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Review Paper: Arbuscular Mycorrhiza: Biological, Chemical, and Molecular Aspects

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Abstract

Mycorrhizas are the most important mutualistic symbioses on earth. The most prevalent type are the arbuscular mycorrhizas (AMs) that develop between roots of most terrestrial plants and fungal species of the Zygomycota. The AM fungi are able to grow into the root cortex forming intercellular hyphae from which highly branched structures, arbuscules, originate within cortex cells. The arbuscules are responsible for nutrient exchange between the host and the symbiont, transporting carbohydrates from the plant to the fungus and mineral nutrients, especially phosphate, and water from the fungus to the plant. Plants adapt their phosphate uptake to the interaction with the AM fungus by synthesis of specific phosphate transporters. Colonization of root cells induces dramatic changes in the cytoplasmic organization: vacuole fragmentation, transformation of the plasma membrane to a periarbuscular membrane covering the arbuscule, increase of the cytoplasm volume and numbers of cell organelles, as well as movement of the nucleus into a central position. The plastids form a dense network covering the symbiotic interface. In some of these changes, microtubules are most likely involved. With regard to the molecular crosstalk between the two organisms, a number of phytohormones (cytokinins, abscisic acid, jasmonate) as well as various secondary metabolites have been examined: (i) Jasmonates occur at elevated level, which is accompanied by cell-specific expression of genes involved in jasmonate biosynthesis that might be linked to strong carbohydrate sink function of AM roots and induced defense reactions; (ii) apocarotenoids (derivatives of mycorradicin and glycosylated cyclohexenones) accumulate in most mycorrhizal roots examined so far. Their biosynthesis via the nonmevalonate methylerythritol phosphate (MEP) pathway has been studied resulting in new insights into AM-specific gene expression and biosynthesis of secondary isoprenoids.

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References

  • Allen, M. F. 1996. The ecology of arbuscular mycorrhizas: A look back into the 20th century and a peak into the 21st. Mycol. Res. 100:769–782.

    Google Scholar 

  • Allen, M. F., Moore, T. S., Jr., and Christensen, M. 1980. Phytohormone changes in Bouteloua gracilis infected by vesicular-arbuscular mycorrhizae. Can. J. Bot. 58:371–374.

    Google Scholar 

  • Augé, R. M. 2001. Water relations, drought and VA mycorrhizal symbiosis. Mycorrhiza 11:3–42.

    Google Scholar 

  • Bago, B., Zipfel, W., Williams, R. M., Jun, J., Arreola, R., Lammers, P. J., Pfeffer, P. E., and Shachar-hill, Y. 2002. Translocation and utilization of fungal storage lipid in the arbuscular mycorrhizal symbiosis. Plant Physiol. 128:108–124.

    PubMed  Google Scholar 

  • Balestrini, R., Romera, C., Puigdomenech, P., and Bonfante, P. 1994. Location of a cell wall hydroxyproline-rich glycoprotein, cellulose and β-1,3-glucans in apical and differentiated regions of maize mycorrhizal roots. Planta 195:201–209.

    Google Scholar 

  • Barker, S. J. and Tagu, D. 2000. The roles of auxins and cytokinins in mycorrhizal symbioses. J. Plant Growth Regul. 19:144–154.

    PubMed  Google Scholar 

  • Becker, N. N. and Gerdemann, J. W. 1977. Colorimetric quantification of vesicular-arbuscular mycorrhizal infection in onion. New Phytol. 78:289–295.

    Google Scholar 

  • Bethlenfalvay, G. J. and Lindermann, R. G. 1992. Mycorrhizae in Sustainable Agriculture (Special Publication No. 54). Agronomy Society of America, Madison, Wisconsin.

    Google Scholar 

  • Bever, J. D. 2002. Host-specificity of AM fungal population growth rates can generate feedback on plant growth. Plant Soil 244:281–290.

    Google Scholar 

  • Bidartondo, M. I., Redecker, D., Hijri, I., Wiemken, A., Bruns, T. D., Dominguez, L., Sersic, A., Leake, J. R., and Read, D. J. 2002. Epiparasitic plants specialized on arbuscular mycorrhizal fungi. Nature 26:345–346.

    Google Scholar 

  • Blancaflor, E. B., Zhao, L. M., and Harrison, M. J. 2001. Microtubule organization in root cells of Medicago truncatula during development of an arbuscular mycorrhizal symbiosis with Glomus versiforme. Protoplasma 217:154–165.

    PubMed  Google Scholar 

  • Blee, K. A. and Anderson, A. J. 1996. Defense-related transcript accumulation in Phaseolus vulgaris L. colonized by the arbuscular mycorrhizal fungus Glomus intraradices Schenck & Smith. Plant Physiol. 110:675–688.

    PubMed  Google Scholar 

  • Bødker, L., Kjøllerz, R., and Rosendahl, S. 1998. Effect of phosphate and the arbuscular mycorrhizal fungus Glomus intraradices on disease severity of root rot of peas (Pisum sativum) caused by Aphanomyces euteiches. Mycorrhiza 8:169–174.

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Brundrett, M. C., Abbott, L. K., and Jasper, D. A. 1999. Glomalean mycorrhizal fungi from tropical Australia. I: Comparison of the effectiveness and specificity of different isolation procedures. Mycorrhiza 8:305–314.

    Google Scholar 

  • Carvalho, S. M., Caçador, I., and Martins-loução, A. 2001. Temporal and spatial variation of arbuscular mycorrhizas in salt marsh plants of the Tagus estuary (Portugal). Mycorrhiza 11:303–309.

    Google Scholar 

  • Cordier, C., Gianinazzi, S., and Gianinazzi-Pearson, V. 1996. Colonisation patterns of roots tissues by Phytophthora nicotianae var. parasitica related to reduced disease in mycorrhizal tomato. Plant Soil 185:223–232.

    Google Scholar 

  • Corkidi, L. and Rincón, E. 1997. Arbuscular mycorrhizae in a tropical sand dune ecosystem on the Gulf of Mexico. I: Mycorrhizal status and inoculum potential along a successional gradient. Mycorrhiza 7:9–15.

    Google Scholar 

  • Daft, M. and Nicholson, T. H. C. 1969. Effect of Endogone mycorrhiza on plant growth. III: Influence of inoculum concentration on growth and infection in tomato. New Phytol. 68:953–963.

    Google Scholar 

  • Dalpé, Y., Diop, T. A., Plenchette, C., and Gueye, M. 2000. Glomales species associated with surface and deep rhizosphere of Faidherbia albida in Senegal. Mycorrhiza 10:125–129.

    Google Scholar 

  • Danneberg, G., Latus, C., Zimmer, W., Hundeshagen, B., Schneider-poetsch, H., and Bothe, H. 1992. Influence of vesicular-arbuscular mycorrhiza on phytohormone balances in maize (Zea mays L.). J. Plant Physiol. 141:33–39.

    Google Scholar 

  • Douds, D. D., Pfeffer, P. E., and Shachar-hill, Y. 2000. Application of in vitro methods to study carbon uptake and transport by AM fungi. Plant Soil 226:255–261.

    Google Scholar 

  • Dugassa, G. D., VON Alten, H., and Schönbeck, F. 1996. Effects of arbuscular mycorrhiza (AM) on health of Linum usitatissimum L. infected by fungal pathogens. Plant Soil 185:173–182.

    Google Scholar 

  • Elias, K. S. and Safir, G. R. 1987. Hyphal elongation of Glomus fasciculatus in response to root exudates. Appl. Environ. Microbiol. 53:1928–1933.

    Google Scholar 

  • Elsen, A., Declerck, S., and De Waele, D. 2001. Effects of Glomus intraradices on the reproduction of the burrowing nematode (Radopholus similis) in dixenic culture. Mycorrhiza 11:49–51.

    Google Scholar 

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

    PubMed  Google Scholar 

  • Fester, T., Maier, W., and Strack, D. 1999. Accumulation of secondary compounds in barley and wheat roots in response to inoculation with an arbuscular mycorrhizal fungus and co-inoculation with rhizosphere bacteria. Mycorrhiza 8:241–246.

    Google Scholar 

  • Fester, T., Schmidt, D., Lohse, S., Walter, M. H., Giuliano, G., Bramley, P. M., Fraser, P. D., Hause, B., and Strack, D. 2002b Stimulation of carotenoid metabolism in arbuscular mycorrhizal roots. Planta 216:148–154.

    PubMed  Google Scholar 

  • Fester, T., Strack, D., and Hause, B. 2001. Reorganization of tobacco root plastids during arbuscule development. Planta 213:864–868.

    PubMed  Google Scholar 

  • Fitter, A. H. and Moyersoen, B. 1996. Evolutionary trends in root-microbe symbioses. Philos. Trans. R. Soc. B 351:1367–1375.

    Google Scholar 

  • Francis, R., Finlay, R. D., and Read, D. J. 1986. Vesicular-arbuscular mycorrhiza in natural vegetation. IV: Transfer of nutrients in inter-and intra-specific combinations of host plants. New Phytol. 102:103–111.

    Google Scholar 

  • Francis, R. and Read, D. J. 1994. The contributions of mycorrhizal fungi to the determination of plant community structure. Plant Soil 159:11–25.

    Google Scholar 

  • Frank, B. 1885. Ueber die auf Wurzelsymbiose beruhende Ernährung gewisser Bäume durch unterirdische Pilze. Ber. Dtsch. Bot. Ges. 3:128–145.

    Google Scholar 

  • Frank, B. 1888. über die physiologische Bedeutung der Mycorrhiza. Ber. Dtsch. Bot. Ges. 6:248–269.

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Fyson, A. and Oaks, A. 1992. Rapid methods for quantifying VAM fungal infections in maize roots. Plant Soil 147:317–319.

    Google Scholar 

  • Gaur, A. and Adholeya, A. 2002. Arbuscular-mycorrhizal inoculation of five tropical fodder crops and inoculum production in marginal soil amended with organic matter. Biol. Fertil. Soils 35:214–218.

    Google Scholar 

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

    Google Scholar 

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

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

    Google Scholar 

  • Gianinazzi-pearson, V., Smith, S. E., Gianinazzi, S., and Smith, F. A. 1991. Enzymatic studies on the metabolism of vesicular-arbuscular mycorrhizas. V: Is H+-ATPase a component of ATP-hydrolysing enzyme activities in plant-fungus interfaces? New Phytol. 117:61–74.

    Google Scholar 

  • Guadarrama, P. and álvarez-sánchez, F. J. 1999. Abundance of arbuscular mycorrhizal fungi spores in different environments in a tropical rain forest, Veracruz, Mexico. Mycorrhiza 8:267–270.

    Google Scholar 

  • Hans, J. 2003, in press. Doctoral Thesis. University Halle-Wittenberg, Halle, Germany.

  • Harborne, J. B. 1993. Introduction to Ecological Biochemistry, 4th Edition Academic Press, London.

    Google Scholar 

  • Harley, J. L. and Smith, S. E. 1983. Mycorrhizal Symbiosis. Academic Press, London.

    Google Scholar 

  • Harrison, M. J., Dewbre, G. R., and 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.

    PubMed  Google Scholar 

  • Harrison, M. J. and Dixon, R. A. 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. 6:643–654.

    Google Scholar 

  • Hartnett, D. C. and Wilson, G. W. T. 2002. The role of mycorrhizas in plant community structure and dynamics: Lessons from grasslands. Plant Soil 244:319–331.

    Google Scholar 

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

    PubMed  Google Scholar 

  • Imhof, S. 1999. Root morphology, anatomy and mycotrophy of the achlorophyllous Voyria aphylla (Jacq.) Pers. (Gentianaceae). Mycorrhiza 9:33–39.

    Google Scholar 

  • Jacquelinet-Jeanmougin, J., Gianinazzi-pearson, V., and Gianinazzi, S. 1987. Endomycorrhizas in the Gentianaceae. II: Ultrastructural aspects of symbiont relationships in Gentiana lutea L. Symbiosis 3:269–286.

    Google Scholar 

  • Jeffries, P. and Barea, J. M. 2001. Arbuscular mycorrhiza—A key component of sustainable plant-soil ecosystems, pp. 95–113, in B. Hock (Ed.)The Mycota, Vol. IX: Fungal Associations. Springer-Verlag, Berlin.

    Google Scholar 

  • Jones, F. R. 1924. A mycorrhizal fungus in the roots of legumes and some other plants. J. Agric. Res. 29:459–470.

    Google Scholar 

  • Journet, E.-P., van tuinen, D., Gouzy, J., Crespeau, H., Carreau, V., Farmer, M.-J., Niebel, A., Schiex, T., Jaillon, O., Chatagnier, O., Godiard, L., Micheli, F., Kahn, D., Gianinazzi-pearson, V., and Gamas, P. 2002. Exploring root symbiotic programs in the model legume Medicago truncatula using EST analysis. Nucleic Acids Res. 30:5579–5592.

    PubMed  Google Scholar 

  • Khan, A. G. (1993). Occurrence and importance of mycorrhizae in aquatic trees of New South Wales, Australia. Mycorrhiza 3:31–38.

    Google Scholar 

  • Kiers, E. T., West, S. A., and Denison, R. F. 2002. Mediating mutualisms: Farm management practices and evolutionary changes in symbiont co-operation. J. Appl. Ecol. 39:745–754.

    Google Scholar 

  • Kistner, C. and Parniske, M. 2002. Evolution of signal transduction in intracellular symbiosis. Trends Plant Sci. 7:511–518.

    PubMed  Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Köhler, R. H. and Hanson, M. R. 2000. Plastid tubules of higher plants are tissue-specific and developmentally regulated. J. Cell Sci. 113:81–89.

    PubMed  Google Scholar 

  • Koide, R. T. and Dickie, I. A. 2002. Effects of mycorrhizal fungi on plant populations. Plant Soil 244:307–317.

    Google Scholar 

  • Krajinski, F., Hause, B., Gianinazzi-Pearson, V., and Franken, P. 2002. Mtha1, a plasma membrane H+-ATPase gene from Medicago truncatula, shows arbuscule-specific induced expression in mycorrhizal tissue. Plant Biol. 4:754–761.

    Google Scholar 

  • Lambais, M. R. and Mehdy, M. C. 1993. Suppression of endochitinase, beta-1,3-endoglucanase, and chalcone isomerase expression in bean vesicular-arbuscular mycorrhizal roots under different soil phosphate conditions. Mol. Plant-Microbe Interact. 6:75–83.

    Google Scholar 

  • Lammers, P. J., Jun, J., Abubaker, J., Arreola, R., Gopalan, A., Bago, B., Hernandez-sebastia, C., Allen, J. W., Douds, D. D., Pfeffer, P. E., and Shachar-hill, Y. 2001. The glyoxylate cycle in the arbuscular mycorrhizal fungus. Carbon flux and gene expression. Plant Physiol. 127:1287–1298.

    PubMed  Google Scholar 

  • Landwehr, M., Hildebrandt, U., Wilde, P., Nawrath, K., Tóth, T., Biró, B., and Bothe, H. 2002. The arbuscular mycorrhizal fungus Glomus geosporum in European saline, sodic and gypsum soils. Mycorrhiza 12:199–211.

    PubMed  Google Scholar 

  • Lapopin, L. and Franken, P. 2000. Modification of plant gene expression, pp. 69–84, in Y. Kapulnik and D. D. Douds Jr. (Eds.). Arbuscular Mycorrhizas: Physiology and Function. Kluwer, Dordrecht, The Netherlands.

    Google Scholar 

  • Lichtenthaler, H. K., Schwender, J., Disch, A., and Rohmer, M. 1997. Biosynthesis of isoprenoids in higher plant chloroplasts proceeds via a mevalonate-independent pathway. FEBS Lett. 400:271–274.

    PubMed  Google Scholar 

  • Mäder, P., Edenhofer, S., Boller, T., Wiemken, A., and Niggli, U. 2000. Arbuscular mycorrhizae in a long-term field trial comparing low-input (organic, biological) and high-input (conventional) farming systems in a crop rotation. Biol. Fertil. Soils 31:150–156.

    Google Scholar 

  • Maier, W., Hammer, K., Dammann, U., Schulz, B., and Strack, D. 1997. Accumulation of sesquiterpenoid cyclohexenone derivatives induced by an arbuscular mycorrhizal fungus in members of the Poaceae. Planta 202:36–42.

    Google Scholar 

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

    PubMed  Google Scholar 

  • Maier, W., Schmidt, J., Nimtz, M., Wray, V., and Strack, D. 2000. Secondary products in mycorrhizal roots of tobacco and tomato. Phytochemistry 54:473–479.

    PubMed  Google Scholar 

  • Maier, W., Schmidt, J., Wray, V., Walter, M. H., and Strack, D. 1999. The mycorrhizal fungus, Glomus intraradices, induces the accumulation of cyclohexenone derivatives in tobacco roots. Planta 207:620–623.

    Google Scholar 

  • Maier, W., Schneider, B., and Strack, D. 1998. Biosynthesis of sesquiterpenoid cyclohexenone derivatives in mycorrhizal barley roots proceeds via the glyceraldehyde 3-phosphate/pyruvate pathway. Tetrahedron Lett. 39:521–524.

    Google Scholar 

  • Morton, J. B. and Benny, G. L. 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 emendation of Glomaceae. Mycotaxon 37:471–492.

    Google Scholar 

  • Nemec, S. and Lund, E. 1990. Leaf volatiles of mycorrhizal and nonmycorrhizal Citrus jambhiri Lush. J. Essent. Oil Res. 2:287–297.

    Google Scholar 

  • Paszkowski, U., Kroken, S., Roux, C., and Briggs, S. P. 2002. Rice phosphate transporters include an evolutionary divergent gene specifically activated in arbuscular mycorrhizal symbiosis. Proc. Natl. Acad. Sci. USA 99:13324–13329.

    PubMed  Google Scholar 

  • Peipp, H., Maier, W., Schmidt, J., Wray, V., and Strack, D. 1997 Arbuscular mycorrhizal fungus-induced changes in the accumulation of secondary compounds in barley roots. Phytochemistry 44:581–587.

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Perotto, S., Girlanda, M., and Martino, E. 2002. Ericoid mycorrhizal fungi: Some new perspectives on old acquaintances. Plant Soil 244:41–53.

    Google Scholar 

  • Pfeffer, P. E., Bago, B., and Shachar-hill, Y. 2001. Exploring mycorrhizal function with NMR spectroscopy. New Phytol. 150:543–553.

    Google Scholar 

  • Pfeffer, P. E., Douds, D. D., Bécard, G., and Shachar-hill, Y. 1999. Carbon uptake and the metabolism and transport of lipids in an arbuscular mycorrhiza. Plant Physiol. 120:587–598.

    PubMed  Google Scholar 

  • Phillips, J. M. and Hayman, D. S. 1970. Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans. Br. Mycol. Soc. 55:158–162.

    Google Scholar 

  • Rasmussen, H. N. 2002. Recent developments in the study of orchid mycorrhiza. Plant Soil 244:149–163.

    Google Scholar 

  • Rausch, C. and Bucher, M. 2002. Molecular mechanisms of phosphate transport in plants. Planta 216:23–37.

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • Read, D. J., Duckett, J. G., Francis, R., Ligrone, R., and Russell, A. 2000. Symbiotic fungal associations in “lower” land plants. Philos. Trans. R. Soc. B 355:815–831.

    Google Scholar 

  • Redecker, D., Kodner, R., and Graham, L. E. 2000. Glomalean fungi from the Ordovician. Science 289:1920–1921.

    PubMed  Google Scholar 

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

    Google Scholar 

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

    PubMed  Google Scholar 

  • Rodriguez-concepcion, M. and Boronat, A. 2002. Elucidation of the methylerythritol phosphate pathway for isoprenoid biosynthesis in bacteria and plastids. A metabolic milestone achieved through genomics. Plant Physiol. 130:1079–1089.

    PubMed  Google Scholar 

  • Rohmer, M. 1999. The mevalonate-independent methylerythritol 4-phosphate (MEP) pathway for isoprenoid biosynthesis, including carotenoids. Pure Appl. Chem. 71:2279–2284.

    Google Scholar 

  • Ryan, M. G. and Graham, J. H. 2002. Is there a role for arbuscular mycorrhizal fungi in production agriculture? Plant Soil 244:263–271.

    Google Scholar 

  • Saito, M. and Marumoto, T. 2002. Inoculation with arbuscular mycorrhizal fungi: The status quo in Japan and the future prospects. Plant Soil 244:273–279.

    Google Scholar 

  • Sanders, F. E., Tinker, B. P., Black, R. L. B., and Palmerly, S. M. 1977. The development of endomycorrhizal root systems. I: Speed of infection and growth-promoting effects with four species of vesicular-arbuscular endophyte. New Phytol. 78:257–268.

    Google Scholar 

  • Sanders, I. R., Clapp, J. P., and Wiemken, A. 1996. The genetic diversity of arbuscular mycorrhizal fungi in natural ecosystems—A key to understanding the ecology and functioning of the mycorrhizal symbiosis. New Phytol. 133:123–134.

    Google Scholar 

  • Schmitz, O., Danneberg, G., Hundeshagen, B., Klingner, A., and Bothe, H. 1991. Quantification of vesicular-arbuscular mycorrhiza by biochemical parameters. J. Plant Physiol. 139:106–114.

    Google Scholar 

  • Schüßler, A. 2000. Glomus claroideum forms an arbuscular mycorrhiza-like symbiosis with the hornwort Anthoceros punctatus. Mycorrhiza 10:15–21.

    Google Scholar 

  • Schüßler, A. 2002. Molecular phylogeny, taxonomy, and evolution of Geosiphon pyriformis and arbuscular mycorrhizal fungi. Plant Soil 244:75–83.

    Google Scholar 

  • Schüßler, A., Schwarzott, D., and walker, C. 2001. A new fungal phylum, the Glomeromycota: Phylogeny and evolution. Mycol. Res. 105:1413–1421.

    Google Scholar 

  • Schwartz, S. H., Qin, X. Q., and Zeevaart, J. A. D. 2001. Characterization of a novel carotenoid cleavage dioxygenase from plants. J. Biol. Chem. 276:25208–25211.

    PubMed  Google Scholar 

  • Sengupta, A. and Chaudhuri, S. 2002. Arbuscular mycorrhizal relations of mangrove plant community at the Ganges river estuary in India. Mycorrhiza 12:169–174.

    PubMed  Google Scholar 

  • Simon, L., Bousquet, J., Levesque, R. C., and Lalonde, M. 1993. Origin and diversification of endomycorrhizal fungi and coincidence with vascular land plants. Nature 363:67–69.

    Google Scholar 

  • Siqueira, J. O. and Saggin-júnior, O. J. 2001. Dependency on arbuscular mycorrhizal fungi and responsiveness of some Brazilian native woody species. Mycorrhiza 11:245–255.

    Google Scholar 

  • Slezack, S., Dumas-Gaudot, E., Paynot, M., and Gianinazzi, S. 2000. Is a fully established arbuscular mycorrhizal symbiosis required for bioprotection of Pisum sativum roots against Aphanomyces euteiches? Mol. Plant-Microbe Interact. 13:238–241.

    PubMed  Google Scholar 

  • Smith, S. E. and Read, D. J. 1997. Mycorrhizal Symbiosis, 2nd edn. Academic Press, London.

    Google Scholar 

  • Stougaard, J. 2001. Genetics and genomics of root symbiosis. Curr. Opin. Plant Biol. 4:328–335.

    PubMed  Google Scholar 

  • Stracke, S., Kistner, C., Yoshida, S., Mulder, L., Sato, S., Kaneko, T., Tabata, S., Sandal, N., Szczyglowski, K., and Parniske, M. 2002. A plant receptor-like kinase required for both bacterial and fungal symbionts. Nature 417:959–962.

    PubMed  Google Scholar 

  • Tagu, D., Lapeyrie, F., and Martin, F. 2002. The ectomycorrhizal symbiosis: Genetics and development. Plant Soil 244:97–105.

    Google Scholar 

  • Tan, B. C., Schwartz, S. H., Zeevaart, J. A. D., and Mccarty, D. R. 1997. Genetic control of abscisic acid biosynthesis in maize. Proc. Natl. Acad. Sci. USA 94:12235–12240.

    PubMed  Google Scholar 

  • Timonen, S. and Peterson, R. L. 2002. Cytoskeleton in mycorrhizal symbiosis. Plant Soil 244:199–210.

    Google Scholar 

  • Titus, J. H., Titus, P. J., Nowak, R. S., and Smith, S. D. 2002. Arbuscular mycorrhizae of Mojave Desert plants. Western N. Amer. Naturalist 62:327–334.

    Google Scholar 

  • Trapp, S. C. and Croteau, R. B. 2001. Genomic organization of plant terpene synthases and molecular evolutionary implications. Genetics 158:811–832.

    PubMed  Google Scholar 

  • Tsai, S. M. and Phillips, D. A. 1991. Flavonoids released naturally from alfalfa promote development of symbiotic Glomus spores in vitro. Appl. Environ. Microbiol. 57:1485–1488.

    Google Scholar 

  • Vaast, Ph., Caswell-chen, E. P., and Zasoski, R. J. 1998. Influences of a root-lesion nematode, Pratylenchus coffeae, and two arbuscular mycorrhizal fungi, Acaulospora mellea and Glomus clarum on coffee (Coffea arabica L.). Biol. Fertil. Soils 26:130–135.

    Google Scholar 

  • vAN DER Heijden, M. G. A., Klironomos, J. N., Ursic, M., Moutoglis, P., Streitwolf-engel, R., Boller, T., Wiemken, A., and Sanders, I. R. 1998. Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396:69–72.

    Google Scholar 

  • Vassilev, N., Vassileva, M., Azcon, R., and Medina, A. 2001. Application of free and Ca-alginate-entrapped Glomus deserticola and Yarowia lipolytica in a soil-plant system. J. Biotechnol. 91:237–242.

    PubMed  Google Scholar 

  • Vázquez, M. M., Azcon, R., and Barea, J. M. 2001. Compatibility of a wild type and its genetically modified Sinorhizobium strain with two mycorrhizal fungi on Medicago species as affected by drought stress. Plant Sci. 161:347–358.

    PubMed  Google Scholar 

  • Vázquez, M. M., César, S., Azcón, R., and Barea, J. M. 2000. Interactions between arbuscular mycorrhizal fungi and other microbial inoculants (Azospirillum, Pseudomonas, Trichoderma) and their effects on microbial population and enzyme activities in the rhizosphere of maize plants. Appl. Soil Ecol. 15:261–272.

    Google Scholar 

  • Vierheilig, H., Alt, M., Mohr, U., Boller, T., and Wiemken, A. 1994. Ethylene biosynthesis and activities of chitinase and beta-1,3-glucanase in the roots of host and nonhost plants of vesicular-arbuscular mycorrhizal fungi after inoculation with Glomus mosseae. J. Plant Physiol. 143:337–343.

    Google Scholar 

  • Vierheilig, H., Iseli, B., Alt, M., Raikhel, N., Wiemken, A., and Boller, T. 1996. Resistance of Urtica dioica to mycorrhizal colonization: A possible involvement of Urtica dioica agglutinin. Plant Soil 183:131–136.

    Google Scholar 

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

    Google Scholar 

  • Voiblet, C., Duplessis, S., Encelot, N., and Martin, F. 2001. Identification of symbiosis-regulated genes in Eucalyptus globulus-Pisolithus tinctorius ectomycorrhiza by differential hydridization of arrayed cDNAs. Plant J. 25:181–191.

    PubMed  Google Scholar 

  • Volpin, H., Elkind, Y., Okon, Y., and Kapulnik, Y. 1994. A vesicular-arbuscular mycorrhizal fungus (Glomus intraradix) induces a defense response in alfalfa root. Plant Physiol. 104:683–689.

    PubMed  Google Scholar 

  • Walter, M. H., Fester, T., and Strack, D. 2000. Arbuscular mycorrhizal fungi induce the nonmevalonate methylerythritol phosphate pathway of isoprenoid biosynthesis correlated with accumulation of the “yellow pigment” and other apocarotenoids. Plant J. 21:571–578.

    PubMed  Google Scholar 

  • Walter, M. H., Hans, J., and 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  Google Scholar 

  • Wasternack, C. and Hause, B. 2002. Jasmonates and octadecanoids: Signals in plant stress responses and development. Prog. Nucleic Acids Res. Mol. Biol. 72:165–221.

    Google Scholar 

  • Wright, D. P., Read, D. J., and Scholes, J. D. 1998. Mycorrhizal sink strength influences whole plant carbon balance of Trifolium repens L. Plant Cell Environ. 21:881–891.

    Google Scholar 

  • Yamato, M. 2001. Identification of a mycorrhizal fungus in the roots of achlorophyllous Sciaphila tosaensis Makino (Triuridaceae). Mycorrhiza 11:83–88.

    Google Scholar 

  • Yano-melo, A. M., Maia, L. C., Saggin, O. J. Jr., Lima-filho, J. M., and Melo, N. F. 1999. Effect of arbuscular mycorrhizal fungi on the acclimatization of micropropagated banana plantlets. Mycorrhiza 9:119–123.

    Google Scholar 

  • Zhao, Z.-W., Xia, Y.-M., Qin, X.-Z., Li, X.-W., Cheng, L.-Z., Sha, T., and Wang, G.-H. 2001. Arbuscular mycorrhizal status of plants and the spore density of arbuscular mycorrhizal fungi in the tropical rain forest of Xishuangbanna, southwest China. Mycorrhiza 11:159–162.

    Google Scholar 

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Strack, D., Fester, T., Hause, B. et al. Review Paper: Arbuscular Mycorrhiza: Biological, Chemical, and Molecular Aspects. J Chem Ecol 29, 1955–1979 (2003). https://doi.org/10.1023/A:1025695032113

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