Advertisement

Signalling in Ectomycorrhizal Symbiosis

  • Judith Felten
  • Francis Martin
  • Valérie LeguéEmail author
Chapter
Part of the Signaling and Communication in Plants book series (SIGCOMM, volume 11)

Abstract

The mechanism by which tree roots and soil fungi interact and form their common, symbiotic organ, the ectomycorrhiza (ECM), involves numerous steps. During this ontogenic process, the developmental programs of both partners are modified in order to enable symbiosis establishment. Both roots and fungus release an array of various metabolites (morphogens and signalling molecules) that establish a molecular cross-talk between symbionts. In contrast to some other plant–microbe interactions, such as rhizobia or arbuscular mycorrhiza symbiosis, the characterization of these signalling molecules and their impact on developmental pathways is poorly known. Recent studies have provided new insights into specific phases and signalling pathways of ECM development on a molecular level and have thereby started to fill the gaps in our understanding of root–fungus communication. Based on this knowledge and recent data from ECM interaction, we will identify possible crosstalk between ECM signalling and root development.

Keywords

Root Hair Polar Auxin Transport Abietic Acid Root Cell Wall Lateral Root Primordium 
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.

References

  1. Aguilar JMM, Shby AM, Richards AJM, Loake GJ, Watson MD, Shaw CH (1988) Chemotaxis of rhizobium leguminosarum biovar phaseoli towards flavonoid inducers of the symbiotic nodulation genes. J Gen Microbiol 134:2741–2746Google Scholar
  2. Al-Abras K, Bilger I, Martin F, Le Tacon F, Lapeyrie F (1988) Morphological and physiological changes in ectomycorrhizas of spruce (Picea excelsa (lam.) link) associated with ageing. New Phytol 110:535–540CrossRefGoogle Scholar
  3. Alexander IJ (2006) Ectomycorrhizas – out of Africa? New Phytol 172:589–591PubMedCrossRefGoogle Scholar
  4. Bari R, Jones JD (2009) Role of plant hormones in plant defence responses. Plant Mol Biol 69:473–488PubMedCrossRefGoogle Scholar
  5. Bates TR, Lynch JP (2000) Plant growth and phosphorus accumulation of wild type and two root hair mutants of Arabidopsis thaliana (Brassicaceae). Am J Bot 87:958–963PubMedCrossRefGoogle Scholar
  6. Beguiristain A, Lapeyrie F (1997) Host plant stimulates hypaphorine accumulation in Pisolithus tinctorius hyphae during ectomycorrhizal infection while excreted fungal hypaphorine controls root hair development. New Phytol 136:525–532CrossRefGoogle Scholar
  7. Benkova E, Hejatko J (2009) Hormone interactions at the root apical meristem. Plant Mol Biol 69:383–396PubMedCrossRefGoogle Scholar
  8. Blasius D, Feil W, Kottke I, Oberwinkler F (1986) Hartig net structure and formation in fully ensheathed ectomycorrhizas. Nord J Bot 6:837–842CrossRefGoogle Scholar
  9. 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 104:1366–1371CrossRefGoogle Scholar
  10. Boller T, He SY (2009) Innate immunity in plants: an arms race between pattern recognition receptors in plants and effectors in microbial pathogens. Science 324:742–744PubMedCentralPubMedCrossRefGoogle Scholar
  11. Buée M, Reich M, Murat C, Morin E, Nilsson RH, Uroz S, Martin F (2009) 454 Pyrosequencing analyses of forest soils reveal an unexpectedly high fungal diversity. New Phytol 184:449–456PubMedCrossRefGoogle Scholar
  12. Chalot M, Blaudez D, Brun A (2006) Ammonia: a candidate for nitrogen transfer at the mycorrhizal interface. Trends Plant Sci 11:263–266PubMedCrossRefGoogle Scholar
  13. Charvet-Candela V, Hitchin S, Ernst D, Sandermann H Jr, Marmeisse R, Gay G (2002) Characterization of an aux/iaa cDNA upregulated in Pinus pinaster roots in response to colonization by the ectomycorrhizal fungus Hebeloma cylindrosporum. New Phytol 154:769–777CrossRefGoogle Scholar
  14. Creelman RA, Mullet JE (1997) Biosynthesis and action of jasmonates in plants. Annu Rev Plant Physiol Plant Mol Biol 48:355–381PubMedCrossRefGoogle Scholar
  15. Dauphin A, Gerard J, Lapeyrie F, Legue V (2007) Fungal hypaphorine reduces growth and induces cytosolic calcium increase in root hairs of eucalyptus globulus. Protoplasma 231:83–88PubMedCrossRefGoogle Scholar
  16. Dexheimer J, Pargney JC (1991) Comparative anatomy of the host-fungus interface in mycorrhizas. Experientia 47:312–320CrossRefGoogle Scholar
  17. Dexheimer J, Aubert-Dufresne M-P, Gerard J, Le Tacon F, Mousain D (1986) Ultrastructural localization of acid phosphatase activities in two ectomycorhizas: Pinus nigra nigricans/Hebeloma crustiliniforme and Pinus pinaster/Pisolithus tinctorius. Lett Botaniq 133:343–352Google Scholar
  18. D’Haeze W, Holsters M (2002) Nod factor structures, responses, and perception during initiation of nodule development. Glycobiology 12:79R–105RPubMedCrossRefGoogle Scholar
  19. 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 13:151–158PubMedCrossRefGoogle Scholar
  20. Ditengou FA, Beguiristain T, Lapeyrie F (2000) Root hair elongation is inhibited by hypaphorine, the indole alkaloid from the ectomycorrhizal fungus Pisolithus tinctorius, and restored by indole-3-acetic acid. Planta 211:722–728PubMedCrossRefGoogle Scholar
  21. Ditengou FA, Raudaskoski M, Lapeyrie F (2003) Hypaphorine, an indole-3-acetic acid antagonist delivered by the ectomycorrhizal fungus Pisolithus tinctorius, induces reorganisation of actin and the microtubule cytoskeleton in Eucalyptus globulus ssp bicostata root hairs. Planta 218:217–225PubMedCrossRefGoogle Scholar
  22. Duplessis S, Courty PE, Tagu D, Martin F (2005) Transcript patterns associated with ectomycorrhiza development in eucalyptus globulus and Pisolithus microcarpus. New Phytol 165:599–611PubMedCrossRefGoogle Scholar
  23. Ek M, Ljungquist PO, Stenström E (1983) Indole-3-acetic acid production by mycorrhizal fungi determined by gas chromatography-mass spectrometry. New Phytol 94:401–407CrossRefGoogle Scholar
  24. 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 151:1991–2005PubMedCentralPubMedCrossRefGoogle Scholar
  25. Felten J, Legue V, Ditengou FA (2010) Lateral root stimulation in the early interaction between arabidopsis thaliana and the ectomycorrhizal fungus Laccaria bicolor: is fungal auxin the trigger? Plant Signal Behav 5:864–867PubMedCentralPubMedCrossRefGoogle Scholar
  26. Fries N, Serck-Hanssen K, Dimberg LH, Theander O (1987) Abietic acid, an activator of Basidiospore germination inectomycorrhizal species of the genus Suillus (Boletaceae). Exp Mycol 11:360–363CrossRefGoogle Scholar
  27. Fukaki H, Tasaka M (2009) Hormone interactions during lateral root formation. Plant Mol Biol 69:437–449PubMedCrossRefGoogle Scholar
  28. Gafur A, Schützendübel A, Langenfeld-Heyser R, Frizt E, Polle A (2004) Compatible and incompetent Paxillus involutus isolates for ectomycorrhiza formation in vitro with poplar (Populus x canescens) differ in H2O2 production. Plant Biol 2004:91–99Google Scholar
  29. Gherbi H, Markmann K, Svistoonoff S, Estevan J, Autran D, Giczey G, Auguy F, Peret B, Laplaze L, Franche C, Parniske M, Bogusz D (2008) SYMRK defines a common genetic basis for plant root endosymbioses with arbuscular mycorrhiza fungi, rhizobia, and Frankia bacteria. Proc Natl Acad Sci USA 105:4928–4932PubMedCrossRefGoogle Scholar
  30. Gogala N (1991) Regulation of mycorrhizal infection by hormonal factors produced by hosts and fungi. Experientia 47:331–340CrossRefGoogle Scholar
  31. Gomez-Roldan V, Fermas S, Brewer PB, Puech-Pages V, Dun EA, Pillot JP, Letisse F, Matusova R, Danoun S, Portais JC, Bouwmeester H, Becard G, Beveridge CA, Rameau C, Rochange SF (2008) Strigolactone inhibition of shoot branching. Nature 455:189–194PubMedCrossRefGoogle Scholar
  32. Graham JH, Linderman RG (1980) Ethylene production by ectomycorrhizal fungi, Fusarium oxysporum f. Sp. Pini, and by aseptically synthesized ectomycorrhizae and fusarium-infected douglas-fir roots. Can J Microbiol 26:1340–1347PubMedCrossRefGoogle Scholar
  33. Grove M, Spencer G, Rowwedder W, Mandava N, Worley J, Warthen J, Steffens G, Flippen-Anderson J, Cook J (1979) Brassinolide, a plant growth-promoting steroid isolated from Brassica napus pollen. Nature 281:216–217CrossRefGoogle Scholar
  34. Gutjahr C, Paszkowski U (2009) Weights in the balance: jasmonic acid and salicylic acid signaling in root-biotroph interactions. Mol Plant Microbe Interact 22:763–772PubMedCrossRefGoogle Scholar
  35. Hibbett DS, Gilbert LB, Donoghue MJ (2000) Evolutionary instability of ectomycorrhizal symbioses in basidiomycetes. Nature 407:506–508PubMedCrossRefGoogle Scholar
  36. Hilbert JL, Martin F (1988) Regulation of gene expression in ectomycorrhizas. I. Protein changes and the presence of ectomycorrhiza specific polypeptides in the Pisolithus eucalyptus symbiosis. New Phytol 110:339–346CrossRefGoogle Scholar
  37. Hilbert JL, Costa G, Martin F (1991) Ectomycorrhizin synthesis and polypeptide changes during the early stage of eucalypt mycorrhiza development. Plant Physiol 97:977–984PubMedCentralPubMedCrossRefGoogle Scholar
  38. Ho I (1987a) Comparison of eight Pisolithus tinctorius isolates for growth rate, enzyme activity, and phytohormone production. Can J For Res 17:31–35CrossRefGoogle Scholar
  39. Ho I (1987b) Enzyme activity and phytohormone production of a mycorrhizal fungus, Laccaria laccata. Can J For Res 17:855–858CrossRefGoogle Scholar
  40. Horan DP, Chilvers GA (1990) Chemotropism – the key to ectomycorrhiza formation. New Phytol 116:297–301CrossRefGoogle Scholar
  41. Horan DP, Chilvers GA, Lapeyrie F (1988) Time sequence of the infection process in eucalypt ectomycorrhizas. New Phytol 109:451–458CrossRefGoogle Scholar
  42. Ivanchenko MG, Muday GK, Dubrovsky JG (2008) Ethylene-auxin interactions regulate lateral root initiation and emergence in Arabidopsis thaliana. Plant J 55:335–347PubMedCrossRefGoogle Scholar
  43. Jacobs PF, Peterson RL, Massicotte G (1989) Altered fungal morphogenesis during early stages of ectomycorrhiza formation in Eucalyptus pilularis. Scanning Microsc 3:249–255Google Scholar
  44. Jambois A, Dauphin A, Kawano T, Ditengou FA, Bouteau F, Legue V, Lapeyrie F (2005) Competitive antagonism between IAA and indole alkaloid hypaphorine must contribute to regulate ontogenesis. Physiol Plant 123:120–129CrossRefGoogle Scholar
  45. Jones AR, Kramer EM, Knox K, Swarup R, Bennett MJ, Lazarus CM, Leyser HM, Grierson CS (2009) Auxin transport through non-hair cells sustains root-hair development. Nat Cell Biol 11:78–84PubMedCentralPubMedCrossRefGoogle Scholar
  46. Kamoun S (2007) (2007) Groovy times: filamentous pathogen effectors revealed. Curr Opin Plant Biol 187:920–928Google Scholar
  47. 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 140:723–733CrossRefGoogle Scholar
  48. Kende H, Zeevaart J (1997) The five “classical” plant hormones. Plant Cell 9:1197–1210PubMedCentralPubMedCrossRefGoogle Scholar
  49. Laajanen K, Vuorinen I, Salo V, Juuti J, Raudaskoski M (2007) Cloning of Pinus sylvestris scarecrow gene and its expression pattern in the pine root system, mycorrhiza and NPA-treated short roots. New Phytol 175:230–243PubMedCrossRefGoogle Scholar
  50. Lagrange H, Jay-Allemand C, Lapeyrie F (2001) Rutin, the phenolglycoside from Eucalyptus root exudates stimulates Pisolithus hyphal growth at picomolor concentrations. New Phytol 150:349–355CrossRefGoogle Scholar
  51. Landeweert R, Hoffland E, Finlay RD, Kuyper TW, van Breemen N (2001) Linking plants to rocks: ectomycorrhizal fungi mobilize nutrients from minerals. Trends Ecol Evol 16:248–254PubMedCrossRefGoogle Scholar
  52. Le Quere A, Wright DP, Soderstrom 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 18:659–673PubMedCrossRefGoogle Scholar
  53. Martin F (2007) Fair trade in the underworld: The ectomycorrhizal symbiosis, vol 2, The mycota biology of the fungal cell. Springer, HeidelbergGoogle Scholar
  54. Martin F, Nehls U (2009) Harnessing ectomycorrhizal genomics for ecological insights. Curr Opin Plant Biol 12:508–515PubMedCrossRefGoogle Scholar
  55. Martin F, Tagu D (1999) Developmental biology of a plant-fungus-symbiosis: the ectomycorrhiza. In: Varma A, Hock B (eds), Mycorrhiza: structure, function, molecular biology and biotechnology, vol 2. Springer-Verlag berlin, Heidelberg, 51–73Google Scholar
  56. Martin F, Duplessis S, Ditengou F, Lagrange H, Voiblet C, Lapeyrie F (2001) Developmental cross talking in the ectomycorrhizal symbiosis: signals and communication genes. New Phytol 151:145–154CrossRefGoogle Scholar
  57. Martin F, Aerts A, Ahren D, Brun A, Danchin EG, Duchaussoy F, Gibon J, Kohler A, Lindquist E, Pereda V, Salamov A, Shapiro HJ, Wuyts J, Blaudez D, Buee M, Brokstein P, Canback B, Cohen D, Courty PE, Coutinho PM, Delaruelle C, Detter JC, Deveau A, DiFazio S, Duplessis S, Fraissinet-Tachet L, Lucic E, Frey-Klett P, Fourrey C, Feussner I, Gay G, Grimwood J, Hoegger PJ, Jain P, Kilaru S, Labbe J, Lin YC, Legue V, Le Tacon F, Marmeisse R, Melayah D, Montanini B, Muratet M, Nehls U, Niculita-Hirzel H, Oudot-Le Secq MP, Peter M, Quesneville H, Rajashekar B, Reich M, Rouhier N, Schmutz J, Yin T, Chalot M, Henrissat B, Kues U, Lucas S, Van de Peer Y, Podila GK, Polle A, Pukkila PJ, Richardson PM, Rouze P, Sanders IR, Stajich JE, Tunlid A, Tuskan G, Grigoriev IV (2008) The genome of laccaria bicolor provides insights into mycorrhizal symbiosis. Nature 452:88–92PubMedCrossRefGoogle Scholar
  58. Massicote HB, Perterson RL, Ashford AE (1987) Ontogeny of Eucalyptus pilulirisPisolithus tinctorius ectomycorrhizae. I. Light microscopy and scanning electron microscopy. Can J Bot 65:1927–1939CrossRefGoogle Scholar
  59. Mensen R, Hager A, Salzer P (1998) Elicitor-induced changes of wall-bound and secreted peroxidase activities in suspension-cultured spruce (Picea abies) cells are attenuated by auxins. Physiol Plant 102:539–546CrossRefGoogle Scholar
  60. Miersch O, Bohlmann H, Wasternack C (1999) Jasmonates and related compounds from Fusarium oxysporum. Phytochemistry 50:517–523CrossRefGoogle Scholar
  61. Moyersoen B (2006) Pakaraimaea dipterocarpacea is ectomycorrhizal, indicating an ancient gondwanaland origin for the ectomycorrhizal habit in Dipterocarpaceae. New Phytol 172:753–762PubMedCrossRefGoogle Scholar
  62. Nylund JE (1980) Symplastic continuity during hartig net formation in Norway spruce ectomycorrhizas. New Phytol 86:373CrossRefGoogle Scholar
  63. Nylund JE, Unestam T (1982) Structure and physiology of ectomycorrhizae I. The process of mycorrhiza formation in Norway spruce in vitro. New Phytol 91:63–79CrossRefGoogle Scholar
  64. Olah B, Briere C, Becard G, Denarie J, Gough C (2005) Nod factors and a diffusible factor from arbuscular mycorrhizal fungi stimulate lateral root formation in Medicago truncatula via the DMI1/DMI2 signalling pathway. Plant J 44:195–207PubMedCrossRefGoogle Scholar
  65. Pitts RJ, Cernac A, Estelle M (1998) Auxin and ethylene promote root hair elongation in Arabidopsis. Plant J 16:553–560PubMedCrossRefGoogle Scholar
  66. Plett JM (2010) Ethylene – a key arbitrator to plant–fungal symbiotic interactions? New Phytol 185:868–871PubMedCrossRefGoogle Scholar
  67. Rahman A, Hosokawa S, Oono Y, Amakawa T, Goto N, Tsurumi S (2002) Auxin and ethylene response interactions during Arabidopsis root hair development dissected by auxin influx modulators. Plant Physiol 130:1908–1917PubMedCentralPubMedCrossRefGoogle Scholar
  68. Raudaskoski M, Salo V (2008) Dichotomization of mycorrhizal and NPA-treated short roots in Pinus sylvestris. Plant Signal Behav 3:113–115PubMedCentralPubMedCrossRefGoogle Scholar
  69. Rayle DL, Cleland RE (1992) The acid growth theory of auxin-induced cell elongation is alive and well. Plant Physiol 99:1271–1274PubMedCentralPubMedCrossRefGoogle Scholar
  70. Reddy SM, Hitchin S, Melayah D, Pandey AK, Raffier C, Henderson J, Marmeisse R, Gay G (2006) The auxin-inducible GH3 homologue pp-gh3.16 is downregulated in Pinus pinaster root systems on ectomycorrhizal symbiosis establishment. New Phytol 170:391–400PubMedCrossRefGoogle Scholar
  71. Regvar M, Gogala N, Znidarsic N (1997) Jasmonic acid affects mycorrhization of spruce seedlings with Laccaria laccata. Trees 11:511–514Google Scholar
  72. Reineke G, Heinze B, Schirawski J, Buettner H, Kahmann R, Basse CW (2008) Indole-3-acetic acid (IAA) biosynthesis in the smut fungus Ustilago maydis and its relevance for increased IAA levels in infected tissue and host tumour formation. Mol Plant Pathol 9:339–355PubMedCrossRefGoogle Scholar
  73. Rincon A, Gerard J, Dexheimer J, Le Tacon F (2001) Effect of an auxin transport inhibitor on aggregation and attachment processes during ectomycorrhiza formation between Laccaria bicolor S238N and Picea abies. Can J Bot 79:1152–1160CrossRefGoogle Scholar
  74. Rincon A, Priha O, Sotta B, Bonnet M, Le Tacon F (2003) Comparative effects of auxin transport inhibitors on rhizogenesis and mycorrhizal establishment of spruce seedlings inoculated with Laccaria bicolor. Tree Physiol 23:785–791PubMedCrossRefGoogle Scholar
  75. Rousseau JVD, Sylvia DM, Fox AJ (1994) Contribution of ectomycorrhiza of the potential nutrient-absorbing surface of pine. New Phytol 128:639–644CrossRefGoogle Scholar
  76. Rudawska ML, Kieliszewska-Rokicka B (1997) Mycorrhizal formation by Paxillus involutus strains in relation to their IAA-synthesizing activity. New Phytol 137:509–515CrossRefGoogle Scholar
  77. Rupp LA, DeVries HE, Mudge KW (1989) Effect of aminocyclopropane carboxylic acid and aminoethoxyvinylglycine on ethylene production by ectomycorrhizal fungi. Can J Bot 67:483–485CrossRefGoogle Scholar
  78. Sebastiana M, Figueiredo A, Acioli B, Sousa L, Pessoa F, Balde A, Pais MS (2009) Identification of plant genes involved on the initial contact between ectomycorrhizal symbionts (Castanea sativa – European chestnut and Pisolithus tinctorius). Eur J Soil Biol 45:275–282CrossRefGoogle Scholar
  79. Simon L, Bousquet J, Levesque RC, Lalonde M (1993) Origin and diversification of endomycorrhizal fungi and coincidence with vascular land plants. Natures 363:67–69CrossRefGoogle Scholar
  80. Slankis V (1950) Effect of naphthalene acetic acid on dichotomous branching of isolates roots of Pinus sylvestris. Physiol Plant 3:40–44CrossRefGoogle Scholar
  81. Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic, LondonGoogle Scholar
  82. 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 150:2018–2029PubMedCentralPubMedCrossRefGoogle Scholar
  83. Staswick PE, Serban B, Rowe M, Tiryaki I, Maldonado MT, Maldonado MC, Suza W (2005) Characterization of an arabidopsis enzyme family that conjugates amino acids to indole-3-acetic acid. Plant Cell 17:616–627PubMedCentralPubMedCrossRefGoogle Scholar
  84. Stepanova AN, Yun J, Likhacheva AV, Alonso JM (2007) Multilevel interactions between ethylene and auxin in Arabidopsis roots. Plant Cell 19:2169–2185PubMedCentralPubMedCrossRefGoogle Scholar
  85. Stracke S, Kistner C, Yoshida S, Mulder L, Sato S, Kaneko T, Tabata S, Sandal N, Stougaard J, Szczyglowski K, Parniske M (2002) A plant receptor-like kinase required for both bacterial and fungal symbiosis. Nature 417:959–962PubMedCrossRefGoogle Scholar
  86. Sun J, Xu Y, Ye S, Jiang H, Chen Q, Liu F, Zhou W, Chen R, Li X, Tietz O, Wu X, Cohen JD, Palme K, Li C (2009) Arabidopsis asa1 is important for jasmonate-mediated regulation of auxin biosynthesis and transport during lateral root formation. Plant Cell 21:1495–1511PubMedCentralPubMedCrossRefGoogle Scholar
  87. Swarup K, Benkova E, Swarup R, Casimiro I, Peret B, Yang Y, Parry G, Nielsen E, De Smet I, Vanneste S, Levesque MP, Carrier D, James N, Calvo V, Ljung K, Kramer E, Roberts R, Graham N, Marillonnet S, Patel K, Jones JD, Taylor CG, Schachtman DP, May S, Sandberg G, Benfey P, Friml J, Kerr I, Beeckman T, Laplaze L, Bennett MJ (2008) The auxin influx carrier LAX3 promotes lateral root emergence. Nat Cell Biol 10:946–954PubMedCrossRefGoogle Scholar
  88. Tagu D, De Bellis R, Balestrini R, De Vries OMH, Piccoli G, Stocchi V, Bonfante P, Martin F (2001) Immunolocalization of hydrophobin HYDPt-1 from the ectomycorrhizal basidiomycete Pisolithus tinctorius during colonization of Eucalyptus globulus roots tinctorius during colonization of Eucalyptus globulus roots. New Phytol 149:127–135CrossRefGoogle Scholar
  89. Taylor AFS (2002) Fungal diversity in ectomycorrhizal communities: sample efforts and species detection. Plant Soil 244:753–760CrossRefGoogle Scholar
  90. Terpstra I, Heidstra R (2009) Stem cells: the root of all cells. Semin Cell Dev Biol 20:1089–1096PubMedCrossRefGoogle Scholar
  91. Tranvan H, Habricot Y, Jeannette E, Gay G, Sotta B (2000) Dynamics of symbiotic establishment between an IAA-overproducing mutant of the ectomycorrhizal fungus Hebeloma cylindrosporum and Pinus pinaster. Tree Physiol 20:123–129PubMedCrossRefGoogle Scholar
  92. Umehara M, Hanada A, Yoshida S, Akiyama K, Arite T, Takeda-Kamiya N, Magome H, Kamiya Y, Shirasu K, Yoneyama K, Kyozuka J, Yamaguchi S (2008) Inhibition of shoot branching by new terpenoid plant hormones. Nature 455:195–200PubMedCrossRefGoogle Scholar
  93. Wallender H, Nylund JE, Sundberg B (1992) Ectomycorrhiza and nitrogen effects on root IAA: result contrary to current theory. Mycorrhiza 1:91–92CrossRefGoogle Scholar
  94. Wang JW, Wang LJ, Mao YB, Cai WJ, Xue HW, Chen XY (2005) Control of root cap formation by microRNA-targeted auxin response factors in Arabidopsis. Plant Cell 17:2204–2216PubMedCentralPubMedCrossRefGoogle Scholar
  95. Wessels JGH (1997) Hydrophobins: proteins that change the nature of the fungal surface. Adv Microb Physiol 38:1–45PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  • Judith Felten
    • 1
    • 2
  • Francis Martin
    • 1
  • Valérie Legué
    • 1
    Email author
  1. 1.UMR 1136 Interactions Arbres Micro-organismes, Centre INRA de NancyChampenouxFrance
  2. 2.Department of Forest Genetics and Plant Physiology, Umeå Plant Science CentreSwedish University of Agricultural SciencesUmeåSweden

Personalised recommendations