. Curr. Biol. 9, 85-88.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. INRA, UMR INRA/UHP 1136 ``Interactions Arbres/Micro-Organismes'', 54280, Champenoux, France

    Denis Tagu, Frédéric Lapeyrie & Francis Martin

Authors
  1. Denis Tagu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Frédéric Lapeyrie
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Francis Martin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Denis Tagu.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Tagu, D., Lapeyrie, F. & Martin, F. The ectomycorrhizal symbiosis: genetics and development. Plant and Soil 244, 97–105 (2002). https://doi.org/10.1023/A:1020235916345

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1020235916345

Search

Navigation