Skip to main content
SpringerLink
Log in

Mechanisms of nutrient transport across interfaces in arbuscular mycorrhizas

  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Bidirectional nutrient transfer between the plant and the fungus is a key feature of arbuscular mycorrhizal symbiosis. The major nutrients exchanged between the symbiotic partners are reduced carbon, assimilated through the plant photosynthesis and phosphate, taken up by the fungal hyphae exploring soil microhabitats. This nutrient exchange takes place across the symbiotic interfaces which are bordered by the plant and fungal plasma membranes. This review provides an overview of the current knowledge of the mechanisms underlying nutrient transport processes in the symbiosis, with special emphasis on recent developments in the molecular biology of the plant and fungal primary (H+-ATPases) and secondary transporters.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Alexander T, Toth R, Meier R and Weber HC 1989 Dynamics of arbuscule development and degeneration in onion, bean, and tomato with reference to vesicular-arbuscular mycorrhizas in grasses. Can. J. Bot. 67, 2505-2513.

    Google Scholar 

  • Balestrini R, José-Estanyol M, Puigdomenech P and Bonfante P 1997 Hydroxyproline-rich glycoprotein mRNA accumulation in maize root cells colonized by an arbuscular mycorrhizal fungus as revealed by in situ hybridisation. Protoplasma 198, 36-42.

    Google Scholar 

  • Benabdellah K 1999 Alteraciones bioquímicas inducidas en membranas de células radicales de tomate (Lycopersicon esculentum Mill.) por la formación de micorrizas arbusculares. PhD Thesis. University of Granada, Spain.

    Google Scholar 

  • Benabdellah K, Azcón-Aguilar C and 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, 747-754.

    Google Scholar 

  • Blee KA and Anderson AJ 1998 Regulation of arbuscule formation by carbon in the plant. Plant J. 16, 523-530.

    Google Scholar 

  • Bonfante P 2001 At the interface between mycorrhizal fungi and plants: the structural organization of cell wall, plasma membrane and cytoskeleton. In The Mycota: Fungal Associations. Ed. B. Hock. pp. 45-61. Springer, Berlin.

    Google Scholar 

  • Bonfante P and Perotto S 1995 Strategies of arbuscular mycorrhizal fungi when infecting host plants. New Phytol. 130, 3-21.

    Google Scholar 

  • Bonfante-Fasolo P, Faccio A, Perotto S and Schubert A 1990 Correlation between chitin distribution and cell wall morphology in the mycorrhizal fungus Glomus versiforme. Mycol. Res. 94, 157-165.

    Google Scholar 

  • Clarkson DT 1985 Factors affecting mineral nutrient acquisition by plants. Annu. Rev. Plant Physiol. 36, 77-115.

    Google Scholar 

  • Cox G and Tinker PB 1976 Translocation and transfer of nutrients in vesicular-arbuscular mycorrhizas. New Phytol. 77, 371-378.

    Google Scholar 

  • Cox G, Moran KJ, Sanders F, Nockolds C and Tinker PB 1980 Translocation and transfer of nutrients in vesicular-arbuscular mycorrhizas. 3. Polyphosphate granules and phosphorus translocation. New Phytol. 84, 649-659.

    Google Scholar 

  • De Witt ND, Harper JF and Sussman MR 1991 Evidence for a plasma membrane proton pump in phloem cells of higher plants. Plant J. 1, 121-128.

    Google Scholar 

  • Dexheimer J, Gérard J, Ayatti H and Ghanbaja J 1996 Etude de l'origine et de la répartition des granules vacuolaires dans les hyphes d'une endomycorhize à vésicules et arbuscules. Acta Bot. Gallica 143, 167-180.

    Google Scholar 

  • Dickson S and Kolesik P 1999 Visualisation of mycorrhizal fungal structures and quantification of their surface area and volume using laser scanning confocal microscopy. Mycorrhiza 9, 205-213.

    Google Scholar 

  • Douds DD Jr., Johnson CR and Koch KE 1988 Carbon cost of the fungal symbiont relative to net leaf P accumulation in a split-root VA mycorrhizal symbiosis. Plant Physiol. 86, 491-496.

    Google Scholar 

  • Douds DD Jr, Pfeffer PE and Shachar-Hill Y 2000 Carbon partitioning, cost, and metabolism of arbuscular mycorrhizas. In Arbuscular Mycorrhizas: Physiology and Function. Eds. Y Kapulnik and DD Douds Jr. pp. 107-130. Kluwer Academic Publishers, Dordrecht.

    Google Scholar 

  • Ezawa T, Saito M and Yoshiada T 1995 Comparison of phosphatase localization in the intraradical hyphae of arbuscular mycorrhizal fungus, Glomus spp. and Gigaspora ssp. Plant Soil 176, 57-63.

    Google Scholar 

  • Ezawa T, Smith SE and Smith FA 2001 Differentiation of polyphosphate metabolism between the extra-and intraradical hyphae of arbuscular mycorrhizal fungi. New Phytol. 149, 555-563.

    Google Scholar 

  • Ferrol N, Barea JM and Azcón-Aguilar C 2000 The plasma membrane H+-ATPase gene family in the arbuscular mycorrhizal fungus Glomus mosseae. Curr. Genet. 37, 112-118.

    Google Scholar 

  • Ferrol N, Pozo MJ, Antelo M and Azcón-Aguilar C 2002 Arbuscular mycorrhizal simbiosis regulates plasma membrane H+-ATPase gene expression in tomato plants. J. Exp. Bot. (in press).

  • Gianinazzi-Pearson V, Smith SE, Gianinazzi S and 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, 61-79.

    Google Scholar 

  • Gianinazzi-Pearson V, Arnould C, Oufattole M, Arango M and Gianinazzi S 2000 Differential activation of H+-ATPase genes by an arbuscular mycorrhizal fungus in root cells of transgenic tobacco. Planta 211, 609-613.

    Google Scholar 

  • Gollotte A, Cordier C, Lemoine MC and Gianinazzi-Pearson V 1997 Role of fungal wall components in interactions between endomycorrhizal symbionts. In Eukaryotism and Symbiosis: Intertaxonomic Combination versus Symbiotic Adaptation. Eds. HEA Schenk, R Herrman, KW Jeon, NE Muller and Schwemmler. pp. 417-427. Springer, Belin, Heidelberg, New York.

    Google Scholar 

  • Graham JH 2000 Assessing costs of arbuscular mycorrhizal symbiosis in agroecosystems. In Current Advances in Mycorrhizae Research. Eds. GK Podila and DD Douds Jr. pp. 127-140. APS Press, St. Paul.

    Google Scholar 

  • Graham JH, Duncan LW and Eissenstat DM 1997 Carbohydrate allocation patterns in citrus genotypes as affected by phosphorus nutrition, mycorrhizal colonisation and mycorrhizal dependency. New Phytol. 135: 335-343.

    Google Scholar 

  • Harley JL and Smith SE 1983 Mycorrhizal Symbiosis. Academic Press, London.

    Google Scholar 

  • Harrison MJ 1996 A sugar transporter from Medicago truncatula: altered expression pattern in roots during vesicular-arbuscular (VA) mycorrhizal associations. Plant J. 9, 491-503.

    Google Scholar 

  • Harrison MJ and van Buuren ML 1995 A phosphate transporter from the mycorrhizal fungus Glomus versiforme. Nature 378, 625-629.

    Google Scholar 

  • Jabari-Hare SH, Therien J and Charest PM 1990 High resolution cytochemical study of the vesicular-arbuscular mycorrhizal association, Glomus clarum-Allium porrum. New Phytol. 114, 481-496.

    Google Scholar 

  • Jackobsen I 1999 Transport of phosphorus and carbon in arbuscular mycorrhizas. In Mycorrhiza: Structure, Function, Molecular Biology and Biotechnology. Eds. A Varma and B Hock. pp. 305-332. Springer, Berlin.

    Google Scholar 

  • Jennings DH 1995 The Physiology of Fungal Nutrition. Cambridge University Press, Cambridge.

    Google Scholar 

  • Kucey RMN and Paul EA 1982 Carbon flow, photosynthesis, and N2 fixation in mycorrhizal and nodulated faba beans (Vicia faba L.) Soil Biol. Biochem. 14, 407-412.

    Google Scholar 

  • Maldonado-Mendoza IE and Harrison MJ 1998 A xyloglucan endotransglycosylase (XET) gene from Medicago truncatula induced in arbuscular mycorrhizae. In Abstract 2nd Int. Conf. on Mycorrhiza, 5-10 July, 1998, Uppsala, Sweden.

  • Murphy J, Langridge P and 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, 291-301.

    Google Scholar 

  • Nehls U, Wiese J, Guttenberger M and Hampp R 1998 Carbon allocation in ectomycorrhizas: Identification and expression analysis of an Amanita muscaria monosaccharide transporter. Mol. Plant-Microb. Interact. 14, 334-338.

    Google Scholar 

  • Nemec S and Vu JCV 1990 Effects of soil phosphorus and Glomus intraradices on growth, non-structural carbohydrates, and photosynthetic activity of Cytrus aurantium. Plant Soil 128, 257-264.

    Google Scholar 

  • Palmgren MG and Harper JF 1999 Pumping with plant P-type ATPases. J. Exp. Bot. 50, 883-893.

    Google Scholar 

  • Pearson JN and Jakobsen I 1993 Symbiotic exchange of carbon and phosphorus between cucumber and three arbuscular mycorrhizal fungi. New Phytol. 124, 481-488.

    Google Scholar 

  • Perotto S, Brewin N and Bonfante P 1994 Colonization of pea roots by the mycorrhizal fungus Glomus versiforme and by Rhizobium bacteria: immunological comparison using monoclonal antibodies as probes for plant cell surface components. Mol. Plant-Microbe Interact. 7, 91-98.

    Google Scholar 

  • Rasmussen N, Lloyd DC, Ratcliffe G, Hansen PE and Jackobsen I 2000 31P NMR for the study of P metabolism and translocation in arbuscular mycorrhizal fungi. Plant Soil 226, 245-253.

    Google Scholar 

  • Rosewarne GM, Barker SJ, Smith SE, Smith FA and Schachtman DP 1999 A Lycopersicon esculentum phosphate transporter (LePT1) involved in phosphorus uptake from a vesiculararbuscular mycorrhizal fungus. New Phytol. 144, 507-516.

    Google Scholar 

  • Serrano R 1989 Structure and function of plasma membrane ATPase. Annu. Rev. Plant Physiol. Plant Mol. Biol. 40, 61-94.

    Google Scholar 

  • Shachar-Hill Y, Pfeffer PE, Douds D, Osman SF, Doner LW and Ratcliffe RG 1995 Partitioning of intermediate carbon metabolism in VAM colonized leek. Plant Physiol. 108, 7-15.

    Google Scholar 

  • Smith SE and Read DJ 1997 Mycorrhizal Symbiosis. Academic Press, London.

    Google Scholar 

  • Smith FA and Smith SE 1997 Structural diversity in (vesicular)-arbuscular mycorrhizal symbioses. New Phytol. 137, 373-388.

    Google Scholar 

  • Smith SE and Smith FA 1990 Structure and function of the interfaces in biotrophic symbioses as they relate to nutrient transport. New Phytol. 114, 1-38.

    Google Scholar 

  • Solaiman MD and Saito M 1997 Use of sugars by intraradical hyphae of arbuscular mycorrhizal fungi revealed by radiorespirometry. New Phytol. 136, 533-538.

    Google Scholar 

  • Tisserant B, Gianinazzi-Pearson V, Gianinazzi S and Gollotte A 1992 In planta histochemical staining of fungal alkaline phosphatase activity for analysis of efficient arbuscular mycorrhizal infections. Mycol. Res. 97, 245-250.

    Google Scholar 

  • van Buuren ML, Trieu AT, Blaylock LA and Harrison MJ 1999 Novel genes induced during an arbuscular mycorrhizal (AM) symbiosis formed between Medicago truncatula and Glomus versiforme. Mol. Plant-Microb. Interact. 12, 171-181.

    Google Scholar 

  • Wiese J, Kleber R, Hampp R, Nehls U 2000 Functional characterization of the Amanita muscaria monosaccharide transporter, AmMst1. Plant Biol. 2, 278-282.

    Google Scholar 

  • Villalba JM, Lützelschwab M and Serrano R 1991 Immunocytolocalization of plasma membrane H+-ATPase in maize coleoptiles and enclosed leaves. Planta 185, 485-461.

    Google Scholar 

  • Woolhouse HW 1975 Membrane structure and transport problems considered in relation to phosphorus and carbohydrate movements and regulation of endotrophic mycorrhizal association. In Endomycorrhizas. Eds. FE Sanders, B Mosse and PB Tinker. pp. 209-230. Academic Press, London.

    Google Scholar 

  • Wright DP, Read DJ and Scholes J 1998 Mycorrhizal sink strength influences whole plant carbon balance of Trifolium repens L. Plant Cell Environ. 21, 881-891.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Departamento de Microbiología del Suelo y Sistemas Simbióticos, Estación Experimental del Zaidín, Consejo Superior de Investigaciones Científicas, Profesor Albareda 1, 18008, Granada, Spain

    N. Ferrol, J.M. Barea & C. Azcón-Aguilar

Authors
  1. N. Ferrol
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. J.M. Barea
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. C. Azcón-Aguilar
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to N. Ferrol.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ferrol, N., Barea, J. & Azcón-Aguilar, C. Mechanisms of nutrient transport across interfaces in arbuscular mycorrhizas. Plant and Soil 244, 231–237 (2002). https://doi.org/10.1023/A:1020266518377

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1020266518377

Search

Navigation