Skip to main content
Log in

Chemotropism in the arbuscular mycorrhizal fungus Glomus mosseae

  • Original Paper
  • Published:
Mycorrhiza Aims and scope Submit manuscript

Abstract

In this work, we report the occurrence of chemotropism in the arbuscular mycorrhizal (AM) fungus Glomus mosseae. Fungal hyphae were able to respond to host-derived signals by reorienting their growth towards roots and to perceive chemotropic signals at a distance of at least 910 μm from roots. In order to reach the source of chemotropic signals, hyphal tips crossed interposed membranes emerging within 1 mm from roots, eventually establishing mycorrhizal symbiosis. The specificity of chemotropic growth was evidenced by hyphal growth reorientation and membrane penetration occurring only in experimental systems set up with host plants. Since pre-symbiotic growth is a critical stage in the life cycle of obligate AM fungal symbionts, chemotropic guidance may represent an important mechanism functional to host root location, appressorium formation and symbiosis establishment.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Notes

  1. The chemical nature of branching factors has been recently described (Akiyama et al. Nature 635:826–827).

References

  • Aguilar JMM, Ashby AM, Richards AJM, Loake GA, Watson MD, Shaw CH (1992) Chemotaxis of Rhizobium leguminosarum biovar phaseoli towards flavonoid inducers of the symbiotic nodulation genes. J Gen Microbiol 134:2741–2746

    Google Scholar 

  • Ashby AM, Watson MD, Shaw CH (1987) A Ti plasmid-determined function is responsible for chemotaxis of Agrobacterium tumefaciens towards the plant wound product acetosyringone. FEMS Microbiol Lett 41:189–192

    Article  Google Scholar 

  • Ashby AM, Watson MD, Loake GJ, Shaw CH (1988) Ti plasmid-specified chemotaxis of Agrobacterium tumefaciens C58C toward vir-inducing phenolic compounds and soluble factors from monocotyledonous and dicotyledonous plants. J Bacteriol 170:4181–4187

    PubMed  Google Scholar 

  • Balaji B, Poulin MJ, Vierheilig H, Piché Y (1995) Responses of an arbuscular mycorrhizal fungus, Gigaspora margarita, to exudates and volatiles from the Ri T-DNA-transformed roots of nonmycorrhizal and mycorrhizal mutants of Pisum sativum. Exp Mycol 19:275–283

    Article  Google Scholar 

  • Bécard G, Piché Y (1989) Fungal growth stimulation by CO2 and root exudates in vesicular–arbuscular mycorrhizal symbiosis. Appl Environ Microbiol 55:2320–2325

    Google Scholar 

  • Berbara RLL, Morris BM, Fonseca HMAC, Reid B, Gow NAR, Daft MJ (1995) Electrical currents associated with arbuscular mycorrhizal interactions. New Phytol 129:433–438

    Google Scholar 

  • Bergman K, Gulashe-Hoffee M, Hovestadt RE, Larosiliere RC, Ronco PG, Su L (1988) Physiology of behavioral mutants of Rhizobium meliloti. J Bacteriol 170:3249–3254

    PubMed  Google Scholar 

  • 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 13:693–698

    Google Scholar 

  • Caetano-Anolles G, Wall LH, DeMicheli AT, Macchi EM, Bauer WD, Favelukes G (1988) Role of motility and chemotaxis in efficiency of nodulation by Rhizobium meliloti. Plant Physiol 86:1228–1235

    Google Scholar 

  • 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 156:265–273

    Article  Google Scholar 

  • Chi CC, Sabo FE (1978) Chemotaxis of zoospores of Phytophthora megasperma to primary roots of alfalfa seedlings. Can J Bot 56:795–800

    Google Scholar 

  • Currier WW, Strobel GA (1986) Chemotaxis of Rhizobium spp. to plant root exudates. Plant Physiol 59:820–823

    Google Scholar 

  • Deacon JW (1996) Ecological implications of recognition events in the pre-infection stages of root pathogens. New Phytol 133:135–145

    Google Scholar 

  • Dharmatilake AJ, Bauer WD (1992) Chemotaxis of Rhizobium meliloti towards nodulation gene-inducing compounds from alfalfa roots. Appl Environ Microbiol 58:1153–1158

    Google Scholar 

  • Douds DD, Nagahashi G, Abney GD (1996) The differential effects of cell wall associated phenolics, cell walls, and cytosolic phenolics of host and non host roots on the growth of two species of AM fungi. New Phytol 133:289–294

    Google Scholar 

  • Garriock ML, Peterson RL, Ackerley CA (1989) Early stages in colonization of Allium porrum (leek) roots by the vesicular–arbuscular mycorrhizal fungus, Glomus versiforme. New Phytol 112:85–92

    Google Scholar 

  • Gemma JN, Koske RE (1988) Pre-infection interactions between roots and the mycorrhizal fungus Gigaspora gigantea: chemotropism of germ-tubes and root growth response. Trans Br Mycol Soc 91:123–132

    Google Scholar 

  • Gianinazzi-Pearson V (1996) Plant cell responses to arbuscular mycorrhizal fungi: getting to the roots of the symbiosis. Plant Cell 8:1871–1883

    Article  PubMed  Google Scholar 

  • Giovannetti M, Mosse B (1980) An evaluation of techniques for measuring vesicular–arbuscular mycorrhizal infection in roots. New Phytol 84:489–500

    Google Scholar 

  • Giovannetti M, Avio L, Sbrana C, Citernesi AS (1993a) Factors affecting appressorium development in the vesicular–arbuscular mycorrhizal fungus Glomus mosseae (Nicol. and Gerd.) Gerd. and Trappe. New Phytol 123:114–122

    Google Scholar 

  • Giovannetti M, Sbrana C, Avio L, Citernesi AS, Logi C (1993b) Differential hyphal morphogenesis in arbuscular mycorrhizal fungi during pre-infection stages. New Phytol 125:587–594

    Google Scholar 

  • Giovannetti M, Sbrana C, Logi C (1994) Early processes involved in host recognition by arbuscular mycorrhizal fungi. New Phytol 127:703–709

    Google Scholar 

  • Giovannetti M, Sbrana C, Citernesi AS, Avio L (1996) Analysis of factors involved in recognition responses in arbuscular mycorrhizal fungi. New Phytol 133:65–71

    Google Scholar 

  • Harrison MJ (1999) Molecular and cellular aspects of the arbuscular mycorrhizal symbiosis. Annu Rev Plant Physiol Plant Mol Biol 50:361–389

    Google Scholar 

  • Hernandez JBP, Remy S, Sauco VG, Swennen R, Sagi L (1999) Chemotactic movement and attachment of Agrobacterium tumefaciens to banana cells and tissues. J Plant Physiol 155:245–250

    Google Scholar 

  • Holligan PM, Gooday GW (1975) Symbiosis in Convoluta roscoffensis. Symp Soc Exp Biol 29:205–227

    PubMed  Google Scholar 

  • Horan DP, Chilvers GA (1990) Chemotropism—the key to ectomycorrhizal formation? New Phytol 116:297–301

    Google Scholar 

  • Jansson H-B, Johansson T, Nordbring-Hertz B, Tunlid A, Odham G (1988) Chemotropic growth of germ-tubes of Cochliobolus sativus to barley roots or root exudates. Trans Br Mycol Soc 90:647–650

    Google Scholar 

  • Koide RT, Schreiner RP (1992) Regulation of the vesicular–arbuscular mycorrhizal symbiosis. Annu Rev Plant Physiol Plant Mol Biol 43:557–581

    Article  Google Scholar 

  • Koske RE (1982) Evidence for a volatile attractant from plant roots affecting germ tubes of a VA mycorrhizal fungus. Trans Br Mycol Soc 79:305–310

    Google Scholar 

  • 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 131:952–962

    Article  PubMed  Google Scholar 

  • McGillivray AM, Gow NAR (1986) Applied electrical fields polarize the growth of mycelial fungi. J Gen Microbiol 132:2515–2525

    Google Scholar 

  • Mehrota RS (1972) Behavior of zoospores of Phytophthora megasperma var. sojae and P. drechsleri in soil. Can J Bot 50:2125–2130

    Google Scholar 

  • Miller-Wideman MA, Watrud LS (1984) Sporulation of Gigaspora margarita on root cultures of tomato. Can J Microbiol 30:642–646

    Google Scholar 

  • Mitchell RT, Deacon JW (1986) Differential (host-specific) accumulation of zoospores of Pythium on roots of graminaceous and non-graminaceous plants. New Phytol 102:113–122

    Google Scholar 

  • Mosse B (1988) Some studies relating to “independent” growth of vesicular–arbuscular endophytes. Can J Bot 66:2533–2540

    Google Scholar 

  • Mosse B, Hepper CM (1975) Vesicular–arbuscular mycorrhizal infections in root organ cultures. Physiol Plant Pathol 5:215–223

    Google Scholar 

  • Muller D, Jaffe LF (1965) A quantitative study of cellular rheotropism. Biophys J 5:317–335

    Google Scholar 

  • Nagahashi G, Douds DD Jr (1997) Appressorium formation by AM fungi on isolated cell walls of carrot roots. New Phytol 136:299–304

    Article  Google Scholar 

  • Nagahashi G, Douds DD Jr (1999) Rapid and sensitive bioassay to study signals between root exudates and arbuscular mycorrhizal fungi. Biotechnol Tech 13:893–897

    Article  Google Scholar 

  • Nagahashi G, Douds DD Jr, Abney GD (1996) Phosphorus amendment inhibits hyphal branching of the VAM fungus Gigaspora margarita directly and indirectly through its effect on root exudation. Mycorrhiza 6:403–408

    Article  Google Scholar 

  • Phillips JM, Hayman DS (1970) Improved procedure for clearing roots and staining parasites and vesicular–arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Br Mycol Soc 55:158–161

    Google Scholar 

  • Powell CL (1976) Development of mycorrhizal infections from Endogone spores and infected root fragments. Trans Br Mycol Soc 66:439–445

    Google Scholar 

  • Raper JR (1952) Chemical regulation of sexual processes in the tallophytes. Bot Rev 18:447–545

    Google Scholar 

  • 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 135:711–722

    Article  Google Scholar 

  • Suriyapperuma SP, Koske RE (1995) Attraction of germ tubes and germination of spores of the arbuscular mycorrhizal fungus Gigaspora gigantea in the presence of roots of maize exposed to different concentrations of phosphorus. Mycologia 87:772–778

    Google Scholar 

  • Tamasloukht M, Sejalon DN, 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 131:1468–1478

    Article  PubMed  Google Scholar 

  • Tawaraya K, Watanabe S, Yoshida E, Wagatsuma T (1996) Effect of onion (Allium cepa) root exudates on the hyphal growth of Gigaspora margarita. Mycorrhiza 6:57–59

    Article  Google Scholar 

  • Vande Broek A, Lambrecht M, Vanderleyden J (1998) Bacterial chemotactic motility is important for the initiation of wheat root colonization by Azospirillum brasilense. Microbiology 144:2599–2606

    PubMed  Google Scholar 

  • Vierheilig H, Alt M, Mader P, Boller T, Wiemken A (1995) Spreading of Glomus mosseae, a vesicular–arbuscular mycorrhizal fungus, across the rhizosphere of host and non-host plants. Soil Biol Biochem 27:1113–1115

    Article  Google Scholar 

  • Vierheilig H, AltHug M, EngelStreitwolf R, Mader P, Wiemken A (1998) Studies on the attractional effect of root exudates on hyphal growth of an arbuscular mycorrhizal fungus in a soil compartment-membrane system. Plant Soil 203:137–144

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to C. Sbrana.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sbrana, C., Giovannetti, M. Chemotropism in the arbuscular mycorrhizal fungus Glomus mosseae. Mycorrhiza 15, 539–545 (2005). https://doi.org/10.1007/s00572-005-0362-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00572-005-0362-5

Keywords

Navigation