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The Old Arbuscular Mycorrhizal Symbiosis in the Light of the Molecular Era

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Progress in Botany

Part of the book series: Progress in Botany ((BOTANY,volume 65))

Abstract

Mycorrhiza, from the Greek terms myco (=fungus) and rhiza (=root), is the predominant root symbiosis. More than 90% of land plants form mycorrhiza with soil fungi belonging to three different phyla (Smith and Read 1997). A few plant families (e.g. Cruciferae, Chenopodiaceae, Proteaceae) as well as some genera (e.g. Lupinus) have been described as non-mycorrhizal. It is speculated that the mycorrhizal character has possibly arisen several times during evolution (Trappe 1987), but the mechanisms of mycorrhiza exclusion have not yet been identified. From the different types of mycorrhiza existing in nature arbuscular mycorrhizas are the oldest and most widespread symbiosis (Remy et al. 1994). Recent fossil studies and molecular data have tracked the presence of this symbiosis all the way to the Ordovician era, i.e. to be at least 460 million years old (Redecker et al. 2000b). The fungi forming this mutualistic symbiosis have been recently recognized as belonging to an independent phylum, the Glomeromycota (Schüßler et al. 2001b) with a monophyletic origin. The permanence of this mutualistic association during evolution reflects its importance in nature. The reciprocal benefit, achieved by the nutrient exchange between both partners in intimate contact, is possibly the reason for this durability. However, the benefits of the symbiosis to the maintenance of natural ecosystems cannot be only estimated in terms of improved plant nutrition.

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References

  • Abbas JD, Hetrick, BAD, Jurgensen JE (1996) Isolate specific detection of mycorrhizal fungi using genome specific primer pairs. Mycologia 88:939–946

    Article  CAS  Google Scholar 

  • Abbott LK (1983) Comparative anatomy of vesicular-arbuscular mycorrhizae formed on subterranean clover. Aust J Bot 30:485–495

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Alexander T, Meier R, Toth R, Weber HC (1988) Dynamics of arbuscule development and degeneration in mycorrhizas of Triticum aestivum L. and Avena sativa L. with reference to Zea mays L. New Phytol 110:363–370

    Article  Google Scholar 

  • Alexander T, Meier R, Toth R, Weber HC (1989) Dynamics of arbuscule development and degeneration in onion, bean and tomato with reference to vesicular-arbuscular mycorrhizas with grasses. Can J Bot 67:2505–2513

    Article  Google Scholar 

  • Allen MF, Allen EB, Friese CF (1989) Responses of the non-mycotrophic plant Salsola kali to invasion by vesicular-arbuscular mycorrhizal fungi. New Phytol 111:45–49

    Article  Google Scholar 

  • Antonionelli ZI, Schachtman DP, Ophel-Keller K, Smith SE (2000) Variation in rDNA ITS sequences in Glomus mosseae and Gigaspora margarita spores from a permanent pasture. Mycol Res 104:708–715

    Article  Google Scholar 

  • Aström H, Giovannetti M, Raudaskoski M (1994) Cytoskeletal components in the arbuscular mycorrhizal fungus Glomus mosseae. Mol Plant Microbe Interact 7:309–312

    Article  Google Scholar 

  • Bago B, Bentivenga SP, Brenac V, Dodd JC, Piche Y, Simon L (1998) Molecular analysis of Gigaspora (Glomales, Gigasporaceae). New Phytol 139:581–588

    Article  CAS  Google Scholar 

  • Bago B, Pfeffer PE, Douds DD Jr, Brouillette J, Becard G, Shachar-Hill Y (1999) Carbon metabolism in spores of the arbuscular mycorrhizal fungus Glomus intraradices as revealed by nuclear magnetic resonance spectroscopy. Plant Physiol 121:263–272

    Article  PubMed  CAS  Google Scholar 

  • Bago B, Zipfel W, Williams RM, Jun J, Arreola R, Lammers PJ, Pfeffer PE, Shachar-Hill Y (2002) Translocation and utilization of fungal storage lipid in the arbuscular mycorrhizal symbiosis. Plant Physiol 128:108–124

    Article  PubMed  CAS  Google Scholar 

  • Balestrini R, Romero C, Puigdoménech P, Bonfante P (1994) Location of a cell-wall hydroxyproline-rich glycoprotein, cellulose and (ß-l,3-glucans in apical and differentiated regions of maize mycorrhizal roots. Planta 195195:2016209

    Article  Google Scholar 

  • Balestrini R, Hahn MG, Faccio A, Mendgen K, Bonfante P (1996) Differential localization of carbohydrate epitopes in plant cell walls in the presence and absence of arbuscular mycorrhizal fungi. Plant Physiol 111:203–213

    PubMed  CAS  Google Scholar 

  • Balestrini R, José-Estanyol M, Puigdoménech P, Bonfante P (1997) Hydroxyproline-rich glycoprotein mRNA accumulation in maize root cells colonized by an arbuscular mycorrhizal fungus as revealed by in situ hybridization. Protoplasma 198:36–42

    Article  CAS  Google Scholar 

  • Barea JM, Jeffries PJ (1995) Arbuscular mycorrhizas in sustainable soil-plant systems. In: Varma A, Hock B (eds) Mycorrhiza. Springer, Berlin Heidelberg New York, pp 521–560

    Google Scholar 

  • Barker SJ, Tagu D, Delp G (1998) Regulation of root and fungal morphogenesis in mycorrhizal symbiosis. Plant Physiol 116:1201–1207

    Article  CAS  Google Scholar 

  • Bécard G, Piché Y (1989a) New aspects on the acquisition of biotrophic status by a vesicular-arbuscular mycorrhizal fungus, Gigaspora margarita. New Phytol 112:77–83

    Article  Google Scholar 

  • Bécard G, Piché Y (1989b) Fungal growth stimulation by CO2 and root exudates in vesicular-arbuscular mycorrhizal symbiosis. Appl Environ Microb 55:2320–2325

    Google Scholar 

  • Bécard G, Taylor LP, Douds DD, Pfeffer PE, Doner LW (1995) Flavonoids are not necessary plant signal compounds in arbuscular mycorrhizal symbioses. Mol Plant Microbe Interact 8:252–258

    Article  Google Scholar 

  • Bethlenfalvay GJ, Cantrell IC, Mihara KL, Schreiner RP (1998) Relationships between soil aggregation and mycorrhizae as influenced by soil biota and nitrogen nutrition. Biol Fertil Soils 28:356–363

    Article  Google Scholar 

  • Bianciotto V, Bonfante P (1993) Evidence of DNA replication in an arbuscular mycorrhizal fungus in the absence of the host plant. Protoplasma 176:100–105

    Article  CAS  Google Scholar 

  • Bianciotto V, Barbiero G, Bonfante P (1995) Analysis of the cell cycle in an arbuscular mycorrhizal fungus by flow cytometry and bromodeoxyuridine labeling. Protoplasma 188:161–169

    Article  Google Scholar 

  • Blancaflor EB, Zhao LM, Harrison MJ (2001) Microtubule organization in root cells of Medicago truncatula during development of an arbuscular mycorrhizal symbiosis with Glomus versiforme. Protoplama 217:154–165

    Article  CAS  Google Scholar 

  • Blee KA, Anderson AJ (1996) Defense related transcript accumulation in Phaseolus vulgaris L. colonized by the arbuscular mycorrhiizal fungus Glomus intraradices. Schenk and Smith. Plant Physiol 110:675–688

    PubMed  CAS  Google Scholar 

  • Blilou I, Bueno P, Ocampo JA, García-Garrido JM (2000a) Induction of catalase and ascorbate peroxidase activities in tobacco roots inoculated with the arbuscular mycorrhizal fungus Glomus mosseae. Mycol Res 104:722–725

    Article  CAS  Google Scholar 

  • Blilou I, Ocampo JA, García-Garrido JM (2000b) Induction of Ltp (Lipid tranfer protein) and Pal (phenylalanine ammonia-lyase) gene expression in rice roots colonized by the arbuscular mycorrhizal fungus Glomus mosseae. J Exp Bot 51:1969–1977

    Article  PubMed  CAS  Google Scholar 

  • Bonamoni A, Oetiker JH, Guggenheim R, Boller T, Wiemken A, Vögeli-Lange R (2001) Arbuscular mycorrhizas in mini-mycorrhizotrons:first contact of Medicago truncatula roots with Glomus intraradices induces chalcone synthase. New Phytol 150:573–582

    Article  Google Scholar 

  • Bonfante P, Bianciotto V (1995) Presymbiontic versus symbiontic phase in arbuscular endomycorrhizal fungi:morphology and cytology. In: Varma A, Hock B (eds) Mycorrhiza. Springer, Berlin Heidelberg New York, pp 229–247

    Google Scholar 

  • Bonfante P, Perotto S (1992) The cellular basis of plant-fungus interchanges in mycorrhizal associations. In: Allen MG (ed) Functioning of mycorrhizae. Chapman and Hall, New York, pp 65–101

    Google Scholar 

  • Bonfante P, Perotto S (1995) Strategies of arbuscular mycorrhizal fungi when infecting host plants. New Phytol 130:3–21

    Article  Google Scholar 

  • Bonfante P, Bergero R, Uribe X, Romera C, Rigau J, Puigdomenech P (1996) Transcriptional activation of a maize alpha-tubulin gene in mycorrhizal maize and transgenic tobacco plants. Plant J 9:737–743

    Article  CAS  Google Scholar 

  • Bonfante P, Genre A, Faccio A, Martinin I, Schauser L, Stougaard J, Webb J, Parniske M (2000) The Lotus japonicus LjSym4 gene is required for the successful symbiotic infection of root epidermal cells. Mol Plant Microbe Interact 13:1109–1120

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  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

    Article  CAS  Google Scholar 

  • Chelius M, Triplett E (1999) Rapid detection of arbuscular mycorrhizae in roots and soil of an intensively managed turfgrass system by PCR amplification of small subunit rDNA. Mycorrhiza 9:61–64

    Article  CAS  Google Scholar 

  • Clapp JP, Young JPW, Merryweather JW, Fitter AH (1995) Diversity of fungal symbionts in arbuscular mycorrhizas from a natural community. New Phytol 130:259–265

    Article  Google Scholar 

  • Clapp JP, Fitter AH, Young JPW (1999) Ribosomal small sunbunit sequence variation within spores of an arbuscular mycorrhizal fungus, Scutellospora sp. Mol Ecol 8:915–921

    Article  PubMed  CAS  Google Scholar 

  • Clapp JP, Rodriguez A, Dodd JD (2001) Inter-and intra-isolate rRNA large subunit variation in Glomus coronatum spores. New Phytol 149:539–554

    Article  CAS  Google Scholar 

  • Cordier C, Gianinazzi-Pearson V, Gianinazzi S (1996) An immunological approach for the study of spatial relationships between mycorrhizal fungi in planta. In: Azcón-Aguilar C, Barrea JM (eds) Mycorrhizas in integrated systems:from genes to plant development. European Commision, EUR 16728, Luxembourg, pp 25–30

    Google Scholar 

  • Cordier C, Pozo MJ, Barea JM, Gianinazzi S, Gianinazzi-Pearson V (1998) Cell defense responses associated with localized and systemic resistance to Phytophthora induced in tomato by an arbuscular mycorrhizal fungus. Mol Plant Microbe Interact 11:1017–1028

    Article  CAS  Google Scholar 

  • Dangl JL, Dietrich RA, Richberg MH (1996) Death don’t have no mercy:cell death programs in plant-microbe interactions. Plant Cell 8:1793–1807

    PubMed  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 colonizatiomplant resistance to infection by fungal spores but not extra-radical hyphae. Plant J 27:561–569

    Article  PubMed  CAS  Google Scholar 

  • Davis RM, Menge JA (1980) Influence of Glomus fasciculatus and soil phosphorus on Phytophthora root rot of citrus. Phytopathology 70:447–452

    Article  CAS  Google Scholar 

  • Di Bonito R, Elliott ML, Jardin EA (1995) Detection of an arbuscular mycorrhizal fungus in roots of different plant species with the PCR. Appl Environ Microbiol 61:2809–2810

    PubMed  CAS  Google Scholar 

  • Dodd JC (1994) Approaches to the study of the extraradical mycelium of arbuscular mycorrhizal fungi. In: Gianinazzi S, Schüepp H (eds) Impact of arbuscular mycorrhizas on sustainable agriculture and natural ecosystems. Birkhäuser, Basel, pp 147–166

    Chapter  Google Scholar 

  • Douds DD, Galvez L, Bécard G, Kapulnik K (1998) Regulation of arbuscular mycorrhizal development by plant host and fungus species in alfalfa. New Phytol 138:27–35

    Article  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

    Article  Google Scholar 

  • Franken P, Gnädinger F (1994) Analysis of parsley arbuscular endomycorrhizal: infection development and mRNA levels of defense related genes. Mol Plant Microbe Interact 7:612–620

    Article  CAS  Google Scholar 

  • Franken P, Requena N (2001a) Mol ecular analyisis of arbuscular mycorrhiza. In: Hock B (ed) The mycota, vol IX. Springer, Berlin Heidelberg New York, pp 19–28

    Google Scholar 

  • Franken P, Requena N (2001b) Analysis of gene expression in arbuscular mycorrhizasmew approaches and challenges. New Phytol 150:517–523

    Article  CAS  Google Scholar 

  • Friese CF, Allen MF (1991) The spread of VA mycorrhizal fungi in the soil:inoculum types and external hyphal architecture. Mycologia 83:409–418

    Article  Google Scholar 

  • Fry SC, Smith RC, Renwick KF, Martin DJ, Hodge SK, Matthews KJ (1992) Xyloglucan endotransglycosylase, a new wall-loosening enzyme activity from plants. Biochem J 282:821–828

    PubMed  CAS  Google Scholar 

  • Gadkar V, David-Schwartz R, Kunik T, Kapulnik Y (2001) Arbuscular mycorrhizal fungal colonization. Factors involved in host recognition. Plant Physiol 127:1493–1499

    Article  PubMed  CAS  Google Scholar 

  • Gallaud I (1905) Études sur les mycorrhizes endotrophs. Rev Générale Bot 17:5–48, 66-83, 123-135, 223-239, 313-325, 425-433, 479-500

    Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Garcia-Garrido JM, Cabello MN, Garcia-Romero I, Ocampo JA (1992a) Endonuclease activity in letucce plants colonized with the vesicular-arbuscular mycorrhizal fungus Glomus fasciculatum. Soil Biol Biochem 24:955–959

    Article  CAS  Google Scholar 

  • Garcia-Garrido JM, Garcia-Romero I, Ocampo JA (1992b) Cellulase production by the vesicular arbuscular mycorrhizal fungus Glomus mosseae. New Phytol 121:221–226

    Article  CAS  Google Scholar 

  • Garcia-Garrido JM, Garcia-Romero I, Parra-Garcia MD, Ocampo JA (1996) Purification of an arbuscular mycorrhizal endoglucanase from onion roots colonized by Glomus mosseae. Soil Biol Biochem 25:1443–1449

    Article  Google Scholar 

  • Garcia-Romera I, Garcia-Garrido JM, Ocampo JA (1991) Pectinolytic enzymes in vesicular-arbuscular mycorrhizal fungus Glomus mosseae. FEMS Microbiol Lett 78:343–346

    Article  CAS  Google Scholar 

  • Garriock ML, Peterson RL, Ackerley CA (1989) Early stages in colonization of Allium porrum (leek) roots by the vesicular-arbuscular mycorrhizal fungus Glomus versiforme. New Phytol 112:85–92

    Article  Google Scholar 

  • Gehrig H, Schüßler A, Kluge M (1996) Geosiphon pyriformis, a fungus forming endocytobiosis with Nostoc (Cyanobacteria), is an ancestral member of the Glomales:evidence by SSU rRNA analysis. J Mol Evol 43:71–81

    Article  PubMed  CAS  Google Scholar 

  • Genre A, Bonfante P (1997) A mycorrhizal fungus changes microtubule orientation in tobacco root cells. Protoplasma 199:30–38

    Article  Google Scholar 

  • Genre A, Bonfante P (1998) Actin versus tubulin configuration in arbuscule-containing cells from mycorrhizal tobacco roots. New Phytol 140:745–752

    Article  CAS  Google Scholar 

  • Genre A, Bonfante P (2002) Epidermal cells of a symbiosis-defective mutant of Lotus japonicus show altered cytoskeleton organisation in the presence of a mycorrhizal fungus. Protoplasma 219:43–50

    Article  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 early hyphal growth of a vesicular-arbuscular mycorrhizal fungus by host root exudares and plant flavonoids. Symbiosis 7:243–255

    CAS  Google Scholar 

  • Gianinazzi-Pearson V, Smith SE, Gianinazzi S, Smith FA (1991) Enzymatic studies on the metabolism of vesicular-arbuscular mycorrhizas: V. H+-ATPase a component of ATP-hydrolyzing enzyme activities in plant-fungus interfaces? New Phytol 117:61–74

    Article  CAS  Google Scholar 

  • Gianinazzi-Pearson V, Dumas-Gaudot E, Gollotte A, Tahiri-Alaoui A, Gianinazzi S (1996) Cellular and molecular defense-related root responses to invasion by arbuscular mycorrhizal fungi. New Phytol 133:45–57

    Article  Google Scholar 

  • Gianinazzi-Pearson V, Arnould C, Oufattole M, Arango M, Gianinazzi S (2000) Differential activation of H+-ATPase genes by an arbuscular mycorrhizal fungus in root cells of transgenic tobacco. Planta 211:609–613

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Giovannetti M, Sbrana C, Avio L (1993b) Differential hyphal morphogenesis in arbuscular mycorrhizal fungi during preinfection stage. New Phytol 125:587–593

    Article  Google Scholar 

  • Giovannetti M, Sbrana C, Citernesi AS, Avio L, Gollote A, Gianinazzi-Pearson V, Gianinazzi S (1995) Recognition and infection process, basis for host specificity of AMF. In: Gianinazzi S, Schüepp H (eds) Impact of arbuscular mycorrhizas on sustainable agriculture and natural ecosystems. Birkhäuser, Basel, pp 61–72

    Google Scholar 

  • Giovannetti M, Sbrana C, Citernesi AS, Avio L (1996) Analysis of factors involved in fungal recognition responses to host derived signals by arbuscular mycorrhizal fungi. New Phytol 133:65–71

    Article  Google Scholar 

  • Giovannetti M, Azzolini D, Citernesi AS (1999) Anastomosis formation and nuclear and protoplasmic exchange in arbuscular mycorrhizal fungi. Appl Environ Microbiol 65:5571–5575

    PubMed  CAS  Google Scholar 

  • Giovannetti M, Fortuna P, Citernesi AS, Morini S, Nuti MP (2001) The occurrence of anastomosis formation and nuclear exchange in intact arbuscular mycorrhizal networks. New Phytol 151:717–724

    Article  Google Scholar 

  • Giovannetti M, Sbrana C, Strani P, Agnolucci M, Rinaudo V, Avio L (2003) Genetic diversity of isolates of Glomus mosseae from different geographic areas detected by vegetative compatibility testing and biochemical and molecular analysis. Appl Environ Microbiol 69:616–624

    Article  PubMed  CAS  Google Scholar 

  • Gollote 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” mutant Pisum sativum L. Planta 191:112–122

    Article  Google Scholar 

  • Grippiolo R, Bonfante P (1994) Sporopollenin and melanin-like pigments in the wall of a Glomus spore. Giorn Bot Ital 118:88–90

    Google Scholar 

  • Guttenberger M (2000) Arbuscules of vesicular-arbuscular mycorrhizal fungi inhabit an acid compartment within plant roots. Planta 211:299–304

    Article  PubMed  CAS  Google Scholar 

  • Hahn A, Horn K, Hock B (1995) Serological properties of mycorrhizas. In: Varma A, Hock B (eds) Mycorrhiza. Springer, Berlin Heidelberg New York, pp 181–201

    Google Scholar 

  • Harrison M, Dixon R (1993) Isoflavonoid accumulation and expression of defense gene transcripts during the establishment of vesicular arbuscular mycorrhizal associations in roots of Medicago truncatula. Mol Plant Microbe Interact 6:643–659

    Article  CAS  Google Scholar 

  • Harrison MJ, van Buuren ML (1995) A phosphate transporter from the mycorrhizal fungus Glomus versiforme. Nature 378:626–629

    Article  PubMed  CAS  Google Scholar 

  • Harrison MJ, Dewbre GR, Liu J (2002) A phosphate transporter from Medicago truncatula involved in the acquisition of phosphate released by arbuscular mycorrhizal fungi. Plant Cell 14:2413–2429

    Article  PubMed  CAS  Google Scholar 

  • Hawkins HJ, Johansen A, George E (2000) Uptake and transport of organic and inorganic nitrogen by arbuscular mycorrhizal fungi. Plant Soil 226:275–285

    Article  CAS  Google Scholar 

  • Helgason T, Daniell TJ, Husband R, Fitter AH, Young YPW (1998) Ploughing up the wood-wide web? Nature 394:431

    Article  PubMed  CAS  Google Scholar 

  • Hepper CM (1979) Germination and growth of Glomus caledonius spores:the effect of inhibitors and nutrients. Soil Biol Biochem 2:269–277

    Article  Google Scholar 

  • Hepper CM, Sen R, Maskall CS (1986) Identification of vesicular-arbuscular mycorrhizal fungi in roots of leek (Allium porrum L.) and maize (Zea mays L.) on the basis of enzyme mobility during Polyacrylamide gel electrophoresis. New Phytol 102:529–539

    Article  Google Scholar 

  • Hijri M, Hosny M, van Tuinen D, Dulieu H (1999) Intraspecific ITS polymorphism in Scutellospora castanea (Glomales, Zygomycota) is structured within multinucleate spores. Fungal Genet Biol 26:141–151

    Article  PubMed  CAS  Google Scholar 

  • Hosny M, Hijri M, Passerieux E, Dulieu H (1999) rDNA units are highly polymorphic in Scutellospora castanea (Glomales, Zygomycetes). Gene 226:61–71

    Article  PubMed  CAS  Google Scholar 

  • Jacquot D, van Tuinen D, Gianinazzi S, Gianinazzi-Pearson V (2000) Monitoring species of arbuscular mycorrhizal fungi inplanta and in soil by nested PCR: application to the study of the impact of sewage sludge. Plant Soil 226:179–188

    Article  CAS  Google Scholar 

  • Jakobsen I (1995) Transport of phosphorus and carbon in VA mycorrhizas. In: Varma A, Hock B (eds) Mycorrhiza. Springer, Berlin Heidelberg New York, pp 297–324

    Google Scholar 

  • Johansen A, Jakobsen I, Jensen ES (1992) Hyphal transport of 15N-labelled nitrogen by a vesicular-arbuscular mycorrhizal fungus and its effect on depletion of inorganic soil N. New Phytol 122:61–68

    Article  Google Scholar 

  • Johansen A, Jakobsen I, Jensen ES (1993) External hyphae of vesicular-arbuscular mycorrhizal fungi associated with Trifolium subterraneum L. 3. Hyphal transport of 32P and 15N. New Phytol 124:61–68

    Article  CAS  Google Scholar 

  • Johansen A, Jakobsen I, Jensen ES (1994) Hyphal transport by vesicular-arbuscular mycorrhizal fungus on N applied to the soil as ammonium or nitrate. Biol Fertil Soils 16:66–70

    Article  Google Scholar 

  • Johansen A, Finlay RD, Olsson PA (1996) Nitrogen metabolism of external hyphae of the arbuscular mycorrhizal fungus Glomus intraradices. New Phytol 133:705–712

    Article  CAS  Google Scholar 

  • Journet E-P, El-Gachtouli N, Vernoud V, de Billy F, Pichon M, Dedieu A, Arnould C, Morandi D, Barker DG, Gianinazzi-Pearson V (2001) Medicago truncatula ENODll:a novel RPRP-encoding early nodulin gene expressed during mycorrhization in arbuscule-containing cells. Mol Plant Microbe Interact 14:737–748

    Article  PubMed  CAS  Google Scholar 

  • Kjøller R, Rosendahl S (2000) Detection of arbuscular mycorrhizal fungi (Glomales) in roots by nested PCR and SSCP (Single Stranded Conformation Polymorphism). Plant Soil 226:189–196

    Article  Google Scholar 

  • Kjøller R, Rosendahl S (2001) Mol ecular diversity of glomalean (arbuscular mycorrhizal) fungi dtermined as distinct Glomus-specific DNA sequences from roots of filed grown peas. Mycol Res 105:1027–1032

    Article  Google Scholar 

  • Kobayashi I, Kobayashi Y, Hardham AR (1994) Dynamic reorganization of microtubules and microfilaments in flax cells during the resistance response to flax rust infection. Planta 195:237–247

    Article  CAS  Google Scholar 

  • Kobayashi Y, Kobayashi I, Funaki Y, Fujimoto S, Takemoto T, Kunoh H (1997) Dynamic reorganization of microfilaments and microtubules is necessary for the expression of non-host resistance in barley coleoptile cells. Plant J 11:525–537

    Article  CAS  Google Scholar 

  • Koske RE (1981) Multiple germination by spores of Gigaspora gigantea. Trans Br Mycol Soc 76:320–330

    Google Scholar 

  • Kozlova N, Strunnikova O, Labutova N, Muromtsev G (2001) Production and specificity of polyclonal antibodies against soluble proteins from the arbuscular mycorrhizal fungus Glomus intraradices. Mycorrhiza 10:301–305

    Article  CAS  Google Scholar 

  • Krajinski F, Alexander B, Schubert D, Gianinazzi-Pearson V, Kaldenhoff R, Franken P (2000) Arbuscular mycorrhiza development regulates the mRNA abundance of Mtaqpl encoding a mercury-intensitive aquaporin of Medicago truncatula. Planta 211:85–90

    Article  PubMed  CAS  Google Scholar 

  • Kuhn G, Hijri M, Sanders IR (2001) Evidence for the evolution of multiple genomes in arbuscular mycorrhizal fungi. Nature 414:745–748

    Article  PubMed  CAS  Google Scholar 

  • Lambais MR, Mehdy MC (1993) Suppression of endochitinase, (β-l,3-endoglucanase and chalcone isomerase expression in bean vesicular arbuscular mycorrhizal roots under different soil phosphate conditions. Mol Plant Microbe Interact 6:75–83

    Article  CAS  Google Scholar 

  • Lambais MR, Mehdy MC (1996) Soybean roots infected by Glomus intraradices strains differing in infectivity exhibit differential chitinase and (β-1,3-endoglucanase expression. New Phytol 134:531–538

    Article  CAS  Google Scholar 

  • Lambais MR, Mehdy MC (1998) Spatial distribution of chitinases and (β-l,3-glucanase transcripts in bean arbuscular mycorrhizal roots under low and high phosphate conditions. New Phytol 140:33–42

    Article  CAS  Google Scholar 

  • Lanfranco L, Perotto S, Bonfante P (1998) Application of PCR for studying the biodiversity of mycorrhizal fungi. In: Bridge PD, Arora DK, Reddy CA, Elander RP (eds) Application of PCR in mycology. CAB International, Wallingford, pp 107–124

    Google Scholar 

  • Lanfranco L, Delpero M, Bonfante P (1999) Intrasporal variability of ribosomal sequences in the endomycorrhizal fungus Gigaspora margarita. Mol Ecol 8:37–45

    Article  PubMed  CAS  Google Scholar 

  • Lapopin L, Gianinazzi-Pearson V, Franken P (1999) Comparative differential RNA display analysis of arbuscular mycorrhiza in Pisum sativum wild type and a mutant defective in late stage development. Plant Mol Biol 41:669–677

    Article  PubMed  CAS  Google Scholar 

  • Lloyd-Macglip SA, Chambers SM, Dodd JC, Fitter AH, Walker C, Young YPW (1996) Diversity of the ribosomal internal spacers within and among isolates of Glomus mosseae and related mycorrhizal fungi. New Phytol 133:103–111

    Article  Google Scholar 

  • Logi C, Sbrana C, Giovanetti M (1998) Cellular events involved in survival of individual arbuscular mycorrhizal symbionts growing in the absence of the host. Appl Environ Microbiol 64:3473–3479

    PubMed  CAS  Google Scholar 

  • Longato S, Bonfante P (1997) Mol ecular identification of mycorrhizal fungi by direct amplification of microsatellite regions. Mycol Res 101:425–432

    Article  CAS  Google Scholar 

  • Maldonado-Mendoza IE, Dewbre GR, Harrison MJ (2001) A phosphate transporter gene from extra-radical mycelium of an arbuscular mycorrhizal fungus Glomus intraradices ie regulated in response to phosphate in the environment. Mol Plant Microbe Interact 10:1140–1148

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Martin-Laurent F, van Tuinen D, Dumas-Gaudot E, Gianinazzi-Pearson V, Gianinazzi S, Franken P (1997) Differential display analysis of RNA accumulation in arbuscular mycorrhiza of pea and isolation of a novel symbiosis-regulated plant gene. Mol Gen Genet 256:37–44

    Article  PubMed  CAS  Google Scholar 

  • Merryweather J, Fitter A (1998) The arbuscular mycorrhizal fungi of Hyacinthoides nonscripta:I. Diversity of fungal taxa. New Phytol 138:117–129

    Article  Google Scholar 

  • Millner PD, Mulbry WW, Reynolds SL, Patterson CA (1998) A taxon-specific oligonucleotide probe for temperate soil isolates of Glomus mosseae. Mycorrhiza 8:19–27

    Article  CAS  Google Scholar 

  • Millner PD, Mulbry WW, Reynolds SL (2001) Taxon-specific oligonucleotide primers for detection of Glomus etunicatum. Mycorrhiza 10:259–265

    Article  CAS  Google Scholar 

  • Morandi D, Bailey JA, Gianinazzi-Pearson V (1994) Isoflavonoid accumulation in soybean roots infected with vesicular arbuscular mycorrhizal fungi. Physiol Plant Pathol 24:357–364

    Article  Google Scholar 

  • Morton JB, Benny GL (1990) Revised classification of arbuscular mycorrhizal fungi (Zygomycetes):a new order, Glomales, two new suborders Glomineae and Gigasporineae, and two new families, Acaulosporaceae and Gigasporaceae, with an endemedation of Glomaceae. Mycotaxon 37:471–491

    Google Scholar 

  • Morton JB, Bentivenga SP (1994) Levels of diversity in endomycorrhizal fungi (Glomales, Zygomycetes) and their role in defining taxonomic and non taxonomic groups. Plant Soil 159:47–59

    Google Scholar 

  • Morton JB, Redecker D (2001) Two new families of Glomales, Archaeosporaceae and Paraglomaceae, with two new genera, Archaeospora and Paraglomus, based on concordant molecular and morphological characters. Mycologia 93:185–195

    Article  Google Scholar 

  • Mosse B (1959) The regular germination of resting spores and some observations in the growth requirements of an Endogone sp. causing vesicular-arbuscular mycorrhiza. Trans Br Mycol Soc 42:273–286

    Google Scholar 

  • Mosse B (1988) Some studies relating to “independent” growth of vesicular-arbuscular endophytes. Can J Bot 66:2533–2540

    Article  Google Scholar 

  • Murphy PJ, Langridge P, Smith SE(1997) Cloning plant genes differentially expressed during colonization of roots of Hordeum vulgare by the vesicular-arbuscular mycorrhizal fungus Glomus intraradices. New Phytol 135:291–301

    Article  CAS  Google Scholar 

  • Nagahashi G, Douds DD (1997) Appressorium formation by AM fungi on isolated cell walls of carrot roots. New Phytol 136:299–304

    Article  Google Scholar 

  • Nair MG, Safir GR, Siqueira JO (1991) Isolation and identification of vesicular-arbuscular mycorrhiza stimulatory compounds from clover (Trifolium repens) root. Appl Environ Microbiol 57:434–439

    PubMed  CAS  Google Scholar 

  • Novero M, Faccio A, Genre A, Stougaard J, Webb KJ, Mulder L, Parniske M, Bonfante P (2002) Dual requirement of the LjSym4 gene for mycorrhizal development in epidermal and cortical cells of Lotus japonicus roots. New Phytol 154:741–749

    Article  CAS  Google Scholar 

  • Paszkowski U, Shi L, Bi-Yu Li, Xun Wang, Briggs S, Boller T (2001) A single gene mutation in the maize nopel mutant abolishes the recognition of arbuscular mycorrhizal fungi. In: 10th International Congress, Molecular Plant-Microbe Interactions, Madison, WI, Julyl0-14, Poster abstract no 686

    Google Scholar 

  • Perotto S, Brewin NJ, Bonfante P (1994) Colonization of pea roots by the mycorrhizal fungus Glomus versiforme and by Rhizobium bacteria:immunological comparison using monoclonal antibodies as probes for plant cell surface components. Mol Plant Microbe Interact 7:91–98

    Article  Google Scholar 

  • Peretto P, Bettini V, Favaron F, Alghisi P, Bonfante P (1995) Polygalacturonase activity and location in arbuscular mycorrrhizal roots of Allium porrum L. Mycorrhiza 5:157–163

    Article  CAS  Google Scholar 

  • Pfeffer PE, Douds DD Jr, Bécard G, Shachar-Hill Y (1999) Carbon uptake and the metabolism and transport of lipids in an arbuscular mycorrhiza. Plant Physiol 120:587–598

    Article  PubMed  CAS  Google Scholar 

  • Pirozynski KA, Malloch DW (1975) The origin of land plants a matter of mycotrophism. Biosystems 6:153–164

    Article  PubMed  CAS  Google Scholar 

  • Pozo MJ, Dumas-Gaudot E, Slezack S, Cordier C, Asselin A, Gianinazzi S, Gianinazzi-Pearson V (1996) Detection of new chitinase isoforms in arbuscular mycorrhizal tomato roots:possible implications in protection against Phytophthora nicotianae var. parasitica. Agronomie 16:689–697

    Article  Google Scholar 

  • Pozo MJ, Azcón-Aguilar C, Dumas-Gaudot E, Barea JM (1998) Chitosanase and chitinase activities in tomato roots during interactions with arbuscular mycorrhizal fungi or Phytophthora parasitica. J Exp Bot 49:1729–1739

    CAS  Google Scholar 

  • Pozo MJ, Azcón-Aguilar C, Dumas-Gaudot E, Barea JM (1999) (β-1,3-Glucanase activities in tomato roots inoculated with arbuscular mycorrhizal fungi and/or Phytophthora parasitica and their possible involvement in bioprotection. Plant Sci 141:149–157

    Article  CAS  Google Scholar 

  • Pozo MJ, Cordier C, Dumas-Gaudot E, Gianinazzi S, Barea JM, Azcon-Aguilar C (2002) Localized versus systemic effect of arbuscular mycorrhizal fungi on defense responses to Phytophthora infection in tomato plants. J Exp Bot 53:525–534

    Article  PubMed  CAS  Google Scholar 

  • Pringle A, Moncalvo JM, Vilgalys R (2000) High levels of variation in ribosomal DNA sequences within and among spores of natural population of the arbuscular mycorrhizal fungus Acaulospora colossica. Mycologia 92:259–168

    Article  CAS  Google Scholar 

  • Rausch C, Daram P, Brunner S, Jansa J, Laloi M, Leggewie N, Bucher M (2001) A phosphate transporter expressed in arbuscule-containing cells in potato. Nature 414:462–466

    Article  PubMed  CAS  Google Scholar 

  • Redecker D (2000) Specific PCR primers to identify arbuscular mycorrhizal fungi within colonized roots. Mycorrhiza 10:73–80

    Article  CAS  Google Scholar 

  • Redecker D (2001) Mol ecular identification and phylogeny of arbuscular mycorrhizal fungi. Plant Soil 244:67–73

    Article  Google Scholar 

  • Redecker D, Thierfelder H, Walker C, Werner D (1997) Restriction analysis of PCR-amplified internal transcribed spacers of ribosomal DNA as a tool for species identification in different genera of the order Glomales. Appl Environ Microbiol 63:1756–1761

    PubMed  CAS  Google Scholar 

  • Redecker D, Morton JB, Bruns TD (2000a) Ancestral lineages of arbuscular mycorrhizal fungi (Glomales). Mol Phylogenet Evol 14:276–284

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Rejón-Palomares A, Garcia-Garrido JM, Ocampo JA, Garcia-Romera I (1996) Presence of xyloglucan-hydrolysing glucanases (xyloglucanases) in arbuscular mycorrhizsl symbiosis. Symbiosis 21:249–261

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Requena N (1998) Mycorrhizal interactions in the rhizosphere. In: Varma A (ed) Microbes: for health, wealth and sustainable environment. MPH New Delhi, India, pp 726–735

    Google Scholar 

  • Requena N, Jeffries P, Barea JM (1996) Assessment of natural mycorrhizal potential in a desertified semiarid ecosystem. Appl Environ Microbiol 62:842–847

    PubMed  CAS  Google Scholar 

  • Requena N, Jimenez I, Toro M, Barea JM (1997) Interactions between plant-growth-promoting rhizobacteria (PGPR), arbuscular mycorrhizal fungi and Rhizobium spp. in the rhizosphere of Anthyllis cytisoides, a model legume for revegetation in mediterranean semi-arid ecosystems. New Phytol 136:667–677

    Google Scholar 

  • Requena N, Füller P, Franken P (1999) Molecular characterization of GmFOX2 an evolutionary highly conserved gene from the mycorrhizal fungus Glomus mosseae, down-regulated during interaction with rhizobacteria. Mol Plant Microb Interact 12:934–942

    Article  CAS  Google Scholar 

  • Requena N, Mann P, Franken P (2000) A homologue of the cell-cycle check-point TOR2 from yeast exists in the arbuscular mycorrhizal fungus Glomus mosseae. Protoplasma 211:89–98

    Article  Google Scholar 

  • Requena N, Pérez-Solis E, Azcón-Aguilar C, Jeffries P, Barea M (2001) Increased establishment of mycorrhizal plants inoculated with native endophytes in semi-arid degraded mediterranean ecosystems. Appl Environ Microbiol 67:495–498

    Article  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 GmGINl, a novel gene with homology to the C-terminus of metazoan hedgehog proteins. Plant Soil 244:129–139

    Article  CAS  Google Scholar 

  • Requena N, Breuninger M, Franken P, Ocón A (2003) Symbiotic status, phosphate and sucrose regulate the expression of two plasma membrane H+-ATPase genes from the arbuscular mycorrhizal fungus Glomus mosseae. Plant Physiol 132 (in press)

    Google Scholar 

  • Rosendahl S, Taylor JW (1997) Development of multiple genetic markers for studies of genetic variation in arbuscular mycorrhizal fungi using AFLP. Mol Ecol 6:821–829

    Article  CAS  Google Scholar 

  • Rosendahl S, Sen R, Hepper CM, Azcon-Aguilar C (1989) Quantification of three vesicular-arbuscular mycorrhizal fungi (Glomus spp) in the roots of leek (Allium porum) on the basis of the activity of diagnostic enzymes after Polyacrylamide gel electrophoresis. Soil Biol Biochem 21:519–522

    Article  Google Scholar 

  • Roussel H, van Tuinen D, Franken P, Gianinazzi S, Gianinazzi-Pearson V (2001) Signalling between arbuscular mycorrhizal fungi and plants: identification of a gene expressed during early interactions by differential RNA display analysis. Plant Soil 232:13–19

    Article  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Saito M (1995) Enzyme activities of the internal hyphae and germinated spores of an arbuscular mycorrhizal fungus Gigaspora margarita (Becker & Hall). New Phytol 129:425–431

    Article  CAS  Google Scholar 

  • Salzer P, Corbière H, Boller T (1999) Hydrogen peroxide accumulation in Medicago truncatula roots colonized by the arbuscular mycorrhiza-forming fungus Glomus mosseae. Planta 208:319–325

    Article  CAS  Google Scholar 

  • Salzer P, Bonamoni A, Beyer K, Vögeli-Lange R, Aeschbacher RA, Lang J, Wiemken A, Kim D, Cook DR, Boller T (2000) Differential expression of eight chitinase genes in Medicago truncatula roots during mycorrhiza formation, nodulation and pathogen infection. Mol Plant Microbe Interact 13:763–777

    Article  PubMed  CAS  Google Scholar 

  • Sanders IR (1999) No sex please, we’re fungi. Nature 399:737–739

    Article  PubMed  CAS  Google Scholar 

  • Sanders IR, Ravolanirina F, Gianinazzi-Pearson V, Pearson S, Lemoine MC (1992) Detection of specific antigens in the vesicular-arbuscular mycorrhizal fungi Gigaspora margarita and Acaulospora laevis using polyclonal antibodies to soluble spore fractions. Mycol Res 96:477–480

    Article  Google Scholar 

  • Sanders IR, Alt M, Groppe K, Boller T, Wiemken A (1995) Identification of ribosomal DNA polymorphism among and within spores of the Glomales: application to studies on the genetic diversity of AMF communities. New Phytol 130:419–427

    Article  CAS  Google Scholar 

  • Sanders IR, Clapp JP, Wiemken A (1996) The genetic diversity of AMF in natural ecosystems-a key to understanding the ecology and functioning of the mycorrhizal symbiosis. New Phytol 133:123–134

    Article  Google Scholar 

  • Schenck NC, Perez Y (1990) Manual for the identification of vesicular-arbuscular mycorrhizal fungi, 3rd edn. INVAM, Gainsville, Florida, USA.

    Google Scholar 

  • Scheres B, van de Wiel C, Zalensky A, Horvath B, Spaink H, van Eck H, Zwartkruis F, Wolters AM, Gloudemans T, van Kämmen A (1990) The ENOD12 gene product is involved in the infection process during the pea-Rhizobium interaction. Cell 60:281–294

    Article  PubMed  CAS  Google Scholar 

  • Schüßler A (1999) Glomales SSU rRNA gene diversity. New Phytol 144:205–207

    Article  Google Scholar 

  • Schüßler A, Kluge M (2001) Geosiphon pyriformis, an endocytobiosis between fungus and cyanobacteria, and its meaning as a model system for arbuscular macorrhizal research. In: Hock B (ed) The Mycota, vol IX. Springer, Berlin Heidelberg New York, pp 151–161

    Google Scholar 

  • Schüßler A, Mollenhauer D, Schnepf, E, Kluge M (1994) Geosiphon pyriformis, an endosymbiotic association of fungus and cyanobacteria:the spore structure resembles that of arbuscular mycorrhizal (AM) fungi. Bot Acta 107:36–45

    Google Scholar 

  • Schüßler A, Bonfante P, Schnepf E, Mollenhauer D, Kluge M (1996) Characterization of the Geosiphon pyriformis symbiosome by affinity techniques:confocal laser scanning microscopy (CLSM) and electron microscopy. Protoplasma 190:53–67

    Article  Google Scholar 

  • Schüßler A, Gehrig H, Schwarzott D, Walker C (2001a) Analysis of partial Glomales SSU rRNA gene sequencesdmplications for primer design and phylogeny. Mycol Res 105:5–15

    Article  Google Scholar 

  • Schüßler A, Schwarzott D, Walker C (2001b) A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycol Res 105:1413–1421

    Article  Google Scholar 

  • Schwarzott D, Walker C, Schüßler A (2001) Glomus, the largest genus of the arbuscular mycorrhizal fungi (Glomerales) is non-monophyletic. Mol Phylogenet Evol 21:190–197

    Article  PubMed  CAS  Google Scholar 

  • Shachar-Hill Y, Pfeffer PE, Douds D, Osman SF, Doner LW, Ratcliffe RG (1995) Partitioning of intermediary carbon metabolism in vesicular-arbuscular mycorrhizal leek. Plant Physiol 108:7–15

    PubMed  CAS  Google Scholar 

  • Simon L (1996) Phylogeny of the Glomales:deciphering the past to understand the present. New Phytol 133:95–101

    Article  Google Scholar 

  • Simon L, Lalonde M, Bruns TD (1992) Specific amplification of 18S ribosomal genes from VAM-fungi colonizing roots. Appl Environ Microbiol 58:291–295

    PubMed  CAS  Google Scholar 

  • Simon L, Levesque RC, Lalonde M (1993a). Identification of endomycorrhizal fungi colonizing roots by fluorescent single-strand conformation polymorphism-polymerase chain reaction. Appl Environ Microbiol 59:4211–4215

    PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Smith FA, Smith SE (1997) Structural diversity in (vesicular)-arbuscular mycorrizal symbiosis. New Phytol 137:373–388

    Article  Google Scholar 

  • Smith SE, Read DJ (1997) Mycorrhizal symbiosis, 2nd edn. Academic Press, London

    Google Scholar 

  • Smith SE, Smith FA (1990) Structure and function of the interfaces in biotrophic symbiosis as they relate to nutrient transport. New Phytol 114:1–38

    Article  CAS  Google Scholar 

  • Smith SE, St John BJ, Smith FA, Nicholas DJD (1985) Activity of glutamine synthetase and glutamate dehydrogenase in Trifolium subterraneum L. and Allium cepa L.:effects of mycorrhizal infection and phosphate nutrition. New Phytol 99:211–227

    Article  CAS  Google Scholar 

  • Somssich IE, Hahlbrock K (1998) Pathogen defence in plants:a paradigm of biological complexity. Trends Plant Sci 3:86–90

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • 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 417:959–962

    Article  PubMed  CAS  Google Scholar 

  • Talbot NJ, Foster AJ (2001) Genetics and genomics of the rice blast fungus Magnaporthe grisea:developing an experimental model for understanding fungal deseases of cereals. Adv Bot Res 34:263–287

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Timonen S, Smith FA, Smith SE (2001) Microtubules of the mycorrhizal fungus Glomus intraradices in symbiosis with tomato roots. Can J Bot 79:307–313

    Google Scholar 

  • Tisserant B, Brenac V, Requena N, Jeffries P, Dodd JC (1998) The detection of Glomus spp. (arbuscular mycorrhizal fungi) forming mycorrhizas in three plants, at different stages of seedling development, using mycorrhiza-specifi isozymes. New Phytol 138:225–239

    Article  CAS  Google Scholar 

  • Tobar R, Azcon R, Barea JM (1994) Improved nitrogen uptake and transport from 15N-labelled nitrate by external hyphae of arbuscular mycorrhiza under water-stressed conditions. New Phytol 126:119–122

    Article  Google Scholar 

  • Tommerup IC (1984) Persistence of infectivity by germinated spores of vesicular-arbuscular mycorrhizal fungi in soil. Trans Br Mycol Soc 82:275–282 aiTrappe JM (1987) Phylogenetic and ecological aspects of mycotrophy in the angiosperms from an evolutionary standpoint. In: Safir GR (ed) Ecophysiology of VA mycorrhizal plants. CRC Press, Boca Raton, FL, pp 2–25

    Google Scholar 

  • Turnau K, Ryszka P, Gianinazzi-Pearson V, van Tuinen D (2001) Identification of arbuscular mycorrhizal fungi in soils and roots of plants colonizing zinc wastes in southern Poland. Mycorrhiza 10:169–174

    Article  CAS  Google Scholar 

  • van Buuren ML, Maldonado-Mendoza IE, Trieu AT, Blaylock LA, Harrison MJ (1999) Novel genes induced during an arbuscular mycorrhizal (AM) symbiosis formed between Medicago truncatula and Glomus versiforme. Mol Plant Microbe Interact 12:171–81

    Article  PubMed  Google Scholar 

  • Vandenkoornhuyse P, Leyval C (1998) SSU rDNA sequencing and PCR-fingerprinting reveal genetic variation within Glomus mosseae. Mycologia 90:791–797

    Article  CAS  Google Scholar 

  • van der Heijden MGA, Klironomos JN, Ursic M, Moutoglis P, Streitwolf-Engel R, Boller T, Wiemken A, Sanders IR (1998) Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396:69–72

    Article  CAS  Google Scholar 

  • van Rhijn P, Fang Y, Galili S, Shaul O, Atzmon N, Wininger S, Eshed Y, Lum M, LiY, To V, Fujishige N, Kapulnik Y, Hirsch AM (1997) Expression of early nodulin genes in alfalfa mycorrhizae indicates that signal transduction pathways used in forming arbuscular mycorrhizae andRhizobium-induced nodules maybe conserved. Proc Natl Acad Sci USA 94:5467–5472

    Article  PubMed  Google Scholar 

  • van Tuinen D, Jacquot E, Zhao B, Gollotte A, Gianinazzi-Pearson V (1998) Characterization of root colonization profiles by microcosm community of arbuscular mycorrhizal fungi using 25S rRNA-target nested PCR. Mol Ecol 7:879–887

    Article  PubMed  Google Scholar 

  • Vierheilig H, Alt M, Neuhaus JM, Boller T, Wiemken A (1993) Colonization of transgenic Nicotiana sylvestris plants, expressing different forms of Nicotiana tabacum chitinase, by root pathogen Rhizoctonia solani and the mycorrhizal symbiont Glomus mosseae. Mol Plant Microbe Interact 6:261–264

    Article  CAS  Google Scholar 

  • Vierheilig H, Alt M, Lange J, Gut-Rella M, Wiemken A, Boller T (1995) Colonization of transgenic tobacco constitutively expressing pathogenesis-related proteins vesicular-arbuscular mycorrhizal fungus Glomus mosseae. Appl Environ Microbiol 61:3031–3034

    PubMed  CAS  Google Scholar 

  • Volpin H, Phillips D, Ocón Y, Kapulnik Y (1995) Suppression of an isoflavonoid phytoalexin defense response in mycorrhizal alfalfa roots. Plant Physiol 108:1449–1454

    PubMed  CAS  Google Scholar 

  • Walker C (1992) Systematics and taxonomy of the arbuscular endomycorrhizal fungi (Glomales)-a possible way forward. Agronomie 12:887–897

    Article  Google Scholar 

  • Walker C, Trappe JM (1993) Names and epithets in the Glomales and Endogonaceae. Mycol Res 97:339–344

    Article  Google Scholar 

  • Wegel E, Schauser L Sandal N Stougaard J Parniske M (1998) Mycorrhiza mutants of Lotus japonicus define genetically independent steps during symbiotic infection. Mol Plant Microbe Interact 11:933–936

    Article  CAS  Google Scholar 

  • Wright SF, Morton JB (1989) Detection of vesicular-arbuscular mycorrhizal fungus colonization of roots by using a dot-immunoblot assay. Appl Environ Microbiol 55:761–763

    PubMed  CAS  Google Scholar 

  • Wright SF, Upadhyaya A (1996) Extraction of an abundant and unusual protein from soil and comparison with hyphal protein of arbuscular mycorrhizal fungi. Soil Sci 161:575–586

    Article  CAS  Google Scholar 

  • Wyss P, Bonfante P (1993) Amplification of genomic DNA of arbuscular-mycorrhizal (AM) fungi by PCR using short arbitrary primers. Mycol Res 97:1351–1357

    Article  CAS  Google Scholar 

  • Zéze A, Sulistyowati E, Ophel-Keller K, Barker S, Smith SE (1997) Intrasporal genetic variation of Gigaspora margarita, a vesicular arbuscular mycorrhizal fungus, revealed by M13 minisatellite-primed PCR. Appl Environ Microbiol 63:676–678

    PubMed  Google Scholar 

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Requena, N., Breuninger, M. (2004). The Old Arbuscular Mycorrhizal Symbiosis in the Light of the Molecular Era. In: Esser, K., Lüttge, U., Beyschlag, W., Murata, J. (eds) Progress in Botany. Progress in Botany, vol 65. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-18819-0_13

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