, Volume 16, Issue 8, pp 509–524 | Cite as

Fungal and plant gene expression in arbuscular mycorrhizal symbiosis



Arbuscular mycorrhizas (AMs) are a unique example of symbiosis between two eukaryotes, soil fungi and plants. This association induces important physiological changes in each partner that lead to reciprocal benefits, mainly in nutrient supply. The symbiosis results from modifications in plant and fungal cell organization caused by specific changes in gene expression. Recently, much effort has gone into studying these gene expression patterns to identify a wider spectrum of genes involved. We aim in this review to describe AM symbiosis in terms of current knowledge on plant and fungal gene expression profiles.


Arbuscular mycorrhizas Cellular modification Plant and fungal gene expression Symbiosis Functional genomics 


  1. Albrecht C, Geurts R, Bisseling T (1998) Legume nodulation and mycorrhizae formation; two extremes in host specificity meet. EMBO J 18:281–288Google Scholar
  2. Akiyama K, Matsuzaki K, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435:824–827PubMedGoogle Scholar
  3. Ané JM, Kiss GB, Riely BK, Penmetsa RV, Oldroyd GE, Ayax C, Levy J, Debelle F, Baek JM, Kalo P et al (2004) Medicago truncatula DMI1 required for bacterial and fungal symbioses in legumes. Science 303:1364–1367PubMedGoogle Scholar
  4. Aono T, Maldonado-Mendoza IE, Dewbre GR, Harrison MJ, Saito M (2004) Expression of alkaline phosphatase genes in arbuscular mycorrhizas. New Phytol 162:525–553Google Scholar
  5. Ayling SM, Smith SE, Smith FA (2000) Transmembrane electric potential difference of germ tubes of arbuscular mycorrhizal fungi responds to external stimuli. New Phytol 147:631–639Google Scholar
  6. Bago B, Chamberland H, Goulet A, Vierheilig H, Lafontaine JG, Piché Y (1996) Effect of nikkomycin Z, a chitin-synthase inhibitor, on hyphal growth and cell wall structure of two arbuscular–mycorrhizal fungi. Protoplasma 192:80–92Google Scholar
  7. Bago B, Shachar-Hill Y, Pfeffer PE (2000) Dissecting carbon pathways in arbuscular mycorrhizas with NMR spectroscopy. In: Podila GK, Douds DD (eds) Current advances in mycorrhizae research. APS, St. Paul, USA, pp 111–126Google Scholar
  8. Bago B, Zipfel W, Williams RC, Jun J, Arreola R, Pfeffer PE, Lammers PJ, Shachar-Hill Y (2002) Translocation and utilization of fungal storage lipid in the arbuscular mycorrhizal symbiosis. Plant Physiol 128:108–124PubMedGoogle Scholar
  9. Bago B, Pfeffer PE, Abubaker J, Jun J, Allen JW, Brouillette J, Douds DD, Lammers PJ, Shachar-Hill Y (2003) Carbon export from arbuscular mycorrhizal roots involves the translocation of carbohydrate as well as lipid. Plant Physiol 131:1496–1507PubMedGoogle Scholar
  10. Balestrini R, Bonfante P (2005) The interface compartment in arbuscular mycorrhizae: a special type of plant cell wall? Plant Biosyst 139:8–15Google Scholar
  11. Balestrini R, Josè-Estanyol M, Puigdomènech P, Bonfante P (1997) Hydroxyproline rich glycoprotein mRNA accumulation in maize root cells colonized by the arbuscular mycorrhizal fungus as revealed by in situ hybridization. Protoplasma 198:36–42Google Scholar
  12. Balestrini R, Perotto S, Gasverde E, Dahiya P, Guldmann LL, Brewin NJ, Bonfante P (1999) Transcription of a gene encoding a lectin like glycoprotein is induced in root cells harbouring arbuscular mycorrhizal fungi in Pisum sativum. Mol Plant-Microb Interact 12:785–791Google Scholar
  13. Balestrini R, Cosgrove DJ, Bonfante P (2005) Differential location of alpha-expansin proteins during the accommodation of root cells to an arbuscular mycorrhizal fungus. Planta 220:889–899PubMedGoogle Scholar
  14. Beilby JP, Kidby DK (1980) Biochemistry of ungerminated and germinated spores of the vesicular–arbuscular mycorrhizal fungus Glomus caledonium: changes in neutral and polar lipids. J Lipid Res 21:739–750PubMedGoogle Scholar
  15. Benedetto A, Magurno F, Bonfante P, Lanfranco L (2005) Expression profiles of a phosphate transporter gene (GmosPT) from the endomycorrhizal fungus Glomus mosseae. Mycorrhiza 15:620–627PubMedGoogle Scholar
  16. Berta G, Fusconi A, Sampo S, Lingua G, Perticone S, Repetto O (2000) Polyploidy in tomato roots as affected by arbuscular mycorrhizal colonization. Plant Soil 226:37–44Google Scholar
  17. Bestel-Corre G, Dumas-Gaudot E, Gianinazzi S (2003) Proteomics as a tool to monitor plant–microbe endosymbioses in the rhizosphere. Mycorrhiza 14:1–10PubMedGoogle Scholar
  18. Bianciotto V, Barbiero G, Bonfante P (1995) Analysis of the cell-cycle in an arbuscular mycorrhizal fungus by flow-cytometry and bromodeoxyuridine labelling. Protoplasma 188:161–169Google Scholar
  19. Bianciotto V, Perotto S, Ruiz-Lozano JM, Bonfante P (2002) Arbuscular mycorrhizal fungi and soil bacteria: from cellular investigations to biotechnological perspectives. In: Gianinazzi S, Schüepp H, Barea JM, Haselwandter K (eds) Mycorrhizal technology in agriculture. Birknäuser Verlag, Switzerland, pp 19–31Google Scholar
  20. Blancaflor EB, Zhao L, Harrison MJ (2001) Microtubule organization in root cells of Medicago truncatula during development of an arbuscular mycorrhizal symbiosis with Glomus versiforme. Protoplasma 217:154–165PubMedGoogle Scholar
  21. Blee KA, Anderson AJ (2000) Defense responses in plants to arbuscular mycorrhizal fungi. In: Podila GK, Douds DD (eds) Current advances in mycorrhizae research. APS, St. Paul, USA, pp 27–44Google Scholar
  22. Blilou I, Bueno P, Ocampo JA, Garcia-Garrido J (2000) Induction of catalase and ascorbate peroxidase activities in tobacco roots inoculated with the arbuscular mycorrhizal Glomus mosseae. Mycol Res 104:722–725Google Scholar
  23. Bonanomi 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 150:573–582Google Scholar
  24. Bonfante P (2001) At the interface between mycorrhizal fungi and plants: the structural organization of cell wall, plasma membrane and cytoskeleton. In: Esser K, Hock B (eds) The mycota IX. Springer, Berlín Heidelberg New York, pp 45–61Google Scholar
  25. Bonfante P, Balestrini R, Mendgen K (1994) Storage and secretion processes in the spore of Gigaspora margarita Becker and Hall as revealed by high-pressure freezing and freeze substitution. New Phytol 128:93–101Google Scholar
  26. Bonfante P, Bergero R, Uribe X, Romera C, Rigau J, Puigdoménech P (1996) Transcriptional activation of a maize-tubulin gene in mycorrhizal maize and transgenic tobacco plants. Plant J 9:737–743Google Scholar
  27. Bonfante P, Genre A, Faccio A, Martini 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-Microb Interact 13:1109–1120Google Scholar
  28. Brechenmacher L, Weidmann S, van Tuinen D, Chatagnier O, Gianinazzi S, Franken P, Gianinazzi-Pearson V (2004) Expression profiling of up-regulated plant and fungal genes in early and late stages of Medicago truncatula–Glomus mosseae interactions. Mycorrhiza 14:253–262PubMedGoogle Scholar
  29. Breuninger M, Requena N (2004) Recognition events in AM symbiosis: analysis of fungal gene expression at the early appressorium stage. Fungal Genet Biol 41:794–804PubMedGoogle Scholar
  30. Breuninger M, Trujillo CG, Serrano E, Fischer R, Requena N (2004) Different nitrogen sources modulate activity but not expression of glutamine synthetase in arbuscular mycorrhizal fungi. Fungal Genet Biol 41:542–552PubMedGoogle Scholar
  31. Brewin NJ (2004) Plant cell wall remodelling in the Rhizobium–legume symbiosis. Crit Rev Plant Sci 23:293–316Google Scholar
  32. Brummell DA, Bird CR, Schuch W, Bennett AB (1997) An endo-1, 4-β-glucanase expressed at high levels in rapidly expanding tissues. Plant Mol Biol 33:87–95PubMedGoogle Scholar
  33. Bucking H, Shachar-Hill Y (2005) Phosphate uptake, transport and transfer by the arbuscular mycorrhizal fungus Glomus intraradices is stimulated by increased carbohydrate availability. New Phytol 165:899–912PubMedGoogle Scholar
  34. Buée 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-Microb Interact 13:693–698Google Scholar
  35. Burleigh SH (2001) Relative quantitative PCR to study nutrient transport processes in arbuscular mycorrhizas. Plant Sci 160:899–904PubMedGoogle Scholar
  36. Burleigh SH, Harrison MJ (1997) A novel gene whose expression in Medicago truncatula roots is suppressed in response to colonization by vesicular arbuscular mycorrhizal (VAM) fungi and to phosphate nutrition. Plant Mol Biol 34:199–208PubMedGoogle Scholar
  37. 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 156:265–273Google Scholar
  38. Day RC, Grossniklaus U, Macknight RC (2005) Be more specific! Laser-assisted microdissection of plant cells. Trends Plant Sci 10:340–397Google Scholar
  39. Delledonne M, Zeier J, Marocco A, Lamb C (2001) Signal interactions between nitric oxide and reactive oxygen intermediates in the plant hypersensitive disease resistance response. Proc Natl Acad Sci USA 98:13454–13459PubMedGoogle Scholar
  40. Delp G, Timonen S, Rosewarne GM, Barker SJ, Smith S (2003) Differential expression of Glomus intraradices genes in external mycelium and mycorrhizal roots of tomato and barley. Mycol Res 107:1083–1093PubMedGoogle Scholar
  41. Demartsev V, Aussenberg ER, Gadkar V, Koltai H, Zilberstein A, Kapulnik Y (2005) Alteration in tomato (Lycopersicon esculentum) gene expression during early stages of the interaction with Glomus intraradices. In: Management committee and final meeting on “Achievements and Future Landscape for Arbuscular Mycorrhiza Research”, Dijon, France, 2–4 June 2005Google Scholar
  42. Doll J, Hause B, Demchenko K, Pawlowski K, Krajinski F (2003) A member of the germin-like protein family is a highly conserved mycorrhiza-specific induced gene. Plant Cell Physiol 44:1208–1214PubMedGoogle Scholar
  43. Duc G, Trouvelet A, Gianinazzi-Pearson V, Gianinazzi S (1989) First report of nonmycorrhizal plant mutants (Myc-) obtained in pea (Pisum sativum L.) and fababean (Vicia faba L.). Plant Sci 60:215–222Google Scholar
  44. Endre G, Kereszt A, Kevei Z, Mihacea S, Kaló, P, Kiss GB (2002) A receptor kinase gene regulating symbiotic nodule development. Nature 417:962–966PubMedGoogle Scholar
  45. Ezawa T, Hayatsu M, Saito M (2005) A new hypothesis on the strategy for acquisition of phosphorus in arbuscular mycorrhiza: up-regulation of secreted acid phosphatase gene in the host plant. Mol Plant-Microb Interact 18:1046–1053Google Scholar
  46. Fehlberg V, Vieweg MF, Dohmann EMN, Hohnjec N, Pühler A, Perlick AM, Küster H (2005) The promoter of the leghaemoglobin gene VfLb29: functional analysis and identification of modules necessary for its activation in the infected cells of root nodules and in the arbuscule-containing cells of mycorrhizal roots. J Exp Bot 56:799–806PubMedGoogle Scholar
  47. Fester T, Hause G (2005) Accumulation of reactive oxygen species in arbuscular mycorrhizal roots. Mycorrhiza 15:373–379PubMedGoogle Scholar
  48. Fester T, Schmidt D, Lohse S, Walter MH, Giuliano G, Bramley PM, Fraser PD, Hause B, Strack D (2002a) Stimulation of carotenoid metabolism in arbuscular mycorrhizal roots. Planta 216:148–154PubMedGoogle Scholar
  49. Fester T, Hause B, Schmidt D, Halfmann K, Schmidt J, Wray V, Hause G, Strack D (2002b) Occurrence and localization of apocarotenoids in arbuscular mycorrhizal plant roots. Plant Cell Physiol 43:256–265PubMedGoogle Scholar
  50. Frenzel A, Manthey K, Perlick AM, Meyer F, Puhler A, Kuster H, Krajinski F (2005) Combined transcriptome profiling reveals a novel family of arbuscular mycorrhizal-specific Medicago truncatula lectin genes. Mol Plant-Microb Interact 18:771–782Google Scholar
  51. Garcia-Garrido JM, Ocampo JA (2002) Regulation of the plant defence response in arbuscular mycorrhizal symbiosis. J Exp Bot 53:1377–1386PubMedGoogle Scholar
  52. García-Rodríguez S, Pozo MJ, Azcón-Aguilar C, Ferrol N (2005) Expression of a tomato sugar transporter is increased in leaves of mycorrhizal or Phytophthora parasitica-infected plants. Mycorrhiza 15:489–496PubMedGoogle Scholar
  53. Gaspar L, Pollero RJ, Cabello M (1994) Triacylglycerol consumption during spore germination of vesicular–arcuscular mycorrhizal fungi. J Am Oil Chem Soc 71:449–452Google Scholar
  54. Genre A, Bonfante P (2005) Building a mycorrhizal cell: How to reach compatibility between plants and arbuscular mycorrhizal fungi. J Plant Interact 1:3–13Google Scholar
  55. Genre A, Chabaud M, Timmers T, Bonfante P, Barker DG (2005) Arbuscular mycorrhizal fungi elicit a novel intracellular apparatus in Medicago truncatula root epidermal cells before infection. Plant Cell 17:3489–3499PubMedGoogle Scholar
  56. Gianinazzi-Pearson V, Denarié J (1997) Red carpet genetic programmes for root endosymbioses. Trends Plant Sci 10:371–372Google Scholar
  57. Gianinazzi-Pearson V, Gollotte A, Lherminier J, Tisserant B, Franken P, Dumas-Gaudot E, Lemoine MC, van Tuinen D, Gianinazzi S (1995) Cellular and molecular approaches in the characterization of symbiotic events in functional arbuscular mycorrhizal associations. Can J Bot 73:S526–S532Google 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 211:609–613PubMedGoogle Scholar
  59. Giovannetti M, Sbrana C, Avio L, Citernesi AS, Logi C (1993) Differential hyphal morphogenesis in arbuscular mycorrhizal fungi during pre-infection stages. New Phytol 125:587–594Google Scholar
  60. Govindarajulu M, Pfeffer PE, Jin HR, Abubaker J, Douds DD, Allen JW, Bucking H, Lammers PJ, Shachar-Hill Y (2005) Nitrogen transfer in the arbuscular mycorrhizal symbiosis. Nature 435:819–823PubMedGoogle Scholar
  61. Grunwald U, Nyamsuren O, Tamasloukht M, Lapopin L, Becker A, Mann P, Gianinazzi-Pearson V, Krajinski F, Franken P (2004) Identification of mycorrhiza-regulated genes with arbuscule development-related expression profile. Plant Mol Biol 55:553–566PubMedGoogle Scholar
  62. Güimil S, Chang H-S, Zhu T, Sesma A, Osbourn A, Roux C, Ioannidis V, Oakeley EJ, Docquier M, Descombes P, Briggs SP, Paszkowski U (2005) Comparative transcriptomics of rice reveals an ancient pattern of response to microbial colonization. Proc Natl Acad Sci USA 102:8066–8070PubMedGoogle Scholar
  63. 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 134:614–624PubMedGoogle Scholar
  64. Harrison MJ (1996) A sugar transporter from Medicago truncatula: altered expression pattern in roots during vesicular–arbuscular (VA) mycorrhizal associations. Plant J 9:491–503PubMedGoogle Scholar
  65. Harrison MJ (2005) Signaling in the arbuscular mycorrhizal symbiosis. Annu Rev Microbiol 59:19–42PubMedGoogle Scholar
  66. Harrison MJ, Dixon RA (1993) Isoflavonoid accumulation and expression of defense gene transcripts during the establishment of vesicular–arbuscular mycorrhizal associations in roots of Medicago truncatula. Mol Plant-Microb Interact 6:643–654Google Scholar
  67. 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 6:9–20Google Scholar
  68. Harrison MJ, van Buuren ML (1995) A phosphate transporter from the mycorrhizal fungus Glomus versiforme. Nature 378:626–629PubMedGoogle Scholar
  69. 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 14:2413–2429PubMedGoogle Scholar
  70. Hause B, Fester T (2005) Molecular and cell biology of arbuscular mycorrhizal symbiosis. Planta 221:184–196PubMedGoogle Scholar
  71. He XL, Mouratov S, Steinberger Y (2002) Temporal and spatial dynamics of vesicular–arbuscular mycorrhizal fungi under the canopy of Zygophyllum dumosum Boiss. in the Negev Desert. J Arid Environ 52:379–387Google Scholar
  72. Hildebrandt U, Schmelzer E, Bothe H (2002) Expression of nitrate transporter genes in tomato colonized by an arbuscular mycorrhizal fungus. Physiol Plant 115:125–136PubMedGoogle Scholar
  73. Hirsch AM, Kapulnik Y (1998) Signal transduction pathways in mycorrhizal associations: comparisons with the Rhizobium–legume symbiosis. Fungal Genet Biol 23:205–212PubMedGoogle Scholar
  74. Hodge A, Campbell CD, Fitter AH (2001) An arbuscular mycorrhizal fungus accelerates decomposition and acquires nitrogen directly from organic material. Nature 413:297–299PubMedGoogle Scholar
  75. 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-Microb Interact 16:903–915Google Scholar
  76. Hohnjec N, Vieweg MF, Pühler A, Becker A, Küster H (2005) Overlaps in the transcriptional profiles of Medicago truncatula roots inoculated with two different Glomus fungi provide insights into the genetic program activated during arbuscular mycorrhiza. Plant Physiol 137:1283–1301PubMedGoogle Scholar
  77. Imaizumi-Anraku H, Takeda N, Charpentier M, Perry J, Miwa H, Umehara Y, Kouchi H, Murakami Y, Mulder L, Vickers K, Pike J, Downie JA, Wang T, Sato S, Asamizu E, Tabata S, Yoshikawa M, Murooka Y, Wu GJ, Kawaguchi M, Kawasaki S, Parniske M, Hayashi M (2005) Plastid proteins crucial for symbiotic fungal and bacterial entry into plant roots. Nature 433:527–531PubMedGoogle Scholar
  78. Ivashuta S, Liu J, Liu J, Lohar DP, Haridas S, Bucciarelli B, VandenBosch KA, Vance CP, Harrison MJ, Gantt JS (2005) RNA interference identifies a calcium dependent protein kinase involved in Medicago truncatula root development. Plant Cell 17:2911–2921PubMedGoogle Scholar
  79. Johansen A, Jakobsen I, Jensen ES (1993) Hyphal transport by a vesicular–arbuscular mycorrhizal fungus of N applied to the soil as ammonium or nitrate. Biol Fertil Soils 16:66–70Google Scholar
  80. Journet EP, El-Gachtouli N, Vernoud V, de Billy F, Pichon M, Dedieu A, Arnould C, Morandi D, Barker DG, Gianinazzi-Pearson V (2001) Medicago truncatula ENOD11: a novel RPRP-encoding early nodulin gene expressed during mycorrhization in arbuscule-containing cells. Mol Plant-Microb Interact 14:737–748Google Scholar
  81. Journet EP, van Tuinen D, Gouzy J, Crespeau H, Carreau V, Farmer MJ, Niebel A, Schiex T, Jaillon O, Chatagnier O et al (2002) Exploring root symbiotic programs in the model legume Medicago truncatula using EST analysis. Nucleic Acids Res 30:5579–5592PubMedGoogle Scholar
  82. Jun J, Abubaker J, Rehrer C, Pfeffer PE, Shachar-Hill Y, Lammers PJ (2002) Expression in an arbuscular mycorrhizal fungus of genes putatively involved in metabolism, transport, the cytoskeleton and the cell cycle. Plant Soil 244:141–148Google Scholar
  83. Kapulnik Y, Volpin H, Itzhaki H, Ganon D, Galili S, David R, Shaul O, Elad Y, Chet I, Okon Y (1996) Suppression of defence responses in mycorrhizal alfalfa and tobacco roots. New Phytol 133:59–64Google Scholar
  84. Karandashov V, Bucher M (2005) Symbiotic phosphate transport in arbuscular mycorrhizas. Trends Plant Sci 10:22–29PubMedGoogle Scholar
  85. Kistner C, Parniske M (2002) Evolution of signal transduction in intracellular symbiosis. Trends Plant Sci 7:511–518PubMedGoogle Scholar
  86. Kistner C, Winzer T, Pitzschke A, Mulder L, Sato S, Kaneko T, Tabata S, Sandal N, Stougaard J, Webb KJ, Szczyglowski K, Parniske M (2005) Seven Lotus japonicus genes required for transcriptional reprogramming of the root during fungal and bacterial symbiosis. Plant Cell 17:2217–2229PubMedGoogle Scholar
  87. Kosuta S, Chabaud M, Lougnon G, Gough C, Denarie J, Barker DG, Becard G (2003) A diffusible factor from arbuscular mycorrhizal fungi induces symbiosis specific MtENOD11 expression in roots of Medicago truncatula. Plant Physiol 131:952–962PubMedGoogle Scholar
  88. Krajinski F, Martin-Laurent F, Gianinazzi S, Gianinazzi-Pearson V, Franken F (1998) Cloning and analysis of psam2, a gene from Pisum sativum L. regulated insymbiotic arbuscular mycorrhiza and pathogenic root–fungus interactions. Physiol Plant Mol Pathol 52:297–307Google Scholar
  89. 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 4:754–761Google Scholar
  90. Kuster H, Hohnjec, Krajinski F, El Yahyaoui F, Manthey K, Gouzy J, Dondrup M, Meyer F, Kalinowski J, Brechenmacher L, van Tuinen D, Gianinazzi-Pearson V, Puhler A, Gamas P, Becker A (2004) Construction and validation of cDNA-based Mt6k-RIT macro- and microarrays to explore root endosymbioses in the model legume Medicago truncatula. J Biotechnol 108:95–113PubMedGoogle Scholar
  91. Lambais MR, Mehdy MC (1993) Suppression of endochitinase, β-1, 3-endoglucanase and chalcone isomerase expression in bean vesicular–arbuscular mycorrhizal roots under different soil phosphate conditions. Mol Plant-Microb 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 140:33–42Google Scholar
  93. Lammers PJ, Jun J, Abubaker J, Arreola R, Gopalan A, Bago B, Hernandez-Sebastia C, Allen JW, Douds DD, Pfeffer PE et al (2001) The glyoxylate cycle in an arbuscular mycorrhizal fungus: gene expression and carbon flow. Plant Physiol 127:1287–1298PubMedGoogle Scholar
  94. Lanfranco L, Gabella S, Bonfante P (2000) EST as a useful tool for studying gene expression in arbuscular mycorrhizal fungi. In: Weber H, Imhof S, Zeuske D (eds) Abstract and papers of the Third International Congress on Symbiosis. University of Marburg, 13–19 August 2000, Marburg, Germany, pp 108–114Google Scholar
  95. Lanfranco L, Bolchi A, Ros EC, Ottonello S, Bonfante P (2002) Differential expression of a metallothionein gene during the presymbiotic versus the symbiotic phase of an arbuscular mycorrhizal fungus. Plant Physiol 130:58–67PubMedGoogle Scholar
  96. Lanfranco L, Novero M, Bonfante P (2005) The mycorrhizal fungus Gigaspora margarita possesses a CuZn superoxidedismutase which is up-regulated during the symbiosis with legume hosts. Plant Physiol 137:1319–1330PubMedGoogle Scholar
  97. Lei J, Bécard G, Catford JG, Piché Y (1991) Root factors stimulate 32P uptake and plasmalemma ATPase activity in vesicular–arbuscular mycorrhizal fungus, Gigaspora margarita. New Phytol 118:289–294Google Scholar
  98. Lévy J, Bres C, Geurts R, Chalhoub B, Kulikova O, Duc G, Journet EP, Ane JM, Lauber E, Bisseling T et al (2004) A putative Ca2+ and calmodulin-dependent protein kinase required for bacterial and fungal symbioses. Science 303:1361–1364PubMedGoogle Scholar
  99. Liu J, Blaylock LA, Endre G, Cho J, Town CD, Vanden Bosch KA, Harrison MJ (2003) Transcript profiling coupled with spatial expression analyses reveals genes involved in distinct developmental stages of the arbuscular mycorrhizal symbiosis. Plant Cell 15:2106–2123PubMedGoogle Scholar
  100. Liu J, Blaylock LA, Harrison MJ (2004) cDNA arrays as a tool to identify mycorrhiza-regulated genes: identification of mycorrhiza-induced genes that encode or generate signaling molecules implicated in the control of root growth. Can J Bot 82:1177–1185Google Scholar
  101. 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-Microb Interact 14:1140–1148Google Scholar
  102. Maldonado-Mendoza IE, Dewbre GR, van Buuren ML, Versaw WK, Harrison MJ (2002) Methods to estimate the proportion of plant and fungal RNA in an arbuscular mycorrhiza. Mycorrhiza 12:67–74PubMedGoogle Scholar
  103. Maldonado-Mendoza IE, Dewbre GR, Blaylock L, Harrison MJ (2005) Expression of a xyloglucan endotransglucosylase/hydrolase gene, Mt-XTH1, from Medicago truncatula is induced systemically in mycorrhizal roots. Gene 345:191–197PubMedGoogle Scholar
  104. Manthey K, Krajinski F, Hohnjec N, Firnhaber C, Puhler A, Perlick AM, Kuster H (2004) Transcriptome profiling in root nodules and arbuscular mycorrhiza identifies a collection of novel genes induced during Medicago truncatula root endosymbioses. Mol Plant-Microb Interact 17:1063–1077Google Scholar
  105. Marsh JF, Schultze M (2001) Analysis of arbuscular mycorrhizas using symbiosis defective plant mutants. New Phytol 150:525–532Google Scholar
  106. 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 256:37–44PubMedGoogle Scholar
  107. Morandi D, Prado E, Sagan M, Duc G (2005) Characterization of new symbiotic Medicago truncatula (Gaertn.) mutants, and phenotypic or genotypic complementary information on previously described mutants. Mycorrhiza 15:283–289PubMedGoogle Scholar
  108. Mosse B, Hepper CM (1975) Vesicular–arbuscular mycorrhizal infections in root organ cultures. Physiol Plant Pathol 5:215–223CrossRefGoogle Scholar
  109. 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 135:291–301Google Scholar
  110. Nagahashi G, Douds DD (1997) Appressorium formation by AM fungi on isolated cell walls of carrot roots. New Phytol 136:299–304Google Scholar
  111. Nagahashi G, Douds DD (2000) Partial separation of the root exudates components and their effects upon the growth of germinated spores of AM fungi. Mycol Res 104:1453–1464Google Scholar
  112. Nagy R, Karandashov V, Chague V, Kalinkevich K, Tamasloukht MB, Xu G, Jakobsen I, Levy AA, Amrhein N, Bucher M (2005) The characterization of novel mycorrhiza specific phosphate transporters from Lycopersicon esculentum and Solanum tuberosum uncovers functional redundancy in symbiotic phosphate transport in solanaceous species. Plant J 42:236–250PubMedGoogle Scholar
  113. Olah B, Brière C, Bécard G, Dénarie’ J, Gough C (2005) Nod factors and a diffusible factor from arbuscular mycorrhizal fungi stimulate lateral root formation in Medicago truncatula via the DMI1/DMI2 signalling pathway. Plant J 44:195–207PubMedGoogle Scholar
  114. Oldroyd GED, Harrison MJ, Udvardi M (2005) Peace talks and trade deals. Keys to long-term harmony in legume–microbe symbioses. Plant Physiol 137:1205–1210PubMedGoogle Scholar
  115. Parniske M (2004) Molecular genetics of the arbuscular mycorrhizal symbiosis. Curr Opin Plant Biol 7:414–421PubMedGoogle Scholar
  116. 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 99:13324–13329PubMedGoogle Scholar
  117. Podila GK, Lanfranco L (2004) Genomics approaches to unravel mycorrhizal symbiosis. In: Varma A, Werner H (eds) Plant surface microbiology. Springer, Berlin Heidelberg New York, pp 561–592Google Scholar
  118. 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 414:462–466PubMedGoogle Scholar
  119. Ravnskov S, Wu Y, Graham JH (2003) Arbuscular mycorrhizal fungi differentially affect expression of genes coding for sucrose synthases in maize roots. New Phytol 157:539–545Google Scholar
  120. Requena N, Fuller P, Franken P (1999) Molecular characterization of Gm-FOX2, an evolutionarily highly conserved gene from the mycorrhizal fungus Glomus mosseae, down-regulated during interaction with rhizobacteria. Mol Plant-Microb Interact 12:934–942Google Scholar
  121. Requena N, Mann P, Franken P (2000) A homologue of the cell cycle check point TOR2 from Saccharomyces cerevisiae exists in the arbuscular mycorrhizal fungus Glomus mosseae. Protoplasma 212:89–98Google Scholar
  122. Requena N, Mann P, Hampp R, Franken P (2002) Early developmentally regulated genes in the arbuscular mycorrhizal fungus Glomus mosseae: identification of GmGIN1, a novel gene with homology to the C-terminus of metazoan hedgehog proteins. Plant Soil 244:129–139Google Scholar
  123. 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 mycorrhizal fungus Glomus mosseae. Plant Physiol 132:1–10Google Scholar
  124. Rhody D, Stommel M, Roeder C, Mann P, Franken P (2003) Differential RNA accumulation of two β-tubulin genes in arbuscular mycorrhizal fungi. Mycorrhiza 13:137–142PubMedGoogle Scholar
  125. Rosewarne G, Barker SJ, Smith SE, Smith FA, Schachtman DP (1999) A Lycopersicon esculetum phosphate transporter (LePT1) involved in phosphorus uptake from a vesicular–arbuscular mycorrhizal fungus. New Phytol 144:507–516Google Scholar
  126. 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 232:13–19Google Scholar
  127. Ruíz-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-Microb Interact 12:976–984Google Scholar
  128. Ruiz-Lozano JM, Collados C, Barea JM, Azcon R (2001) Cloning of cDNAs encoding SODs from lettuce plants which show differential regulation by arbuscular mycorrhizal symbiosis and by drought stress. J Exp Bot 52:2241–2242PubMedGoogle Scholar
  129. Ruiz-Lozano JM, Collados C, Porcel R, Azcon R, Barea JM (2002) Identification of a cDNA from the arbuscular mycorrhizal fungus Glomus intraradices that is expressed during mycorrhizal symbiosis and up-regulated by N fertilization. Mol Plant-Microb Interact 15:360–367Google Scholar
  130. Salzer P, Corbière H, Boller T (1999) Hydrogen peroxide accumulation in Medicago truncatula roots colonized by the arbuscular mycorrhiza-forming fungus Glomus intraradices. Planta 208:319–325Google Scholar
  131. Salzer P, Bonanomi 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-Microb Interact 13:763–777Google Scholar
  132. Sanchez L, Weidmann S, Arnould C, Bernard AR, Gianinazzi S, Gianinazzi-Pearson V (2005) Pseudomonas fluorescens and Glomus mosseae trigger DMI3-dependent activation of genes related to a signal transduction pathway in roots of Medicago truncatula. Plant Physiol 139:1065–1077PubMedGoogle Scholar
  133. Sawaki H, Saito M (2001) Expressed genes in the extraradical hyphae of an arbuscular mycorrhizal fungus, Glomus intraradices, in the symbiotic phase. FEMS Microbiol Lett 195:109–113PubMedGoogle Scholar
  134. 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-Microb Interact 13:238–241Google Scholar
  135. Smith SE, Read DJ (1997) Mycorrhizal symbiosis, 2nd edn. Academic, London, UKGoogle Scholar
  136. Smith SE, Smith AF, Jakobsen I (2003) Mycorrhizal fungi can dominate phosphate supply to plants irrespective of growth responses. Plant Physiol 133:16–20PubMedGoogle Scholar
  137. Spanu P, Boller T, Ludwig A, Wiemken A, Faccio A (1989) Chitinase in roots of mycorrhizal Allium porrum: regulation and localization. Planta 177:447–455Google Scholar
  138. Stommel M, Mann P, Franken P (2001) EST-library construction using spore RNA of the arbuscular mycorrhizal fungus Gigaspora rosea. Mycorrhiza 10:281–285Google Scholar
  139. Stougaard J (2001) Genetics and genomics of root symbiosis. Curr Opin Plant Biol 4:328–335PubMedGoogle Scholar
  140. Tahiri-Alaoui A, Lingua G, Avrova A, Sampò S, Fusconi A, Antoniw J, Berta G (2002) A cullin gene is induced in tomato roots forming arbuscular mycorrhizae. Can J Bot 80:607–616Google Scholar
  141. 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 131:1468–1478PubMedGoogle Scholar
  142. Tisserant B, Gianinazzi-Pearson V, Gianinazzi S, Gollotte A (1993) In planta histochemical staining of fungal alkaline phosphatase activity for analysis of efficient arbuscular mycorrhizal infections. Mycol Res 97:245–250CrossRefGoogle Scholar
  143. Trépanier M, Bécard G, Moutoglis P, Willemot C, Gagné S, Avis TJ, Rioux JA (2005) Dependence of arbuscular mycorrhizal fungi on their plant host for palmitic acid synthesis. Appl Environ Microbiol 71:5341–5347PubMedGoogle Scholar
  144. 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-Microb Interact 12:171–181Google Scholar
  145. Versaw WK, Chiou TJ, Harrison MJ (2002) Phosphate transporters of Medicago truncatula and arbuscular mycorrhizal fungi. Plant Soil 244:239–245Google Scholar
  146. Vieweg MF, Fruhling M, Quandt HJ, Heim U, Baumlein H, Puhler A, Kuster H, Perlick AM (2004) The promoter of the Vicia faba L. leghemoglobin gene VfLb29 is specifically activated in the infected cells of root nodules and in the arbuscule-containing cells of mycorrhizal roots from different legume and non legume plants. Mol Plant-Microb Interact 17:62–69Google Scholar
  147. Walter MH, Fester T, 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 21:571–578PubMedGoogle Scholar
  148. Weidmann S, Sanchez L, Descombin J, Chatagnier O, Gianinazzi S, Gianinazzi-Pearson V (2004) Fungal elicitation of signal transduction-related plant genes precedes mycorrhiza establishment and requires the dmi3 gene in Medicago truncatula. Mol Plant-Microb Interact 17:1385–1393Google Scholar
  149. 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-Microb Interact 16:306–314Google Scholar

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© Springer-Verlag 2006

Authors and Affiliations

  1. 1.Istituto per la Protezione delle Piante—Sezione di Torino-CNRTurinItaly
  2. 2.Dipartimento di Biologia VegetaleUniversità di TorinoTurinItaly

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