Signalling and the Re-structuring of Plant Cell Architecture in AM Symbiosis

  • Andrea GenreEmail author
Part of the Signaling and Communication in Plants book series (SIGCOMM, volume 11)


Arbuscular mycorrhizas are widespread and ancient plant symbioses that were already established by the first land plants when they abandoned the water environment. Arbuscular mycorrhizal fungi scavenge mineral nutrients and water from the soil improving the overall plant fitness, receiving in exchange carbohydrates that are indispensable to complete their life cycle. In spite of their importance in natural and agricultural ecosystems, many biological aspects of these interactions are still partially obscure, especially concerning the early stages of symbiosis establishment which involve a signal exchange between the partners. Nonetheless, recent advancements have started to shed light on plant–fungus signalling mechanisms and their relation with the cell responses that culminate in fungal accommodation in the root cells. This chapter is focused on such advances and the new views that they have suggested.


Arbuscular Mycorrhiza Arbuscular Mycorrhiza Calcium Spike Intracellular Hypha Symbiosis Establishment 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



I am grateful to Paola Bonfante and Luisa Lanfranco for useful discussion and critical reading of the manuscript. Experimental work described here was supported by grants to Paola Bonfante from Compagnia di San Paolo and Converging technologies-CIPE BIOBIT project.


  1. Akiyama K, Matsuzaki K, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435:824–827PubMedCrossRefGoogle Scholar
  2. Akiyama K, Ogasawara S, Ito S, Hayashi H (2010) Structural requirements of strigolactones for hyphal branching in AM fungi. Plant Cell Physiol 51:1104–1117PubMedCrossRefGoogle Scholar
  3. Allen GJ, Kwak JM, Chu SP, Llopis J, Tsien RY, Harper JF, Schroeder JI (1999) Cameleon calcium indicator reports cytoplasmic calcium dynamics in Arabidopsis guard cells. Plant J 19:735–747PubMedCrossRefGoogle Scholar
  4. Ané JM, 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, Dénarie J, Cook DR (2004) Medicago truncatula DMI1 required for bacterial and fungal symbioses in legumes. Science 303:1364–1367PubMedCrossRefGoogle Scholar
  5. Arite T, Umehara M, Ishikawa S, Hanada A, Maekawa M, Yamaguchi S, Kyozuka J (2009) d14, a strigolactone insensitive mutant of rice, shows an accelerated outgrowth of tillers. Plant Cell Physiol 50:1416–1424PubMedCrossRefGoogle Scholar
  6. Balestrini R, Gómez-Ariza J, Lanfranco L, Bonfante P (2007) Laser microdissection reveals that transcripts for five plant and one fungal phosphate transporter genes are contemporaneously present in arbusculated cells. Mol Plant -Microbe Interact 20:1055–1062PubMedCrossRefGoogle Scholar
  7. Barker SJ, Stummer B, Gao L, Dispain I, O'Connor PJ, Smith SE (1998) A mutant in Lycopersicon esculentum Mill, with highly reduced VA mycorrhizal colonization: isolation and preliminary characterization. Plant J 15:791–797CrossRefGoogle Scholar
  8. Bastmeyer M, Deising H, Bechinger C (2002) Force exertion in fungal infection. Annu Rev Biophys Biomol Struct 31:321–341PubMedCrossRefGoogle Scholar
  9. Bécard G, Fortin JA (1988) Early events of vesicular-arbuscular mycorrhiza formation on Ri T-DNA transformed roots. New Phytol 108:211–218CrossRefGoogle Scholar
  10. Besserer A, Puech-Pagès V (2006) Strigolactones stimulate arbuscular mycorrhizal fungi by activating mitochondria. PLoS Biol 4:1239–1247CrossRefGoogle Scholar
  11. Besserer A, Becard G, Jauneau A, Roux C, Sejalon-Delmas N (2008) GR24, a synthetic analog of strigolactones, stimulates the mitosis and growth of the arbuscular mycorrhizal fungus Gigaspora rosea by boosting its energy metabolism. Plant Physiol 148:402–413PubMedCentralPubMedCrossRefGoogle Scholar
  12. 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 217:154–165PubMedCrossRefGoogle Scholar
  13. Bonfante P (2001) At the interface between mycorrhizal fungi and plants: the structural organization of cell wall, plasma membrane and cytoskeleton. In: Hock B (ed) Mycota, vol IX, Fungal associations. Springer, Heidelberg, pp 45–91Google Scholar
  14. Bonfante P, Genre A (2008) Plants and arbuscular mycorrhizal fungi: an evolutionary-developmental perspective. Trends Plant Sci 13:492–498PubMedCrossRefGoogle Scholar
  15. Bonfante P, Genre A (2010) Mechanisms underlying beneficial plant–fungus interactions in mycorrhizal symbiosis. Nature Commun 1:48CrossRefGoogle Scholar
  16. Branscheid A, Sieh D, Pant BD, May P, Devers EA, Elkrog A, Schauser L, Scheible WR, Krajinski F (2010) Expression pattern suggests a role of MiR399 in the regulation of the cellular response to local Pi increase during arbuscular mycorrhizal symbiosis. Mol Plant Microbe Interact 23:915–926PubMedCrossRefGoogle Scholar
  17. Buee M, Rossignol M, Jauneau A, Ranjeva R, Becard G (2000) The pre-symbiotic growth of arbuscular mycorrhizal fungi is induced by a branching factor partially purified from plant root exudates. Mol Plant Microbe Interact 13:693–698PubMedCrossRefGoogle Scholar
  18. Cano C, Dickson S, González-Guerrero M, Bago A (2008) In vitro cultures open new prospects for basic research in arbuscular mycorrhizas. In: Mycorrhiza: state of the art, genetics and molecular biology, eco-function, biotechnology, eco-physiology, structure and systematics, 3 rd ed. Springer, Heidelberg, pp 627–654Google Scholar
  19. Catanzariti AM, Dodds PN, Lawrence GJ, Ayliffe MA, Ellisa JG (2006) Haustorially expressed secreted proteins from flax rust are highly enriched for avirulence elicitors. Plant Cell 18:243–256PubMedCentralPubMedCrossRefGoogle Scholar
  20. Cavagnaro TR, Smith FA, Hay G, Carne-Cavagnaro VL, Smith SE (2004) Inoculum type does not affect overall resistance of an arbuscular mycorrhiza-defective tomato mutant to colonisation but inoculation does change competitive interactions with wild-type tomato. New Phytol 161:485–494CrossRefGoogle Scholar
  21. Chabaud M, Venard C, Defaux-Petras A, Becard G, Barker DG (2002) Targeted inoculation of Medicago truncatula in vitro root cultures reveales MtENOD11 expression during early stages of infection by arbuscular mycorrhizal fungi. New Phytol 156:265–273CrossRefGoogle Scholar
  22. Chabaud M, Genre A, Sieberer BJ, Faccio A, Fournier J, Novero M, Barker DG, Bonfante P (2010) Arbuscular mycorrhizal hyphopodia and germinated spore exudates trigger Ca2+ spiking in the legume and nonlegume root epidermis. New Phytol 189:347–355PubMedCrossRefGoogle Scholar
  23. Charpentier M, Bredemeier R, Wanner G, Takeda N, Schleiff E, Parniske P (2008) Lotus japonicus CASTOR and POLLUX are ion channels essential for perinuclear calcium spiking in legume root endosymbiosis. Plant Cell 20:3467–3479PubMedCentralPubMedCrossRefGoogle Scholar
  24. Cook CE, Whichard LP et al (1966) Germination of witchweed (Striga Lutea Lour): isolation and properties of a potent stimulant. Science 154:1189–1190PubMedCrossRefGoogle Scholar
  25. Croll D, Giovannetti M, Koch A, Sbrana C, Ehinger M, Lammers P, Sanders I (2009) Nonself vegetative fusion and genetic exchange in the arbuscular mycorrhizal fungus Glomus intraradices. New Phytol 181:924–937PubMedCrossRefGoogle Scholar
  26. 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 27:561–569PubMedCrossRefGoogle Scholar
  27. Delaux PM, Bécard G, Séjalon-Delmas N (2009) Evolutive origin of strigolactones. Proceedings of the 6th international conference on Mycorrhiza, 9–14 August 2009. International Mycorrhiza Society, Belo Horizonte, BrazilGoogle Scholar
  28. Dickson S (2004) The Arum–Paris continuum of mycorrhizal symbioses. New Phytol 163:187–200CrossRefGoogle Scholar
  29. Dickson S, Kolesik P (1999) Visualisation of mycorrhizal fungal structures and quantification of their surface area and volume using laser scanning confocal microscopy. Mycorrhiza 9:205–213CrossRefGoogle Scholar
  30. Drissner D, Kunze G, Callewaert N, Gehrig P, Tamasloukht MB, Boller T, Felix G, Amrhein N, Bucher M (2007) Lysophosphatidylcholine is a signal in the arbuscular mycorrhizal symbiosis. Science 318:265–268PubMedCrossRefGoogle Scholar
  31. Erhardt DW, Wais R, Long SR (1996) Calcium spiking in plant root hairs responding to Rhizobium nodulation signals. Cell 85:673–681CrossRefGoogle Scholar
  32. Feraru E, Friml J (2008) PIN polar targeting. Plant Physiol 147:1553–1559PubMedCentralPubMedCrossRefGoogle Scholar
  33. Fiorilli V, Catoni M, Miozzi L, Novero M, Accotto GP, Lanfranco L (2009) Global and cell-type gene expression profiles in tomato plants colonized by an arbuscular mycorrhizal fungus. New Phytol 184:975–987PubMedCrossRefGoogle Scholar
  34. Geldner N, Robatzek S (2008) Plant receptors go endosomal: a moving view on signal transduction. Plant Physiol 147:1565–1574PubMedCentralPubMedCrossRefGoogle Scholar
  35. 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 17:3489–3499PubMedCentralPubMedCrossRefGoogle Scholar
  36. Genre A, Chabaud M, Faccio A, Barker DG, Bonfante P (2008) Prepenetration apparatus assembly precedes and predicts the colonization patterns of arbuscular mycorrhizal fungi within the root cortex of both Medicago truncatula and Daucus carota. Plant Cell 20:1407–1420PubMedCentralPubMedCrossRefGoogle Scholar
  37. Genre A, Ortu G, Bertoldo C, Martino E, Bonfante P (2009) Biotic and abiotic stimulation of root epidermal cells reveals common and specific responses to arbuscular mycorrhizal fungi. Plant Physiol 149:1424–1434PubMedCentralPubMedCrossRefGoogle Scholar
  38. Gómez-Roldán V, Fermas S, Brewer PB, Puech-Pagès V, Dun EA, Pillot JP, Letisse F, Matusova R, Danoun S, Portais JC, Bouwmeester H, Bécard G, Beveridge CA, Rameau C, Rochange SF (2008) Strigolactone inhibition of shoot branching. Nature 455:189–194PubMedCrossRefGoogle Scholar
  39. Gu M, Xu K, Chen A, Zhu Y, Tang G, Xu G (2010) Expression analysis suggests potential roles of microRNAs for phosphate and arbuscular mycorrhizal signaling in Solanum lycopersicum. Physiol Plant 138:226–237PubMedCrossRefGoogle Scholar
  40. Guether M, Neuhauser B, Balestrini R, Dynowski M, Ludewig U, Bonfante P (2009) A mycorrhizal specific ammonium transporter from Lotus japonicus acquires nitrogen. Plant Physiol 150:73–83PubMedCentralPubMedCrossRefGoogle Scholar
  41. Gutjahr C, Paszkowski U (2009) Weights in the balance: jasmonic acid and salicylic acid signaling in root-biotroph interactions. Mol Plant Microbe Interact 22:763–772PubMedCrossRefGoogle Scholar
  42. Gutjahr C, Banba M, Croset V, An K, Miyao A, An G, Hirochika H, Imaizumi-Anraku H, Paszkowski U (2008) Arbuscular mycorrhiza-specific signaling in rice transcends the common symbiosis signaling pathway. Plant Cell 20:2989–3005PubMedCentralPubMedCrossRefGoogle Scholar
  43. Gutjahr C, Novero M, Guether M, Montanari O, Udvardi M, Bonfante P (2009) Presymbiotic factors released by the arbuscular mycorrhizal fungus Gigaspora margarita induce starch accumulation in Lotus japonicus roots. New Phytol 183:53–61PubMedCrossRefGoogle Scholar
  44. Harper JF, Harmon A (2005) Plants, symbiosis and parasites: a calcium signalling connection. Nat Rev Mol Cell Biol 6:555–566PubMedCrossRefGoogle Scholar
  45. Harrison MJ (2005) Signaling in the arbuscolar mycorrhizal symbiosis. Annu Rev Microbiol 59:19–42PubMedCrossRefGoogle Scholar
  46. Hause B, Schaarschmidt S (2009) The role of jasmonates in mutualistic symbioses between plants and soil-born microoganisms. Phytochemistry 70:1589–1599PubMedCrossRefGoogle Scholar
  47. Hazledine S, Sun J, Wysham D, Downie JA, Oldroyd GE, Morris RJ (2009) Nonlinear time series analysis of nodulation factor induced calcium oscillations: evidence for deterministic chaos? PLoS One 4:e6637PubMedCentralPubMedCrossRefGoogle Scholar
  48. Helber N, Requena N (2008) Expression of the fluorescence markers DsRed and GFP fused to a nuclear localization signal in the arbuscular mycorrhizal fungus Glomus intraradices. New Phytol 177:537–548PubMedGoogle Scholar
  49. Hetherington AM, Brownlee C (2004) The generation of Ca2+ signals in plants. Annu Rev Plant Biol 55:401–427PubMedCrossRefGoogle Scholar
  50. Hijri M, Sanders IR (2005) Low gene copy number shows that arbuscular mycorrhizal fungi inherit genetically different nuclei. Nature 433:161–163CrossRefGoogle Scholar
  51. Ishikawa S, Maekawa M, Arite T, Onishi K, Takamure I, Kyozuka J (2005) Suppression of tiller bud activity in tillering dwarf mutants of rice. Plant Cell Physiol 46:79–86PubMedCrossRefGoogle Scholar
  52. Javot H, Penmetsa RV, Terzaghi N, Cook DR, Harrison MJ (2007) A Medicago truncatula phosphate transporter indispensable for the arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci USA 104:1720–1725PubMedCrossRefGoogle Scholar
  53. Jentschel K, Thiel D, Rehn F, Ludwig-Müller J (2007) Arbuscular mycorrhiza enhances auxin levels and alters auxin biosynthesis in Tropaeolum majus during early stages of colonization. Physiol Plant 129:320–333CrossRefGoogle Scholar
  54. Kanamori N, Madsen LH, Radutoiu S, Frantescu M, Quistgaard EMH, Miwa H, Downie JA, James EK, Felle HH, Haaning LL (2006) A nucleoporin is required for induction of Ca2+ spiking in legume nodule development and essential for rhizobial and fungal symbiosis. Proc Natl Acad Sci USA 103:359–364PubMedCrossRefGoogle Scholar
  55. 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 17:2217–2229PubMedCentralPubMedCrossRefGoogle Scholar
  56. Kobae K, Hata S (2010) Dynamics of periarbuscular membranes visualized with a fluorescent phosphate transporter in arbuscular mycorrhizal roots of rice. Plant Cell Physiol 51:341–353PubMedCrossRefGoogle Scholar
  57. Koltai H, LekKala SP, Bahattacharya C, Mayzlish-Gati E, Resnick N, Wininger S, Dor E, Yoneyama K, Yoneyama K, Hershenhorn J, Joel DM, Kapulnik YC (2010) A tomato strigolactone-impaired mutant displays aberrant shoot morphology and plant interactions. J Exp Bot 61:1739–1749PubMedCrossRefGoogle Scholar
  58. Kosuta S, Chabaud M, Lougnon G, Gough C, Dénarié J, Barker DG, Bécard G (2003) A diffusible factor from arbuscular mycorrhizal fungi induces symbiosis-specific MtENOD11 expression in roots of Medicago truncatula. Plant Physiol 131:952–962PubMedCentralPubMedCrossRefGoogle Scholar
  59. Kosuta S, Hazledine S, Sun J, Miwa H, Morris RJ, Downie JA, Oldroyd GE (2008) Differential and chaotic calcium signatures in the symbiosis signaling pathway of legumes. Proc Natl Acad Sci USA 105:9823–9828PubMedCrossRefGoogle Scholar
  60. Kuhn H, Kuster H, Requena N (2010) Membrane steroid-binding protein 1 induced by a diffusible fungal signal is critical for mycorrhization in Medicago truncatula. New Phytol 185:716–733PubMedCrossRefGoogle Scholar
  61. Lee SH, Cho HT (2006) PINOID positively regulates auxin efflux in Arabidopsis root hair cells and tobacco cells. Plant Cell 18:1604–1616PubMedCentralPubMedCrossRefGoogle Scholar
  62. Leeper GW (1952) Factors affecting availability of inorganic nutrients in soils with special reference to micronutrient metals. Annu Rev Plant Physiol 3:1–16CrossRefGoogle Scholar
  63. Leight J, Hodge A, Fitter AH (2009) Arbuscular mycorrhizal fungi can transfer substantial amounts of nitrogen to their host plant from organic material. New Phytol 181:199–207CrossRefGoogle Scholar
  64. Lévy J, Bres C, Geurts R, Chalhoub B, Kulikova O, Duc G, Journet EP, Ané JM, Laubert E, Bisseling T, Dénarié J, Rosenberg C, Debellé F (2004) A putative Ca2+ and calmodulin-dependent protein kinase required for bacterial and fungal symbioses. Science 303:1361–1364PubMedCrossRefGoogle Scholar
  65. Liu JY, Maldonado-Mendoza I, Lopez-Meyer M, Cheung F, Town CD, Harrison MJ (2007) Arbuscular mycorrhizal symbiosis is accompanied by local and systemic alterations in gene expression and an increase in disease resistance in the shoots. Plant J 50:529–544PubMedCrossRefGoogle Scholar
  66. López-Ráez JA, Verhage A, Fernández I, García JM, Azcón-Aguilar C, Flors V, Pozo MJ (2010) Hormonal and transcriptional profiles highlight common and differential host responses to arbuscular mycorrhizal fungi and the regulation of the oxylipin pathway. J Exp Bot 61:2589–2601PubMedCrossRefGoogle Scholar
  67. Ludwig-Müller J, Güther M (2007) Auxins as signals in arbuscular mycorrhiza formation. Plant Signal Behav 2:194–196PubMedCentralPubMedCrossRefGoogle Scholar
  68. Maillet F, Poinsot V, Andre O, Puech-Pages V, Haouy A, Gueunier M, Giraudet D, Formey D, Martinez EA, Driguez H, Becard G, Dénarié J (2011) Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature 69:58–63CrossRefGoogle Scholar
  69. Markmann K, Parniske M (2009) Evolution of root endosymbiosis with bacteria: how novel are nodules? Trends Plant Sci 14:77–86PubMedCrossRefGoogle Scholar
  70. Markmann K, Giczey G, Parniske M (2008) Functional adaptation of a plant receptor-kinase paved the way for the evolution of intracellular root symbioses with bacteria. PLoS Biol 6:e68PubMedCentralPubMedCrossRefGoogle Scholar
  71. Messinese E, Mun JH, Yeun LH, Jayaraman D, Rougé P, Barre A, Lougnon G, Schornack S, Bono JJ, Cook DR, Ané JM (2007) A novel nuclear protein interacts with the symbiotic DMI3 calcium- and calmodulin-dependent protein kinase of Medicago truncatula. Mol Plant Microbe Interact 20:912–921PubMedCrossRefGoogle Scholar
  72. Morandi D, Prado E, Sagan M, Duc G (2005) Characterisation of new symbiotic Medicago truncatula (Gaertn.) mutants, and phenotypic or genotypic complementary information on previously described mutants. Mycorrhiza 15:283–289PubMedCrossRefGoogle Scholar
  73. Navazio L, Moscatiello R, Genre A, Novero M, Baldan B, Bonfante P, Mariani P (2007) A diffusible signal from arbuscular mycorrhizal fungi elicits a transient cytosolic calcium elevation in host plant cells. Plant Physiol 144:673–681PubMedCentralPubMedCrossRefGoogle Scholar
  74. Novero M, Faccio A, Genre A, Stougaard J, Webb K, Mulder L, Parniske M, Bonfante P (2002) Dual requierment of the LjSYM4 gene for mycorrhizal development in epidermal and cortical cells of Lotus japonicus roots. New Phytol 154:741–749CrossRefGoogle Scholar
  75. O’Connell RJ, Panstruga R (2006) Tête à tête inside a plant cell: establishing compatibility between plants and biotrophic fungi and oomycetes. New Phytol 171:699–718PubMedCrossRefGoogle Scholar
  76. Olah B, Briere C, Becard G, Denarie 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 44:195–207PubMedCrossRefGoogle Scholar
  77. Oldroyd GED, Downie JA (2006) Nuclear calcium changes at the core of symbiosis signalling. Curr Opin Plant Biol 9:351–357PubMedCrossRefGoogle Scholar
  78. Parniske M (2008) Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat Rev Microbiol 6:763–775PubMedCrossRefGoogle Scholar
  79. Paszkowski U (2006a) A journey through signaling in arbuscular mycorrhizal symbioses. New Phytol 172:35–46PubMedCrossRefGoogle Scholar
  80. Paszkowski U (2006b) Mutualism and parasitism: the yin and yang of plant symbioses. Curr Opin Plant Biol 9:364–370PubMedCrossRefGoogle Scholar
  81. Paszkowski U, Jakovleva L, Boller T (2006) Maize mutants affected at distinct stages of the arbuscular mycorrhizal symbiosis. Plant J 47:165–173PubMedCrossRefGoogle Scholar
  82. Pawlowska TE, Taylor JW (2004) Organization of genetic variation in individuals of arbuscular mycorrhizal fungi. Nature 427:733–737PubMedCrossRefGoogle Scholar
  83. Pumplin N, Harrison MJ (2009) Live-cell imaging reveals periarbuscular membrane domains and organelle location in Medicago truncatula roots during arbuscular mycorrhizal symbiosis. Plant Physiol 151:809–819PubMedCentralPubMedCrossRefGoogle Scholar
  84. Pumplin N, Mondo SJ, Topp S, Starker CG, Gantt JS, Harrison MJ (2010) Medicago truncatula Vapyrin is a novel protein required for arbuscular mycorrhizal symbiosis. Plant J 61:482–494PubMedCrossRefGoogle Scholar
  85. Reddy DMRS, Schorderet M, Feller U, Reinhardt D (2007) A petunia mutant affected in intracellular accommodation and morphogenesis of arbuscular mycorrhizal fungi. Plant J 51:739–750CrossRefGoogle Scholar
  86. Remy W, Taylor TN, Hass H, Kerp H (1994) Four hundred-million-year-old vesicular arbuscular mycorrhizae. Proc Natl Acad Sci USA 91:11841–11843PubMedCrossRefGoogle Scholar
  87. Saito K, Yoshikawa M, Yano K, Miwa H, Uchida H, Asamizu E, Sato S, Tabata S, Imaizumi-Anraku H, Umehara Y, Kouchi H, Murooka Y, Szczyglowski K, Downie JA, Parniske M, Makoto Hayashi M, Masayoshi Kawaguchi M (2007) NUCLEOPORIN85 is required for calcium spiking, fungal and bacterial symbioses, and seed production in Lotus japonicus. Plant Cell 19:610–624PubMedCentralPubMedCrossRefGoogle Scholar
  88. Sanders IR, Croll D (2010) Arbuscular mycorrhiza: the challenge to understand the genetics of the fungal partner. Annu Rev Genet 44:271–292PubMedCrossRefGoogle Scholar
  89. Sanders D, Pelloux J, Brownlee C, Harper JF (2002) Calcium at the crossroads of signaling. Plant Cell 14:S401–S417PubMedCentralPubMedGoogle Scholar
  90. Sbrana C, Giovannetti M (2005) Chemotropism in the arbuscular mycorrhizal fungus Glomus mosseae. Mycorrhiza 15:539–545PubMedCrossRefGoogle Scholar
  91. Sieberer BJ, Chabaud M, Timmers AC, Monin A, Fournier J, Barker DG (2009) A nuclear-targeted cameleon demonstrates intranuclear Ca2+ spiking in Medicago truncatula root hairs in response to rhizobial nodulation factors. Plant Physiol 151:1197–1206PubMedCentralPubMedCrossRefGoogle Scholar
  92. Smit P, Raedts J, Portyanko V, Debellé F, Gough C, Bisseling T, Geurts R (2005) NSP1 of the GRAS protein family is essential for rhizobial Nod factor-induced transcription. Science 308:1789–1791PubMedCrossRefGoogle Scholar
  93. Smith SE, Read DJ (2008) Mycorrhiza symbiosis, 3rd edn. Academic, San DiegoGoogle Scholar
  94. Soto MJ, Fernandez-Aparicio M, Castellanos-Morales V, Carcia-Garrido JM, Ocampo JA (2010) First indications for the involvement of strigolactones on nodule formation in alfalfa (Medicago sativa). Soil Biol Biochem 42:383–385CrossRefGoogle Scholar
  95. Valent B, Khang CH (2010) Recent advances in rice blast effector research. Curr Opin Plant Biol 13:434–441PubMedCrossRefGoogle Scholar
  96. Vandenkoornhuyse P, Leyval C, Bonnin I (2001) High genetic diversity in arbuscular mycorrhizal fungi: evidence for recombination events. Heredity 87:243–253PubMedCrossRefGoogle Scholar
  97. Walker SA, Viprey V, Downie JA (2000) Dissection of nodulation signaling using pea mutants defective for calcium spiking induced in root hairs by Nod factors and chitin oligomers. Proc Natl Acad Sci USA 97:13413–13418PubMedCrossRefGoogle Scholar
  98. 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 Microbe Interact 17:1385–1393PubMedCrossRefGoogle Scholar
  99. Zwanenburg B, Mwakaboko AS, Reizelman A, Anilkumar G, Sethumadhavan D (2009) Structure and function of natural and synthetic signalling molecules in parasitic weed germination. Pest Manag Sci 65:478–491PubMedCrossRefGoogle Scholar

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© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  1. 1.Dipartimento di Biologia VegetaleUniversità di TorinoTorinoItaly

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