Skip to main content

6 De-Constructing a Mutualist: How the Molecular Blueprints of Model Symbiotic Fungi Are Changing Our Understanding of Mutualism

Part of the The Mycota book series (MYCOTA,volume 9)

Abstract

A fascinating example of a class of organisms able to control and restructure their environment are the mutualistic ectomycorrhizal (ECM) fungi. These fungi are present in the soils of most forest environments, where they colonize tree roots to exchange nutrients that supports both tree and fungal growth. Very few plant defenses are raised against the invading hyphae of ECM fungi, likely due to the manipulation of conserved signaling protein ‘hubs’ within the host root. In this chapter, we will consider the role of both plant and ECM fungal signals involved in the structuring of their environment during the colonization of plant tissues. We will use as a basis of comparison the role of secreted proteins in pathogenic interactions in performing similar tasks. The chapter will conclude with an overview of the different signaling hubs that ECM fungi must overcome or control to establish a nutrient exchange between both partners—an exchange critical to the sustainability of our forest ecosystems.

Keywords

  • Mycorrhizal Fungus
  • Root Exudate
  • Fungal Hypha
  • Host Root
  • Host Colonization

These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

This is a preview of subscription content, access via your institution.

Buying options

Chapter
USD   29.95
Price excludes VAT (USA)
  • DOI: 10.1007/978-3-642-30826-0_6
  • Chapter length: 25 pages
  • Instant PDF download
  • Readable on all devices
  • Own it forever
  • Exclusive offer for individuals only
  • Tax calculation will be finalised during checkout
eBook
USD   189.00
Price excludes VAT (USA)
  • ISBN: 978-3-642-30826-0
  • Instant PDF download
  • Readable on all devices
  • Own it forever
  • Exclusive offer for individuals only
  • Tax calculation will be finalised during checkout
Softcover Book
USD   249.99
Price excludes VAT (USA)
Hardcover Book
USD   249.99
Price excludes VAT (USA)
Fig. 6.1.
Fig. 6.2.
Fig. 6.3.

References

  • Abdel-Fattah GM, Mohamedin AH (2000) Interactions between a vesicular–arbuscular mycorrhizal fungus (Glomus intraradices) and Streptomyces coelicolor and their effects on sorghum plants grown in soil amended with chitin of brawn scales. Biol Fertil Soils 32:401–409

    Google Scholar 

  • Adams F, Reddell P, Webb MJ, Shipton WA (2006) Arbuscular mycorrhizas and ectomycorrhias on Eucalyptus grandis (Myrtaceae) trees and seedlings in native forests of tropical north-eastern Australia. Aust J Bot 54:271–281

    Google Scholar 

  • Adomas A, Heler G, Olson A, Osborne J, Karlsson M, Nahalkova J, Van Zyl L, Sederoff R, Stenlid J, Finlay R, Asiegbu FO (2008) Comparative analysis of transcript abundance in Pinus sylvestris after challenge with a saprotrophic, pathogenic or mutualistic fungus. Tree Physiol 28:885–897

    PubMed  CAS  Google Scholar 

  • Aimanianda V, Bayry J, Bozza S, Kniemeyer O, Perruccio K, Elluru SR, Clavaud C, Paris S, Brakhage AA, Kaveri SV, Romani L, Latge J-P (2009) Surface hydrophobin prevents immune recognition of airborne fungal spores. Nature 460:1117–1121

    PubMed  CAS  Google Scholar 

  • Akiyama K, Hayashi H (2008) Plastid-derived strigolactones show the way to roots for symbionts and parasites. New Phytol 178:695–698

    PubMed  CAS  Google Scholar 

  • Akiyama K, Matsuzaki K, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435:824–827

    PubMed  CAS  Google Scholar 

  • Albrecht C, Asselin A, Piché Y, Lapeyrie F (1994) Chitinase activities are induced in Eucalyptus globulus roots by ectomycorrhizal or pathogenic fungi, during early colonization. Physiol Plant 91:104–110

    CAS  Google Scholar 

  • Artursson V, Finlay RD, Jansson JK (2006) Interactions between arbuscular mycorrhizal fungi and bacteria and their potential for stimulating plant growth. Environ Microbiol 8:1–10

    PubMed  CAS  Google Scholar 

  • Bendel CM, Hostetter MK (1993) Distinct mechanisms of epithelial adhesion for Candida albicans and Candida tropicalis. J Clin Invest 92:1840–1849

    PubMed  CAS  Google Scholar 

  • Besserer A, Puech-Pages V, Kiefer P, Gomez-Roldan V, Jauneau A, Roy S, Portais JC, Roux C, Becard G, Sejalon-Delmas N (2006) Strigoactones stimulate arbuscular mycorrhizal fungi by activating mitochondria. PLoS Biol 4:e226

    PubMed  Google Scholar 

  • Besserer A, Becard G, Jauneau A, Roux C, Sejalon-Delmas N (2008) GR24, a synthetic analog of strigolactones, stimulates the mitosis and growth of the arbuscular mycorrhizal fungus Gigaspora rosea by boosting its energy metabolism. Plant Physiol 148:402–413

    PubMed  CAS  Google Scholar 

  • Beyrle H (1995) The role of phytohormones in the function and biology of mycorrhizas. In: Varma AK, Hock B (eds) Mycorrhiza: structure, molecular biology and function. Springer, Berlin, p 365

    Google Scholar 

  • Bomberg M, Timonen S (2007) Distribution of Cren- and Euryarchaeota in Scots pine mycorrhizospheres and boreal forest humus. Microb Ecol 54:406–416

    PubMed  CAS  Google Scholar 

  • Bonfante P, Genre A (2010) Mechanisms underlying beneficial plant-fungus interactions in mycorrhizal symbiosis. Nat Commun 1:48

    PubMed  Google Scholar 

  • Bouwmeester HJ, Matusova R, Zhongkui S, Beale MH (2003) Secondary metabolite signalling in host-parasitic plant interactions. Curr Opin Plant Biol 6:358–364

    PubMed  CAS  Google Scholar 

  • Bowden CG, Smalley E, Guries RP, Hubbes M, Temple B, Horgen PA (1996) Lack of association between cerato-ulmin production and virulence in Ophiostoma novo-ulmi. Mol Plant Microbe Interact 9:556–564

    PubMed  CAS  Google Scholar 

  • Brachmann A, Parniske M (2006) The most widespread symbiosis on Earth. PLoS Biol 4:1111–1112

    CAS  Google Scholar 

  • Brady NC (1990) The nature and properties of soils, 10th edn. Macmillan, New York

    Google Scholar 

  • Brandes B, Godbold DL, Kuhn AJ, Jentschke G (1998) Nitrogen and phosphorus acquisition by the mycelium of the ectomycorrhizal fungus Paxillus involutus and its effect on host nutrition. New Phytol 140:735–743

    CAS  Google Scholar 

  • Brasier CM, Kirk SA, Tegli S (1995) Naturally occurring noncerato-ulmin producing mutants of Ophiostoma novo-ulmi are pathogenic but lack aerial mycelium. Mycol Res 99:436–440

    Google Scholar 

  • Brulé C, Frey-Klett P, Pierrat JC, Courier S, Gerard F, Lemoine MC, Rousselet JL, Sommer G, Garbaye J (2001) Survival in the soil of the ectomycorrhizal fungus Laccaria bicolor and the effect of a mycorrhiza helper Pseudomonas fluorescens. Soil Biol Biochem 33:1683–1694

    Google Scholar 

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

    Google Scholar 

  • Buée M, Vairelles D, Garbaye J (2005) Year-round monitoring of diversity and potential metabolic activity of the ectomycorrhizal community in a beech (Fagus silvatica) forest subjected to two thinning regimes. Mycorrhiza 15:235–245

    PubMed  Google Scholar 

  • Buée M, De Boer W, Martin F, van Overbeek L, Jurkevitch E (2009) The rhizosphere zoo: an overview of plant-associated communities of microorganisms, including phages, bacteria, archaea and fungi, and of some of their structuring factors. Plant Soil 321:189–212

    Google Scholar 

  • Burgess T, Laurent P, Dell B, Malajczuk N, Martin F (1995) Effect of the fungal isolate aggressivity on the biosynthesis of symbiosisrelated polypeptides in differentiating eucalypt ectomycorrhiza. Planta 195:408–417

    CAS  Google Scholar 

  • Camehl I, Sherameti I, Venus Y, Bethke G, Varma A, Lee J, Oelmuller R (2010) 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

    PubMed  CAS  Google Scholar 

  • Calera JA, Calderone RA (1999) Identification of a putative response regulator, two-component phosphorelay gene (CaSSK1) from Candida albicans. Yeast 15:1243–1254

    PubMed  CAS  Google Scholar 

  • Calera JA, Zhao XJ, Calderone R (2000) Defective hyphal development and avirulence caused by a deletion of the SSK1 response regulator gene in Candida albicans. Infect Immun 68:518–525

    PubMed  CAS  Google Scholar 

  • Catford JG, Staehelin C, Lerat S, Piché Y, Vierheilig H (2003) Suppression of arbuscular mycorrhizal colonization and nodulation in split-root systems of alfalfa after pre-inoculation and treatment with Nod factors. J Exp Bot 54:1481–1487

    PubMed  CAS  Google Scholar 

  • Catford JG, Staehelin C, Larose G, Piché Y, Vierheilig H (2006) Systemically suppressed isoflavonoids and their stimulating effects on nodulation and mycorrhization in alfalfa split-root systems. Plant Soil 285:257–266

    CAS  Google Scholar 

  • Chapin FS III, Moilanen L, Kielland K (1993) Preferential use of organic nitrogen by non-mychorrhizal Arctic sedge. Nature 361:150–153

    CAS  Google Scholar 

  • Chauhan N, Inglis D, Roman E, Pla J, Li D, Calera JA, Calderone R (2003) Candida albicans response regulator gene SSK1 regulates a subset of genes whose functions are associated with cell wall biosynthesis and adaptation to oxidative stress. Eukaryot Cell 2:1018–1024

    PubMed  CAS  Google Scholar 

  • Chaucheyras-Durand F, Fonty G (2001) Establishment of cellulolytic bacteria and development of fermentative activities in the rumen of gnotobiotically-reared lambs receiving the microbial additive Saccharomyces cerevisiae CNCM I–1077. Reprod Nutr Dev 41:57–68

    PubMed  CAS  Google Scholar 

  • Chen Z, Agnew JL, Cohen JD, He P, Shan L, Sheen J, Kunkel BN (2007) Pseudomonas syringae type III effector AvrRpt2 alters Arabidopsis thaliana auxin physiology. Proc Natl Acad Sci USA 104:20131–20136

    PubMed  CAS  Google Scholar 

  • Cole DW (1981) Nitrogen uptake and translocation by forest ecosystems. Ecol Bull 33:219–232

    CAS  Google Scholar 

  • Correa A, Staples RC, Hoch HC (1996) Inhibition of thigmostimulated cell differentiation with RDG-peptides in Uromyces germlings. Protoplasma 194:91–102

    CAS  Google Scholar 

  • Corvis Y, Walcarius A, Rink R, Mrabet NT, Rogalska E (2005) Preparing catalytic surfaces for sensing applications by immobilizing enzymes via hydrophobin layers. Anal Chem 77:1622–1630

    PubMed  CAS  Google Scholar 

  • Corvis Y, Brezesinski G, Rink R, Walcarius A, Van der Heyden A, Mutelet F, Rogalska E (2006) Analytical investigation of the interactions between SC3 hydrophobin and lipid layers: elaborating of nanostructured matrixes for immobilizing redox systems. Anal Chem 78:4850–4864

    PubMed  CAS  Google Scholar 

  • Corvis Y, Trzcinska K, Rink R, Bilkova P, Gorecka E, Bilewicz R, Rogalska E (2007) Electron donor-acceptor fullerene derivative retained on electrodes using SC3 hydrophobin. J Phys Chem C 111:1176–1179

    CAS  Google Scholar 

  • Courty P-E, Pouysegur R, Buee M, Garbaye J (2006) Laccase and phosphatase activities of the dominant ectomycorrhizal types in a lowland oak forest. Soil Biol Biochem 38:1219–1222

    CAS  Google Scholar 

  • Courty P-E, Breda N, Garbaye J (2007) Relation between oak tree phenology and the secretion of organic matter degrading enzymes by Lactarius quietus ectomycorrhizas before and during bud break. Soil Biol Biochem 39:1655–1663

    CAS  Google Scholar 

  • da Silva CI, de Queiroz MV, Costa MD, Kasuva MCM, de Araujo EF (2010) Identification of differentially expressed genes of the fungus Hydnangium sp. during the pre-symbiotic phase of the ectomycorrhizal association with Eucalyptus grandis. Mycorrhiza 20:531–540

    Google Scholar 

  • De Boer W, Folman LB, Summerbell RC, Boddy L (2005) Living in a fungal world: impact of fungi on soil bacterial niche development. FEMS Microbiol Rev 29:795–811

    PubMed  Google Scholar 

  • De Carvalho D (1994) Contribution à l’étude des protéines régulées par la symbiose ectomycorhizienne. PhD thesis, Ecole Nationale de Génie Rurale et Forestier, Nancy

    Google Scholar 

  • Deveau A, Palin B, Delaruelle C, Peter M, Kohler A, Pierrat JC, Sarniguet A, Garbaye J, Martin F, Frey-Klett P (2007) The mycorrhiza helper Pseudomonas fluorescens BBc6R8 has a specific priming effect on the growth, morphology and gene expression of the ectomycorrhizal fungus Laccaria bicolor S238N. New Phytol 175:743–755

    PubMed  CAS  Google Scholar 

  • Ditengou FA, 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

    PubMed  CAS  Google Scholar 

  • Ditengou FA, Béguiristain T, 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

    PubMed  CAS  Google Scholar 

  • Dou D, Kale SD, Wang X, Jiang RHY, Bruce NA, Arredondo FD, Zhang X, Tyler BM (2008) RXLR-mediated entry of phytophthora sojae effector Avr1b into soybean cells does not require pathogen-encoded machinery. Plant Cell 20:1930–1947

    PubMed  CAS  Google Scholar 

  • Duplessis S, Sorin C, Voiblet C, 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 

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

    PubMed  CAS  Google Scholar 

  • Fassler JS, West AH (2011) Fungal Skn7 stress responses and their relationship to virulence. Eukaryot Cell 10:156–167

    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 

  • Fray RG (2002) Altering plant–microbe interaction through artificially manipulating bacterial quorum sensing. Ann Bot 89:245–253

    PubMed  CAS  Google Scholar 

  • Freeling M (2009) Bias in plant gene content following different sorts of duplication: tandem, whole-genome, segmental, or by transposition. Annu Rev Plant Biol 60:433–533

    PubMed  CAS  Google Scholar 

  • Frey-Klett P, Chavatte M, Clausse M-L, Courrier S, Le Roux C, Raaijmakers J, Martinotti MG, Pierrat J-C, Garbaye J (2005) Ectomycorrhizal symbiosis affects functional diversity of rhizosphere fluorescent pseudomonads. New Phytol 165:317–328

    PubMed  Google Scholar 

  • Frey-Klett P, Garbaye J, Tarkka MT (2007) The mycorrhiza helper bacteria revisited. New Phytol 176:22–36

    PubMed  CAS  Google Scholar 

  • Fries N, Serck-Hanssen K, Dimberg LH, Theander O (1989) In vitro enhancement of spore germination and early hyphal growth of a vesicular-arbuscular mycorrhizal fungus by host root exudates and plant flavonoids. Symbiosis 7:243–255

    Google Scholar 

  • Garbaye J (1994) Helper bacteria: a new dimension to the mycorrhizal symbiosis. New Phytol 128:197–210

    Google Scholar 

  • Gay G, Normand L, Marmeisse R, Sotta B, Debaud JC (1994) Auxin overproducer mutants of Hebeloma cylindrosporum Romagnési have increased mycorrhizal activity. New Phytol 128:645

    CAS  Google Scholar 

  • Gea L, Normand L, Vian B, Gay G (1994) Structural aspects of ectomycorrhiza of Pinus pinaster (Ait.) Sol. formed by an IAA-overproducer mutant of Hebeloma cylindrosporum Romagnési. New Phytol 128:659

    Google Scholar 

  • Gil ML, Penalver MC, Lopez-Ribot JL, O’Connor JE, Martinez JP (1996) Binding of extracellular matrix proteins to Aspergillus fumigatus conidia. Infect Immun 64:5239–5247

    PubMed  CAS  Google Scholar 

  • Gogala N (1991) Regulation of mycorrhizal infection by hormonal factors produced by hosts and fungi. Cell Mol Life Sci 47:331–340

    CAS  Google Scholar 

  • Grant CM (2001) Role of the glutathione/glutaredoxin and thioredoxin systems in yeast growth and response to stress conditions. Mol Microbiol 39:533–541

    PubMed  CAS  Google Scholar 

  • Hamill JD (1993) Alterations in auxin and cytokinin metabolism of higher plants due to expression of specific genes from pathogenic bacteria: a review. Aust J Plant Physiol 20:405

    CAS  Google Scholar 

  • Heller G, Adomas A, Li G, Osborne J, van Zyl L, Sederoff R, Finlay RD, Stenlid J, Asiegbu FO (2008) Transcriptional analysis of Pinus sylvestris roots challenged with the ectomycorrhizal fungus Laccaria bicolor. BMC Plant Biol 8:19

    PubMed  Google Scholar 

  • Hilbert JL, Costa G, Martin F (1991) Ectomycorrhizal synthesis and polypeptide changes during the early stage of eucalypt mycorrhiza development. Plant Physiol 97:977–984

    PubMed  CAS  Google Scholar 

  • Högberg P, Hordgre A, Buchmann N, Taylor AFS, Ekblad A, Högberg MN, Nyberg G, Ottosson-Löfvenius M, Read DJ (2001) Largescale forest girdling shows that current photosynthesis drives soil respiration. Nature 411:789–792

    PubMed  Google Scholar 

  • Holder DJ, Keyhani NO (2005) Adhesion of the entomopathogenic fungus Beauveria (Cordyceps) bassiana to substrata. Appl Environ Microbiol 71:5260–5266

    PubMed  CAS  Google Scholar 

  • Horan DP, Chilvers GA, Lapeyrie F (1988) Time sequence of the infection process in eucalypt ectomycorrhizas. New Phytol 109:451–458

    Google Scholar 

  • Hostetter M (2000) RGD-mediated adhesion in fungal pathogens of humans, plants and insects. Curr Opin Microbiol 3:344–348

    PubMed  CAS  Google Scholar 

  • Ingram DS, Tommerup IC (1972) The life history of Plasmodiophora brassicae Woron. Proc R Soc Lond Ser B 180:103–112

    Google Scholar 

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

    CAS  Google Scholar 

  • Jensen BG, Andersen MR, Pedersen MH, Frisvad JC, Sondergaard I (2010) Hydrophobins from Aspergillus species cannot be clearly divided into two classes. BMC Res Notes 3:344

    PubMed  CAS  Google Scholar 

  • Kale SD, Gu B, Capelluto DGS, Feldman E, Rumore A, Arredondo FD, Hanlon R, Fudal I, Rouxel T, Lawrence CB, Shan W, Tyler BM (2010) External lipid PI3P mediates entry of eukaryotic pathogen effectors into plant and animal host cells. Cell 142:284–295

    PubMed  CAS  Google Scholar 

  • Kambara K, Ardissone S, Kobayashi H, Saad MM, Schumpp O, Broughton WJ, Deakin WJ (2009) Rhizobia utilize pathogen-like effector proteins during symbiosis. Mol Microbiol 71:92–106

    PubMed  CAS  Google Scholar 

  • Karabaghli-Degron C, Sotta B, Bonnet M, Gay G, 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

    CAS  Google Scholar 

  • Kaska DD, Myllylä R, Cooper JB (1999) Auxin transport inhibitors act through ethylene to regulate dichotomous branching of lateral root meristems in pine. New Phytol 142:49

    CAS  Google Scholar 

  • Kawano T, Kawano N, Hosoya H, Lapeyrie F (2001) Fungal auxin antagonist hyphphorine competitively inhibits indole-3-acetic acid-dependent superoxide generation by horseradish peroxidase. Biochem Biophys Res Commun 288:546–551

    PubMed  CAS  Google Scholar 

  • Kazmierczak P, Pfeiffer P, Zhang L, Van Alfen NK (1996) Transcriptional repression of specific host genes by the mycovirus Cryphonectria-hypovirus-1. J Virol 70:1137–1142

    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 

  • Kershaw MJ, Thornton CR, Wakley GE, Talbot NJ (2005) Four conserved intramolecular disulphide linkages are required for secretion and cell wall localization of a hydrophobin during fungal morphogenesis. Mol Microbiol 56:117–125

    PubMed  CAS  Google Scholar 

  • Kielland K (1990) Processes controlling nitrogen release and turnover in arctic tundra. PhD thesis, University of Alaska, Alaska

    Google Scholar 

  • Kikuchi K, Matsushita N, Suzuki K, Hogetsu T (2007) Flavonoids induce germination of basidiospores of the ectomycorrhizal fungus Suillus bovinus. Mycorrhiza 17:563–570

    PubMed  CAS  Google Scholar 

  • Kim S, Ahn I-P, Rho H-S, Lee Y-H (2005) MPH1, a Magnaporthe grisea hydrophobin gene, is required for fungal development and plant colonization. Mol Microbiol 57:1224–1237

    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 

  • Knee EM, Gong FC, Gao M, Teplitski M, Jones AR, Foxworthy A, Mort AJ, Bauer WD (2001) Root mucilage from pea and its utilization by rhizosphere bacteria as a sole carbon source. Mol Plant Microbe Interact 14:775–784

    PubMed  CAS  Google Scholar 

  • Kondoh O, Muto A, Kajiwara S, Takagi J, Saito Y, Shishido K (1995) Fruiting body-specific cDNA, mfbAc, from the mushroom Lentinus edodes encodes a high-molecular-weight cell-adhesion protein containing an Arg-Gly-Asp motif. Gene 154:31–37

    PubMed  CAS  Google Scholar 

  • Köttke I, Oberwinkler F (1986) Root-Fungus interactions observed on initial stages of mantle formation and Hartig net establishment in mycorrhizas of Amanita muscaria on Picea abies in pure culture. Can J Bot 64:2348–2354

    Google Scholar 

  • Kottke I, Oberwinkler F (1987) Cellular structure and function of the Hartig net: coenocytic and transfer cell-like organization. Nord J Bot 7:85–95

    Google Scholar 

  • Kroehler CJ, Linkins AE (1991) The absorption of inorganic phosphate from 32P labeled inositol hexaphosphate by Eriophorum vainatum. Oecologia 85:424–428

    Google Scholar 

  • Kunkel BN, Bent AF, Dahlbeck D, Innes RW, Staskawicz BJ (1993) RPS2, an Arabidopsis disease resistance locus specifying recognition of Pseudomonas syringae strains expressing the avirulence gene avrRpt2. Plant Cell 5:865–875

    PubMed  CAS  Google Scholar 

  • Labbé J, Jorge V, Kohler A, Vion P, Marcais B, Bastien C, Tuskan GA, Martin F, Le Tacon F (2010) 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 Genomics 7:617–627

    Google Scholar 

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

    CAS  Google Scholar 

  • Larose G, Chenevert R, Moutoglis P, Gagne S, Piché Y, Vierheilig H (2002) Flavonoid levels in roots of Medicago sativa are modulated by the developmental stage of the symbiosis and the root colonizing arbuscular mycorrhizal fungus. J Plant Physiol 159:1329–1339

    CAS  Google Scholar 

  • Larsen PE, Trivedi G, Sreedasyam A, Lu V, Podila GK, Collart FR (2010) Using deep RNA sequencing for the structural annotation of the Laccaria bicolor mycorrhizal transcriptome. PLoS One 5:e9780

    PubMed  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 (1995) Contribution à l’étude des protéines régulées par la symbiose chez l’ectomycorhize d’Eucalyptus – Pisolithus. Caractérisation de mannoprotéines pariétales chez le basidiomycete Pisolithus tinctorius. PhD thesis, University Henri Poincaré, Nancy

    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, Eriksen KA, Rajashekar B, Schützendübel A, Canbäck B et al (2006) Screening for rapidly evolving genes in the ectomycorrhizal fungus Paxillus involutus using cDNA microarrays. Mol Ecol 15:535–550

    PubMed  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 

  • Linder MB, Szilvay GR, Nakari-Setala T, Penttila ME (2005) Hydrophobins: the protein amphiphiles of filamentous fungi. FEMS Microbiol Rev 29:877–896

    PubMed  CAS  Google Scholar 

  • Ludwig-Müller J, Bendel U, Thermann P, Ruppel M, Epstein E, Hilgenberg W (1993) Concentrations of indole-3-acetic acid in plants of tolerant and susceptible varieties of Chinese cabbage infected with Plasmodiophora brassicae Woron. New Phytol 125:763–769

    Google Scholar 

  • Ludwig-Müller J, Epstein E, Hilgenberg W (1996) Auxin-conjugate hydrolysis in Chinese cabbage: characterization of an amidohydrolase and its role during infection with clubroot disease. Physiol Plant 97:627–634

    Google Scholar 

  • Lundeberg G (1970) Utilisation of various nitrogen sources, in particular bound soil nitrogen, by mycorrhizal fungi. Stud For Suec 79:11–17

    Google Scholar 

  • Luo ZB, Janz D, Jiang X, Gobel C, Wildhagen H, Tan Y, Rennenberg H, Feussner I, Polle A (2009) Upgrading root physiology for stress tolerance by ectomycorrhizas: insights from metabolite and transcriptional profiling into reprogramming for stress anticipation. J Plant Physiol 151:1902–1917

    CAS  Google Scholar 

  • Maier A (2003) Einfluss bakterieller Stoffwechselprodukte auf Wachstum und Proteom des Ektomykorrhizapilzes Amanita muscaria. PhD thesis, University of Tubingen, Tubingen

    Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Martin F (2007) Fair trade in the underworld: the ectomycorrhizal symbiosis. In: Howard RJ, Gow NAR (eds) Biology of the fungal cell, 2nd edn, The mycota VIII. Springer-Verlag, Berlin, Heidelberg, pp 291–308

    Google Scholar 

  • Martin F, Perotto S, Bonfante P (2007) Mycorrhizal fungi: a fungal community at the interface between soil and roots. In: Pinton R, Varanini Z, Nannipieri P (eds) The rhizosphere. Biochemistry and organic substances at the soil–plant interface. Dekker, New York, pp 263–296

    Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Martin F, Kohler A, Murat C, Balestrini R, Coutinho PM et al (2010) Périgord 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 A, Spatafora JW, Baker SE, Grigoriev IV. (2011) Sequencing the Fungal Tree of Life. New Phytologist 190: 818–821

    PubMed  CAS  Google Scholar 

  • Meixner C, Ludwig-Müller J, Miersch O, Gresshoff P, Staehelin C, Vierheilig H (2005) Lack of mycorrhizal autoregulation and phytohormonal changes in the supernodulating soybean mutant nts1007. Planta 222:709–715

    PubMed  CAS  Google Scholar 

  • Meixner C, Vegvari G, Ludwig-Müller J, Gagnon H, Steinkellner S, Staehelin C, Gresshoff P, Vierheilig H (2007) Two defined alleles of the LRR receptor kinase GmNARK in supernodulating soybean govern differing autoregulation of mycorrhization. Physiol Plant 130:261–270

    CAS  Google Scholar 

  • Mengel K, Kirby EA (1987) Plant nutrients. In: Mengel K, Kirby EA (eds) Principles of plant nutrition. International Potash Institute, Geneva, pp 11–24

    Google Scholar 

  • Mitchell TK, Dean RA (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

    PubMed  CAS  Google Scholar 

  • Montanini B, Levati E, Bolchi A, Kohler A, Morin E, Tisserant E, Martin F, Ottonello S (2011) Genome-wide search and functional identification of transcription factors in the mycorrhizal fungus Tuber melanosporum. New Phytol 189:736–750

    PubMed  CAS  Google Scholar 

  • Morandi D, Branzanti B, Gianinazzi-Pearson V (1984) Isoflavonoid accumulation in soybean roots infected with vesicular-arbuscular mycorrhizal fungi. Physiol Plant Pathol 24:357–364

    CAS  Google Scholar 

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

    PubMed  Google Scholar 

  • Mukhtar MS, Carvunis A-R, Dreze M, Epple P, Steinbrenner J et al (2011) Independently evolved virulence effectors converge onto hubs in a plant immune system network. Science 333:576–601

    Google Scholar 

  • Müller O, Schreier PH, Uhrig JF (2008) Identification and characterization of secreted and pathogenesis-related proteins in Ustilago maydis. Mol Genet Genomics 279:27–39

    PubMed  Google Scholar 

  • Narasimhan S, Armstrong MY, Rhee K, Edman JC, Richards FF, Spicer E (1994) Gene for an extracellular matrix receptor protein from Pneumocystis carinii. Proc Natl Acad Sci USA 91:7440–7444

    PubMed  CAS  Google Scholar 

  • Nehls U, Béguiristain T, Ditengou F, Lapeyrie F, 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

    PubMed  CAS  Google Scholar 

  • Nurmiaho-Lassila EL, Timonen S, Haahtela K, Sen R (1997) Bacterial colonization patterns of intact Pinus sylvestris mycorrhizospheres in dry pine forest soil: an electron microscopy study. Can J Microbiol 43:1017–1035

    CAS  Google Scholar 

  • Ochsenreiter T, Selezi D, Quaiser A, Bonch-Osmolovskaya L, Schleper C (2003) Diversity and abundance of Crenarchaeota in terrestrial habitats studied by 16S RNA surveys and real time PCR. Environ Microbiol 5:787–797

    PubMed  CAS  Google Scholar 

  • Parta M, Chang Y, Rulong S, Pinto-DaSilva P, Kwon-Chung KJ (1994) HYP1, a hydrophobin gene from Aspergillus fumigatus, complements the rodletless phenotype in Aspergillus nidulans. Infect Immun 62:4389–4395

    PubMed  CAS  Google Scholar 

  • Penalver MC, O’Connor JE, Martinez JP, Gil ML (1996) Binding of human fibronectin to Aspergillus fumigatus conidia. Infect Immun 64:1146–1153

    PubMed  CAS  Google Scholar 

  • Pérez-García A, Olalla L, Rivera E, Del Pino D, Canovas I, De Vicente A, Torés JA (2001) Development of Sphaerotheca fusca on susceptible, resistant, and temperature-sensitive resistant cultivars. Mycol Res 105:1216–1222

    Google Scholar 

  • Pierchbacher MD, Ruoslahti E (1984) Cell attachment activity of fibronectin can be duplicated by small synthetic fragments of the molecule. Nature 309:30–33

    Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Plett JM, Kemppainen M, Kale SD, Kohler A, Legue V, Brun A, Tyler B, Pardo A, 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, Kues U, Grigoriev IV, Martin F (2012) Phylogenetic, genomic organization and expression analysis of hydrophobin genes in the ectomycorrhizal basidiomycete Laccaria biocolor. Fungal Genet Biol 49:199–209

    PubMed  CAS  Google Scholar 

  • Qin M, Wang L-K, Feng X-Z, Yang Y-L, Wang R, Wang C, Yu L, Shao B, Qiao M-Q (2007) Bioactive surface modification of mica and poly(dimethylsiloxane) with hydrophobins for protein immobilization. Langmuir 23:4465–4471

    PubMed  CAS  Google Scholar 

  • Rajashekar B, Samson P, Johansson T, Tunlid A (2007) Evolution of nucleotide sequences and expression patterns of hydrophobin genes in the ectomycorrhizal fungus Paxillus involutus. New Phytol 174:399–411

    PubMed  CAS  Google Scholar 

  • Rasmussen TB, Skindersoe ME, Bjarnsholt T, Phipps RK, Christensen KB, Jensen PO, Andersen JB, Koch B, Larsen TO, Hentzer M, Eberl L, Hoiby N, Givskov M (2005) Identity and effects of quorum-sensing inhibitors produced by Penicillium species. Microbiology 151:1325–1340

    PubMed  CAS  Google Scholar 

  • Read DJ, Perez-Moreno J (2003) Mycorrhizas and nutrient cycling in ecosystems – a journey towards relevance? New Phytol 157:475–492

    Google Scholar 

  • Regenfelder E, Spellig T, Hartmann A, Lauenstein S, Bolker M, Kahmann R (1997) G proteins in Ustilago maydis: transmission of multiple signals? EMBO J 16:1934–1942

    PubMed  CAS  Google Scholar 

  • Rikhvanov EG, Varakina NN, Sozinov DY, Voinikov VK (1999) Association of bacteria and yeasts in hot springs. Appl Environ Microbiol 65:4292–4293

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Ruess RW, Hendrick RL, Burton AJ, Pregitzer KS, Sveinbjornsson B, Allen ME, Maurer GE (2003) Coupling fine root dynamics with ecosystem carbon cycling in black spruce forests of interior Alaska. Ecol Monogr 73:643–662

    Google Scholar 

  • Ruoslahti E (1996) RGD and other recognition sequences for integrins. Annu Rev Cell Dev Biol 12:697–715

    PubMed  CAS  Google Scholar 

  • Rupp LA, Mudge KW (1985) Ethephon and auxin induce mycorrhiza-like changes in the morphology of root organ cultures of Mugo pine. Physiol Plant 64:316

    CAS  Google Scholar 

  • Rupp LA, Mudge KW, Negm FB (1989) Involvement of ethylene in ectomycorrhiza formation and dichotomous branching of roots of mugo pine seedlings. Can J Bot 67:477

    CAS  Google Scholar 

  • Scherrer S, Honegger R (2003) Inter- and intraspecific variation of homologous hydrophobin (H1) gene sequences among Xanthoria spp. (lichen-forming ascomycetes). New Phytol 158:375–389

    CAS  Google Scholar 

  • Scherrer S, Haisch A, Honegger R (2002) Characterization and expression of XPH1, the hydrophobin gene of the lichen-forming ascomycete Xanthoria parietina. New Phytol 154:175–184

    CAS  Google Scholar 

  • Schrey SD, Tarkka MT (2008) Friends and foes: streptomycetes as modulators of plant disease and symbiosis. Antonie Leeuwenhoek 94:11–19

    PubMed  Google Scholar 

  • Schrey SD, Schellhammer M, Ecke M, Hampp R, Tarkka MT (2005) Mycorrhiza helper bacterium Streptomyces AcH 505 induces differential gene expression in the ectomycorrhizal fungus Amanita muscaria. New Phytol 168:205–216

    PubMed  CAS  Google Scholar 

  • Selosse MA, Richard F, He X, Simard SW (2006) Mycorrhizal networks:des liaisons dangereuses? Trends Ecol Evol 21:621–628

    PubMed  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 β-glucan fragment that elicits phytoalexin accumulation in soybean. J Biol Chem 25:11312–11320

    Google Scholar 

  • Singh P, Chauhan N, Ghosh A, Dixon F, Calderone R (2004) SKN7 of Candida albicans: mutant construction and phenotype analysis. Infect Immun 72:2390–2394

    PubMed  CAS  Google Scholar 

  • Spanu P, Bonfante-Fasolo P (1988) Cell wall-bound peroxidase activity in roots of mycorrhizal Allium porrum. New Phytol 109:119–124

    CAS  Google Scholar 

  • Spanu P, Boller T, Ludwig A, Wiemken A, Faccio A, Bonfante-Fasolo P (1989) Chitinase in roots of mycorrhizal Allium porrum: regulation and localization. Planta 177:447–455

    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 

  • Sundaram S, Kim SJ, Suzuki H, McQuattie CJ, Hiremath ST, Podila GK (2001) Isolation and characterization of a symbiosis-regulated ras from the ectomycorrhizal fungus Laccaria bicolor. Mol Plant Microbe Interact 14:618–628

    PubMed  CAS  Google Scholar 

  • Sunde M, Kwan AHY, Templeton MD, Beever RE, Mackay JP (2008) Structural analysis of hydrophobins. Micron 39:773–784

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Tagu D, Kottke I, Martin F (1998) Hydrophobins in ectomycorrhizal symbiosis: hypothesis. Symbiosis 25:5–18

    CAS  Google Scholar 

  • Tagu D, De Bellis R, Balestrini R, De Vries O, Piccoli G, Stocchi V, Bonfante P, Martin F (2001) Immunolocalization of hydrophobin HYDPt-1 from the ectomycorrhizal basidiomycete Pisolithus tinctorius during colonisation of Eucalyptus globulus roots. New Phytol 149:127–135

    CAS  Google Scholar 

  • Talbot NJ, Ebbole DJ, Hamer JE (1993) Identification and characterization of MPG1, a gene involved in pathogenicity from the rice blast fungus Magnaporthe grisea. Plant Cell 5:1575–1590

    PubMed  CAS  Google Scholar 

  • Talbot NJ, Kershaw MJ, Wakley GE, de Vries OMH, Wessels JGH, Hamer JE (1996) MPG1 encodes a fungal hydrophobin involved in surface interactions during infection related development by the rice blast fungus Magnaporthe grisea. Plant Cell 8:985–999

    PubMed  CAS  Google Scholar 

  • Tarkka MT, Frey-Klett P (2008) Mycorrhiza helper bacteria. In: Varma A (ed) Mycorrhiza, 3rd edn. Springer, Berlin, pp 113–132

    Google Scholar 

  • Tarkka MT, Sarniguet A, Frey-Klett P (2009) Inter-kingdom encounters: recent advances in molecular bacterium–fungus interactions. Curr Genet 55:233–243

    PubMed  CAS  Google Scholar 

  • Taylor AFS, Martin F, Read DJ (2000) Fungal diversity in ectomycorrhizal communities of Norway spruce Picea abies (L.) Karst. and beech (Fagus sylvatica L.) along north–south transects in Europe. Ecol Stud 142:343–365

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Teplitski M, Robinson JB, Bauer WD (2000) Plants secrete substances that mimic bacterial N-acyl homoserine lactone signal activities and affect population density-dependent behaviors in associated bacteria. Mol Plant Microbe Interact 13:637–648

    PubMed  CAS  Google Scholar 

  • Thau N, Monod M, Cretani B, Rolland C, Tronchin G et al (1994) Rodletless mutants of Aspergillus fumigatus. Infect Immun 62:4380–4388

    PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Tibbett M, Sanders FE, Minto SJ, Dowell M, Cairney JWG (1998) Utilization of organic nitrogen by ectomycorrhizal fungi (Hebeloma spp.) of arctic and temperate origin. Mycol Res 102(12):1525–1532

    CAS  Google Scholar 

  • Tibbett M, Sanders FE, Cairney JWG (1999) Long term storage of ectomycorrhizal basidiomycetes (Hebeloma spp.) at low temperature. J Basic Microbiol 39:381–384

    Google Scholar 

  • Tisserant E, Da Silva C, Kohler A, Morin E, Wincker P, Martin F (2011) Deep RNA sequencing improved the structural annotation of the Tuber melanosporum transcriptome. New Phytol 189:883–891

    PubMed  CAS  Google Scholar 

  • Trembley ML, Ringli C, Honegger R (2002a) Differential expression of hydrophobins DGH1, DGH2 and DGH3 and immunolocalization of DGH1 in strata of the lichenized basidiocarp of Dictyonema glabratum. New Phytol 15:185–195

    Google Scholar 

  • Trembley ML, Ringli C, Honegger R (2002b) Hydrophobins DGH1, DGH2, and DGH3 in the lichen-forming Basidiomycete Dictyonema glabratum. Fungal Genet Biol 3:247–259

    Google Scholar 

  • Tuskan GA, Difazio S, Jansson S, Bohlmann J, Grigoriev I et al (2006) The genome of black cottonwood, Populus trichocarpa. Science 313:1596–1604

    PubMed  CAS  Google Scholar 

  • Urbanek H, Kaczmarek A (1985) Extracellular proteinases of the isolate of Botrytis cinerea virulent to apple tissues. Acta Biochim Pol 32:101–109

    PubMed  CAS  Google Scholar 

  • Urbanek H, Yirdaw G (1984) Hydrolytic ability of acid protease of Fusarium culmorum and role in phytopatogenesis. Acta Microbiol Pol 33:131–136

    PubMed  CAS  Google Scholar 

  • Uroz S, Heinonsalo J (2008) Inactivation of N-acyl homoserine lactone quorum sensing molecules by forest soil fungi. FEMS Microbiol Ecol 65:271–278

    PubMed  CAS  Google Scholar 

  • Uroz S, Dangelo D, Carlier A, Faure D, Petit A, Oger P, Sicot C, Dessaux Y (2003) Novel bacteria degrading N-acyl homoserine lactones and their use as quenchers of quorum-sensing regulated functions of plant pathogenic bacteria. Microbiology 149:1981–1989

    PubMed  CAS  Google Scholar 

  • Vierheilig H (2004) Further root colonization by arbuscular mycorrhizal fungi in already mycorrhizal plants is suppressed after a critical level of root colonization. J Plant Physiol 161:339–341

    PubMed  CAS  Google Scholar 

  • Vierheilig H, Garcia-Garrido JM, Wyss U, Piché Y (2000a) Systemic suppression of mycorrhizal colonization of barley roots already colonized by AM fungi. Soil Biol Biochem 32:589–595

    CAS  Google Scholar 

  • Vierheilig H, Maier W, Wyss U, Samson J, Strack D, Piché Y (2000b) Cyclohexenone derivative and phosphate-levels in split-root systems and their role in the systemic suppression of mycorrhization in precolonized barley plants. J Plant Physiol 157:593–599

    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 25:181–192

    PubMed  CAS  Google Scholar 

  • Walker TS, Bais HP, Grotewold E, Vivanco JM (2003) Root exudation and rhizosphere biology. Plant Physiol 132:44–51

    PubMed  CAS  Google Scholar 

  • Wang D, Pajerowska-Mukhtar K, Culler AH, Dong X (2007) Salicylic acid inhibits pathogen growth in plants through repression of the auxin signaling pathway. Curr Biol 17:1784–1790

    PubMed  CAS  Google Scholar 

  • Wang X, Wang H, Huang Y, Zhao Z, Qin X, Wang Y, Miao Z, Chen Q, Qiao M (2010) Noncovalently funtionalized multi-wall carbon nanotubes in aqueous solution using the hydrophobin HFBI and their electroanalytical application. Biosens Bioelectron 26:1104–1108

    PubMed  CAS  Google Scholar 

  • Wessels JGH (1996) Hydrophobins: proteins that change the nature of the fungal surface. Adv Microb Physiol 38:1–45

    Google Scholar 

  • Wessels JGH, de Vries OMH, Asgeirsdottir SA, Schuren FHJ (1991) Hydrophobin genes involved in formation of aerial hyphae and fruit bodies in Schizophyllum. Plant Cell 3:793–799

    PubMed  CAS  Google Scholar 

  • Wild A (1988) Plant nutrients in soil. In: Wild A (ed) Russel’s soil conditions and plant growth, 11th edn. Longman, Harlow, pp 695–743

    Google Scholar 

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

    PubMed  Google Scholar 

  • Wösten HAB, Wessels JGH (1997) Hydrophorins, from molecular structure to multiple functions in fungal development. Mycoscience 38:363–374

    Google Scholar 

  • Yasuda T, Shishido K (1997) Aggregation of yeast cells induced by the Arg-Gly-Asp motif-containing fragment of high-molecular mass cell-adhesion protein MFBA, derived from the basidiomycetous mushroom Lentinus edodes. FEMS Microbiol Lett 154:195–200

    PubMed  CAS  Google Scholar 

  • Zampieri E, Balestrini R, Kohler A, Abbà S, Martin F, Bonfante P (2011) The Perigord black truffle responds to cold temperature with an extensive reprogramming of its transcriptional activity. Fungal Genet Biol 48:585–591

    PubMed  CAS  Google Scholar 

  • Zhang L, Villalon D, Sin Y, Kazmierczak P, Van Alfen NK (1994) Virus-associated down-regulation of the gene encoding cryparin, an abundant cell surface protein of the chestnut blight fungus Cryphonectria parasitica. Gene 139:59–64

    PubMed  CAS  Google Scholar 

  • Zhao Z-X, Qiao M-Q, Yin F, Shao B, Wu B-Y, Wang Y-Y, Wang X-S, Qin X, Li S, Yu L, Chen Q (2007) Amperometric glucose biosensor based on self-assembly hydrophobin with high efficiency of enzyme utilization. Biosens Bioelectron 22:3021–3027

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to F. Martin .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and Permissions

Copyright information

© 2012 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Plett, J.M., Kohler, A., Martin, F. (2012). 6 De-Constructing a Mutualist: How the Molecular Blueprints of Model Symbiotic Fungi Are Changing Our Understanding of Mutualism. In: Hock, B. (eds) Fungal Associations. The Mycota, vol 9. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-30826-0_6

Download citation