Abstract
The persistence through evolution of the arbuscular mycorrhiza (AM) symbiosis between Glomeromycota and plants is probably due to a widespread molecular dialogue between the two partners. Most studies have focussed on established mycorrhizal systems whilst evidence for cellular commitment of the symbiotic partners during early developmental phases is recent. Whereas spore germination by AM fungi can occur spontaneously, subsequent hyphal branching, appressoria differentiation, root penetration and intraradical development leading to symbiosis establishment are under the control of molecular interactions between the two partners. In this chapter, recent work on AM fungus–plant interactions is presented in such a way as to highlight the subtlety of this ancestral molecular complicity between the two partners.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Similar content being viewed by others
References
Akiyama K Matsuzaki K Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi Nature 435824–827
Albrecht C Geurts R Lapeyrie F Bisseling T (1998) Endomycorrhizae and rhizobial Nod factors both requireSYM8 to induce the expression of the early nodulin genesPsENOD5 andPsENOD12A Plant J 15605–614
Aréchiga-Carvajal ET Ruiz-Herrera J (2005) The RIM101/pacC homologue from the basidiomyceteUstilago maydis is functional in multiple pH-sensitive phenomena Euk Cell 4999–1008
Bécard G Douds DD Pfeffer PE (1992) Extensive hyphal growth of vesicular-arbuscular mycorrhizal fungi in the presence of CO2 and flavonols Appl Env Microb 58821–825
Bécard G Kosuta S Tamasloukht M Séjalon-Delmas N Roux C (2004) Partner communication in the arbuscular mycorrhizal interaction Can J Bot 821186–1197
Besserer A Puech-Pagès V Kiefer P Gomez-Roldan V Jauneau A Roy S Portais JC Roux C Bécard G Séjalon-Delmas N (2006) Strigolactones stimulate arbuscular mycorrhizal fungi by activating mitochondria PLoS Biol 4e226
Blilou I Ocampo JA Garcia-Garrido JM (1999) Resistance of pea roots to an endomycorrhizal fungus orRhizobium correlates with enhanced levels of endogenous salicylic acid J Exp Bot 501663–1668
Blilou I Ocampo JA Garcia-Garrido JM (2000) Induction ofLtp (Lipid transfer protein) andPal (Phenylalanine ammonia-lyase) gene expression in rice roots colonized by the arbuscular mycorrhizal fungusGlomus mosseae J Exp Bot 511969–1977
Bouwmeester HJ Toux C Lopez-Raez JA Bécard G (2007) Rhizosphere communication of plants, parasitic plants and AM fungi Trends Plant Sci 12224–230
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 ofMedicago truncatula-Glomus mosseae interactions Mycorrhiza 14253–262
Breuninger M Requena N (2004) Recognition events in AM symbiosis: analysis of fungal gene expression at the early appressorium stage Fungal Gen Biol 41794–804
Buée M Rossignol M Jauneau A Ranjeva R Bécard 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 13693–698
Catoira R Galera R de Billy F Penmetsa V Journet E-P Mailler F Rosenberg C Cook D Gough C Dénarié J (2000) Four genes ofMedicago truncatula controlling components of a Nod factor transduction pathway Plant Cell 121647–1665
Chabaud M Venard C Defaux-Petras A Bécard G Barker DG (2002) Targeted inoculation ofMedicago truncatula in vitro root cultures revealsMtENOD11 expression during early stages of infection by arbuscular mycorrhizal fungi New Phytol 156265–273
Gadkar V David-Schwartz R Nagahashi G Douds DD Wininger S Kapulnik Y (2003) Root exudate ofpmi tomato mutant M161 reduces AM fungal proliferation in vitro FEMS Microbiol Lett 223193–198
Gao LL Smith FA Smith SE (2006) The rmc locus does not affect plant interactions or defence-related gene expression when tomato (Solanum lycopersicon) is infected with the root fungal parasiteRhizoctonia Funct Plant Biol 33289–296
García-Garrido JM Ocampo JA (2002) Regulation of the plant defence response in arbuscular mycorrhizal symbiosis J Exp Bot 531377–1386
Genre A Chabaud M Timmers T Bonfante P Barker DG (2005) Arbuscular mycorrhizal fungi elicit a novel intracellular apparatus inMedicago truncatula root epidermal cells before infection Plant Cell 173489–3499
Gianinazzi-Pearson V Branzanti B Gianinazzi S (1989) In vitro enhancement of spore germination and hyphal growth of a vesicular-arbuscular mycorrhizal fungus by host root exudates and plant flavonoids Symbiosis 7243–255
Gianinazzi-Pearson V Gollotte A Dumas-Gaudot E Franken P Gianinazzi S (1994) Gene expression and molecular modifications associated with plant responses to infection by arbuscular mycorrhizal fungi. In Downie DM Osbourn AE Advances in molecular genetics of plant-microbe interactions, vol 3 Kluwer Boston, pp 179–186
Gianinazzi-Pearson V Weidmann S Seddas P Massoumo M van Tuinen D Gianinazzi S (2006) Signal-related gene responses in beneficial root interactions with non-rhizobial microorganisms. In Sanchez F Quinto C Lopez-Lara IM Geiger O Biology of plant-microbe interactions vol 5 IS-MPMI St Paul, Minnesota, pp 516–524
Gianinazzi-Pearson V Séjalon-Delmas N Genre A Jeandroz S Bonfante P (2007) Plants and arbuscular mycorrhizal fungi: cues and communication in the early steps of symbiotic interactions Adv Bot Res 46181–219
Giovannetti M Sbrana C Logi C (1994) Early processes involved in host recognition by arbuscular mycorrhizal fungi New Phytol 127703–709
Giovannetti M Sbrana C Citernesi AS Avio L (1996) Analysis of factors involved in fungal recognition responses to host-derived signals by arbuscular mycorrhizal fungi New Phytol 13365–71
Goldwasser Y Yoder JI (2001) Differential induction ofOrobanche seed germination byArabidopsis thaliana Plant Sci 160951–959
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’ myc- mutant ofPisum sativum (L.) Planta 191112–122
Hause B Mrosk C Isayenkov S Strack D (2007) Jasmonates in arbuscular mycorrhizal interactions Phytochemistry 68101–110
Kosuta S Chabaud M Lougnon G Gough C Dénarie J Barker DG Bécard G (2003) A diffusible factor from arbuscular mycorrhizal fungi induces symbiosis-specificMtENOD11 expression in roots ofMedicago truncatula Plant Physiol 131952–962
Larose G Chênevert R Moutoglis P Gagne S Piché Y Vierheilig H (2002) Flavonoid levels in roots ofMedicago sativa are modulated by the development stage of the symbiosis and the root colonizing arbuscular-mycorrhizal fungus J Plant Phys 1591329–1339
Liu J Maldonado-Mendoza I Lopez-Meyer M Cheung F Tow 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 50529–544
Massoumou M van Tuinen D Chatagnier O Arnould C Brechenmacher L Sanchez L Selim S Gianinazzi S Gianinazzi-Pearson V (2007) Medicago truncatula gene responses specific to arbuscular mycorrhiza interactions with different species and genera of Glomeromycota Mycorrhiza 17223–234
Mellersh D Parniske M (2006) Common symbiosis genes ofLotus japonicus are not required for intracellular accommodation of the rust fungusUromyces loti New Phytol 170641–644
Nagahashi G Douds DD (2000) Partial separation of root exudate components and their effects upon the growth of germinated spores of AM fungi Mycol Res 1041453–1464
Navazio N Moscatiello R Genre A Novero M Baldan B Bonfante P Mariani P (2006) A diffusible signal from arbuscular mycorrhizal fungi elicits a transient cytosolic calcium elevation in host plant cells Plant Physiol 144673–681
Okazaki N Okasaki K Watanabe Y Kato-Hayashi M Yamamoto M Okayama H (1998) Novel factor highly conserved among eukaryotes controls sexual development in fission yeast Mol Cell Biol 18887–895
Oldroyd GED Downie JA (2006) Nuclear calcium changes at the core of symbiosis signalling Curr Op Plant Biol 9351–357
Pozo MJ Azcon-Aguilar C (2007) Unraveling mycorrhiza-induced resistance Curr Op Plant Biol 10393–398
Redecker D Kodner R Graham LE (2000) Glomalean fungi from the Ordovician Science 2891920–1921
Requena N Mann P Hampp R Franken P (2002) Early developmentally regulated genes in the arbuscular mycorrhizal fungusGlomus mosseae: identification ofGmGIN1, a novel gene with homology to the C-terminus of metazoan hedgehog proteins Plant Soil 244129–139
Ruiz-Lozano JM Roussel H Gianinazzi S Gianinazzi-Pearson V (1999) Defence genes are differentially induced by a mycorrhizal fungus andRhizobium in wild type and symbiosis-defective pea genotypes Mol Plant-Microbe Interact 12976–984
Sabbagh SK (2008) Adaptation à la pénétration racinaire de deux Ustilaginaceae parasites du maïsUstilago maydis etSporisorium reilianum – Analyse microscopique et transcriptomique. Doctoral thesis, University of Toulouse III, F, 97 pages
Sanchez L Weidmann S Arnould C Bernard AR Gianinazzi S Gianinazzi-Pearson V (2005) P. fluorescens andG. mosseae triggerDMI3-dependent activation of genes related to a signal transduction pathway in roots ofMedicago truncatula Plant Physiol 1391065–1077
Scervino JM Ponce MA Erra-Bassells R Bompadre J Vierheilig H Ocampo JA Godeas A (2005) Flavonoids exhibit fungal species and genus effects on the presymbiotic growth ofGigaspora andGlomus Mycol Res 109789–794
Scervino JM Ponce MA Erra-Bassells R Bompadre MJ Vierheilig H Ocampo JA Godeas A (2006) Glycosidation of apigenin results in a loss of its activity on different growth parameters of arbuscular mycorrhizal fungi from the genusGlomus andGigaspora Soil Biol Biochem 382919–2922
Seddas PMA, Arnould C, Tollot M, Arias CM, Gianinazzi-Pearson V (2008) Spatial monitoring of gene activity in extraradical and intraradical developmental stages of arbuscular mycorrhizal fungi by direct fluorescent in situ RT-PCR Fungal Gen Biol 451155–1165
Siciliano V Genre A Balestrini R Cappellazzo G deWit PJGM Bonfante P (2007) transcriptome analysis of arbuscular mycorrhizal roots during development of the prepenetration apparatus Plant Physiol 1441455–1466
Steinkellner S Lendzemo V Langer I Schweiger P Khaosaad T Toussaint JP Vierheilig H (2007) Flavonoids and strigolactones in root exudates as signals in symbiotic and pathogenic plant-fungus interactions Molecules 121290–1306
Stöhr C Stremlau S (2006) Formation and possible roles of nitric oxide in plant roots J Exp Bot 57463–470
Tamasloukht MB Sejalon-Delmas N Kluver A Roux C Bécard 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 fungusGigaspora rosea Plant Physiol 1311468–1478
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 Env Microb 715341–5347
Vierheilig H Bago B Albrecht C Poulin M-P Piché Y (1998) Flavonoids and arbuscular-mycorrhizal fungi. In Manthey JA Buslig BS Flavonoids in the living system Plenum Press New York, pp 9–33
Vieweg MF Hohnjec N Küster H (2005) Two genes encoding truncated hemoglobins are regulated during root nodule and arbuscular mycorrhiza symbioses ofMedicago truncatula Planta 220757–766
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 inMedicago truncatula Mol Plant-Microbe Interact 171385–1393
Westwood JH (2000) Characterization of theOrobanche-Arabidopsis system for studying parasite-host interactions Weed Sci 48742–748
Xu JR Hamer JE (1996) MAP kinase and cAMP signaling regulate infection structure formation and pathogenic growth in the rice blast fungusMagnaporthe grisae Genes Devel 102696–2706
Xu JR Staiger CJ Hamer JE (1998) Inactivation of the mitogen-activated protein kinase Mps1 from the rice blast fungus prevents penetration of the host cells but allows activation of plant defence responses Proc Natl Acad Sci USA 9512713–12718
Yamasaki H Sakihama Y (2000) Simultaneous production of nitric oxide and peroxynitrite by plant nitrate reductase: in vitro evidence for the NR-dependent formation of active nitrogen species FEBS Lett 46889–92
Acknowledgements
The authors are grateful to INRA and the Conseil Régional de Bourgogne for financial support for part of the work reported here.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2009 Springer-Verlag Berlin Heidelberg
About this chapter
Cite this chapter
Gianinazzi-Pearson, V., Tollot, M., Seddas, P.M. (2009). Dissection of Genetic Cell Programmes Driving Early Arbuscular Mycorrhiza Interactions. In: Azcón-Aguilar, C., Barea, J., Gianinazzi, S., Gianinazzi-Pearson, V. (eds) Mycorrhizas - Functional Processes and Ecological Impact. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-540-87978-7_3
Download citation
DOI: https://doi.org/10.1007/978-3-540-87978-7_3
Published:
Publisher Name: Springer, Berlin, Heidelberg
Print ISBN: 978-3-540-87977-0
Online ISBN: 978-3-540-87978-7
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)