Skip to main content

10 New Insights into Ectomycorrhizal Symbiosis Evolution and Function

  • Chapter
  • First Online:
Book cover Agricultural Applications

Part of the book series: The Mycota ((MYCOTA,volume 11))

Abstract

Boreal and temperate forest ecosystems rely on ectomycorrhizal (ECM) symbiosis for tree nutrition, productivity, and stress resilience. The ECM lifestyle appears several times during fungal evolution. In this chapter, we will consider how comparative genomics has changed and specified our understanding of the evolution of the ECM symbiosis lifestyle within the fungal kingdom and the rhizospheric zoo. During development of ECM symbiosis, only a few plant defense responses are triggered. In this chapter, we will consider which strategies (molecules, factors) ECM fungi developed in order to avoid plant immune system detection. We will in particular highlight the roles of cell wall remodeling enzymes and symbiosis effectors displaying similarities to those of plant pathogens. Understanding of the biology of ectomycorrhizal fungi is important to inform models of sustainable forest management and to improve the productivity of tree plantations in marginal soils. Thus, the chapter will conclude with eco-biotechnological applications of ECM symbiosis in forestry and bioremediation.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 229.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 299.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 299.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Aimanianda V, Bayry J, Bozza S, Kniemeyer O, Perruccio K et al (2009) Surface hydrophobin prevents immune recognition of airborne fungal spores. Nature 460:1117–1121

    PubMed  CAS  Google Scholar 

  • Balestrini R, Hahn MG, Bonfante P (1996) Location of cell-wall components in ectomycorrhizae of Corylus avellana and Tuber magnatum. Protoplasma 191:55–69

    Google Scholar 

  • Baxter L, Tripathy S, Ishaque N, Boot N, Cabral A, Kemen E, Thines M, Ah-Fong A, Anderson R, Badejoko W et al (2010) Signatures of adaptation to obligate biotrophy in the Hyaloperonospora arabidopsidis genome. Science 330:1549–1551

    PubMed  CAS  Google Scholar 

  • Beimforde C, Schaefer N, Doerfelt H, Nascimbene PC, Singh H, Heinrichs J, Reitner J, Rana RS, Schmidt AR (2011) Ectomycorrhizas from a Lower Eocene angiosperm forest. New Phytol 192:988–996

    PubMed  Google Scholar 

  • Bellion M, Courbot M, Jacob C, Blaudez D, Chalot M (2006) Extracellular and cellular mechanisms sustaining metal tolerance in ectomycorrhizal fungi. FEMS Microbiol Lett 254:173–181

    PubMed  CAS  Google Scholar 

  • Biswas B, Scott PT, Gresshoff PM (2011) Tree legumes as feedstock for sustainable biofuel production: opportunities and challenges. J Plant Physiol 168:1877–1884

    PubMed  CAS  Google Scholar 

  • Blaudez D, Jacob C, Turnau K, Colpaert JV, Ahonen-Jonnarth U, Finlay R, Botton B, Chalot M (2000) Differential responses of ectomycorrhizal fungi to heavy metals in vitro. Mycol Res 104:1366–1371

    CAS  Google Scholar 

  • Bonfante P, Balestrini R, Martino E, Perotto S, Plassard C, Mousain D (1998) Morphological analysis of early contacts between pine roots and two ectomycorrhizal Suillus strains. Mycorrhiza 8:1–10

    Google Scholar 

  • Brundrett MC (2002) Coevolution of roots and mycorrhizas of land plants. New Phytol 2002(154):275–304

    Google Scholar 

  • Buist G, Steen A, Kok J, Kuipers OP (2008) LysM, a widely distributed protein motif for binding to (peptido)glycans. Mol Microbiol 68:838–847

    PubMed  CAS  Google Scholar 

  • Camehl I, Sherameti I, Venus Y, Bethke G, Varma A, Lee J, Oelmuller R (2009) Ethylene signalling and ethylene-targeted transcription factors are required to balance beneficial and nonbeneficial traits in the symbiosis between the endophytic fungus Piriformospora indica and Arabidopsis thaliana. New Phytol 185:1062–1073

    Google Scholar 

  • Canut H, Carrasco A, Galaud JP, Cassan C, Bouyssou H, Vita N, Ferrara P, Pont-Lezica R (1998) High affinity RGD-binding sites at the plasma membrane of Arabidopsis thaliana links the cell wall. Plant J 16:63–71

    PubMed  CAS  Google Scholar 

  • Carrillo-González R, González-Chavez MCA (2012) Tolerance to and accumulation of cadmium by the mycelium of the fungi Scleroderma citrinum and Pisolithus tinctorius. Biol Trace Elem Res 146:388–395

    PubMed  Google Scholar 

  • Castellano MA (1994) Current status of outplanting studies using ectomycorrhiza-inoculated forest trees. In: Pfleger FL, Linderman RG (eds) Mycorrhizae and plant health. APS Press, St. Paul

    Google Scholar 

  • Chalot M, Plassard C (2011) Ectomycorrhiza and nitrogen provision to the host tree. In: Polacco JC, Todd CD (eds) Ecological aspects of nitrogen metabolism in plants, Wiley, Hoboken. doi:10.1002/ 9780470959404.ch4

  • Chalot M, Blaudez D, Brun A (2006) Ammonia: a candidate for nitrogen transfer at the mycorrhizal interface. Trends Plant Sci 11:263–266

    PubMed  CAS  Google Scholar 

  • Chen LQ, Hou BH, Lalonde S, Takanaga H, Hartung ML, Qu XQ, Guo WJ, Kim JG, Underwood W, Chaudhuri B et al (2010) Sugar transporters for intercellular exchange and nutrition of pathogens. Nature 468:527–532

    PubMed  CAS  Google Scholar 

  • Chevalier G (2010) The truffle of Europe (Tuber aestivum): geographic limits, ecology and possibility of cultivation. Osterreichische Zeitschrift fur Pilzkunde 19:249–259

    Google Scholar 

  • Chevalier G, Gregori G, Frochot H, Zambonelli A (2002) The cultivation of the Burgundy truffle. In: Proceedings of the second international conference on edible mycorrhizal fungi, Christchurch, pp 0–12

    Google Scholar 

  • Courty P-E, Franc A, Garbaye J (2010) Temporal and functional pattern of secreted enzyme activities in an ectomycorrhizal community. Soil Biol Biochem 42:2022–2025

    CAS  Google Scholar 

  • Cuomo CA, Guldener U, Xu JR, Trail F, Turgeon BG, Di Pietro A, Walton JD, Ma LJ, Baker SE, Rep M et al (2007) The Fusarium graminearum genome reveals a link between localized polymorphism and pathogen specialization. Science 317:1400–1402

    PubMed  CAS  Google Scholar 

  • Danell E (2002) Current research on chanterelle cultivation in Sweden. In: Proceedings of the second international conference on edible mycorrhizal fungi, Christchurch, pp 0–4

    Google Scholar 

  • Danell E (2005) The chanterelle: an edible ectomycorrhizal mushroom. In: Deshmukh SK, Rai MK (eds) Biodiversity of fungi: their role in human life. Science, Enfield, pp 329–339

    Google Scholar 

  • de Jonge R, van Esse HP, Kombrink A, Shinya T, Desaki Y, Bours R, van der Krol S, Shibuya N, Joosten MH, Thomma BP (2010) Conserved fungal LysM effector Ecp6 prevents chitin-triggered immunity in plants. Science 329:953–955

    PubMed  Google Scholar 

  • Dexheimer J, Pargney JC (1991) Comparative anatomy of the host-fungus interface in mycorrhizas. Experientia 47:312–321

    Google Scholar 

  • Doidy J, Grace E, Kuhn C, Simon-Plas F, Casieri L, Wipf D (2012) Sugar transporters in plants and in their interactions with fungi. Trends Plant Sci 17:413–422

    PubMed  CAS  Google Scholar 

  • Ducousso M, Bena G, Bourgeois C, Buyck B, Eyssartier G, Vincelette M, Rabevohitra R, Randrihasipara L, Dreyfus B, Prin Y (2004) The last common ancestor of Sarcolaenaceae and Asian dipterocarp trees was ectomycorrhizal before the India-Madagascar separation, about 88 million years ago. Mol Ecol 13:231–236

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Duplessis S, Courty PE, Tagu D, Martin F (2005) Transcript patterns associated with ectomycorrhiza development in Eucalyptus globulus and Pisolithus microcarpus. New Phytol 165:599–611

    PubMed  CAS  Google Scholar 

  • Duplessis S, Cuomo CA, Lin YC, Aerts A, Tisserant E, Veneault-Fourrey C, Joly DL, Hacquard S, Amselem J, Cantarel BL et al (2011) Obligate biotrophy features unraveled by the genomic analysis of rust fungi. Proc Natl Acad Sci USA 108:9166–9171

    PubMed  CAS  Google Scholar 

  • Eastwood DC, Floudas D, Binder M, Majcherczyk A, Schneider P, Aerts A, Asiegbu FO, Baker SE, Barry K, Bendiksby M et al (2011) The plant cell wall-decomposing machinery underlies the functional diversity of forest fungi. Science 333:762–765

    PubMed  CAS  Google Scholar 

  • Ellis C, Karafyllidis I, Wasternack C, Turner JG (2002) The Arabidopsis mutant cev1 links cell wall signaling to jasmonate and ethylene responses. Plant Cell 14:1557–1566

    PubMed  CAS  Google Scholar 

  • Fellbaum CR, Gachomo EW, Beesetty Y, Choudhari S, Strahan GD, Pfeffer PE, Kiers ET, Bucking H (2012) Carbon availability triggers fungal nitrogen uptake and transport in arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci USA 109:2666–2671

    PubMed  CAS  Google Scholar 

  • Felten J, Kohler A, Morin E, Bhalerao RP, Palme K, Martin F, Ditengou FA, Legue V (2009) The ectomycorrhizal fungus Laccaria bicolor stimulates lateral root formation in poplar and Arabidopsis through auxin transport and signaling. Plant Physiol 151:1991–2005

    PubMed  CAS  Google Scholar 

  • Finlay RD (2008) Ecological aspects of mycorrhizal symbiosis: with special emphasis on the functional diversity of interactions involving the extraradical mycelium. J Exp Bot 59:1115–1126

    PubMed  CAS  Google Scholar 

  • Floudas D, Binder M, Riley R, Barry K, Blanchette RA, Henrissat B, Martinez AT, Otillar R, Spatafora JW, Yadav JS et al (2012) The paleozoic origin of enzymatic lignin decomposition reconstructed from 31 fungal genomes. Science 336:1715–1719

    PubMed  CAS  Google Scholar 

  • Fomina MA, Alexander IJ, Colpaert JV, Gadd GM (2005) Solubilization of toxic metal minerals and metal tolerance of mycorrhizal fungi. Soil Biol Biochem 37:851–866

    CAS  Google Scholar 

  • Gadd GM (2007) Geomycology: biogeochemical transformations of rocks, minerals, metals and radionuclides by fungi, bioweathering and bioremediation. Mycol Res 111:3–49

    PubMed  CAS  Google Scholar 

  • Gao H, Gong Y-W, Yuan Y-J (2007) RGD-dependent mechanotransduction of suspension cultured Taxus cell in response to shear stress. Biotechnol Prog 23:673–679

    PubMed  CAS  Google Scholar 

  • Garbaye J (2000) The role of ectomycorrhizal symbiosis in the resistance of forest to water stress. Outlook Agric 29:63–69

    Google Scholar 

  • Genney DR, Alexander IJ, Killham K, Meharg AA (2004) Degradation of the polycyclic aromatic hydrocarbon (PAH) fluorene is retarded in a Scots pine ectomycorrhizosphere. New Phytol 163:641–649

    CAS  Google Scholar 

  • Giollant M, Guillot J, Damez M, Dusser M, Didier P, Didier E (1993) characterization of a lectin from Lactarius-deterrimus – research on the possible involvement of the fungal lectin in recognition between mushroom and spruce during the early stages of mycorrhizae formation. Plant Physiol 101:513–522

    PubMed  CAS  Google Scholar 

  • Grigoriev IV, Cullen D, Hibbett D, Goodwin SB, Jeffries TW, Kubiek CP, Kuske C, Magnuson J, Martin F, Spatafora JW, Tsang A, Baker S (2011) Fueling the future with fungal genomics. Mycology 2(3):192–209

    Google Scholar 

  • Gust AA, Willmann R, Desaki Y, Grabherr HM, Nurnberger T (2012) Plant LysM proteins: modules mediating symbiosis and immunity. Trends Plant Sci. doi:10.1016/j.tplants.2012.04.003

    PubMed  Google Scholar 

  • Hahn MG (1996) Microbial elicitors and their receptors in plants. Annu Rev Phytopathol 34:387–412

    PubMed  CAS  Google Scholar 

  • Harfouche A, Meilan R, Altman A (2011) Tree genetic engineering and applications to sustainable forestry and biomass production. Trends Biotechnol 29:9–17

    PubMed  CAS  Google Scholar 

  • Harms H, Schlosser D, Wick LY (2011) Untapped potential: exploiting fungi in bioremediation of hazardous chemicals. Nat Rev Microbiol 9:177–192

    PubMed  CAS  Google Scholar 

  • Hibbett DS, Matheny PB (2009) The relative ages of ectomycorrhizal mushrooms and their plant hosts estimated using Bayesian relaxed molecular clock analyses. BMC Biol 7:13

    PubMed  Google Scholar 

  • Hibbett DS, Gilbert LB, Donoghue MJ (2000) Evolutionary instability of ectomycorrhizal symbioses in basidiomycetes. Nature 407:506–508

    PubMed  CAS  Google Scholar 

  • Hollister JD, Smith LM, Guo YL, Ott F, Weigel D, Gaut BS (2011) Transposable elements and small RNAs contribute to gene expression divergence between Arabidopsis thaliana and Arabidopsis lyrata. Proc Natl Acad Sci USA 108:2322–2327

    PubMed  CAS  Google Scholar 

  • Jairus T, Mpumba R, Chinoya S, Tedersoo L (2011) Invasion potential and host shifts of Australian and African ectomycorrhizal fungi in mixed eucalypt plantations. New Phytol 192:179–187

    PubMed  Google Scholar 

  • Jambois A, Dauphin A, Kawano T, Ditengou F, Bouteau F, Legué et F, Lapeyrie F (2005) Competitive antagonism between IAA and indole alkaloid hypaphorine must contribute to regulate ontogenesis. Physiol Plant 123:120–129

    CAS  Google Scholar 

  • James TY, Kauff F, Schoch CL, Matheny PB, Hofstetter V, Cox CJ, Celio G, Gueidan C, Fraker E, Miadlikowska J et al (2006) Reconstructing the early evolution of Fungi using a six-gene phylogeny. Nature 443:818–822

    PubMed  CAS  Google Scholar 

  • Javot H, Penmetsa RV, Terzaghi N, Cook DR, Harrison MJ (2007) A Medicago truncatula phosphate transporter indispensable for the arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci USA 104:1720–1725

    PubMed  CAS  Google Scholar 

  • Javot H, Penmetsa RV, Breuillin F, Bhattarai KK, Noar RD, Gomez SK, Zhang Q, Cook DR, Harrison MJ (2011) Medicago truncatula mtpt4 mutants reveal a role for nitrogen in the regulation of arbuscule degeneration in arbuscular mycorrhizal symbiosis. Plant J 68:954–965

    PubMed  CAS  Google Scholar 

  • Jones MD, Smith SE (2004) Exploring functional definitions of mycorrhizas: are mycorrhizas always mutualisms? Can J Bot 82:1089–1109

    Google Scholar 

  • Keeling PJ, Palmer JD (2008) Horizontal gene transfer in eukaryotic evolution. Nat Rev Genet 9:605–618

    PubMed  CAS  Google Scholar 

  • Kemppainen M, Duplessis S, Martin F, Pardo AG (2009) RNA silencing in the model mycorrhizal fungus Laccaria bicolor: gene knock-down of nitrate reductase results in inhibition of symbiosis with Populus. Environ Microbiol 11:1878–1896

    PubMed  CAS  Google Scholar 

  • Kershaw MJ, Talbot NJ (1998) Hydrophobins and repellents: proteins with fundamental roles in fungal morphogenesis. Fungal Genet Biol 23:18–33

    PubMed  CAS  Google Scholar 

  • Kiers ET, Duhamel M, Beesetty Y, Mensah JA, Franken O, Verbruggen E, Fellbaum CR, Kowalchuk GA, Hart MM, Bago A et al (2011) Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science 333:880–882

    PubMed  CAS  Google Scholar 

  • Kloppholz S, Kuhn H, Requena N (2011) A secreted fungal effector of Glomus intraradices promotes symbiotic biotrophy. Curr Biol 21:1204–1209

    PubMed  CAS  Google Scholar 

  • Labbé J, Jorge V, Kohler A, Vion P, Marcais B, Bastien C et al (2011) Identification of quantitative trait loci affecting ectomycorrhizal symbiosis in an interspecific F1 poplar cross and differential expression of genes in ectomycorrhizas of the two parents: Populus deltoides and Populus trichocarpa. Tree Genet Genomes 7:617–627

    Google Scholar 

  • Larsen PE, Sreedasyam A, Trivedi G, Podila GK, Cseke LJ, Collart FR (2011) Using next generation transcriptome sequencing to predict an ectomycorrhizal metabolome. BMC Syst Biol 5:70

    PubMed  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Le Quéré A, Wright DP, Söderström B, Tunlid A, Johansson T (2005) Global patterns of gene regulation associated with the development of ectomycorrhiza between birch (Betula pendula Roth.) and Paxillus involutus (Batsch) Fr. Mol Plant Microbe Interact 18:659–673

    PubMed  Google Scholar 

  • Le Tacon F, Alvarez IF, Bouchard D, Henrion B, Jackson RM, Luff S, Parladé JI, Pera J, Stenström E, Villeneuve N, Walker C (1992) Variations in field response of forest trees to nursery ectomycorrhizal inoculation in Europe. In: Read DJ, Lewis DH, Fitter AH, Alexander IJ (eds) Mycorrhizas in ecosystems. CAB International, Oxford, pp 119–134

    Google Scholar 

  • Leake JR, Johnson D, Donnelly DP, Muckle G, Boddy L, Read D (2004) Networks of power and influence:the role of mycorrhizal mycelium in controlling plant communities and agroecosystem functioning. Can J Bot 82:1016–1045

    Google Scholar 

  • LePage BA, Currah RS, Stockey RA, Rothwell GW (1997) Fossil ectomycorrhizae from the middle Eocene. Am J Bot 84:410–412

    PubMed  CAS  Google Scholar 

  • Leyval C, Turnau K, Haselwandter K (1997) Effect of heavy metal pollution on mycorrhizal colonization and function: physiological, ecological and applied aspects. Mycorrhiza 7:139–153

    CAS  Google Scholar 

  • Lindow SE, Brandl MA (2003) Microbiology of the phyllosphere. Appl Environ Microbiol 69:1875–1883

    PubMed  CAS  Google Scholar 

  • Marshall R, Kombrink A, Motteram J, Loza-Reyes E, Lucas J, Hammond-Kosack KE, Thomma BP, Rudd JJ (2011) Analysis of two in planta expressed LysM effector homologs from the fungus Mycosphaerella graminicola reveals novel functional properties and varying contributions to virulence on wheat. Plant Physiol 156:756–769

    PubMed  CAS  Google Scholar 

  • Martin F, Nehls U (2009) Harnessing ectomycorrhizal genomics for ecological insights. Curr Opin Plant Biol 12:508–515

    PubMed  CAS  Google Scholar 

  • Martin F, Tunlid A (2009) The ectomycorrhizal symbiosis: a marriage of convenience. In: Deising HB (ed) The Mycota, vol 5. Springer, Berlin, pp 237–257

    Google Scholar 

  • Martin F, Kohler A, Duplessis S (2007) Living in harmony in the wood underground: ectomycorrhizal genomics. Curr Opin Plant Biol 10:204–210

    PubMed  CAS  Google Scholar 

  • Martin F, Aerts A, Ahrn D, Brun A, Danchin EGJ et al (2008) The genome sequence of the basidiomycete fungus Laccaria bicolor provides insights into the mycorrhizal symbiosis. Nature 452:88–92

    PubMed  CAS  Google Scholar 

  • Martin F, Kohler A, Murat C, Balestrini R, Coutinho PM, Jaillon O, Montanini B, Morin E, Noel B, Percudani R et al (2010) Perigord black truffle genome uncovers evolutionary origins and mechanisms of symbiosis. Nature 464:1033–1038

    PubMed  CAS  Google Scholar 

  • Martin F, Cullen D, Hibbett D, Pisabarro AG, Spatafora JW, Baker SE, Grigoriev I (2011) Sequencing the fungal tree of life. New Phytol 190(4):818–821

    PubMed  CAS  Google Scholar 

  • Martinez D, Challacombe J, Morgenstern I, Hibbett D, Schmoll M, Kubicek CP, Ferreira P, Ruiz-Duenas FJ, Martinez AT, Kersten P et al (2009) Genome, transcriptome, and secretome analysis of wood decay fungus Postia placenta supports unique mechanisms of lignocellulose conversion. Proc Natl Acad Sci USA 106:1954–1959

    PubMed  CAS  Google Scholar 

  • Meharg AA, Cairney JWG (2000) Ectomycorrhizas – extending the capabilities of rhizosphere remediation? Soil Biol Biochem 32:1475–1484

    CAS  Google Scholar 

  • Meharg AA, Dennis GR, Cairney JWG (1997) Biotransformation of 2,4,6-trinitrotoluene (TNT) by ectomycorrhizal basidiomycetes. Chemosphere 35:513–521

    CAS  Google Scholar 

  • Mellersh DG, Heath MC (2001) Plasma membrane-cell wall adhesion is required for expression of plant defense responses during fungal penetration. Plant Cell 13:413–424

    PubMed  CAS  Google Scholar 

  • Mentlak TA, Kombrink A, Shinya T, Ryder LS, Otomo I, Saitoh H, Terauchi R, Nishizawa Y, Shibuya N, Thomma BP et al (2012) Effector-mediated suppression of chitin-triggered immunity by magnaporthe oryzae is necessary for rice blast disease. Plant Cell 24:322–335

    PubMed  CAS  Google Scholar 

  • Monaghan J, Zipfel C (2012) Plant pattern recognition receptor complexes at the plasma membrane. Curr Opin Plant Biol. doi:dx.doi.org/10.1016/j.pbi.2012.05.006

  • Morel M, Jacob C, Kohler A, Johansson T, Martin F, Chalot M, Brun A (2005) Identification of genes differentially expressed in extraradical mycelium and ectomycorrhizal roots during Paxillus involutus-Betula pendula ectomycorrhizal symbiosis. Appl Environ Microbiol 71:382–391

    PubMed  CAS  Google Scholar 

  • Moyersoen B (2006) Pakaraimaea dipterocarpacea is ectomycorrhizal, indicating an ancient Gondwanaland origin for the ectomycorrhizal habit in Dipterocarpaceae. New Phytol 172:753–762

    PubMed  Google Scholar 

  • Murat C, Riccioni C, Belfiori B, Cichocki N, Labbe J, Morin E, Tisserant E, Paolocci F, Rubini A, Martin F (2010) Distribution and localization of microsatellites in the Perigord black truffle genome and identification of new molecular markers. Fungal Genet Biol 48(6):592–601

    PubMed  Google Scholar 

  • Nagendran S, Hallen-Adams HE, Paper JM, Aslam N, Walton JD (2009) Reduced genomic potential for secreted plant cell-wall-degrading enzymes in the ectomycorrhizal fungus Amanita bisporigera, based on the secretome of Trichoderma reesei. Fungal Genet Biol 46(5):427–435

    PubMed  CAS  Google Scholar 

  • Nehls U, Gohringer F, Wittulsky S, Dietz S (2010) Fungal carbohydrate support in the ectomycorrhizal symbiosis: a review. Plant Biol 12:292–301

    PubMed  CAS  Google Scholar 

  • Newton AC, Haigh JM (1998) Diversity of ectomycorrhizal fungi in Britain: a test of the species-area relationship, and the role of host specificity. New Phytol 138:619–627

    Google Scholar 

  • Niemi K, Scagel C, Haggman H (2004) Application of ectomycorrhizal fungi in vegetative propagation of conifers. Plant Cell Tissue Organ Cult 78:83–91

    Google Scholar 

  • Oliveira RS, Franco AR, Castro PML (2012a) Combined use of Pinus pinaster plus and inoculation with selected ectomycorrhizal fungi as an ecotechnology to improve plant performance. Ecol Eng 43:95–103

    Google Scholar 

  • Oliveira RS, Franco AR, Vosatka M, Castro PML (2012b) Management of nuresery pratices for efficient ectomycorrhizal fungi application in the production of Quercus ilex. Symbiosis 52:125–131

    Google Scholar 

  • Oliver RJ, Finch JW, Taylor G (2009) Second generation bioenergy crops and climate change: a review of the effects of elevated atmospheric CO2 and drought on water use and the implications for yield. Glob Change Biol Bioenergy 1:97–114

    CAS  Google Scholar 

  • Parrent JL, James TY, Vasaitis R, Taylor AF (2009) Friend or foe? Evolutionary history of glycoside hydrolase family 32 genes encoding for sucrolytic activity in fungi and its implications for plant-fungal symbioses. BMC Evol Biol 9:148

    PubMed  Google Scholar 

  • Pennanen T, Garbaye J, Piri T, Timonen S, Rajala T, Müller M et al (2010) Ectomycorrhizal fungi on Norway spruce- a seedling growth rate perspective. In: 9th international mycological congress, Edinburgh

    Google Scholar 

  • Peterson RL, Massicotte HB (2004) Exploring structural definitions of mycorrhizas, with emphasis on nutrient-exchange interfaces. Can J Bot (Revue Canadienne De Botanique) 82:1074–1088

    Google Scholar 

  • Pilz D, Norvell L, Danell E, Molina R (2003) Ecology and management of commercially harvested chanterelle mushrooms. General Technical Report – Pacific Northwest Research Station, USDA Forest Service

    Google Scholar 

  • Plett JM, Martin F (2011) Blurred boundaries: lifestyle lessons from ectomycorrhizal fungal genomes. Trends Genet 27:14–22

    PubMed  CAS  Google Scholar 

  • Plett JM, Kemppainen M, Kale SD, Kohler A, Legue V, Brun A, Tyler BM, Pardo AG, Martin F (2011) A secreted effector protein of Laccaria bicolor is required for symbiosis development. Curr Biol 21:1197–1203

    PubMed  CAS  Google Scholar 

  • Plett JM, Gibon J, Kohler A, Duffy K, Hoegger PJ, Velagapudi R, Han J, Kuees U, Grigoriev IV, Martin F (2012) Phylogenetic, genomic organization and expression analysis of hydrophobin genes in the ectomycorrhizal basidiomycete Laccaria bicolor. Fungal Genet Biol 49:199–209

    PubMed  CAS  Google Scholar 

  • Rabatin S (1980) The occurence of the vesicular-arbuscular mycorrhizal fungus Glomus tenuis with moss. Mycologia 72:191–195

    Google Scholar 

  • Raffaele S, Kamoun S (2012) Genome evolution in filamentous plant pathogens: why bigger can be better. NatRev Microbiol 10:417–430

    CAS  Google Scholar 

  • Rafiqi M, Ellis JG, Ludowici VA, Hardham AR, Dodds PN (2012) Challenges and progress towards understanding the role of effectors in plant-fungal interactions. Curr Opin Plant Biol 15(4):477–482

    PubMed  CAS  Google Scholar 

  • Read DJ, Duckett JG, Francis R, Ligrone R, Russell A (2000) Symbiotic fungal associations in ‘lower’ land plants. Philos Trans R Soc Lond B Biol Sci 355:815–830

    PubMed  CAS  Google Scholar 

  • Remy W, Taylor TN, Hass H, Kerp H (1994) Four hundred-million-year-old vesicular arbuscular mycorrhizae. Proc Natl Acad Sci USA 91:11841–11843

    PubMed  CAS  Google Scholar 

  • Rincon A, Parlade J, Pera J (2005) Effects of ectomycorrhizal inoculation and the type of substrate on mycorrhization, growth and nutrition of containerised Pinus pinea L. seedlings produced in a commercial nursery. Ann Forest Sci 62:817–822

    Google Scholar 

  • Rincon A, Parlade J, Pera J (2007) Influence of the fertilisation method in controlled ectomycorrhizal inoculation of two Mediterranean pines. Ann Forest Sci 64:577–583

    CAS  Google Scholar 

  • Rineau F, Courty P-E (2010) Secreted enzymatic activities of ectomycorrhizal fungi as a case study of functional diversity and functional redundancy. Ann Forest Sci 68:69–80

    Google Scholar 

  • Roby D, Gadelle A, Toppan A (1987) Chitin oligosaccharides as elicitors of chitinase activity in melon plants. Biochem Biophys Res Comm 143:885–892

    PubMed  CAS  Google Scholar 

  • Rouxel T, Grandaubert J, Hane JK, Hoede C, van de Wouw AP, Couloux A, Dominguez V, Anthouard V, Bally P, Bourras S et al (2011) Effector diversification within compartments of the Leptosphaeria maculans genome affected by Repeat-Induced Point mutations. Nat Commun 2:202

    PubMed  Google Scholar 

  • Salzer P, Hebe G, Reith A, ZitterellHaid B, Stransky H, Gaschler K, Hager A (1996) Rapid reactions of spruce cells to elicitors released from the ectomycorrhizal fungus Hebeloma crustuliniforme, and inactivation of these elicitors by extracellular spruce cell enzymes. Planta 198:118–126

    CAS  Google Scholar 

  • Salzer P, Hebe G, Hager A (1997a) Cleavage of chitinous elicitors from the ectomycorrhizal fungus Hebeloma crustuliniforme by host chitinases prevents induction of K + and Cl− release, extracellular alkalinization and H2O2 synthesis of Picea abies cells. Planta 203:470–479

    CAS  Google Scholar 

  • Salzer P, Hubner B, Sirrenberg A, Hager A (1997b) Differential effect of purified spruce chitinases and beta-1,3-glucanases on the activity of elicitors from ectomycorrhizal fungi. Plant Physiol 114:957–968

    PubMed  CAS  Google Scholar 

  • Salzer P, Wiemken A, Boller T (2001) Different roles of plant chitinases in mycorrhizae and pathogenic interactions. In: Muzzarelli RAA (ed) Chitin enzymology 2001. Atec Edizioni, Grottammare, pp 31–40

    Google Scholar 

  • Sarand I, Timonen S, Nurmiaho-Lassila EL, Koivula T, Haahtela K, Romantschuk M, Sen R (1998) Microbial biofilms and catabolic plasmid harbouring degradative fluorescent pseudomonads in Scots pine mycorrhizospheres developed on petroleum contaminated soil. FEMS Microbiol Ecol 27:115–126

    CAS  Google Scholar 

  • Schindler M, Meiners S, Cheresh DA (1989) rgd-dependent linkage between plant-cell wall and plasma-membrane – consequences for growth. J Cell Biol 108:1955–1965

    PubMed  CAS  Google Scholar 

  • Schwartz MW, Hoeksema JD, Gehring CA, Johnson NC, Klironomos JN, Abbott LK, Pringle A (2006) The promise and the potential consequences of the global transport of mycorrhizal fungal inoculum. Ecol Lett 9:501–515

    PubMed  Google Scholar 

  • Schwessinger B, Ronald PC (2012) Plant innate immunity: perception of conserved microbial signatures. Ann Rev Plant Biol 63:451–482. %U http://www.annualreviews.org/doi/abs/410.1146/annurev-arplant-042811-105518

    Google Scholar 

  • Seguin A (2011) How could forest trees play an important role as feedstock for bioenergy production? Curr Opin Environ Sustain 3:90–94

    Google Scholar 

  • Selosse MA, Bouchard D, Martin F, Le Tacon F (2000) Effect of Laccaria bicolor strains inoculated on Douglas-fir (Pseudotsuga menziesii) several years after nursery inoculation. Can J Forest Res (Revue Canadienne De Recherche Forestiere) 30:360–371

    Google Scholar 

  • Sharp JA, McNeil M, Albersheim P (1984a) The primary structure of one elicitor active and seven elicitor-inactive hexa [ß-D-glucopyranolsyl]-D-glucitols isolated from the mycelia walls of Phytophthora megasperma f.sp. glycinea. J Biol Chem 25:11321–11326

    Google Scholar 

  • Sharp JA, Valent B, Albersheim P (1984b) Purification and partial characterization of a ß-glucan fragment that elicits phytoalexin accumulation in soybean. J Biol Chem 25:11312–11320

    Google Scholar 

  • Simon L, Bousquet J, Levesque RC, Lalonde M (1993) Origin and diversification of endomycorrhizal fungi and coincidence with vascular land plants. Nature 363:67–69

    Google Scholar 

  • Sirrenberg A, Salzer P, Hager A (1995) Induction of mycorrhiza-like structures and defense reactions in dual cultures of spruce callus and ectomycorrhizal fungi. New Phytol 130:149–156

    Google Scholar 

  • Smith SE, Read JR (2008) Mycorrhizal symbiosis. Academic, San Diego

    Google Scholar 

  • Sousa NR, Franco AR, Ramos MA, Oliveira RS, Castro PML (2011) Reforestation of burned stands: the effect of ectomycorrhizal fungi on Pinus pinaster establishment. Soil Biol Biochem 43:2115–2120

    CAS  Google Scholar 

  • Sousa NR, Franco AR, Oliveira RS, Castro PML (2012a) Ectomycorrhizal fungi as an alternative to the use of chemical fertilisers in nursery production of Pinus pinaster. J Environ Manage 95:S269–S274

    PubMed  CAS  Google Scholar 

  • Sousa NR, Ramos MA, Marques APGC, Castro PML (2012b) The effect of ectomycorrhizal fungi forming symbiosis with Pinus pinaster seedlings exposed to cadmium. Sci Total Environ 414:63–67

    PubMed  CAS  Google Scholar 

  • Spanu P (1997) HCF-1, a hydrophobin from the tomato pathogen Cladosporium fulvum. Gene 193:89–96

    PubMed  CAS  Google Scholar 

  • Spanu P (2012) The genomics of Obligate (and nonobligate) biotrophs. Annu Rev Phytopathol 50:5.1–5.19

    Google Scholar 

  • Spanu PD, Abbott JC, Amselem J, Burgis TA, Soanes DM, Stuber K, Loren V, van Themaat E, Brown JK, Butcher SA, Gurr SJ et al (2010) Genome expansion and gene loss in powdery mildew fungi reveal tradeoffs in extreme parasitism. Science 330:1543–1546

    PubMed  CAS  Google Scholar 

  • Splivallo R, Fischer U, Gobel C, Feussner I, Karlovsky P (2009) Truffles regulate plant root morphogenesis via the production of auxin and ethylene. Plant Physiol 150:2018–2029

    PubMed  CAS  Google Scholar 

  • Tagu D, Martin F (1996) Molecular analysis of cell wall proteins expressed during the early steps of ectomycorrhiza development. New Phytol 133:73–85

    CAS  Google Scholar 

  • Tang JD, Perkins AD, Sonstegard TS, Schroeder SG, Burgess SC, Diehl SV (2012) Short-read sequencing for genomic analysis of the brown rot fungus Fibroporia radiculosa. Appl Environ Microbiol 78:2272–2281

    PubMed  CAS  Google Scholar 

  • Tedersoo L, May TW, Smith ME (2010) Ectomycorrhizal lifestyle in fungi: global diversity, distribution, and evolution of phylogenetic lineages. Mycorrhiza 20:217–263

    PubMed  Google Scholar 

  • Templeton MD, Rikkerink EHA, Beever RE (1994) Small, cysteine-rich proteins and recognition in fungal-plant interactions. Mol Plant-Microbe Inter 7:320–325

    CAS  Google Scholar 

  • Teste FP, Schmidt MG, Berch SM, Bulmer C, Egger KN (2004) Effects of ectomycorrhizal inoculants on survival and growth of interior Douglas-fir seedlings on reforestation sites and partially rehabilitated landings. Can J Forest Res (Revue Canadienne De Recherche Forestiere) 34:2074–2088

    Google Scholar 

  • Tibbett M (2000) Roots, foraging and the exploitation of soil nutrient patches: the role of mycorrhizal symbiosis. Funct Ecol 14:397–399

    Google Scholar 

  • Vega-Sanchez ME, Verhertbruggen Y, Christensen U, Chen X, Sharma V, Varanasi P, Jobling SA, Talbot M, White RG, Joo M et al (2012) Loss of Cellulose Synthase-Like F6 function affects mixed-linkage glucan deposition, cell wall mechanical properties, and defense responses in vegetative tissues of rice. Plant Physiol 159:56–69

    PubMed  CAS  Google Scholar 

  • Veneault-Fourrey C, Martin F (2011) Mutualistic interactions on a knife-edge between saprotrophy and pathogenesis. Curr Opin Plant Biol 14:444–450

    PubMed  Google Scholar 

  • Vinces MD, Legendre M, Caldara M, Hagihara M, Verstrepen KJ (2009) Unstable tandem repeats in promoters confer transcriptional evolvability. Science 324:1213–1216

    PubMed  CAS  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

    PubMed  CAS  Google Scholar 

  • Wang B, Yeun LH, Xue J-Y, Liu Y, Ane J-M, Qiu Y-L (2010) Presence of three mycorrhizal genes in the common ancestor of land plants suggests a key role of mycorrhizas in the colonization of land by plants. New Phytol 186:514–525

    PubMed  Google Scholar 

  • Weiss M, Selosse MA, Rexer KH, Urban A, Oberwinkler F (2004) Sebacinales: a hitherto overlooked cosm of heterobasidiomycetes with a broad mycorrhizal potential. Mycol Res 108:1003–1010

    PubMed  Google Scholar 

  • Wessels JGH (2000) Hydrophobins, unique fungal proteins. Mycologist 14:153–159

    Google Scholar 

  • Whiteford JR, Spanu PD (2002) Hydrophobins and the interactions between fungi and plants. Mol Plant Pathol 3:391–400

    PubMed  CAS  Google Scholar 

  • Whiteford JR, Lacroix H, Talbot NJ, Spanu PD (2004) Stage-specific cellular localisation of two hydrophobins during plant infection by the pathogenic fungus Cladosporium fulvum. Fungal Genet Biol 41:624–634

    PubMed  CAS  Google Scholar 

  • Wolfe BE, Tulloss RE, Pringle A (2012) The irreversible loss of a decomposition pathway marks the single origin of an ectomycorrhizal symbiosis. PLoS One 7(7):e39597

    PubMed  CAS  Google Scholar 

  • Wosten HAB (2001) Hydrophobins: multipurpose proteins. Annu Rev Microbiol 55:625–646

    PubMed  CAS  Google Scholar 

  • Zamioudis C, Pieterse CM (2012) Modulation of host immunity by beneficial microbes. Mol Plant Microbe Interact 25:139–150

    PubMed  CAS  Google Scholar 

  • Zuccaro A, Lahrmann U, Gueldener U, Langen G, Pfiffi S, Biedenkopf D, Wong P, Samans B, Grimm C, Basiewicz M et al (2011) Endophytic life strategies decoded by genome and transcriptome analyses of the mutualistic root symbiont Piriformospora indica. PLoS Pathog 7(10):e1002290

    PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We would like to thank all members of the “Ecogenomics of Interactions” team for their support and discussions. A special thanks to François Le Tacon and Jean Garbaye for the shared long experience on the use of ECM fungi in forestry. Experiments carried out in the laboratory are supported by grants from INRA, Université de Lorraine, ANR project TRANSMUT, DOE Oak Ridge National Laboratory through the “Plant-Microbes Interfaces” project, and the Laboratory of Excellence (LABEX) ARBRE.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Francis Martin .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2013 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Veneault-Fourrey, C., Martin, F. (2013). 10 New Insights into Ectomycorrhizal Symbiosis Evolution and Function. In: Kempken, F. (eds) Agricultural Applications. The Mycota, vol 11. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-36821-9_10

Download citation

Publish with us

Policies and ethics