Skip to main content
SpringerLink
Log in

Nutrient transport in mycorrhizas: structure, physiology and consequences for efficiency of the symbiosis

  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Nutrient transport in mycorrhizas occurs across specialized interfaces which are the result of corrdinated development of the organisms. The structural modifications give rise to large areas of either inter- or intra-cellular interface in which wall synthesis is frequently modified and in which altered distribution of membrane bound ATPases is important, particularly with respect to mechanisms that may be involved in bidirectional transfer of nutrients. Except in orchid mycorrhizas, net movement of organic carbon from plant to fungus occurs, complemented by mineral nutrient movement in the opposite direction. The general consensus is that sustained transfer at rates that will maintain the growth and development of the organisms requires increases in the rates at which nutrients are lost from the organisms; possible mechanisms for this are discussed. The transfer processes are essential in determining both plant and fungal productivity and an approach to calculating the efficiency of the symbiosis in terms of the expenditure of carbon (or of phosphorus) is discussed.

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

  • AlexanderT, MeierR, TothR and WeberH C, 1988 Dynamics of arbuscule development and degeneration in mycorrhizas of Triticum aestivum L. and Avena sativa L. with reference to Zea mays. New Phytol. 110, 363–370.

    Article  Google Scholar 

  • AllenE B and AllenM F 1984 Competition between plants of different successional stages: mycorrhizas as regulators. Can. J. Bot. 62, 2625–2629.

    Google Scholar 

  • AshfordA E and AllawayW G 1982 A sheathing mycorrhiza on Pisonia grandis R. BR. (Nyctaginaceae) with development of transfer cells rather than a Hartig net. New Phytol. 90, 511–517.

    Article  Google Scholar 

  • AshfordA E, PetersenC A, CarpenterJ L, CairneyJ W G and AllawayW G 1988 Structure and permeability of the fungal sheath in the Pisonia mycorrhiza. Protoplasma 147, 149–161.

    Article  Google Scholar 

  • AshfordA E, AllawayW G, PetersonC A and CairneyJ W G 1989 Nutrient transfer and the fungus-root interface. Aust. J. Plant Physiol. 16, 85–97.

    CAS  Google Scholar 

  • BaonJ B, SmithS E, AlstonA M and WheelerR D 1982 Phosphorus efficiency of three cereals as related to indigenous mycorrhizal infection. Aust. J. Agric. Res. 43, 479–491.

    Article  Google Scholar 

  • BeeverR E and BurnsD J W 1980 Phosphorus uptake, storage and utilization by fungi. Adv. Bot. Res. 8, 127–129.

    CAS  Google Scholar 

  • BevegeD I, BowenG D and SkinnerM F 1975 Comparative carbohydrate physiology of ecto- and endo-mycorrhizas. In Endomycorrhizas. Eds. F ESanders, BMosse and P BTinker. pp 149–174. Academic Press, London.

    Google Scholar 

  • Bonfante-FasoloP 1984 Anatomy and morphology. In VA Mycorrhizas. Eds. C LPowell and D JBagyaraj. pp 5–33. CRC Press, Boca Raton, FL.

    Google Scholar 

  • Bonfante-FasoloP and Gianinazzi-PearsonV 1982 Ultrastructural aspects of endomycorrhiza in the Ericaceae. III. Morphology of the dissociated symbionts and modifications occurring during their reassociation in axenic culture. New Phytol. 91, 691–704.

    Article  Google Scholar 

  • Bonfante-FasoloP and GrippioloR 1982 Ultrastructural and cytochemical changes in the wall of a vesicular-arbuscular mycorrhizal fungus during symbiosis. Can. J. Bot. 60, 2303–2312.

    Google Scholar 

  • Bonfante-FasoloP, VianB, PerottoS, FaccioA and KnoxJ P 1990 Cellulose and pectin localization in roots of mycorrhizal Allium porrum: labelling continuity between host cell wall and interfacial material. Planta 180, 537–547.

    Article  CAS  Google Scholar 

  • Bonfante-FasoloP, TamagnoneL, PerettoR, Esquerré-TugayéD, MazauD, MosiniakM and VianB 1991 Immunocytochemical location of hydroxyproline rich glycoproteins at the interface between a mycorrhizal fungus and its host plants. Protoplasma 165, 127–138.

    Article  CAS  Google Scholar 

  • CairneyJ W G and AlexanderI J 1992a A study of ageing of spruce (Picea sitchensis Bong. Carr.) ectomycorrhizas. II. Carbohydrate allocation in ageing Picea sitchensis/Tylospora fibrillosa (Burt.) Donk ectomycorrhizas. New Phytol. 122, 153–158.

    Article  CAS  Google Scholar 

  • CairneyJ W G and AlexanderI J 1992b A study of ageing of spruce (Picea sitchensis Bong. Carr.) ectomycorrhizas. III. Phosphate absorption and transfer in ageing Picea sitchensis/Tylospora fibrillosa (Burt.) Donk ectomycorrhizas. New Phytol. 122, 159–164.

    Article  CAS  Google Scholar 

  • CairneyJ W G and SmithS E 1992a Influence of intracellular phosphorus concentration on phosphate absorption by the ectomycorrhizal basidiomycete Pisolithus tinctorius. Mycol. Res. 96, 673–676.

    CAS  Google Scholar 

  • CairneyJ W G and SmithS E 1992b Effect of monovalent cations on efflux of phosphate from the ectomycorrhizal fungus Pisolithus tinctorius. In Mycorrhiza in Ecosystems. Eds. D JRead, D HLewis, A HFitter and I JAlexander. pp 352–355. CAB International, Oxon, UK.

    Google Scholar 

  • Cairney, J.W.G. and Smith, S.E. 1993 Efflux of phosphate from the ectomycorrhizal basidiomycete Pisolithus tinctorius: general characteristics and the influence of intracellular phosphorus concentration. Mycol. Res. (in press).

  • CairneyJ W G, AshfordA E and AllawayW G 1989 Distribution of photosynthetically fixed carbon within root systems of Eucalyptus pilularis ectomycorrhizal with Pisolithus tinctorius. New Phytol. 112, 495–500.

    Article  Google Scholar 

  • CampbellB D, GrimeJ P and MackeyJ M L 1991 A trade-off between scale and precision in resource foraging. Oecologia 87, 532–538.

    Article  Google Scholar 

  • ClarksonD T 1985 Factors affecting mineral acquisition by plants. Ann. Rev. Plant Physiol. 36, 77–115.

    CAS  Google Scholar 

  • ClarksonD T and ScattergoodC B 1982 Growth and phosphate transport in barley and tomato plants during the development of, and recovery from, phosphate stress. J. Exp. Bot. 33, 865–875.

    CAS  Google Scholar 

  • ClipsonN J W, CairneyJ W G and JenningsD H 1987 The physiology of basidiomycete linear organs. I. Phosphate uptake by cords and mycelium in the laboratory and in the field. New Phytol. 105, 449–457.

    Article  CAS  Google Scholar 

  • CosgroveD J and HedrichR 1991 Stretch-activated chloride, potassium, and calcium channels coexisting in plasmamembranes of guard cells of Vicia faba L. Planta 186, 143–153.

    Article  PubMed  CAS  Google Scholar 

  • CoxG and TinkerP B 1976 Translocation and transfer of nutrients in vesicular-arbuscular mycorrhizas. I. The arbuscule and phosphorus transfer: a quantitative ultrastructural study. New Phytol. 77, 371–378.

    Article  CAS  Google Scholar 

  • DexheimerJ, GianinazziS and Gianinazzi-PearsonV 1979 Ultrastructural cytochemistry of the host-fungus interfaces in the endomycorrhizal association Glomus mosseae/Allium cepa. Z. Pflanzenphysiol. 92, 191–206.

    Google Scholar 

  • DexheimerJ, Aubert-DufresneM-P, GérardJ, LeTaconF and MousainD 1986 Etude de la localisation ultrastructurale des activités phosphatasiques acides dans deux types d'ectomycorrhizes. Bull. Soc. Bot. Fr. 133, 343–352.

    Google Scholar 

  • DownesG M, AlexanderI J and CairneyJ W G 1992 A study of ageing of spruce (Picea sitchensis Bong. Carr.) ectomycorrhizas. I. Morphological and cellular changes in mycorrhizas formed by Tylospora fibrillosa (Burt.) Donk and Paxillus involutus (Batsch.) Fr. New Phytol. 122, 141–152.

    Article  Google Scholar 

  • DuddridgeJ A 1986 Specificity and recognition in mycorrhizal associations. In Physiological and Genetical Aspects of Mycorrhizae. Eds. VGianinazzi-Pearson and SGianinazzi. pp 45–58 INRA, Paris.

    Google Scholar 

  • DuddrigeJ A and ReadD J 1984 Modification of the host fungus interface in mycorrhizas synthesized between Suillus bovinus (FR.) O. Kuntz and Pinus sylvestris L. New Phytol. 96, 583–588.

    Article  Google Scholar 

  • EissenstatD M and NewmanE I 1990 Seedling establishment near large plants: effects of vesicular-arbuscular mycorrhizas on the intensity of plant competition. Functional Ecol. 4, 95–99.

    Article  Google Scholar 

  • EvansD G and MillerM H 1988 Vesicular-arbuscular mycorrhizas and the soil-disturbance-induced reduction of nutrient absorption in maize. I. Causal relations. New Phytol. 110, 67–74.

    Article  Google Scholar 

  • FairchildG L and MillerM H 1988 Vesicular-arbuscular mycorrhizas and the soil-disturbance-induced reduction of nutrient absorption in maize. II. Development of the effect. New Phytol. 110, 75–84.

    Article  Google Scholar 

  • FinlayR D 1985 Interactions between soil micro-arthropods and endomycorrhizal associations of higher plants. In Ecological Interactions in Soil. Eds. A HFitter, DAtkinson, D JRead and MBUsher. pp 319–331. Blackwell Scientific Publications, Oxford.

    Google Scholar 

  • FitterA H 1985 Functioning of vesicular-arbuscular mycorrhizas under field conditions. New Phytol. 99, 257–265.

    Article  Google Scholar 

  • FitterA H 1977 Influence of mycorrhizal infection on competition for phosphorus and potassium by two grasses. New Phytol. 79, 119–125.

    Article  CAS  Google Scholar 

  • GangeA C, BrownV K and FarmerL M 1990 A test for mycorrhizal benefit in an early successional plant community. New Phytol. 115, 85–91.

    Article  Google Scholar 

  • Garcia RomeraI, Garcia GarridoJ M, Martinez-MolinaE and OcampoJ A 1991 Production of pectolytic enzymes in lettuce root colonized by Glomus mosseae. Soil Biol. Biochem. 23, 597–601.

    Article  CAS  Google Scholar 

  • Gianinazzi-PearsonV 1984 Host-fungus specificity, recognition and compatibility in mycorrhizae. In Genes Involved in Microbe Plant Interactions. Eds. ESDennis, BHohn, ThHohn, PKing, ISchell and DPSVerma. pp 225–253. Springer-Verlag, Vienna.

    Google Scholar 

  • Gianinazzi-PearsonV 1986 Cellular modifications during host-fungus interactions in endomycorrhizae. NATO-ASI, Series H, Vol. 1, 29–37.

    Google Scholar 

  • Gianinazzi-PearsonV, Bonfante-FasoloP and DexheimerJ 1986 Ultrastructural studies of surface interactions during adhesion and infection by ericoid endomycorrhizal fungi. NATO-ASI, Series H, Vol. 4, 273–282.

    Google Scholar 

  • Gianinazzi-PearsonV, GianinazziS and BrewinN J 1990 Immunocytochemical localization of antigenic sites in the perisymbiotic membrane of endomycorrhiza using monoclonal antibodies reacting against the peribacteroid membranes of nodules. Endocytobiology IV. pp 127–131. INRA, Paris.

    Google Scholar 

  • Gianinazzi-PearsonV, SmithSE, GianinazziS and SmithFA 1991 Enzymatic studies on the metabolism of vesicular-arbuscular mycorrhizas. V. Is H+-ATPase a component of ATP-hydrolysing enzyme activities in plant-fungus interface. New Phytol. 117, 61–76.

    Article  CAS  Google Scholar 

  • GrimeJ P, MackeyJ M L, HillierS H and ReadD J 1987 Floristic diversity in a model system using experimental microcosms. Nature 328, 420–422.

    Article  Google Scholar 

  • HadleyG 1975 Organization and fine structure of orchid mycorrhiza. In Endomycorrhizas. Eds. F ESanders, BMosse and P BTinker. pp 335–351. Academic Press, London.

    Google Scholar 

  • HaleK A and SandersF E 1982 Effects of benomyl on vesicular-arbuscular mycorrhizal infection of red clover (Trifolium pratense L.) and consequences for phosphorus inflow. J. Plant Nutr. 5, 1355–1367.

    CAS  Google Scholar 

  • HarleyJ L and SmithS E 1983 Mycorrhizal Symbiosis. Academic Press, London. 483 p.

    Google Scholar 

  • HarleyJ L and BrierleyJ K 1955 The uptake of phosphate by excised mycorrhizal roots of the beech. VII. Active transport of 32P from fungus to host during uptake of phosphate from solution. New Phytol. 54, 296–301.

    Article  CAS  Google Scholar 

  • HarleyJ L and LoughmanB C 1963 The uptake of phosphate by excised mycorrhizal roots of the beech. IX. The nature of the phosphate compounds passing into the host. New Phytol. 62, 350–359.

    Article  CAS  Google Scholar 

  • HedrichR and SchroederJ I 1989 The physiology of ion channels and electrogenic pumps in higher plants. Ann. Rev. Plant Physiol. and Plant Mol. Biol. 40, 539–569.

    Article  Google Scholar 

  • HeldtH H, ChonC J, MarondeD, HeroldA, StankovicZ S and WalkerD A 1977 Role of orthophosphate and other factors in the regulation of starch formation in leaves and isolated chloroplasts. Plant Physiol. 59, 1146–1155.

    PubMed  CAS  Google Scholar 

  • JasperD A, AbbottL K and RobsonA D 1989 Soil disturbance reduces the infectivity of external hyphae of vesicular-arbuscular mycorrhizal fungi. New Phytol. 112, 93–99.

    Article  Google Scholar 

  • JasperD A, AbbottL K and RobsonA D 1989 Hyphae of a vesicular-arbuscular mycorrhizal fungus maintain infectivity in dry soil, except when the soil is disturbed. New Phytol. 112, 101–107.

    Article  Google Scholar 

  • JeanmaireC, DexheimerJ, MarxC, GianinazziS and Gianinazzi-PearsonV 1985 Effect of vesicular-arbuscular mycorrhizal infection on the distribution of neutral phosphatase activities in root cortical cells. J. Plant Physiol. 119, 285–293.

    CAS  Google Scholar 

  • KeiferD W and LucasW J 1982 Potassium channels in Chara corallina. Control and interaction with the electrogenic H+ pump. Plant Physiol. 86, 841–847.

    Google Scholar 

  • KoideR T 1991 Nutrient supply, nutrient demand and plant response to mycorrhizal infection. New Phytol. 117, 365–386.

    Article  CAS  Google Scholar 

  • KoideR T and ElliottG 1989 Cost, benefit and efficiency of the vesicular-arbuscular mycorrhizal symbiosis. Funct. Ecol. 3, 252–255.

    Google Scholar 

  • KoideR T and MooneyH A 1987 Spatial variation in inoculum potential of vesicular-arbuscular mycorrhizal fungi caused by formation of gopher mounds. New Phytol. 107, 173–182.

    Article  Google Scholar 

  • LeeR B 1982 Selectivity and kinetics of ion uptake by barley plants following nutrient deficiency. Ann. Bot. 50, 429–449.

    CAS  Google Scholar 

  • LeiJ and DexheimerJ 1988 Ultrastructural localization of ATPase activity in the Pinus sylvestris/Laccaria laccata ectomycorrhizal association. New Phytol. 108, 329–334.

    Article  CAS  Google Scholar 

  • LeiJ, LapeyrieF, MalajczukN and DexheimerJ, 1990 Infectivity of pine and eucalypt isolates of Pisolithus tinctorius (Pers.) Coker and Couch on roots of Eucalyptus urophylla S. T. Blake in vitro. II. Ultrastructural and biochemical changes at the early stage of mycorrhiza formation. New Phytol. 116, 115–122.

    Article  CAS  Google Scholar 

  • MartinF, RamstedtM and SöderhällK 1987 Carbon and nitrogen metabolism in ectomycorrhizal fungi and ectomycorrhizas. Biochimie 69, 569–581.

    Article  PubMed  CAS  Google Scholar 

  • MarxC, DexheimerJ, Gianinazzi-PearsonV and GianinazziS 1982 Enzymatic studies on the metabolism of vesicular-arbuscular mycorrhizas. IV. Ultrastructural evidence (ATPase) for active transfer processes in the host-arbuscule interface. New Phytol. 90, 37–43.

    Article  CAS  Google Scholar 

  • McGonigleT P 1988 A numerical analysis of published field trials with vesicular-arbuscular mycorrhizal fungi. Functional Ecol. 2, 473–478.

    Article  Google Scholar 

  • McGonigleT P and FitterA H 1988 Ecological consequences of arthropod grazing on VA mycorrhizal fungi. Proc. R. Soc. Edinburgh 94B, 25–32.

    Google Scholar 

  • McGonigleT P and FitterA H 1990 Ecological specificity of vesicular-arbuscular mycorrhizal associations. Mycol. Res. 94, 120–122.

    Article  Google Scholar 

  • MooneyH A 1972 The carbon balance of plants. Annu. Rev. Ecol. Syst. 3, 315–346.

    Article  CAS  Google Scholar 

  • PatrickJ W 1989 Solute efflux from the host at plant-microorganism interfaces. Aust. J. Plant Physiol. 16, 53–67.

    CAS  Google Scholar 

  • PearsonV and ReadD J 1975 The physiology of the mycorrhizal endophyte of Calluna vulgaris L. Hull. Trans. Br. Mycol. Soc. 64, 1–7.

    Google Scholar 

  • PohlavenF 1989 The influence of cytokinin 2iPA on growth, ion transport and membrane fluidity in mycelia of the mycorrhizal fungus Suillus variegatus. Agric. Ecos. Environ. 28, 399–402.

    Article  Google Scholar 

  • RabatinS C and StinnerB R 1988 Indirect effects of interactions between VAM fungi and soil-inhabiting invertebrates on plant processes. Agric. Ecos. Environ. 24, 135–146.

    Article  Google Scholar 

  • ScanneriniS and Bonfante-FasoloP 1983 Comparative ultrastructural analysis of mycorrhizal associations. Can. J. Bot. 61, 917–943.

    Article  Google Scholar 

  • SchwabS M MengeJ A and TinkerP B 1991 Regulation of nutrient transfer between host and fungus in vesicular-arbuscular mycorrhizas. New Phytol. 117, 387–398.

    Article  CAS  Google Scholar 

  • Serrigny J 1982 Etudes cytologique, cytochimique, et cytoenzymologique d'une orchidée tropicale: Epidendrum sp. Diplôme d'Etude Approfondie, Université of Nancy. 32 p.

  • SlaymanC L 1965 Electrical properties of Neurospora crassa. Effects of external cations on the intracellular potential. J. Gen. Physiol. 49, 69–92.

    Article  PubMed  CAS  Google Scholar 

  • SmithD C, MuscatineL and LewisD 1969 Carbohydrate movement from autotrophs to heterotrophs in parasitic and mutualistic symbiosis. Biol. Rev. 44, 17–90.

    PubMed  CAS  Google Scholar 

  • SmithF A and SmithS E 1986 Movement across membranes: physiology and biochemistry. In Physiological and General Aspects of Mycorrhizae. Eds. VGianinazzi-Pearson and SGianinazzi. pp 75–84, INRA, Paris.

    Google Scholar 

  • SmithF A and SmithS E 1989. Membrane transport at the biotrophic interface: an overview. Aust. J. Plant Physiol. 16, 33–43.

    CAS  Google Scholar 

  • Smith S E 1974. Mycorrhizal fungi. CRC Critical Reviews in Microbiology, 275–313.

  • SmithS E and DicksonS 1991 Quantification of active vesicular-arbuscular mycorrhizal infection using image analysis and other techniques. Aust. J. Plant Physiol. 18, 637–648.

    Article  Google Scholar 

  • SmithS E and Gianinazzi-PearsonV 1988 Physiological interactions between symbionts in vesicular-arbuscular mycorrhizal plants. Ann. Rev. Plant Physiol. Mol. Biol. 39, 211–244.

    Article  Google Scholar 

  • SmithS E and SmithF A 1990 Structure and function of the interfaces in biotrophic symbioses as they relate to nutrient transport. New Phytol. 114, 1–38.

    Article  CAS  Google Scholar 

  • SmithS E, LongC M and SmithF A 1989 Infection of roots with a dimorphic hypodermis: possible effects on solute uptake. Agric. Ecosy. Environ. 29, 403–407.

    Article  Google Scholar 

  • SmithS E, RobsonA D and AbbottL K 1992 The involvement of mycorrhizas in the assessment of genetically dependent efficiency of nutrient uptake and use. Plant Soil 146, 169–179.

    Article  CAS  Google Scholar 

  • StrakerC J and MitchellD T 1987 Kinetic characterization of a dual phosphate uptake system in the endomycorrhizal fungus of Erica hispidula L. New Phytol. 106, 129–137.

    Article  CAS  Google Scholar 

  • StrulluD G, GrellierB, GarrecJ P, McCreadyc c and HarleyJ L 1986 Effects of monovalent and divalent cations on phosphate absorption by beech mycorrhizas. New Phytol. 103, 403–416.

    Article  CAS  Google Scholar 

  • TesterM 1990 Plant ion channels: whole-cell and single-channel studies. New Phytol. 114, 305–340.

    Article  Google Scholar 

  • TesterM A, SmithF A and SmithS E 1992 The role of ion channels in controlling solute exchange in mycorrhizal associations. In Mycorrhiza in Ecosystems. Eds. DJRead, DHLewis, AHFitter and IJAlexander. pp 348–351. CAB International, Oxon, UK.

    Google Scholar 

  • ThomsonB D, ClarksonD T and BrainP 1990 Kinetics of phosphorus uptake by the germ-tubes of the vesicular-arbuscular mycorrhizal fungus, Gigaspora margarita. New Phytol. 116, 647–653.

    Article  CAS  Google Scholar 

  • WoolhouseH W 1975 Membrane structure and transport problems considered in relation to phosphorus and carbohydrate movements and the regulation of endotrophic mycorrhizal associations. In Endomycorrhizas. Eds. F ESanders, BMosse and P BTinker. pp 209–239. Academic Press, London.

    Google Scholar 

  • WyseR E, ZamskiE and TomosA D 1986 Effect of turgor on kinetics of sucrose uptake. Plant Physiol. 81, 478–481.

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Soil Science, Waite Institute, The University of Adelaide, 5064, Adelaide, SA, Australia

    S. E. Smith & J. W. G. Cairney

  2. Station d'Amelioration des Plantes, INRA, BV 1540, 21034, Dijon, France

    V. Gianinazzi-Pearson

  3. Department of Biology, Pennsylvania State University, 16802, University Park, PA, USA

    R. Koide

Authors
  1. S. E. Smith
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. V. Gianinazzi-Pearson
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. R. Koide
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. J. W. G. Cairney
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Smith, S.E., Gianinazzi-Pearson, V., Koide, R. et al. Nutrient transport in mycorrhizas: structure, physiology and consequences for efficiency of the symbiosis. Plant Soil 159, 103–113 (1994). https://doi.org/10.1007/BF00000099

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00000099

Key words

Search

Navigation