, Volume 221, Issue 2, pp 184–196 | Cite as

Molecular and cell biology of arbuscular mycorrhizal symbiosis

  • Bettina HauseEmail author
  • Thomas Fester
Original Article


The roots of most extant plants are able to become engaged in an interaction with a small group of fungi of the fungal order Glomales (Glomeromycota). This interaction—arbuscular mycorrhizal (AM) symbiosis—is the evolutionary precursor of most other mutualistic root-microbe associations. The molecular analysis of this interaction can elucidate basic principles regarding such associations. This review summarizes our present knowledge about cellular and molecular aspects of AM. Emphasis is placed on morphological changes in colonized cells, transfer of nutrients between both interacting partners, and plant defence responses. Similarities to and differences from other associations of plant and microorganisms are highlighted regarding defence reactions and signal perception.


Arbuscular mycorrhizal fungi Defence response Induced systemic resistance Morphology of arbuscule-containing cells Nutrient transfer Signal transduction 



Arbuscular mycorrhiza(l)


Calcium and calmodulin-dependent protein kinase




Endoplasmatic reticulum


Expressed sequence tag


Green fluorescent protein


Nodulation receptor kinase


Nod factor receptor


Mutants affected in symbioses


Symbiosis receptor-like kinase



We thank D. Strack for critical reading of the manuscript and S. Schaarschmidt for help in preparing Fig. 3. We apologize to those colleagues whose work was not cited because of space limitations. Our work is supported by the Deutsche Forschungsgemeinschaft (DFG) within the Focus Program “Molecular Basics of Mycorrhizal Symbioses”.


  1. Ané J-M, Lévy J, Thoquet P, Kulikova O, de Billy F, Penmetsa V, Kim DJ, Debelle F, Rosenberg C, Cook DR, Bisseling T, Huguet T, Denarie J (2002) Genetic and cytogenetic mapping of DMI1, DMI2, and DMI3 genes of Medicago truncatula involved in Nod factor transduction, nodulation, and mycorrhization. Mol Plant Microbe Interact 15:1108–1118PubMedGoogle Scholar
  2. 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 303:1364–1367CrossRefPubMedGoogle Scholar
  3. Arines J, Palma JM, Vilarino A (1993) Comparison of protein patterns in non-mycorrhizal and vesicular-arbuscular mycorrhizal roots of red clover. New Phytol 123:736–768Google Scholar
  4. Arines J, Quintela M, Vilarino A, Palma JM (1994a) Protein patterns and superoxide dismutase activity in non-mycorrhizal and arbuscular-mycorrhizal Pisum sativum L. plants. Plant Soil 166:37–45Google Scholar
  5. Arines J, Vilarino A, Palma JM (1994b) Involvement of the superoxide dismutase enzyme in the mycorrhization process. Agric Sci Finl 3:303–306Google Scholar
  6. Asamizu E, Nakamura Y, Sato S, Tabata S (2000) Generation of 7137 non-redundant expressed sequence tags from a legume, Lotus japonicus. DNA Res 7:127–130PubMedGoogle Scholar
  7. Augé R (2001) Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza 11:3–42Google Scholar
  8. 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 128:108–124CrossRefPubMedGoogle Scholar
  9. Bago B, Pfeffer PE, Abubaker J, Jun J, Allen JW, Brouillette J, Douds DD, Lammers PJ, Shachar-Hill Y (2003) Carbon eport from arbuscular mycorrhizal roots involves the translocation of carbohydrate as well as lipid. Plant Physiol 131:1496–1507CrossRefPubMedGoogle Scholar
  10. Balestrini R, Romera C, Puigdomenech P, 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 195:201–209CrossRefGoogle Scholar
  11. Barker SJ, Stummer B, Gao L, Dispain I, O’Connor P, Smith SE (1998) A mutant in Lycopersicon esculentum Mill. with highly reduced VA mycorrhizal colonisation. Isolation and preliminary characterisation. Plant J 15:791–797CrossRefGoogle Scholar
  12. Bell CJ, Dixon RA, Farmer AD, Flores R, Inman J, Gonzales RA, Harrison MJ, Paiva NL, Scott AD, Weller JW, May GD (2001) The medicago genome initiative: a model legume database. Nucleic Acids Res 29:114–117CrossRefPubMedGoogle Scholar
  13. Benabdellah K, Azcon-Aguilar C, Ferrol N (1998) Soluble and membrane symbiosis-related polypeptides associated with the development of arbuscular mycorrhizas in tomato (Lycopersicon esculentum). New Phytol 140:135–143CrossRefGoogle Scholar
  14. Benabdellah K, Azcon-Aguilar C, Ferrol N (2000) Alterations in the plasma membrane polypeptide pattern of tomato roots (Lycopersicon esculentum) during the development of arbuscular mycorrhiza. J Exp Bot 51:747–754CrossRefPubMedGoogle Scholar
  15. Bestel-Corre G, Gianinazzi S, Dumas-Gaudot E (2004) Impact of sewage sludges on Medicago truncatula symbiotic proteome. Phytochemistry 65:1651–1659CrossRefPubMedGoogle Scholar
  16. Bidartondo MI, Redecker D, Hijri I, Wiemken A, Bruns TD, Dominguez L, Sersic A, Leake JR, Read DJ (2002) Epiparasitic plants specialized on arbuscular mycorrhizal fungi. Nature 419:345–346CrossRefPubMedGoogle Scholar
  17. Blancaflor E, Zhao L, Harrison M (2001) Microtubule organization in root cells of Medicago truncatula during development of an arbuscular mycorrhizal symbiosis with Glomus versiforme. Protoplasma 217:154–165PubMedGoogle Scholar
  18. Blee KA, Anderson AJ (1996) Defense-related transcript accumulation in Phaseolus vulgaris L. colonized by the arbuscular mycorrhizal fungus Glomus intraradices Schenk and Smith. Plant Physiol 110:675–699PubMedGoogle Scholar
  19. Blilou I, Bueno P, Ocampo JA, García-Garrido JM (2000) Induction of catalase and ascorbate peroxidase activities in tobacco roots inoculated with the arbuscular mycorrhizal fungus Glomus mosseae. Mycol Res 104:722–725CrossRefGoogle Scholar
  20. Boisson-Dernier A, Chabaud M, Garcia F, Bécard G, Rosenberg C, Barker DG (2001) Agrobacterium rhizogenes-transformed roots of Medicago truncatula for the study of nitrogen-fixing and endomycorrhizal symbiotic associations. Mol Plant-Microbe Interact 14:695–700PubMedGoogle Scholar
  21. Boller T (1987) Hydrolytic enzymes in plant disease resistance. In: Kosuge T, Nester EW (eds) Plant-microbe interactions, vol 2. Macmillan, New York, pp 385–413Google Scholar
  22. Bonanomi A, Wiemken A, Boller T, Salzer P (2001) Local induction of a mycorrhiza-specific class III chitinase gene in cortical root cells of Medicago truncatula containing developing or mature arbuscules. Plant Biol 3:194–200CrossRefGoogle Scholar
  23. Bonfante P, Perotto S (1995) Strategies of arbuscular mycorrhizal fungi when infecting host plants. New Phytol 130:3–21Google Scholar
  24. Bonfante P, Bergero R, Uribe X, Romera C, Rigau J, Puigdomenech P (1996) Transcriptional activation of a maize α–tubulin gene in mycorrhizal maize and transgenic tobacco plants. Plant J 9:737–743CrossRefGoogle Scholar
  25. Bradbury SM, Peterson RL, Bowley SR (1991) Interactions between three alfalfa nodulation genotypes and two Glomus species. New Phytol 119:115–120Google Scholar
  26. Burleigh SH, Harrison MJ (1997) A novel gene whose expression in Medicago truncatula is suppressed in response to colonization by vesicular-arbuscular mycorrhizal fungi and to phosphate nutrition. Plant Mol Biol 34:199–208CrossRefPubMedGoogle Scholar
  27. Buuren ML van , 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 12:171–181PubMedGoogle Scholar
  28. Calantzis C, Morandi D, Gianinazzi-Pearson V (1998) Cellular interactions between G. mosseae and a myc 1nod mutant in Medicago truncatula. In: Ahonen-Jonnarth U, Danell E, Fransson P, Karen O, Lindahl B, Rangel I, Finlay R (eds) Abstract 2nd international Conference on Mycorrhizae. SLU Service/Repro, Uppsala, 1998, pp 38Google Scholar
  29. Carling DE, Brown MF (1982) Anatomy and physiology of vesicular-arbuscular and nonmycorrhizal roots. Phytopathology 72:1108–1114Google Scholar
  30. Catoira R, Galera C, Billy Fd, Penmetsa R, Journet E-P, Maillet F, Rosenberg C, Cook D, Gough C, Dénarié J (2000) Four genes of Medicago truncatula controlling components of a Nod factor transduction pathway. Plant Cell 12:1647–1665CrossRefPubMedGoogle Scholar
  31. Chabaud M, Larsonneau C, Marmouget C, Huguet T (1996) Transformation of barrel medic (Medicago truncatula Gaertn.) by Agrobacterium tumefaciens and regeneration via somatic embryogenesis of transgenic plants with the MtENOD12 nodulin promoter fused to the gus reporter gene. Plant Cell Rep 15:305–310CrossRefGoogle Scholar
  32. Chabaud M, Venard C, Defaux-Petras A, Becard 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 156:265–273CrossRefGoogle Scholar
  33. Collinge DB, Kragh KM, Mikkelsen JD, Nielsen KK, Rasmussen U, Vad K (1993) Plant chitinases. Plant J 3:31–40CrossRefPubMedGoogle Scholar
  34. Cordier C, Pozo M, Barea J, Gianinazzi S, Gianinazzi-Pearson V (1998) Cell defense responses associated with localized and systemic resistance to Phytophthora parasitica induced in tomato by an arbuscular mycorrhizal fungus. Mol Plant-Microbe Interact 11:1017–1028Google Scholar
  35. Dassi B, Samra A, Dumas-Gaudot E, Gianinazzi S (1999) Different polypeptide profiles from tomato roots following interactions with arbuscular mycorrhizal (Glomus mosseae) or pathogenic (Phytophthora parasitica) fungi. Symbiosis 26:65–77Google Scholar
  36. David R, Itzhaki H, Ginzberg I, Gafni Y, Galili G, Kapulnik Y (1998) Suppression of tobacco basic chitinase gene expression in response to colonization by the arbuscular mycorrhizal fungus Glomus intraradices. Mol Plant-Microbe Interact 11:489–497PubMedGoogle Scholar
  37. 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 27:561–569CrossRefPubMedGoogle Scholar
  38. 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 16:382–388PubMedGoogle Scholar
  39. Demchenko K, Winzer T, Stougaard J, Parniske M, Pawlowski K (2004) Distinct roles of Lotus japonicus SYMRK and SYM15 in root colonization and arbuscule formation. New Phytol 163:381–392CrossRefGoogle Scholar
  40. Douds DD, Pfeffer PE, Shachar-Hill Y (2000) Carbon partitioning, cost, and metabolism of arbuscular mycorrhizas. In: Kapulnik Y, Douds DD (eds) Arbuscular mycorrhizas: physiology and function. Kluwer, Dordrecht, pp 107–129Google Scholar
  41. Duc G, Trouvelot A, Gianinazzi-Pearson V, Gianinazzi S (1989) First report of non-mycorrhizal mutants (myc) obtained in pea (Pisum sativum L.) and fababean (Vicia faba L.). Plant Sci 60:215–222CrossRefGoogle Scholar
  42. Dumas-Gaudot E, Guillaume P, Tahiri-Alaoui A, Gianinazzi-Pearson V, Gianinazzi S (1994) Changes in polypeptide patterns in tobacco roots colonised by Glomus species. Mycorrhiza 4:215–221CrossRefGoogle Scholar
  43. Dumas-Gaudot E, Gollotte A, Cordier C, Gianinazzi S, Gianinazzi-Pearson V (2000) Modulation of host defence systems. In: Kapulnik Y, Douds DD (eds) Arbuscular mycorrhizas: physiology and function. Kluwer, Dordrecht, pp 173–200Google Scholar
  44. Endre G, Kereszt A, Kevei Z, Mihacea S, Kalo P, Kiss GB (2002) A receptor kinase gene regulating symbiotic nodule development. Nature 417:962–966CrossRefPubMedGoogle Scholar
  45. Ferrol N, Barea JM, Azcon-Aguilar C (2000) The plasma membrane H+-ATPase gene family in the arbuscular mycorrhizal fungus Glomus mosseae. Curr Genet 37:112–118CrossRefPubMedGoogle Scholar
  46. Fester T, Strack D, Hause B (2001) Reorganization of tobacco root plastids during arbuscule development. Planta 213:864–868PubMedGoogle Scholar
  47. Fester T, Kiess M, Strack D (2002) A mycorrhiza-responsive protein in wheat roots. Mycorrhiza 12:219–222CrossRefPubMedGoogle Scholar
  48. Franken P, Requena N (2001) Molecular approaches to arbuscular mycorrhiza functioning. The mycota IX: fungal associations, Springer, Berlin Heidelberg New YorkGoogle Scholar
  49. Frühling M, Roussel H, Gianinazzi-Pearson V, Puhler A, Perlick AM (1997) The Vicia faba leghemoglobin gene VfLb29 is induced in root nodules and in roots colonized by the arbuscular mycorrhizal fungus Glomus fasciculatum. Mol Plant-Microbe Interact 10:124–131PubMedGoogle Scholar
  50. García-Garrido JM, Ocampo JA (2002) Regulation of the plant defence response in arbuscular mycorrhizal symbiosis. J Exp Bot 53:1377–1386CrossRefPubMedGoogle Scholar
  51. García-Garrido JM, Toro N, Ocampo JA (1993) Presence of specific polypeptides in onion roots colonized by Glomus mosseae. Mycorrhiza 2:175–177Google Scholar
  52. Genre A, Bonfante P (1997) A mycorrhizal fungus changes microtubule orientation in tobacco root cells. Protoplasma 199:30–38Google Scholar
  53. Genre A, Bonfante P (1998) Actin versus tubulin configuration in arbuscule-containing cells from mycorrhizal tobacco roots. New Phytol 140:745–752CrossRefGoogle Scholar
  54. Gianinazzi-Pearson V (1996) Plant cell responses to arbuscular mycorrhizal fungi: getting to the roots of the symbiosis. Plant Cell 8:1871–1883CrossRefPubMedGoogle Scholar
  55. Gianinazzi-Pearson V, Smith SE, Gianinazzi S, Smith FA (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 117:61–76Google Scholar
  56. Gianinazzi-Pearson V, Tahiri-Alaoui A, Antoniw JF, Gianinazzi S, Dumas E (1992) Weak expression of the pathogenesis related PR-b1 gene and localization of related protein during symbiotic endomycorrhizal interactions in tobacco roots. Endocyt Cell Res 8:177–185Google Scholar
  57. Gianinazzi-Pearson V, Dumas-Gaudot E, Gollotte A, Tahiri-Alaoui A, Gianinazzi S (1996) Cellular and molecular defence-related root responses to invasion by arbuscular mycorrhizal fungi. New Phytol 133:45–57Google Scholar
  58. 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 211:609–613CrossRefPubMedGoogle Scholar
  59. 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’ mutant of Pisum sativum (L.). Planta 191:112–122CrossRefGoogle Scholar
  60. Guenoune D, Galili S, Phillips D, Volpin H, Chet I, Okon Y, Kapulnik Y (2001) The defense response elicited by the pathogen Rhizoctonia solani is suppressed by colonization of the AM-fungus Glomus intraradices. Plant Sci 160:925–932CrossRefPubMedGoogle Scholar
  61. Guttenberger M (2000) Arbuscules of vesicular-arbuscular mycorrhizal fungi inhabit an acidic compartment within plant roots. Planta 211:299–304CrossRefPubMedGoogle Scholar
  62. Hans J, Hause B, Strack D, Walter MH (2004) Cloning, characterization, and immunolocalization of a mycorrhiza-inducible 1-deoxy-D-xylulose 5-phosphate reductoisomerase in arbuscule-containing cells of maize. Plant Physiol 134:614–624CrossRefPubMedGoogle Scholar
  63. Harrison MJ (1996) A sugar transporter from Medicago truncatula: altered expression pattern in roots during vesicular-arbuscular (VA) mycorrhizal associations. Plant J 9:491–503CrossRefPubMedGoogle Scholar
  64. Harrison M (1999) Molecular and cellular aspects of the arbuscular mycorrhizal symbiosis. Annu Rev Plant Physiol Plant Mol Biol 50:361–389CrossRefPubMedGoogle Scholar
  65. Harrison M, Dixon R (1994) Spatial patterns of expression of flavonoid/isoflavonoid pathway genes during interactions between roots of Medicago truncatula and the mycorrhizal fungus Glomus versiforme. Plant J 6:9–20CrossRefGoogle Scholar
  66. Harrison MJ, Van Buuren ML (1995) A phosphate transporter from the mycorrhizal fungus Glomus versiforme. Nature 378:626–629CrossRefPubMedGoogle Scholar
  67. 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 14:2413–2429CrossRefPubMedGoogle Scholar
  68. Hause B, Maier W, Miersch O, Kramell R, Strack D (2002) Induction of jasmonate biosynthesis in arbuscular mycorrhizal barley roots. Plant Physiol 130:1213–1220CrossRefPubMedGoogle Scholar
  69. Hayashi M, Miyahara A, Sato S, Kato T, Yoshikawa M, Taketa M, Hayashi M, Pedrosa A, Onda R, Imaizumi-Anraku H, Bachmair A, Sandal N, Stougaard J, Murooka Y, Tabata S, Kawasaki S, Kawaguchi M, Harada K (2001) Construction of a genetic linkage map of the model legume Lotus japonicus using an intraspecific F2 population. DNA Res 8:301–310PubMedGoogle Scholar
  70. Heckman DS, Geiser DM, Eidell BR, Stauffer RL, Kardos NL, Hedges SB (2001) Molecular evidence for the early colonization of land by fungi and plants. Science 293:1129–1133PubMedGoogle Scholar
  71. Hildebrandt U, Schmelzer E, Bothe H (2002) Expression of nitrate transporter genes in tomato colonized by an arbuscular mycorrhizal fungus. Physiol Plant 115:125–136CrossRefPubMedGoogle Scholar
  72. Hodge A, Campbell CD, Fitter AH (2001) An arbuscular mycorrhizal fungus accelerates decomposition and acquires nitrogen directly from organic material. Nature 413:297–299CrossRefPubMedGoogle Scholar
  73. Hohnjec N, Perlick AM, Puhler A, Kuster H (2003) The Medicago truncatula sucrose synthase gene MtSucS1 is activated both in the infected region of root nodules and in the cortex of roots colonized by arbuscular mycorrhizal fungi. Mol Plant-Microbe Interact 16:903–915PubMedGoogle Scholar
  74. Imhof S (1999) Root morphology, anatomy and mycotrophy of the achlorophyllous Voyria aphylla (Jacq.) Pers. (Gentianaceae). Mycorrhiza 9:33–39CrossRefGoogle Scholar
  75. Jacobi LM, Petrova OS, Tsyganov VE, Borisov AY, Tikhonovich IA (2003a) Effect of mutations in the pea genes Sym33 and Sym40. I. Arbuscular mycorrhiza formation and function. Mycorrhiza 13:3–7PubMedGoogle Scholar
  76. Jacobi LM, Zubkova LA, Barmicheva EM, Tsyganov VE, Borisov AY, Tikhonovich IA (2003b) Effect of mutations in the pea genes Sym33 and Sym40. II. Dynamics of arbuscule development and turnover. Mycorrhiza 13:9–16PubMedGoogle Scholar
  77. Jacquelinet-Jeanmougin J, Gianinazzi-Pearson V, Gianinazzi S (1987) Endomycorrhizas in the Gentianaceae. II. Ultrastructural aspects of symbiont relationships in Gentiana lutea L. Symbiosis 3:269–286Google Scholar
  78. Journet EP, van Tuinen D, Gouzy J, Crespeau H, Carreau V, Farmer MJ, Niebel A, Schiex T, Jaillon O, Chatagnier O, Godiard L, Micheli F, Kahn D, Gianinazzi-Pearson V, Gamas P (2002) Exploring root symbiotic programs in the model legume Medicago truncatula using EST analysis. Nucleic Acids Res 30:5579–5592CrossRefPubMedGoogle Scholar
  79. Kaldorf M, Schmelzer E, Bothe H (1998) Expression of maize and fungal nitrate reductase genes in arbuscular mycorrhiza. Mol Plant Microbe Interact 11:439–448PubMedGoogle Scholar
  80. Kato T, Sato S, Nakamura Y, Kaneko T, Asamizu E, Tabata S (2003) Structural analysis of a Lotus japonicus genome. V. Sequence features and mapping of sixty-four TAC clones which cover the 6.4 Mb regions of the genome. DNA Res 10:277–285Google Scholar
  81. Kistner C, Parniske M (2002) Evolution of signal transduction in intracellular symbiosis. Trends Plant Sci 7:511–518 CrossRefPubMedGoogle Scholar
  82. Kjoller R, Rosendahl S (1996) The presence of the arbuscular mycorrhizal fungus Glomus intraradices influences enzymatic activities of the root pathogen Aphanomyces euteiches in pea roots. Mycorrhiza 6:487–491Google Scholar
  83. Kling M, Gianinazzi-Pearson V, Lherminier J, Jakobsen I (1996) The development and functioning of mycorrhizas in pea mutants. In: First International Conference on Mycorrhizae, Program and abstracts, Berkeley, CA, USA, p 71Google Scholar
  84. Köhler R, Hanson M (2000) Plastid tubules of higher plants are tissue-specific and developmentally regulated. J Cell Sci 113:81–89PubMedGoogle Scholar
  85. Kosuta S, Chabaud M, Lougnon G, Gough C, Dénarié J, Barker D, Bécard G (2003) A diffusible factor from arbuscular mycorrhizal fungi induces symbiosis-specific MtENOD11 expression in roots of Medicago truncatula. Plant Physiol 131:952–962CrossRefPubMedGoogle Scholar
  86. Krajinski F, Biela A, Schubert D, Gianinazzi-Pearson V, Kaldenhoff R, Franken P (2000) Arbuscular mycorrhiza development regulates the mRNA abundance of Mtaqp1 encoding a mercury-insensitive aquaporin of Medicago truncatula. Planta 211:85–90CrossRefPubMedGoogle Scholar
  87. Krajinski F, Hause B, Gianinazzi-Pearson V, Franken P (2002) Mtha1, a plasma membrane H+ -ATPase gene from Medicago truncatula, shows arbuscule-specific induced expression in mycorrhizal tissue. Plant Biol 4:754–761CrossRefGoogle Scholar
  88. Kuhn G, Hijri M, Sanders IR (2001) Evidence for the evolution of multiple genomes in arbuscular mycorrhizal fungi. Nature 414:745–748CrossRefPubMedGoogle Scholar
  89. Kulikova O, Gualtieri G, Geurts R, Kim DJ, Cook D, Huguet T, de Jong JH, Fransz PF, Bisseling T (2001) Integration of the FISH pachytene and genetic maps of Medicago truncatula. Plant J 27:49–58CrossRefPubMedGoogle Scholar
  90. Lambais MR (2000) Regulation of plant defence-related genes in arbuscular mycorrhizae. In: Podila GK, Douds DD (eds) Current advances in mycorrhizae research. American Phytopathological Society, Minnesota, pp 45–59Google Scholar
  91. Lambais MR, Mehdy MC (1993) Suppression of endochitinases, β-1,3-endoglucanase, and chalcone isomerase expression in bean vesicular-arbuscular mycorrhiza under different soil phosphate conditions. Mol Plant-Microbe Interact 6:75–83Google Scholar
  92. Lambais MR, Mehdy MC (1998) Spatial distribution of chitinases and β-1,3-glucanase transcripts in bean arbuscular mycorrhizal roots under low and high soil phosphate conditions. New Phytol 140:33–42CrossRefGoogle Scholar
  93. Lamblin AF, Crow JA, Johnson JE, Silverstein KA, Kunau TM, Kilian A, Benz D, Stromvik M, EndrŽ G, VandenBosch KA, Cook DR, Young ND, Retzel EF (2003) MtDB: a database for personalized data mining of the model legume Medicago truncatula transcriptome. Nucleic Acids Res 31:196–201CrossRefPubMedGoogle Scholar
  94. Leake JR (1994) The biology of myco-heterotrophic (‘saprophytic’) plants. New Phytol 127:171–216Google Scholar
  95. Lévy J, Bres C, Geurts R, Chalhoub B, Kulikova O, Duc G, Journet E-P, Rosenberg C, Debellé F (2004) A putative Ca2+ and calmodulin-dependent protein kinase required for bacterial and fungal symbioses. Science 303:1361–1364CrossRefPubMedGoogle Scholar
  96. Linderman RG (2000) Effects of mycorrhizas on plant tolerances to diseases. In: Kapulnik Y, Douds DD (eds) Arbuscular mycorrhizas: physiology and function. Kluwer, Dordrecht, pp 345–365Google Scholar
  97. Liu J, Blaylock LA, Endre G, Choc J, Town CD, VandenBosch KA, Harrison MJ (2003) Transcript profiling coupled with spatial expression analyses reveals genes involved in distinct developmental stages of an arbuscular mycorrhizal symbiosis. Plant Cell 15:2106–2123CrossRefPubMedGoogle Scholar
  98. Long SR (1996) Rhizobium symbiosis: Nod factors in perspective. Plant Cell 8:1885–1898CrossRefPubMedGoogle Scholar
  99. Madsen E, Madsen L, Radutoiu S, Szczyglowski K, Sato S, Kaneko T, Tabata S, Sandal N, Stougaard J (2003) A receptor kinase gene of the LysM type is involved in legume perception of rhizobial signals. Nature 425:637–640CrossRefPubMedGoogle Scholar
  100. Maldonado-Mendoza IE, Dewbre GR, Harrison MJ (2001) A phosphate transporter gene from the extra-radical mycelium of an arbuscular mycorrhizal fungus Glomus intraradices is regulated in response to phosphate in the environment. Mol Plant Microbe Interact 14:1140–1148PubMedGoogle Scholar
  101. 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 256:37–44CrossRefPubMedGoogle Scholar
  102. Marx C, Dexheimer J, Gianinazzi-Pearson V, Gianinazzi S (1982) Enzymatic studies on the metabolism of vesicular-arbuscular mycorrhizas IV. Ultracytoenzymological evidence (ATPase) for active transfer processes in the host-arbuscular interface. New Phytol 90:37–43Google Scholar
  103. Matsubara Y, Uetake Y, Peterson RL (1999) Entry and colonization of Asparagus offizinalis roots by arbuscular mycorrhizal fungi with emphasis on changes in host microtubules. Can J Bot 77:1159–1167CrossRefGoogle Scholar
  104. Meyer J, Dehne H-W (1986) The influence of VA mycorrhizae on biotrophic leaf pathogens. In: Physiological and genetical aspects of mycorrhizae. Proceedings of the First European Symposium on Mycorrhizae, Dijon, pp 781–786Google Scholar
  105. 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 101:4701–4705CrossRefPubMedGoogle Scholar
  106. Morandi D, Bailey JA, Gianinazzi-Pearson V (1984) Isoflavonoid accumulation in soybean roots infected with vesicular-arbuscular mycorrhizal fungi. Physiol Plant Pathol 24:357–364Google Scholar
  107. Morandi D, Sagan M, Prado-Vivant E, Duc G (2000) Influence of genes determining supernodulation on root colonization by the mycorrhizal fungus Glomus mosseae in Pisum sativum and Medicago truncatula mutants. Mycorrhiza 10:37–42CrossRefGoogle Scholar
  108. Murphy PJ, Langridge P, Smith SE (1997) Cloning plant genes differentially expressed during colonisation of Hordeum vulgare L. by the vesicular-arbuscular mycorrhizal fungus Glomus intraradices. New Phytol 135:291–301CrossRefGoogle Scholar
  109. Mylona P, Pawlowski K, Bisseling T (1995) Symbiotic nitrogen fixation. Plant Cell 7:869–885CrossRefPubMedGoogle Scholar
  110. Park KS, Moyne AL, Tuzun S, Kim CH, Kloepper JW (1997) Induction of PR-1 promoter in a transgenic reporter system by selected PGPR strains which induce resistance. In: Ogoshi A, Kobayashi K, Homma Y, Kodama F, Kondo N, Akino S (eds) Plant growth promoting bacteria: present strains and future prospects. Nakanishi Printing, Sapporo, pp 251–255Google Scholar
  111. Parniske M (2004) Molecular genetics of the arbuscular mycorrhizal symbiosis. Curr Opin Plant Biol 7:414–421CrossRefPubMedGoogle Scholar
  112. Paszkowski U, Kroken S, Roux C, Briggs SP (2002) Rice phosphate transporters include an evolutionarily divergent gene specifically activated in arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci USA 99:13,324–13,329Google Scholar
  113. Pawlowska TE, Taylor JW (2004) Organization of genetic variation in individuals of arbuscular mycorrhizal fungi. Nature 427:733–737CrossRefPubMedGoogle Scholar
  114. Peipp H, Maier W, Schmidt J, Wray V, Strack D (1997) Arbuscular mycorrhizal fungus-induced changes in the accumulation of secondary compounds in barley roots. Phytochemistry 44:581–587CrossRefGoogle Scholar
  115. Peretto R, Bettini V, Favaron F, Alghisi P, Bonfante P (1995) Polygalacturonase activity and location in arbuscular mycorrhizal roots of Allium porrum L. Mycorrhiza 5:157–163CrossRefGoogle Scholar
  116. Perotto S, Brewin NJ, 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 7:91–98Google Scholar
  117. Perret X, Staehelin C, Broughton WJ (2000) Molecular basis of symbiotic promiscuity. Microbiol Mol Biol Rev 64:180–201Google Scholar
  118. Perry JA, Wang TL, Welham TJ, Gardner S, Pike JM, Yoshida S, Parniske M (2003) A TILLING reverse genetics tool and a web-accessible collection of mutants of the legume Lotus japonicus. Plant Physiol 131:866–871CrossRefPubMedGoogle Scholar
  119. Peterson RL, Bonfante P (1994) Comparative structure of vesicular-arbuscular mycorrhizas and ectomycorrhizas. Plant Soil 159:79–88Google Scholar
  120. Peterson RL, Guinel FC (2000) The use of plant mutants to study regulation of colonization by AM fungi. In: Kapulnik Y, Douds DD (eds) Arbuscular mycorrhizas: physiology and function. Kluwer, Dordrecht, pp 147–171Google Scholar
  121. Pozo M, Azcón-Aguilar C, Dumas-Gaudot E, Barea J (1999) β-1,3-glucanase in tomato roots inoculated with arbuscular mycorrhizal fungi and/or Phytophthora parasitica and their possible involvement in bioprotection. Plant Sci 141: 149–157CrossRefGoogle Scholar
  122. Pozo M, Cordier C, Dumas-Gautod E, Gianinazzi S, Barea J, Azcón-Aguilar C (2002) Localized versus systemic effect of arbuscular mycorrhizal fungi on defence responses to Phytophthora infection in tomato plants. J Exp Bot 53:525–534CrossRefPubMedGoogle Scholar
  123. Radutoiu S, Madsen L, Madsen E, Felle H, Umehara Y, Gronlund M, Sato S, Nakamura Y, Stougaard J (2003) Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases. Nature 425:585–592CrossRefPubMedGoogle Scholar
  124. Rausch C, Bucher M (2002) Molecular mechanisms of phosphate transport in plants. Planta 216:23–37CrossRefPubMedGoogle Scholar
  125. Rausch C, Daram P, Brunner S, Jansa J, Laloi M, Leggewie G, Amrhein N, Bucher M (2001) A phosphate transporter expressed in arbuscule-containing cells in potato. Nature 414:462–466CrossRefPubMedGoogle Scholar
  126. Ravnskov S, Wu Y, Graham JH (2003) Arbuscular mycorrhizal fungi differentially affect expression of genes coding for sucrose synthases in maize roots. New Phytol 157:539–545CrossRefGoogle Scholar
  127. Redecker D, Kodner R, Graham LE (2000) Glomalean fungi from the Ordovician. Science 289:1920–1921CrossRefPubMedGoogle Scholar
  128. Remy W, Taylor TN, Hass H, Kerp H (1994) Four hundred-million-year-old vesicular arbuscular mycorrhizae. Proc Natl Acad Sci USA 91:11841–11843PubMedGoogle Scholar
  129. Repetto O, Bestel-Corre G, Dumas-Gaudot E, Berta G, Gianinazzi-Pearson V, Gianinazzi S (2003) Targeted proteomics to identify cadmium-induced protein modifications in Glomus mosseae-inoculated pea roots. New Phytol 157:555–567CrossRefGoogle Scholar
  130. Requena N, Breuninger M, Franken P, Ocon A (2003) Symbiotic status, phosphate, and sucrose regulate the expression of two plasma membrane H+ -ATPase genes from the mycorrhizal fungus Glomus mosseae. Plant Physiol 132:1540–1549CrossRefPubMedGoogle Scholar
  131. van Rhijn P, Fang Y, Galili S, Shaul O, Atzmon N, Wininger S, Eshed Y, Lum M, Li Y, 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 and Rhizobium-induced nodules may be conserved. Proc Natl Acad Sci USA 94:5467–5472CrossRefPubMedGoogle Scholar
  132. Rhody D, Stommel M, Roeder C, Mann P, Franken P (2003) Differential RNA accumulation of two beta-tubulin genes in arbuscular mycorrhizal fungi. Mycorrhiza 13:137–142CrossRefPubMedGoogle Scholar
  133. Salzer P, Corbière H, Boller T (1999) Hydrogen peroxide accumulation in Medicago truncatula roots colonized by the arbuscular mycorrhiza-forming fungus Glomus intraradices. Planta 208:319–325CrossRefGoogle Scholar
  134. Salzer P, Bonanomi A, Beyer K, Vögeli-Lange R, Aeschbacher R, Lange J, Wiemken A, Kim D, Cook D, Boller T (2000) Differential expression of eight chitinase genes in Medicago truncatula roots during mycorrhiza formation, nodulation, and pathogen infection. Mol Plant-Microbe Interact 13:763–777PubMedGoogle Scholar
  135. Samra A, Dumas-Gaudot E, Gianinazzi S (1997) Detection of symbiosis-related polypeptides during the early stages of the establishment of arbuscular mycorrhiza between Glomus mosseae and Pisum sativum roots. New Phytol 135:711–722CrossRefGoogle Scholar
  136. Sanders FE, Tinker BP, Black RLB, Palmerly SM (1977) The development of endomycorrhizal root systems. I. Speed of infection and growth-promoting effects with four species of vesicular–arbuscular endophyte. New Phytol 78:257–268Google Scholar
  137. Schellenbaum L, Gianinazzi S, Gianinazzi-Pearson V (1992) Comparison of acid soluble protein synthesis in roots of endomycorrhizal wild type Pisum sativum and corresponding isogenic mutants. J Plant Physiol 141:2–6Google Scholar
  138. Schüßler A (2001) Molecular phylogeny, taxonomy, and evolution of Geosiphon pyriformis and arbuscular mycorrhizal fungi. Plant Soil 244:75–83CrossRefGoogle Scholar
  139. Schüßler A, Schwarzott D, Walker C (2001) A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycol Res 105:1413–1421Google Scholar
  140. Shaul O, Galili S, Volpin H, Ginzberg I, Elad Y, Chet I, Kapulnik Y (1999) Mycorrhiza-induced changes in disease severity and PR protein expression in tobacco leaves. Mol Plant-Microbe Interact 12:1000–1007PubMedGoogle Scholar
  141. Simon L, Bousquet J, Lévesque RC, Lalonde M (1993) Origin and diversification of endomycorrhizal fungi and coincidence with vascular land plants. Nature 363:67–69CrossRefGoogle Scholar
  142. Simoneau P, Louisy-Louis N, Plenchette C, Strullu DG (1994) Accumulation of new polypeptides in Ri T-DNA-transformed roots of tomato (Lycopersicon esculentum) during the development of vesicular-arbuscular mycorrhizae. Appl Environ Microbiol 60:1810–1813Google Scholar
  143. Slezack S, Dumas-Gaudot E, Paynot M, Gianinazzi S (2000) Is a fully established arbuscular mycorrhizal symbiosis required for bioprotection of Pisum sativum roots against Aphanomyces euteiches? Mol Plant-Microbe Interact 13:238–241PubMedGoogle Scholar
  144. Slezack S, Negrel J, Bestel-Corre G, Dumas-Gaudot E, Gianinazzi S (2001) Purification and partial amino acid sequencing of a mycorrhiza-related chitinase isoform from Glomus mosseae-inoculated roots of Pisum sativum L. Planta 213:781–787CrossRefPubMedGoogle Scholar
  145. Smith SE, Read DJ (1997) Mycorrhizal symbiosis. Academic, San DiegoGoogle Scholar
  146. Smith SE, Smith FA, Jakobsen I (2003) Mycorrhizal fungi can dominate phosphate supply to plants irrespective of growth responses. Plant Physiol 133:16–20CrossRefPubMedGoogle Scholar
  147. Stracke S, Kistner C, Yoshida S, Mulder L, Sato S, Kaneko T, Tabata S, Sandal N, Stougaard J, Parniske M (2002) A plant receptor-like kinase required for both bacterial and fungal symbiosis. Nature 417:959–962CrossRefPubMedGoogle Scholar
  148. Tahiri-Alaoui A, Dumas-Gaudot E, Gioaninazzi S (1993) Immunocytochemical localisation of pathogenesis-related PR-1 proteins in tobacco root tissues infected in vitro by the black root rot fungus Chalara elegans. Physiol Mol Plant Pathol 42:69–82CrossRefGoogle Scholar
  149. Tamasloukht MB, Sejalon-Delmas N, Kluever A, Jauneau A, Roux C, Becard 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 131:1468–1478CrossRefPubMedGoogle Scholar
  150. Taylor TN, Remy W, Hass H, Kerp H (1995) Fossil arbuscular mycorrhizae from early devonian. Mycologia 87:560–573Google Scholar
  151. Timonen S, Peterson RL (2002). Cytoskeleton in mycorrhizal symbiosis. Plant Soil 244:199–210CrossRefGoogle Scholar
  152. Trouvelot S, van Tuinen D, Hijri M, Gianinazzi-Pearson V (1999) Visualization of ribosomal DNA loci in spore interphasic nuclei of glomalean fungi by fluorescence in situ hybridization. Mycorrhiza 8:203–206CrossRefGoogle Scholar
  153. Uchiumi T, Shimoda Y, Tsuruta T, Mukoyoshi Y, Suzuki A, Senoo K, Sato S, Kato T, Tabata S, Higashi S, Abe M (2002) Expression of symbiotic and nonsymbiotic globin genes responding to microsymbionts on Lotus japonicus. Plant Cell Physiol 43:1351–1358CrossRefPubMedGoogle Scholar
  154. Vierheilig H, Iseli B, Alt M, Raikhel N, Wiemken A, Boller T (1996). Resistance of Urtica dioica to mycorrhizal colonization: a possible involvement of Urtica dioica agglutinin. Plant Soil 183:131–136Google Scholar
  155. Volpin H, Elkind Y, Okon Y, Kapulnik Y (1994) A vesicular arbuscular mycorrhizal fungus Glomus intraradix induces a defence response in alfalfa roots. Plant Physiol 104:683–689PubMedGoogle Scholar
  156. Walter M.H, 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 31:243–254CrossRefPubMedGoogle Scholar
  157. Watson BS, Asirvatham VS, Wang L, Sumner LW (2003) Mapping the proteome of barrel medic (Medicago truncatula). Plant Physiol 131:1104–1123CrossRefPubMedGoogle Scholar
  158. 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 11:933–936Google Scholar
  159. Wulf A, Manthey K, Doll J, Perlick AM, Linke B, Bekel T, Meyer F, Franken P, Kuster H, Krajinski F (2003) Transcriptional changes in response to arbuscular mycorrhiza development in the model plant Medicago truncatula. Mol Plant-Microbe Interact 16:306–314PubMedGoogle Scholar
  160. Wyss P, Mellor RB, Wiemken A (1990) Vesicular-arbuscular mycorrhizas of wild-type soybean and non-nodulating mutants with Glomus mosseae contain symbiosis-specific polypeptides (mycorrhizins), immunologically cross-reactive with nodulins. Planta 182:22–26CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  1. 1.Department of Secondary MetabolismLeibniz Institute of Plant BiochemistryHalleGermany

Personalised recommendations