Abstract
For the ectomycorrhizal establishment, different signals must be exchanged between plants and fungal partners. After a brief description of the ectomycorrhiza formation, the present chapter highlights the recent works on the nature of the signal molecules involved in this type of plant–microbe interaction. Signals involved in the fungal spore germination and mycelium growth, including the chemoattraction of the mycelium by the root, hyphae–root adhesion, and penetration of the fungus into the root will be addressed. The signals associated to the development of ectomycorrhizal structures will also be overviewed. For the production of signals, formation of symbiotic structures (mantle and Hartig-net), and ectomycorrhizal functioning, a new pattern of gene expression and protein synthesis is required. Studies reporting the involvement of plant defense responses during the early stages of ectomycorrhiza development and the role of reactive oxygen species as signaling molecules will be reviewed.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Acioli-Santos B, Sebastiana M, Pessoa F, Sousa L, Figueiredo A, Fortes AM, Baldé A, Maia LC, Pais MS (2008) Fungal transcript pattern during the preinfection stage (12 h) of ectomycorrhiza formed between Pisolithus tinctorius and Castanea sativa roots, identified using cDNA microarrays. Curr Microbiol 57:620–625
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
Alvarez M, Huygens D, Fernandez C, Gacitúa Y, Olivares E, Saavedra I, Alberdi M, Valenzuela E (2009) Effect of ectomycorrhizal colonization and drought on reactive oxygen species metabolism of Nothofagus dombeyi roots. Tree Physiol 29:1047–1057
Baker CJ, Orlandi EW (1995) Active oxygen in plant pathogenesis. Annu Rev Phytopathol 33: 299–321
Baptista P, Martins A, Pais MS, Tavares RM, Lino-Neto T (2007) Involvement of reactive oxygen species during early stages of ectomycorrhiza establishment between Castanea sativa and Pisolithus tinctorius. Mycorrhiza 17:185–193
Barker SJ, Tagu D (2000) The roles of auxins and cytokinins in mycorrhizal symbioses. J Plant Growth Regul 19:144–154
Barker SJ, Tagu D, Delp G (1998) Regulation of root and fungal morphogenesis in mycorrhizal symbioses. Plant Physiol 116:1201–1207
Béguiristain T, 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 136:525–532
Béguiristain T, Côte R, Rubini P, Jay-Allemand C, Lapeyrie F (1995) Hypaphorine accumulation in the hyphae of the ectomycorrhizal fungus Pisolithus tinctorius. Phytochemistry 40: 1089–1091
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
Brunner I, Frey B (2000) Detection and localization of aluminum and heavy metals in ectomycorrhizal Norway spruce seedlings. Environ Pollut 108:121–128
Cairney J, Burke R (1994) Fungal enzymes degrading plant cell walls: their possible significance in the ectomycorrhizal symbiosis. Mycol Res 98:1345–1356
Carnero Diaz E, Martin F, Tagu D (1996) Eucalypt alpha-tubulin: cDNA cloning and increased level of transcripts in ectomycorrhizal root system. Plant Mol Biol 31:905–910
Critchley DR, Holt MR, Barry ST, Priddle H, Hemmings L, Norman J (1999) Integrin-mediated cell adhesion: the cytoskeletal connection. Biochem Soc Symp 65:6579–6599
Ditengou F, 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. MPMI 13:151–158
Ditengou F, Béguiristain 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 211:722–728
Ditengou F, 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 218:217–225
Dixon RA, Lamb CJ (1990) Molecular communication in interactions between plants and microbial pathogens. Annu Rev Plant Physiol Plant Mol Biol 41:339–367
Doke N, Miura Y, Sanchez LM, Park H-J, Noritake T, Yoshioka H, Kawakita K (1996) The oxidative burst protects plants against pathogen attack: mechanism and role as an emergency signal for plant bio-defence – a review. Gene 179:45–51
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
Duplessis S, Courty P-E, Tagu D, Martin F (2005) Transcript patterns associated with ectomycorrhiza development in Eucalyptus globulus and Pisolithus microcarpus. New Phytol 165: 599–611
Feugey L, Strullu D-G, Poupard P, Simoneau P (1999) Induced defence responses limit Hartig-net formation in ectomycorrhizal birch roots. New Phytol 144:541–547
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
Fries N, Serck-Hanssen K, Hall-Dimberg L, Theander O (1987) Abietic acid, an activator of basidiospore germination in ectomycorrhizal species of the genus Suillus (Boletaceae). Exp Mycol 11:360–363
Davies FT Jr, Svenson SE, Cole JC, Phavaphutanon L, Duray SA, Olalde-Portugal V, Meier CE, Bo SH (1996) Non-nutritional stress acclimation of mycorrhizal woody plants exposed to drought. Tree Physiol 16:985–993
Futai K, Taniguchi T, Kataoka R (2008) Ectomycorrhizae and their importance in forest ecosystems. In: Mycorrhizae: sustainable agriculture and forestry. Springer, Netherlands, pp 241–285
Gay G, Normand L, Marmeisse R, Sotta B, Debaud JC (1994) Auxin overproducer mutants of Hebeloma cylindrosporum Romagnesi have increased mycorrhizal activity. New Phytol 128:645–657
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
Gross E, Casagrande LIT, Caetano FH (2004) Ultrastructural study of ectomycorrhizas on Pinus caribaea Morelet. var. hondurensis Barr. & Golf. seedlings. Acta Botanica Brasilica 18:1–7
Hebe G, Hager A, Salzer P (1999) Initial signalling processes induced by elicitors of ectomycorrhiza-forming fungi in spruce cells can also be triggered by G-protein-activating mastoparan and protein phosphatase-inhibiting cantharidin. Planta 207:418–425
Heller G, Adomas A, Li G, Osborne J, van Zyl L, Sederoff R, Finlay R, Stenlid J, Asiegbu F (2008) Transcriptional analysis of Pinus sylvestris roots challenged with the ectomycorrhizal fungus Laccaria bicolour. BMC Plant Biol 8:19
Horan DP, Chilvers GA (1990) Chemotropism: the key to ectomycorrhizal formation? New Phytol 116:297–301
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 123:120–129
Johansson T, Le Quéré A, Ahren D, Söderström B, Erlandsson R, Lundeberg J, Uhlén M, Tunlid A (2004) Transcriptional responses of Paxillus involutus and Betula pendula during formation of ectomycorrhizal root tissue. MPMI 17:202–215
Karabaghli-Degron C, Sotta B, Bonnet M, Gay G, Le Tacon F (1998) The auxin transport inhibitor 2,3,5-triidobenzoic acid (TIBA) inhibits the stimulation of in vitro lateral root formation and the colonization of the tap-root cortex of Norway spruce (Picea abies) seedlings by the ectomycorrhizal fungus Laccaria bicolor. New Phytol 140:723–733
Kaska DD, Myllylä R, J.B C (1999) Auxin transport inhibitors act through ethylene to regulate dichotomous branching of lateral root meristems in pine. New Phytol 142:49–58
Kershaw MJ, Talbot NJ (1998) Hydrophobins and repellents: proteins with fundamental roles in fungal morphogenesis. Fungal Genet Biol 23:18–33
Kim S-J, Hiremath ST, Podila GK (1999) Cloning and identification of symbiosis-regulated genes from the ectomycorrhizal Laccaria bicolor. Mycol Res 103:168–172
Krüger A, Peskan-Berghöfer T, Frettinger P, Herrmann S, Buscot F, Oelmüller R (2004) Identification of premycorrhiza-related plant genes in the association between Quercus robur and Piloderma croceum. New Phytol 163:149–157
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
Lamb C, Dixon RA (1997) The oxidative burst in plant disease resistance. Annu Rev Plant Physiol Plant Mol Biol 48:251–275
Laurent P, Voiblet C, Tagu D, 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. MPMI 12:862–871
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. MPMI 18:659–673
Lei J, Ding H, Lapeyrie F, Piché Y, Malajczuk N, Dexheimer J (1990a) Ectomycorrhizal formation on the roots of Eucalyptus globulus and Pinus caribaea with two isolates of Pisolithus tinctorius: structural and cytochemical observations. In: Nardon P, Gianinazzi-Pearson V, Greiner AM, Margulis L, Smith DC (eds) Endocytobiology, vol IV. INRA, Paris, France, pp 123–126
Lei J, Lapeyrie F, Malajczuk N, Dexheimer J (1990b) Infectivity of pine and eucalypt isolates of Pisolithus tinctorius (Pers.) Coker & Couch on roots of Eucalyptus urophylla S.T. Blake in vitro. II. Ultrastructural and biochemical changes at the early stage of mycorrhiza formation. New Phytol 116:115–122
Linder MB, Szilvay GR, Nakari-Setälä TN, Penttilä ME (2005) Hydrophobins: the protein-amphiphiles of filamentous fungi. FEMS Microbiol Rev 29:877–896
Mankel A, Krause K, Kothe E (2002) Identification of a hydrophobin gene that is developmentally regulated in the ectomycorrhizal fungus Tricholoma terreum. Appl Environ Microbiol 68:1408–1413
Martin F, Tagu D (1995) Ectomycorrhiza development: a molecular perspective. In: Varma A, Hock B (eds) Mycorrhiza: structure, function, molecular biology and biotechnology. Springer, Berlin, pp 30–58
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
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 151:145–154
Martin F, Kohler A, Duplessis S (2007) Living in harmony in the wood underground: ectomycorrhizal genomics. Curr Opin Plant Biol 10:204–210
Marx DH (1972) Ectomycorrhizae as biological deterrents to pathogenic root infections. Annu Rev Phytopathol 10:429–454
Matevž L, Regvar M (2008) Early defence reactions in Norway spruce seedlings inoculated with the mycorrhizal fungus Pisolithus tinctorius (Persoon) Coker & Couch and the pathogen Heterobasidion annosum. Trees Struct Funct 22:861–868
Mehdy M, Sharma YK, Sathasivan K, Bays NW (1996) The role of activated oxygen species in plant disease resistance. Physiol Plant 98:365–374
Meinhardt SW, Cheng W, Kwon SY, Donohue CM, Rasmussen JB (2002) Role of the Arginyl-Glycyl-Aspartic motif in the action of Ptr ToxA produced by Pyrenophora tritici-repentis. Plant Physiol 130:1545–1551
Mellersh DG, Heath MC (2001) Plasma membrane–cell wall adhesion is required for expression of plant defence responses during fungal penetration. Plant Cell 13:413–424
Menotta M, Amicucci A, Sisti D, Gioacchini AM, Stocchi V (2004) Differential gene expression during pre-symbiotic interaction between Tuber borchii Vittad. and Tilia americana L. Curr Genet 46:158–165
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 102:539–546
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
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
Osonubi O, Mulongoy K, Awotoye OO, Atayese MO, Okali DUU (1991) Effects of ectomycorrhizal and vesicular-arbuscular mycorrhizal fungi on drought tolerance of four leguminous woody seedlings. Plant Soil 136:131–143
Peter M, Courty P-E, Kohler A, Delaruelle C, Martin D, Tagu D, Frey-Klett P, Duplessis S, Chalot M, Podila G, Martin F (2003) Analysis of expressed sequence tags from the ectomycorrhizal basidiomycetes Laccaria bicolor and Pisolithus microcarpus. New Phytol 159:117–129
Peterson RL, Bonfante P (1994) Comparative structure of vesicular-arbuscular mycorrhizas and ectomycorrhizas. Plant Soil 159:79–88
Podila GK (2002) Signalling in mycorrhizal symbioses – elegant mutants lead the way. New Phytol 154:541–545
Podila GK, Zheng J, Balasubramanian S, Sundaram S, Hiremath S, Brand JH, Hymes MJ (2002) Fungal gene expression in early symbiotic interactions between Laccaria bicolor and red pine. Plant Soil 244:117–128
Rincón A, Gérard J, Dexheimer J, Le Tacon F (2001) Effect of an auxin transport inhibitor on aggregation and attachment process during ectomycorrhiza formation between Laccaria bicolor S238N and Picea abies. Can J Bot 79:1152–1160
Salzer P, Hebe G, Reith A, Zitterell-Haid 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
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
Salzer P, Hübner 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
Sauter M, Hager A (1989) The mycorrhizal fungus Amanita muscaria induces chitinase activity in roots and in suspension-cultured cells of its host Picea abies. Planta 179:61–66
Schwacke R, Hager A (1992) Fungal elicitors induce a transient release of active oxygen species from cultured spruce cells that is dependent on Ca2+ and protein-kinase activity. Planta 187:136–141
Sebastiana M, Figueiredo A, Acioli B, Sousa L, Pessoa F, Baldé 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 45:275–282
Sirrenberg A, Salzer P, Hager A (1995) Induction of mycorrhiza-like structures and defence reactions in dual cultures of spruce callus and ectomycorrhizal fungi. New Phytol 130:149–156
Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic Press, London
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. MPMI 14:618–628
Tagu D, Nasse B, Martin F (1996) Cloning and characterization of hydrophobins-enconding cDNAs from the ectomycorrhizal basidiomycete Pisolithus tinctorius. Gene 168:93–97
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. New Phytol 149: 127–135
Tagu D, Lapeyrie F, Martin F (2002) The ectomycorrhizal symbiosis: genetics and development. Plant Soil 244:97–105
Timonen S, Peterson RL (2002) Cytoskeleton in mycorrhizal symbiosis. Plant Soil 244:199–210
Timonen S, Finlay RD, Söderström B, Raudaskoski M (1993) Identification of cytoskeletal components in pine ectomycorrhizas. New Phytol 124:83–92
Timonen S, Söderström B, Raudaskoski M (1996) Dynamics of cytoskeletal proteins in developing pine ectomycorrhiza. Mycorrhiza 5:423–429
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
Weiss M, Mikolajewski S, Peipp H, Schmitt U, Schmidt J, Wray V, Strack D (1997) Tissue-specific and development-dependent accumulation of phenylpropanoids in Larch Mycorrhizas. Plant Physiol 114:15–27
Weiss M, Schmidt J, Neumann D, Wray V, Christ R, Strack D (1999) Phenylpropanoids in mycorrhizas of the Pinaceae. Planta 208:491–502
Wessels JGH (1996) Fungal hydrophobins: proteins that function at an interface. Trends Plant Sci 1:9–15
Wösten HAB (2001) Hydrophobins: multipurpose proteins. Annu Rev Microbiol 55:625–646
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2011 Springer Berlin Heidelberg
About this chapter
Cite this chapter
Baptista, P., Tavares, R.M., Lino-Neto, T. (2011). Signaling in Ectomycorrhizal Symbiosis Establishment. In: Rai, M., Varma, A. (eds) Diversity and Biotechnology of Ectomycorrhizae. Soil Biology, vol 25. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-15196-5_8
Download citation
DOI: https://doi.org/10.1007/978-3-642-15196-5_8
Published:
Publisher Name: Springer, Berlin, Heidelberg
Print ISBN: 978-3-642-15195-8
Online ISBN: 978-3-642-15196-5
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)