Skip to main content
Springer Nature Link
Log in

Communication and Signaling in the Plant–Fungus Symbiosis: The Mycorrhiza

  • Chapter
  • First Online:
Plant-Environment Interactions

Part of the book series: Signaling and Communication in Plants ((SIGCOMM))

  • 2363 Accesses

  • 15 Citations

Abstract

The study of symbiotic mycorrhizal associations is of fundamental and practical interest, raising questions about not only interorganism coevolution but also the ecological significance of the symbiosis in sustainable plant production systems. The partners in these associations belong to the Basidiomycota, Ascomycota or Glomeromycota, and about 95% of extant land plants. Successful colonization of roots by mycorrhizal fungi and subsequent effects on plant processes depend on recognition processes resulting from coordinated genetic programs in both partners and must be driven, at each stage, by reciprocal signaling events. This chapter summarizes current knowledge on communication and signaling in the two most frequent mycorrhizal associations: arbuscular mycorrhiza and ectomycorrhiza.

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

Access this chapter

Log in via an institution

Institutional subscriptions

Similar content being viewed by others

References

  • Akiyama K, Hayashi H (2006) Strigolactones: chemical signals for fungal symbionts and parasitic weeds in plant roots. Ann Bot 97:925–931

    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, Geurts R, Lapeyrie F, Bisseling T (1998) Endomycorrhizae and rhizobial Nod factors both require SYM8 to induce the expression of the early nodulin genes PsENOD5 and PsENOD12A. Plant J 15:605–614

    CAS  Google Scholar 

  • Allen MF, Moore TS, Christensen M (1982) Phytohormone changes in Bouteloua gracilis infected by vesicular-arbuscular mycorrhizae. II. Altered levels of gibberellin-like substances and abscisic acid in the host plant. Can J Bot 60:468–471

    CAS  Google Scholar 

  • Ané J-M, Kiss GB, Riely BK, Penmetsa RV, Oldroyd GED, Ayax C, Lévy J, Debellé F, Baek J-M, Kalo P, Rosenberg C, Roe BA, Long SR, Dénarié J, Cook DR (2004) Medicago truncatula DMI1 required for bacterial and fungal symbioses in legumes. Science 303:1364–1367

    PubMed  Google Scholar 

  • Axelrod DI (1986) Ceoconic history of some western American pines. Ann Bot Gard 73:565–641

    Google Scholar 

  • Balestrini R, Lanfranco L (2006) Fungal and plant gene expression in arbuscular mycorrhizal symbiosis. Mycorrhiza 16:509–524

    PubMed  CAS  Google Scholar 

  • Barlow PW, Baluska F (2000) Cytoskeletal, perspectives on root growth and morphogenesis. Ann Rev Plant Physiol Plant Mol Biol 51:289–322

    CAS  Google Scholar 

  • Bécard G, Douds DD, Pfeffer PE (1992) Extensive hyphal growth of vesicular-arbuscular mycorrhizal fungi in the presence of CO2 and flavonols. Appl Environ Microbiol 58:821–825

    PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Benedito V, Torez-Jerez I, Murray J, Andriankaja A, Allen S, Kakar K, Wandrey M, Verdier J, Zuber H, Ott T, et al. (2008) A gene expression atlas of the model legume Medicago truncatula. Plant J 55:504–513

    PubMed  CAS  Google Scholar 

  • Benjdia M, Rikirsch E, Müller T, Morel M, Zimmermann S, Chalot M, Frommer WB, Wipf D (2006) Peptide uptake in the ectomycorrhizal fungus Hebeloma cylindrosporum: characterization of two di- and tripeptide transporters (HcPTR2A and B). New Phytol 170:401–410

    PubMed  CAS  Google Scholar 

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

    PubMed  Google Scholar 

  • Bick JA, Lange BM (2003) Metabolic cross talk between cytosolic and plastidial pathways of isoprenoid biosynthesis: unidirectional transport of intermediates across the chloroplast envelope membrane. Arch Biochem Biophys 415:146–154

    PubMed  CAS  Google Scholar 

  • Bothe H, Klingner A, Kaldorf M, Schmitz O, Esch H, Hundeshagen B, Kernebeck H (1994) Biochemical approaches to the study of plant–fungal interactions in arbuscular mycorrhiza. Experientia 50:919–925

    CAS  Google Scholar 

  • Bouwmeester HJ, Roux C, Lopez-Raez JA, Bécard G (2007) Rhizosphere communication of plants, parasitic plants and AM fungi. Trends Plant Sci 12:224–230

    PubMed  CAS  Google Scholar 

  • Breuninger M, Requena N (2004) Recognition events in AM symbiosis: analysis of fungal gene expression at the early appressorium stage. Fungal Gen Biol 41:794–804

    CAS  Google Scholar 

  • Brundrett M, Bougher N, Dell B, Grove T, Malajczuk N (1996) Working with mycorrhizas in forestry and agriculture. Australian Centre for International Agricultural Research, Canberra

    Google Scholar 

  • Buée M, Rossignol M, Jauneau A, Ranjeva R, Bécard G (2000) The presymbiotic growth of arbuscular mycorrhizal fungi is induced by a branching factor partially purified from plant root exudates. Mol Plant Microbe Interact 13:693–698

    PubMed  Google Scholar 

  • Bücking H, Abubaker J, Govindarajulu M, Tala M, Pfeffer PE, Hagahashi G, Lammers P, Shachar-Hill Y (2008) Root exudates stimulate the uptake and metabolism of organic carbon in germinating spores of Glomus intraradices. New Phytol (in press)

    Google Scholar 

  • Cairney JW (2000) Evolution of mycorrhiza systems. Naturwissenschaften 87:467–475

    PubMed  CAS  Google Scholar 

  • Catford JG, Staehelin C, Larose G, Piche 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 

  • Chabaud M, Venard C, Defaux-Petras A, Bécard G, Barker DG (2002) Targeted inoculation of Medicago truncatula in vitro root cultures reveals MtENOD11 expression during early stages of infection by arbuscular mycorrhizal fungi. New Phytol 156:265–273

    CAS  Google Scholar 

  • Chappell J (2002) The genetics and molecular genetics of terpene and sterol origami. Curr Opin Plant Biol 5:151–157

    PubMed  CAS  Google Scholar 

  • Dakora FD, Phillips DA (2002) Root exudates as mediators of mineral acquisition in low-nutrient environments. Plant Soil 245:35–47

    CAS  Google Scholar 

  • David-Schwartz R, Badani H, Smadar W, Levy AA, Galili G, Kapulnik Y (2001) Identification of a novel genetically controlled step in mycorrhizal colonization: plant resistance to infection by fungal spores but not extra-radical hyphae. Plant J 27:561–569

    PubMed  CAS  Google Scholar 

  • David-Schwartz R, Gadkar V, Wininger S, Bendov R, Galili G, Levy AA, Kapulnik Y (2003) Isolation of a premycorrhizal infection (pmi2) mutant of tomato, resistant to arbuscular mycorrhizal fungal colonization. Mol Plant Microbe Interact 16:382–388

    PubMed  CAS  Google Scholar 

  • Dénarié J, Debellé F, Promé JC (1996) Rhizobium lipochitooligosaccharide nodulation factors: signaling molecules mediating recognition and morphogenesis. Ann Rev Biochem 65:503–535

    PubMed  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 

  • Divon HH, Fluhr R (2001) Nutrition acquisition strategies during fungal infection of plants. FEMS Microbiol Lett 266:65–74

    Google Scholar 

  • Duc G, Trouvelot A, Gianinazzi-Pearson V, Gianinazzi S (1989) First report of non-mycorrhizal plant mutants (Myc–) obtained in pea (Pisum sativum L.) and fababean (Vicia faba L.). Plant Sci 60:215–222

    Google Scholar 

  • Dudareva N, Negre F (2005) Practical applications of research into the regulation of plant volatile emission. Curr Opin Plant Biol 8:113–118

    PubMed  CAS  Google Scholar 

  • Dumas-Gaudot E, Gollotte A, Cordier C, Gianinazzi S, Gianinazzi-Pearson V (2000) Modulation of host defense system. In: Douds D, Kapulnik Y (eds) Arbuscular mycorrhizas: molecular biology and physiology. Kluwer, Boston, MA, pp 173–200

    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 

  • Endre G, Kereszt A, Kevei Z, Mihacea S, Kalo P, Kiss GB (2002) A receptor kinase gene regulating symbiotic nodule development. Nature 417:962–966

    PubMed  CAS  Google Scholar 

  • Fester T (2008) Plastid reorganization in arbuscular mycorrhizal roots. In: Schoefs B (ed) Plant cell compartments. Selected Topics Research Signpost, Trivandrum 338–345.

    Google Scholar 

  • Fester T, Hause B (2005) Accumulation of reactive oxygen species in arbuscular mycorrhizal roots. Mycorrhiza 15:373–379

    PubMed  CAS  Google Scholar 

  • Fester T, Hause B, Schmidt D, Halfmann K, Schmidt J, Wray V, Hause G, Strack D (2002a) Occurrence and localization of apocarotenoids in arbuscular mycorrhizal plant roots. Plant Cell Physiol 43:256–265

    CAS  Google Scholar 

  • Fester T, Schmidt D, Lohse S, Walter MH, Giuliano G, Bramley PM, Fraser PD, Hause B, Strack D (2002b) Stimulation of carotenoid metabolism in arbuscular mycorrhizal roots. Planta 216:148–154

    CAS  Google Scholar 

  • Floß DS, Hause B, Lange PR, Küster H, Strack D, Walter MH (2008) Knock-down of the MEP pathway isogene 1-deoxy-D-xylulose 5-phosphate synthase 2 inhibits formation of arbuscular mycorrhiza-induced apocarotenoids, and abolishes normal expression of mycorrhiza-specific plant marker genes. Plant J 56:86–100

    PubMed  Google Scholar 

  • Fransson PM, Taylor AF, Finlay RD (2000) Effects of continuous optimal fertilization on belowground ectomycorrhizal community structure in a Norway spruce forest. Tree Physiol 20:599–606

    PubMed  Google Scholar 

  • Frettinger P, Derory J, Herrmann S, Plomion C, Lapeyrie F, Oelmu ller R, Martin F, Buscot F (2007) Transcriptional changes in two types of pre-mycorrhizal roots and in ectomycorrhizas of oak microcuttings inoculated with Piloderma croceum. Planta 225:331–340

    PubMed  CAS  Google Scholar 

  • Fries N, Serck-Hanssen K, Häll 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

    Google Scholar 

  • Fromm J, Lautner S (2007) Electrical signals and their physiological significance in plants. Plant Cell Environ 30:249–257

    PubMed  CAS  Google Scholar 

  • Gadkar V, David-Schwartz R, Nagahashi G, Douds DD, Wininger S, Kapulnik Y (2003) Root exudate of pmi tomato mutant M161 reduces AM fungal proliferation in vitro. FEMS Microbiol Lett 223:193–198

    PubMed  CAS  Google Scholar 

  • Garcia-Garrido JM, Ocampo JA (2002) Regulation of the plant defence response in arbuscular mycorrhzal symbiosis. J Exp Bot 53:1377–1386

    PubMed  CAS  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 128:645–657

    CAS  Google Scholar 

  • Genre A, Chabaud M, Timmers T, Bonfante P, Barker DG (2005) Arbuscular mycorrhizal fungi elicit a novel intracellular apparatus in Medicago truncatula root epidermal cells before infection. Plant Cell 17:3489–3499

    PubMed  CAS  Google Scholar 

  • Gianinazzi-Pearson V (1996) Plant cell responses to arbuscular mycorrhizal fungi: getting to the roots of the symbiosis. Plant Cell 8:1871–1883

    PubMed  Google Scholar 

  • Gianinazzi-Pearson V, Branzanti B, Gianinazzi S (1989) In vitro enhancement of spore germination and hyphal growth of a vesicular-arbuscular mycorrhizal fungus by host root exudates and plant flavonoids. Symbiosis 7:243–255

    CAS  Google Scholar 

  • Gianinazzi-Pearson V., Tollot M., Seddas P. Dissection of genetic cell programmes driving early arbuscular mycorrhiza interactions. In: Mycorrhizas: functional processes and ecological impacts, Springer Verlag, Heidelberg (in press)

    Google Scholar 

  • Gianinazzi-Pearson V, Weidmann S, Seddas P, Massoumou M, van Tuinen D, Gianinazzi S (2006) Signal-related gene responses in beneficial root interactions with non-rhizobial microorganisms. In: Sanchez F, Quinto C, Geiger O (eds) Biology of plant–microbe interactions, vol 5. IS-MPMI, St. Paul, MN, pp 516–524

    Google Scholar 

  • Gianinazzi-Pearson V, Séjalon-Delmas N, Genre A, Jeandroz S, Bonfante P (2007) Plants and arbuscular mycorrhizal fungi: cues and communication in the early steps of symbiotic interactions. Adv Bot Res 46:181–219

    Google Scholar 

  • Giovannetti M, Sbrana C, Avio L, Citernesi AS (1993) Factors affecting appressorium development in the vesicular-arbuscular mycorrhizal fungus Glomus mosseae. New Phytol 123:114–122

    Google Scholar 

  • Giovannetti M, Sbrana C, Logi C (1994) Early processes involved in host recognition by arbuscular mycorrhizal fungi. New Phytol 127:703–709

    Google Scholar 

  • Godt DE, Roitsch T (1997) Regulation and tissue-specific distribution of mRNAs for three extracellular invertase isoenzymes of tomato suggests an important function in establishing and maintaining sink metabolism. Plant Physiol 115:273–282

    PubMed  CAS  Google Scholar 

  • Gogala N (1991) Regulation of mycorrhizal infection by hormonal factors produced by hosts and fungi. Experimentia 47:331–339

    CAS  Google Scholar 

  • Gollotte A, Gianinazzi-Pearson V, Giovannetti M, Sbrana C, Avio L, Gianinazzi S (1993) Cellular localization and cytochemical probing of resistance reactions to arbuscular mycorrhizal fungi in a "locus A" myc– mutant of Pisum sativum (L.). Planta 191:112–122

    CAS  Google Scholar 

  • Hanif M (2004) Characterization of small GTPase Cdc42 from the ectomycorrhizal fungus Suillus bovinus and Agrobacterium tumefaciens-mediated transformation of fungi. Dissertation, University of Helsinki, Finland

    Google Scholar 

  • Harrison MJ (1998) Development of the arbuscular mycorrhizal symbiosis. Curr Opin Plant Biol 1:360–365

    PubMed  CAS  Google Scholar 

  • Harrison MJ (2005) Signaling in the arbuscular mycorrhizal symbiosis. Annu Rev Microbiol 59:19–42

    PubMed  CAS  Google Scholar 

  • Hause B, Fester T (2005) Molecular and cell biology of arbuscular mycorrhizal symbiosis. Planta 221:184–196

    PubMed  CAS  Google Scholar 

  • Hause B, Maier W, Miersch O, Kramell R, Strack C (2002) Induction of jasmonate biosynthesis in arbuscular mycorhizal barley roots. Plant Physiol 130:1213–1220

    PubMed  CAS  Google Scholar 

  • Hause B, Mrosk C, Isayenkov S, Strack D (2007) Jasmonates in arbuscular mycorrhizal interactions. Phytochemistry 68(1):101–110

    PubMed  CAS  Google Scholar 

  • Hedden P, Phillips AI (2000) Gibberellin metabolism: new insights revealed by the genes. Trends Plant Sci 5:523–530

    PubMed  CAS  Google Scholar 

  • Helliwell CA, Sullivan JA, Mould RM, Gray JC, Peacock WJ, Dennis ES (2001) A plastid envelope location of Arabidopsis ent-kaurene oxidase links the plastids to the endoplasmic reticulum steps of the gibberellin biosynthesis pathway. Plant J 28:201–208

    PubMed  CAS  Google Scholar 

  • Herrmann S, Buscot F (2007) Cross talks at the morphogenetic, physiological and gene regulation levels between the mycobiont Piloderma croceum and oak microcuttings (Quercus robur) during formation of ectomycorrhizas. Phytochemistry 68:52–67

    PubMed  CAS  Google Scholar 

  • Horan DP, Chilvers GA (1990) Chemotropism; the key to ectomycorrhizal formation? New Phytol 116:297–301

    CAS  Google Scholar 

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

    Google Scholar 

  • Humphrey AJ, Beale MH (2006) Strigol: biosynthesis and physiological activity. Phytochemistry 67:636–640

    PubMed  CAS  Google Scholar 

  • Imaizumi-Anraku H, Takeda N, Charpentier M, Perry J, Miwa H, Umehara Y, Kouchi H, Murakami Y, Mulder L, Vickers K, Pike J, Downie JA, Wang T, Sato S, Asamizu E, Tabata S, Yoshikawa M, Murooka Y, Wu GJ, Kawaguchi M, Kawasaki S, Parniske M, Hayashi M (2005) Plastid proteins crucial for symbiotic fungal and bacterial entry into plant roots. Nature 433:527–531

    PubMed  CAS  Google Scholar 

  • Isayenkov S, Mrosk C, Stenzel I, Strack D, Hause B (2005) Suppression of allele oxide cyclase in hairy roots of Medicago truncatula reduces jasmonate levels and the degree of mycorrhization with Glomus intraradices. Plant Physiol 139:1401–1410

    PubMed  CAS  Google Scholar 

  • Jacobi LM, Zubkova LA, Barmicheva EM, Tsyganov VE, Borisov AY, Tikhonovich IA (2003) Effect of mutations in the pea genes Sym33 and Sym40 II. Dynamics of arbuscule development and turnover. Mycorrhiza 13:9–16

    CAS  Google Scholar 

  • Javot H, Pemetsa RV, Terzaghi N, Cook DR, Harrisson 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 

  • Jones DL, Hodge A, Kuzyakov Y (2004) Plant and mycorrhizal regulation of rhizodeposition. New Phytol 163:459–480

    CAS  Google Scholar 

  • Kanamori N, Madsen LH, Radutoiu S, Frantescu M, Quistgaard EMH, Miwa H, Downie JA, James EK, Felle HH, Haaning LL, Jensen TH, Sato S, Nakamura Y, Tabata S, Sandal N, Stougaard J (2006) A nucleoporin is required for induction of Ca2+ spiking in legume nodule development and essential for rhizobial and fungal symbiosis. Proc Natl Acad Sci USA 103:359–364

    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 140:723–733

    CAS  Google Scholar 

  • Karandashov V, Bucher M (2005) Symbiotic phosphate transport in arbuscular mycorrhizas. Trends Plant Sci 10:22–29

    PubMed  CAS  Google Scholar 

  • Karandashov V, Nagy R, Wegmuller S, Amrhein N, Bucher M (2004) Evolutionary conservation of a phosphate transporter in the arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci USA 101:6285–6290

    PubMed  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 142:49–58

    CAS  Google Scholar 

  • Klingner A, Bothe H, Wray V, Marner FJ (1995a) Identification of a yellow pigment formed in maize roots upon mycorrhizal colonization. Phytochemistry 38:53–55

    CAS  Google Scholar 

  • Klingner A, Hundeshagen B, Kernebeck H, Bothe H (1995b) Localization of the yellow pigment formed in roots of gramineous plants colonized by arbuscular fungi. Protoplasma 185:50–57

    CAS  Google Scholar 

  • Kosuta S, Chabaud M, Lougnon G, Gough C, Dénarie J, Barker DG, Bécard G (2003) A diffusible factor from arbuscular mycorrhizal fungi induces symbiosis-specific MtENOD11 expression in roots of Medicago truncatula. Plant Physiol 131:952–962

    PubMed  CAS  Google Scholar 

  • Kosuta S, Hazledine S, Sun J, Miwa H, Morris RJ, Downie JA, Oldroyd GED (2008) Differential and chaotic calsium signatures in the symbiosis signalling pathway of legumes. Proc Nat Acad Sci USA 105:9823–9828

    PubMed  CAS  Google Scholar 

  • Kottke I, Oberwinkler F (1987) The cellular structure of Hartig net: coenocytic and transfer cell-like organisation. Nord J Bot:85–95

    Google Scholar 

  • Krings M, Taylor TN, Hass H, Kerp H, Dozler N, Hermsen EJ (2007) Fungal endophytes in a 400-million-yr-old land plant: infection pathways, spatial distribution, and host responses. New Phytol 174:648–657

    PubMed  Google Scholar 

  • Kruger A, Peskan-Berghofer T, Frettinger P, Herrmann S, Buscot F, Oelmuller R (2004) Identification of premycorrhiza-related plant genes in the association between Quercus robur and Piloderma croceum. New Phytol 163:149–157

    Google Scholar 

  • Kuwada K, Kuramoto M, Utamura M, Matsushita I, Shibata Y, Ishii T (2005) Effect of mannitol from Laminaria japonica, other sugar alcohols, and marine alga polysaccharides on in vitro hyphal growth of Gigaspora margarita and root colonization of trifoliate orange. Plant Soil 276:279–286

    CAS  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 150:349–355

    Google Scholar 

  • Lanfranco L, Novero M, Bonfante P (2005) The mycorrhizal fungus Gigaspora margarita possesses a Cu/Zn superoxide dismutase that is up-regulated during symbiosis with legume hosts. Plant Physiol 137:1319–1330

    PubMed  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Lemoine Y, Rmiki N-E, Créach A, Rachidi J, Schoefs B (2008) Cytoplasmic accumulation of astaxanthin by the green alga Haematococcus pluvialis (flotow). In: Schoefs B (ed) Plant cell compartments. Selected Topics Research Signpost. Trivandrum 251–284

    Google Scholar 

  • Le Quéré A, Schutzendubel A, Rajashekar B, Canback B, Hedh J, Erland S, Johansson T, Tunlid A (2004) Divergence in gene expression related to variation in host specificity of an ectomycorrhizal fungus. Mol Ecol 13:3809–3819

    PubMed  Google Scholar 

  • Le Quéré A, Wright D, 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 Quéré A, Eriksen KA, Rajashekar B, Schutzenbubel A, Canback B, Johansson T, Tunlid A (2006) Screening for rapidly evolving genes in the ectomycorrhizal fungus Paxillus involutus using cDNA microarrays. Mol Ecol 15:535–550

    PubMed  Google Scholar 

  • Lévy J, Bres C, Geurts R, Chalhoub B, Kulikova O, Duc G, Journet E-P, Ané J-M, Lauber E, Bisseling T, Dénarié J, Rosenberg C, Debellé F (2004) A putative Ca2+ and calmodulin-dependent protein kinase required for bacterial and fungal symbioses. Science 303:1361–1364

    PubMed  Google Scholar 

  • Liu J, Maldonado-Mendoza I, Lopez-Meyer M, Cheung F, Town CD, Harrison MJ (2007) Arbuscular mycorrhizal symbiosis is accompanied by local and systemic alterations in gene expression and an increase in disease resistance in the shoots. Plant J 50:529–544

    PubMed  CAS  Google Scholar 

  • Lohse S, Schliemann W, Ammer C, Kopka J, Strack D, Fester T (2005) Organization and metabolism of plastids and mitochondria in arbuscular mycorrhizal roots of Medicago truncatula. Plant Physiol 139:329–340

    PubMed  CAS  Google Scholar 

  • Maier W, Peipp H, Schmidt J, Wray V, Strack D (1995) Levels of a terpenoid glycoside (blumenin) and cell wall-bound phenolics in some cereal mycorrhizas. Plant Physiol 109:465–470

    PubMed  CAS  Google Scholar 

  • Marsh J, Schultze M (2001) Analysis of arbuscular mycorrhizas using symbiosis-defective plant mutants. New Phytol 150:525–532

    Google Scholar 

  • 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

    CAS  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, Ahren D, Brun A, Danchin EGJ, Duchaussoy F, Gibon, Kohler A, Lindquist E, Pereda V, et al. (2008) The genome of Laccaria bicolor provides insights into mycorrhizal symbiosis. Nature 452:88–97

    PubMed  CAS  Google Scholar 

  • Matusova R, Rani K, Verstappen FWA, Franssen MCR, Beale MH, Bouwmeester HJ (2005) The strigolactone germination stimulants of the plant-parasitic Striga and Orobanche spp. are derived from the carotenoid pathway. Plant Physiol 139:920–934

    CAS  Google Scholar 

  • Meixner C, Ludwig-Muller 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 

  • 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

    CAS  Google Scholar 

  • Menotta M, Pierleoni R, Amicucci A, Sisti D, Cerasi A, Millo E, Chiarantini L, Stocchi V (2006) Characterization and complementation of a Fus3/Kss1 type MAPK from Tuber borchii, TBMK. Mol Genet Genom 276:126–134

    CAS  Google Scholar 

  • Menotta M, Amicucci A, Basili G, Polidori E, Stocchi V, Rivero F (2008) Molecular and functional characterization of a Rho GDP dissociation inhibitor in the filamentous fungus Tuber borchii. BMC Microbiol 8:57

    PubMed  Google Scholar 

  • Mitra RM, Gleason CA, Edwards A, Hadfield J, Downie JA, Oldroyd GED, Long SR (2004) A Ca2+/calmodulin-dependent protein kinase required for symbiotic nodule development: gene identification by transcript-based cloning. Proc Natl Acad Sci USA 101:4701–4705

    PubMed  CAS  Google Scholar 

  • Moller SG, Chua NH (1999) Interactions and intersections of plant signaling pathays. J Mol Biol 293:219–234

    PubMed  CAS  Google Scholar 

  • Morandi D, Prado E, Sagan M, Duc G (2005) Characterisation of new symbiotic Medicago truncatula (Gaertn.) mutants, and phenotypic or genotypic complementary information on previously described mutants. Mycorrhiza 15:283–289

    PubMed  Google Scholar 

  • Müller T, Avolio M, Olivi M, Benjdia M, Rikirsch E, Kasaras A, Fitz M, Chalot M, Wipf D (2007) Organic nitrogen transport in the ectomycorrhiza on the basis of the Hebeloma cylindrosporum-Pinus pinaster association. Phytochemistry 68:41–51

    PubMed  Google Scholar 

  • Nagahashi G, Douds DD (2000) Partial separation of root exudate components and their effects upon the growth of germinated spores of AM fungi. Mycol Res 104:1453–1464

    Google Scholar 

  • Navazio N, Moscatiello R, Genre A, Novero M, Baldan B, Bonfante P, Mariani P (2007) A diffusible signal from arbuscular mycorrhizal fungi elicits a transient cytosolic calcium elevation in host plant cells. Plant Physiol 144:673–681

    PubMed  CAS  Google Scholar 

  • Nehls U (2004) Carbohydrates and nitrogen: nutrients and signals in ectomycorrhizas. In: Varma A, Abbott L, Werner D, Hampp R (eds) Plant surface microbiology. Springer, Berlin, pp 373–392

    Google Scholar 

  • Nehls U (2008) Mastering ectomycorrhizal symbiosis: the impact of carbohydrates. J Exp Bot 59:1097–1108

    PubMed  CAS  Google Scholar 

  • Nehls U, Wiese J, Guttenberger M, Hampp R (1998) Carbon allocation in ectomycorrhizas: identification and expression analysis of an Amanita muscaria monosaccharide transporter. Mol Plant Microbe Interact 11:167–176

    PubMed  CAS  Google Scholar 

  • Nehls U, Bock A, Ecke M, Hampp R (2001a) Differential expression of hexose-regulated fungal genes within Amanita muscaria/Populus tremula × tremuloides ectomycorrhizas. New Phytol 150:583–589

    CAS  Google Scholar 

  • Nehls U, Mikolajewski S, Magel E, Hampp R (2001b) The role of carbohydrates in ectomycorrhizal functioning: gene expression and metabolic control. New Phytol 150:533–541

    CAS  Google Scholar 

  • Niini SS, Raudaskoski M (1993) Response of ectomycorrhizal fungi to benomyl and nocodazole, growth inhibition and microtubule depolymerization. Mycorrhiza 3:83–91

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Okada A, Shimizu T, Okada K, Kuzuyama T, Koga J, Shibuya N, Nojiri H, Yamane H (2007) Elicitor induced activation of the methylerythritol phosphate pathway toward phytoalexins biosynthesis in rice. Plant Mol Biol 65:177–187

    PubMed  CAS  Google Scholar 

  • Ohlrogge JB, Browse J (1995) Lipid biosynthesis. Plant Cell 7:957–970

    PubMed  CAS  Google Scholar 

  • Ohlrogge JB, Kuhn DN, Stumpf PK (1979) Subcellular localization of acyl carrier protein in leaf protoplasts of Spinacia oleracea. Proc Natl Acad Sci USA 76:1194–1198

    PubMed  CAS  Google Scholar 

  • Parniske M (2004) Molecular genetics of the arbuscular mycorrhizal symbiosis. Curr Opin Plant Biol 7:414–421

    PubMed  CAS  Google Scholar 

  • Paszkowski U, Jakovleva L, Boller T (2006) Maize mutants affected at distinct stages of the arbuscular mycorrizal symbiosis. Plant J 47:165–173

    PubMed  CAS  Google Scholar 

  • Paullilo SM, Fahrenkrog B (2008) The nuclear pore complex: from higher eukaryotes to plants. In: Schoefs B (ed) Plant cell compartments. Selected Topics Research Signpost. trivandrum 1–18

    Google Scholar 

  • Pozo MJ, Azcon-Aguilar C (2007) Unraveling mycorrhiza-induced resistance. Curr Opin Plant Biol 10:393–398

    PubMed  CAS  Google Scholar 

  • Ramos AC, Façanha AR, Feijo JA (2008) Proton (H+) flux signature for the presymbiotic development of the arbuscular mycorrhizal fungi. New Phytol 178:177–188

    PubMed  CAS  Google Scholar 

  • Raudaskoski M, Pardo AG, Tarkka MT, Gorfer M, Hanif M, Laitiainen E (2001) Small GTPases, cytoskeleton and signal transduction in filamentous homobasidiomycetes. In: Geitmann A, Cresti M, Heath IB (eds) Cell biology of plant and fungal tip growth (NATO Science Series 328). IOS, Amsterdam, pp 123–136

    Google Scholar 

  • Raudaskoski M, Tarkka MT, Niini S (2004) Mycorrhizal development and cytoskeleton. In: Varma A, Abott L, Werner D, Hampp R (eds) Plant surface microbiology. Springer, Berlin, pp 293–329

    Google Scholar 

  • Reddy SM, Pandey AK, Melayah D, Marmeisse R, Gay G (2003) The auxin responsive gene Pp-C61 is up-regulated in Pinus pinaster roots following inoculation with ectomycorrhizal fungi. Plant Cell Environ 26:681–691

    CAS  Google Scholar 

  • Redecker D, Kodner R, Graham LE (2000) Glomalean fungi from the Ordovician. Science 289:1920–1921

    PubMed  CAS  Google Scholar 

  • Regvar M, Gogala N, Zalar P (1996) Effects of jasmonic acid on mycorrhiza Allium sativum. New Phytol 134:703–707

    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 

  • Requena N, Mann P, Hampp R, Franken P (2002) Early developmentally regulated genes in the arbuscular mycorrhizal fungus Glomus mosseae: identification of GmGIN1, a novel gene with homology to the C-terminus of metazoan hedgehog proteins. Plant Soil 244:129–139

    CAS  Google Scholar 

  • Riely BK, Lougnon G, Ane JM, Cook DR (2007) The symbiotic ion channel homolog DMI1 is localized in the nuclear membrane of Medicago truncatula roots. Plant J 49:208–216

    PubMed  CAS  Google Scholar 

  • Roughan PG, Slack CR (1982) Cellular organization of glycerolipid metabolism. Annu Rev Plant Physiol Plant Mol Biol 33:97–132

    CAS  Google Scholar 

  • Ruiz-Lozano JM, Roussel H, Gianinazzi S, Gianinazzi-Pearson V (1999) Defence genes are differentially induced by a mycorrhizal fungus and Rhizobium in wild type and symbiosis-defective pea genotypes. Mol Plant Microbe Interact 12:976–984

    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 67:477–482

    CAS  Google Scholar 

  • Salo V, Niini SS, Virtanen I, Raudaskoski M (1989) Comparative immunocytochemistry of the cytoskeleton in filamentous fungi with dikaryotic and multinucleate hyphae. J Cell Sci 94:11–24

    CAS  Google Scholar 

  • Salzer P, Hebe G, Hager A (1997) 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, Corbiere H, Boller T (1999) Hydrogen peroxide accumulation in Medicago truncatula roots colonized by the arbuscular mycorrhiza-forming fungus Glomus intraradices. Planta 208:319–325

    CAS  Google Scholar 

  • Sanchez L, Weidmann S, Arnould C, Bernard AR, Gianinazzi S, Gianinazzi-Pearson V (2005) P. fluorescens and G. mosseae trigger DMI3-dependent activation of genes related to a signal transduction pathway in roots of Medicago truncatula. Plant Physiol 139:1065–1077

    PubMed  CAS  Google Scholar 

  • Sbrana C, Giovannetti M (2005) Chemotropism in the arbuscular mycorrhizal fungus Glomus mossae. Mycorrhiza 15:539–545

    PubMed  CAS  Google Scholar 

  • Scervino JM, Ponce MA, Erra-Bassells R, Bompadre MJ, Vierheilig H, Ocampo JA, Godeas A (2005) Glycosidation of apigenin results in a loss of its activity on different growth parameters of arbuscular mycorrhizal fungi from the genus Glomus and Gigaspora. Soil Biol Biochem 38:2919–2922

    Google Scholar 

  • Schilmiller AL, Howe GA (2005) Systemic signaling in the wound response. Curr Opin Plant Biol 8:369–377

    PubMed  CAS  Google Scholar 

  • Schliemann W, Schmidt J, Nimtz M, Wray V, Thomas F, Strack D (2006) Accumulation of apocarotenoids in mycorrhizal roots of Ornithogalum umbellatum. Phytochemistry 67:1196–1205

    PubMed  CAS  Google Scholar 

  • Schliemann W, Ammer C, Strack D (2008) Metabolite profiling of mycorhizal root of Medicago truncatula. Phytochemistry 69:112–146

    PubMed  CAS  Google Scholar 

  • Schwender J, Ohlrogge JB (2002) Probing in vivo metabolism by stable isotope labelling of storage lipids and proteins in developing Brassica napus embryos. Plant Physiol 130:347–361

    PubMed  CAS  Google Scholar 

  • Seddas PM, Arnould C, Tollot M, Arias CM, Gianinazzi-Pearson V (2008) Spatial monitoring of gene activity in extraradical and intraradical developmental stages of arbuscular mycorrhizal fungi by direct fluorescent in situ RT-PCR. Fungal Genet Biol 45:1155–1165

    PubMed  CAS  Google Scholar 

  • Siciliano V, Genre A, Balestrini R, Cappellazzo G, deWit PJGM, Bonfante P (2007) Transcriptome analysis of arbuscular mycorrhizal roots during development of the prepenetration apparatus. Plant Physiol 144:1455–1466

    PubMed  CAS  Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhiza symbiosis, 3rd edn. Academic, San Diego

    Google Scholar 

  • Soares ACF, Martins MA, Mathias L, Freitas MSM (2005) Arbuscular mycorrhizal fungi and the occurence of flavonoids in roots of passion fruit seedlings. Sci Agric 62:331–336

    CAS  Google Scholar 

  • Somerville C, Browse J (1991) Plant lipids: metabolism, mutants, and membranes. Science 252:80–87

    PubMed  CAS  Google Scholar 

  • Splivallo R, Novero M, Bertea CM, Bossi S, Bonfante P (2007) Truffle volatiles inhibit growth and induce an oxidative burst in Arabidopsis thaliana. New Phytol 175:417–424

    PubMed  CAS  Google Scholar 

  • Strack D, Fester T (2006) Isoprenoid metabolism and plastid reorganization in arbuscular mycorrhizal roots. New Phytol 172:22–34

    PubMed  CAS  Google Scholar 

  • Stracke S, Kistner C, Yoshida S, Mulder L, Sato S, Kaneto 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 417:959–962

    PubMed  CAS  Google Scholar 

  • Strassner J, Schaller F, Frick U, Howe G, Weiler E, Amrhein N, Macheroux P, Schaller A (2002) Characterization and cDNA-microarray expression analysis of 12-oxophytodienoate reductase revleas diffrerential roles for octadecanoid biosynthesis in the local versus of the systemic wound response. Plant J 32:585–601

    PubMed  CAS  Google Scholar 

  • Takano Y, Choi W, Mitchell T, Okuno T, Dean RA (2003) Large scale parallel analysis of gene expression during infection-related morphogenesis of Magnaporthe grisea. Mol Plant Pathol 4:337–346

    PubMed  CAS  Google Scholar 

  • Tamasloukht MB, Séjalon-Delmas N, Kluever A, Jauneau A, Roux C, Bécard G, Franken P (2003) Root factors induce mitochondrial-related gene expression and fungal respiration during the developmental switch from asymbiosis to presymbiosis in the arbuscular mycorrhizal fungus Gigaspora rosea. Plant Physiol 131:1468–1478

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Taylor TN, Remy W, Hass H, Kerp H (1995) Fossil arbuscular mycorrhizae from the early Devonian. Mycologia 87:560–573

    Google Scholar 

  • Thoma I, Loeffler C, Sinha A, Gupta M, Krischke M, Steffan B, Roistch T, Mueller M (2003) Cyclopentenone isoprostanes induced by reactive oxygen species trigger defense gene activation and phytoalexin accumulation in plants. Plant J 34:363–375

    PubMed  CAS  Google Scholar 

  • Timonen S, Finlay RD, Soderstrom B, Raudaskoski M (1993) Identification of cytoskeletal components in pine ectomycorrhizas. New Phytol 124:83–92

    Google Scholar 

  • Tuskan G, DiFazio S, Jansson S, Bohlmann J, Grigoriev I, Hellsten U, Putnam N, Ralph S, Vierheilig H (2004) Regulatory mechanisms during the plant-arbuscular mycorrhizal fungus interaction. Can J Bot 82:1166–1176

    Google Scholar 

  • Vierheilig H, Piché Y (2002) Signalling in arbuscular mycorrhiza: facts and hypotheses. In: Buslig B, Manthey J (eds) Flavonoids in cell function. Kluwer, New York, pp 23–29

    Google Scholar 

  • Vierheilig H, Bago B, Albrecht C, Poulin M-P, Piché Y (1998) Flavonoids and arbuscular-mycorrhizal fungi. In: Manthey JA, Buslig BS (eds) Flavonoids in the living system. Plenum, New York, pp 9–33

    Google Scholar 

  • Vieweg MF, Hohnjec N, Küster H (2005) Two genes encoding truncated hemoglobins are regulated during root nodule and arbuscular mycorrhiza symbioses of Medicago truncatul a. Planta 220:757–766

    PubMed  CAS  Google Scholar 

  • Walter MH, Fester T, Strack D (2000) Arbuscular mycorrhizal fungi induce the non-mevalonate methylerythritol phosphate pathway of isoprenoid biosynthesis correlated with accumulation of the "yellow pigment" and other apocarotenoids. Plant J 21:571–578

    PubMed  CAS  Google Scholar 

  • Walter MH, Hans J, Strack D (2002) Two distantly related genes encoding 1-deoxy-D-xylulose 5-phosphate synthases: differential regulation in shoots and apocarotenoid-accumulating mycorrhizal roots. Plant J 31:243–254

    PubMed  CAS  Google Scholar 

  • Weidmann S, Sanchez L, Descombin J, Chatagnier O, Gianinazzi S, Gianinazzi-Pearson V (2004) Fungal elicitation of signal transduction-related plant genes precedes mycorrhiza establishment and requires the dmi3 gene in Medicago truncatula. Mol Plant Microb Interact 17:1385–1393

    CAS  Google Scholar 

  • Withers ST, Keasling JD (2007) Biosynthesis and engineering of isoprenoid small molecules. Appl Microbiol Biotechnol 73:980–990

    PubMed  CAS  Google Scholar 

  • Wright DP, Johansson T, Le Quere A, Soderstrom B, Tunlid A (2005) Spatial patterns of gene expression in the extramatrical mycelium and mycorrhizal root tips formed by the ectomycorrhizal fungus Paxillus involutus in association with birch (Betula pendula) seedlings in soil microcosms. New Phytol 167:579–596

    PubMed  CAS  Google Scholar 

  • Yoneyama K, Xie XN, Kasumoto D, Sekimoto H, Sugimoto Y, Takeuchi Y, Yoneyama K (2007) Nitrogen deficiency as well as phosphorus deficiency in sorghum promotes the production and exudation of 5-deoxystrigol, the host recognition signal for arbuscular mycorrhizal fungi and root parasites. Planta 227:125–132

    PubMed  CAS  Google Scholar 

  • Yoneyama K, Xie X, Sekimoto H, Takeuchi Y, Ogasawara S, Akiyama K, Hayashi H, Yoneyama K (2008) Strigolactones, host recognition signals for root parasitic plants and arbuscular mycorrhizal fungi, from Fabaceae plants. New Phytol 179:484–494

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Plante-Microbe-Environnement, INRA-CMSE, UMR INRA 1088/CNRS 5184/Université Bourgogne, BP 86510, 21065, Dijon Cedex, France

    Pascale Seddas, Vivienne Gianinazzi-Pearson, Benoit Schoefs & Daniel Wipf

  2. Institute for Plant Genetics, Leibniz Universität Hannover, Herrenhäuser Str. 2, 30419, Hannover, Germany

    Helge Küster

Authors
  1. Pascale Seddas
    View author publications

    Search author on:PubMed Google Scholar

  2. Vivienne Gianinazzi-Pearson
    View author publications

    Search author on:PubMed Google Scholar

  3. Benoit Schoefs
    View author publications

    Search author on:PubMed Google Scholar

  4. Helge Küster
    View author publications

    Search author on:PubMed Google Scholar

  5. Daniel Wipf
    View author publications

    Search author on:PubMed Google Scholar

Corresponding author

Correspondence to Daniel Wipf .

Editor information

Editors and Affiliations

    Rights and permissions

    Reprints and permissions

    Copyright information

    © 2009 Springer-Verlag Berlin Heidelberg

    About this chapter

    Cite this chapter

    Seddas, P., Gianinazzi-Pearson, V., Schoefs, B., Küster, H., Wipf, D. (2009). Communication and Signaling in the Plant–Fungus Symbiosis: The Mycorrhiza. In: Balu¿ka, F. (eds) Plant-Environment Interactions. Signaling and Communication in Plants. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-540-89230-4_3

    Download citation

    Publish with us

    Policies and ethics