Abstract
The function of arbuscular mycorrhizae (AM) is discussed in terms of reciprocal nutrient exchange within single pairs of symbionts. Emphasis is on carbon and phosphate nutrition and on the importance of diversity of the organisms involved. Growth of the obligate biotrophic AM fungi in roots relies on carbon transferred across interfaces between the plant and the fungus. Carbon use by the fungus is discussed in qualitative and quantitative terms. Attention is paid to the plant species-dependent variability in the formation and probably also function of root internal fungal structures where the Paris type of AM may be most important in the ecological perspective. Different fungi vary greatly in the amount of phosphorus transported to the plant. Plant identity is an important determinant of the amount of phosphate transferred from a fungus. Changes in time and space in expression of fungal and plant P transporter genes are discussed with the aim of providing a better understanding of the co-ordination of mechanisms leading to a net transfer of P from fungus to plant in the symbiosis. Future studies with single pairs of symbionts should focus on those fungi which are dominant root colonisers in the field. Careful isolation and controlled experiments with these fungi will contribute to resolving frequent discrepancies between studies in pots and in the field.
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References
Abbott LK, Robson AD, Jasper D, Gazey C (1992) What is the role of VA mycorrhizal hyphae in soil? In: Read DJ, Lewis DH, Fitter AH, Alexander IJ (eds) Mycorrhizas in ecosystems. CAB International, Wallington, pp 37–41
Allen MF (1983) Formation of vesicular-arbuscular mycorrhizae in A triplex gardneri (Chenopodiaceae): seasonal response in a cold desert. Mycologia 75: 773–776
Allsopp N (1998) Effect of defoliation on the arbuscular mycorrhizas of three perennial pasture and rangeland grasses. Plant Soil 202: 117–124
Bago B, Pfeffer PE, Shachar-Hill Y (2000) Carbon metabolism and transport in arbuscular mycorrhizas. Plant Physiol 124: 949–957
Baon JB, Smith SE, Alston AM, Wheeler RD (1992) Phosphorus efficiency of three cereals as related to indigenous mycorrhizal infection. Aust J Agric Res 43: 479–491
Barber SA (1984) Soil Nutrient Bioavailability - a mechanistic approach. Wiley-Interscience, New York
Bergelson JM, Crawley MJ (1988) Mycorrhizal infection and plant species diversity. Nature 334: 202
Blal B, Morel C, Gianinazzi-Pearson V, Fardeau JC, Gianinazzi S (1990) Influence of vesicular-arbuscular mycorrhizae on phosphate fertilizer efficiency in two tropical acid soils planted with micropropagated oil palm (Elaeis guineensis jacq.). Biol Fert Soils 9: 43–48
Blee KA, Anderson AJ (1998) Regulation of arbuscule formation by carbon in the plant. Plant J 16: 523–530
Bürkert B, Robson A (1994) 65Zn uptake in subterranean clover (Trifolium subterraneum L) by 3 vesicular-arbuscular mycorrhizal fungi in a root-free sandy soil. Soil Biol Biochem 26: 1117–1124
Clarkson DT (1985) Factors affecting mineral nutrient acquisition by plants. Annu Rev Plant Physiol 36: 77–115
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: 205–213
Facelli E, Facelli J, McLaughlin MJ, Smith SE (1999) Interactive effects of arbuscular mycorrhizal symbiosis, intraspecific competition and resource availability using Trifolium subterraneum L. cv. Mt Barker. New Phytol 141: 535–547
Function and Diversity of Arbuscular Mycorrhizae in Carbon and Mineral Nutrition 89
Fitter AH (1985) Functioning of vesicular-arbuscular mycorrhizas under field conditions. New Phytol 99: 257–265
Gallaud I (1905) Etudes sur les mycorrhizes endotrophs. Rev Gen Bot 17:5–48, 66–83, 123–135,223–239,313–325,425–433, 479–500
Gange AC, Ayres RL (1999) On the relation between arbuscular mycorrhizal colonisation and plant `benefit’. Oikos 87: 615–621
Gavito ME, Curtis PS, Mikkelsen TN, Jakobsen I (2000) Atmospheric CO2 and mycorrhiza effects on biomass allocation and nutrient uptake of nodulated pea (Pisum sativum) plants. J Exp Bot 51: 1931–1938
George E, Haussler KU, Vetterlein D, Gorgus E, Marschner H (1992) Water and nutrient translocation by hyphae of Glomus mosseae. Can J Bot 70: 2130–2137
Gianinazzi-Pearson V, Smith SE, Gianinazzi S, 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: 61–74
Graham JH, Abbott LK (2000) Wheat responses to aggressive and non-aggressive arbuscular mycorrhizal fungi. Plant Soil 220: 207–218
Graham JH, Leonard RT, Menge JA (1981) Membrane-mediated decrease in root exudation responsible for inhibition of vesicular-arbuscular mycorrhiza formation. Plant Physiol 68: 548–552
Grime JP, Mackey JML, Hillier SH, Read DJ (1987) Floristic diversity in a model system using experimental microcosms. Nature 328: 420–422
Harrison MJ (1999) Molecular and cellular aspects of the arbuscular mycorrhizal symbiosis. Annu Rev Plant Physiol Plant Mol Biol 50: 361–389
Harrison MJ, van Buuren ML (1995) A phosphate transporter from the mycorrhizal fungus Glomus versiforme. Nature 378: 626–632
Hartnett DC, Wilson GWT (1999) Mycorrhizae influence plant community structure and diversity in a tallgrass prairie. Ecology 80: 1187–1195
Hawkins H-J, Johansen A, George E (2000) Uptake, uptake mechanisms and transport of
organic and inorganic nitrogen by arbuscular mycorrhizal fungi. Plant Soil 226:275–285
Imhof S (1999) Root morphology, anatomy and mycotrophy of the achlorophyllous Voyria aphylla (Jaq.) Pers. (Gentianaceae). Mycorrhiza 9: 33–39
Jakobsen I (1999) Transport of phosphorus and carbon in arbuscular mycorrhizas. In: Varma A, Hock B (eds) Mycorrhiza: structure, function, molecular biology and biotechnology, 2nd edn. Springer, Berlin Heidelberg New York, pp 305–332
Jakobsen I, Rosendahl L (1990) Carbon flow into soil and external hyphae from roots of mycorrhizal cucumber plants. New Phytol 115: 77–83
Jakobsen I, Abbott LK, Robson AD (1992a) External hyphae of vesicular-arbuscular mycorrhizal fungi associated with Trifolium subterraneum. 1: Spread of hyphae and phosphorus inflow into roots. New Phytol 120: 371–380
Jakobsen I, Abbott LK, Robson AD (1992b) External hyphae of vesicular-arbuscular mycorrhizal fungi associated with Trifolium subterraneum. 2: Hyphal transport of 32P over defined distances. New Phytol 120: 509–516
Johansen A, Jakobsen I, Jensen ES (1992) Hyphal transport of 15N-labelled nitrogen by a vesicular-arbuscular mycorrhizal fungus and its effect on depletion of inorganic soil N. New Phytol 122: 281–288.
Johansen A, Jakobsen I, Jensen ES (1994) Hyphal N-transport by a vesicular-arbuscular mycorrhizal fungus associated with cucumber grown at three nitrogen levels. Plant Soil 160: 1–9
Johnson NC, Graham JH, Smith FA (1997) Functioning of mycorrhizal associations along the mutualism-parasitism continuum. New Phytol 135: 575–586
Joner E, Jakobsen I (1994) Contribution by two arbuscular mycorrhizal fungi to P uptake by cucumber (Cucumis sativus L.) from 32P-labelled organic matter during mineralization in soil. Plant Soil 163: 203–209
Joner E, Magid J, Gahoonia TS, Jakobsen I (1995) Phosphorus depletion and activity of phosphatases in the rhizosphere of mycorrhizal and non-mycorrhizal cucumber (Cucumis sativus L.). Soil Biol Biochem 27: 1145–1151
Joner EJ, Johansen A (2000) Phosphatase activity of external hyphae of two arbuscular mycorrhizal fungi. Mycol Res 104: 81–86
Joner EJ, Ravnskov S, Jakobsen I (2000) Arbuscular mycorrhizal phosphate transport under monoxenic conditions using radio-labelled inorganic and organic phosphate. Biotechnol Lett 22: 1705–1708
Koide RT (1991) Nutrient supply, nutrient demand and plant response to mycorrhiza 1 infection. New Phytol 117: 365–386
Koide RT, Goff MD, Dickie IA (2000) Component growth efficiencies of mycorrhizal and nonmycorrhizal plants. New Phytol 148: 163–168
Leake JR (1994) The biology of myco-heterotrophic (`saprophytic’) plants. Tansley review no 69. New Phytol 127: 171–216
Lewis DH (1973) Concepts in fungal nutrition and the origin of biotrophy. Biol Rev 48: 261–278
Li X-L, George E, Marschner H (1991) Phosphorus depletion and pH decrease at the root-soil and hyphae-soil interfaces of VA mycorrhizal white clover fertilised with ammonium. New Phytol 119: 397–404
Liu C, Muchhal US, Uthappa M, Kononowicz AK, Ragothama KG (1998) Tomato phosphate transporter genes are differentially regulated in plant tissues by phosphorus. Plant Physiol 116: 91–99
Liu H, Trieu AT, Blaylock LA, Harrison MJ (1998) Cloning and characterisation of two phosphate transporters from Medicago truncatula roots: regulation in response to phosphate and response to colonisation by arbuscular mycorrhizal ( AM) fungi. Mol Plant Microbe Interact 11: 14–22
Marschner H (1995) Mineral nutrition of higher plants. Academic Press, London Merryweather J, Fitter A (1996) Phosphorus nutrition of an obligately mycorrhizal plant
treated with the fungicide benomyl in the field. New Phytol 132:307–311
Mullen RB, Schmidt SK (1993) Mycorrhizal infection, phosphorus uptake and phenology in Ranunculus adoneus: implications for the functioning of mycorrhizas in alpine systems. Oecologia 94: 229–234
Newman EI (1988) Mycorrhizal links between plants: their functioning and ecological significance. Adv Ecol Res 18: 243–270
Oliver AJ, Smith SE, Nicholas DJD, Wallace W, Smith FA (1983) Activity of nitrate reductase in Trifolium subterraneum: effects of mycorrhizal infection and phosphate nutrition. New Phytol 94: 63–79
Olsson PA, Bââth E, Jakobsen I, Söderström B (1995) The use of phospholipid and neutral lipid fatty acids to estimate biomass of arbuscular mycorrhizal fungi in soil. Mycol Res 99: 623–629
Olsson PA, Thingstrup I, Jakobsen I, Bath E (1999) Estimation of the biomass of arbuscular mycorrhizal fungi in a linseed field. Soil Biol Biochem 31: 1879–1887
Pearson JN, Jakobsen I (1993a) Exchange of carbon and phosphorus in symbioses between cucumber and three VA mycorrhizal fungi. New Phytol 124: 481–488
Pearson JN, Jakobsen I (1993b) The relative contribution of hyphae and roots to phosphorus uptake by arbuscular mycorrhizal plants measured by dual labelling with 32P and 33P. New Phytol 124: 489–494
Ravnskov S, Jakobsen I (1995) Functional compatibility in arbuscular mycorrhizas measured as hyphal P transport to the plant. New Phytol 129: 611–618
Read DJ (2000) Links between genetic and functional diversity–a bridge too far? New Phytol 145: 363–365
Remy W, Taylor TN, Hass H, Kerp H (1994) Four hundred-million-year-old vesicular arbuscular mycorrhizas. Proc Natl Acad Sci USA 91: 11841–11843
Function and Diversity of Arbuscular Mycorrhizae in Carbon and Mineral Nutrition 91
Robinson D, Fitter AH (1999) The magnitude and control of carbon transfer between plants linked by a common mycorrhizal network. J Exp Bot 50: 9–13
Rosewarne GM, Barker SJ, Smith SE, Smith FA, Schachtman DP (1999) A Lycopersicon esculentum phosphate transporter (LePTJ) involved in phosphorus uptake from a vesicular-arbuscular mycorrhizal fungus. New Phytol 144: 507–516
Sanders IR, Streitwolf-Engel R, Heijden MGA van der, Boller T, Wiemken A (1998) Increased allocation to external hyphae of arbuscular mycorrhizal fungi under CO, enrichment. Oecologia 117: 496–503
Schachtman DP, Reid RJ, Ayling SM (1998) Phosphorus uptake by plants: from soil to cell. Plant Physiol 116: 447–453
Schweiger PF, Jakobsen I (1999) The role of mycorrhizas in plant P nutrition: fungal uptake kinetics and genotype variation. In: Gissel-Nielsen G, Jensen A (eds) Plant nutrition–molecular biology and genetics. Kluwer, Dordrecht, pp 277–289
Sieverding E, Toro S, Mosquera O (1989) Biomass production and nutrient concentrations in spores of VA mycorrhizal fungi. Soil Biol Biochem 21: 60–72
Smith DC, Muscatine L, Lewis DH (1969) Carbohydrate movement from autotrophs to heterotrophs in parasitic and mutualistic symbioses. Biol Rev 44: 17–90
Smith FA (2000) Measuring the influence of mycorrhizas. New Phytol 148: 4–6
Smith FA, Smith SE (1996) Mutualism and parasitism: diversity in function and structure in the “arbuscular” ( VA) mycorrhizal symbiosis. Adv Bot Res 22: 1–43
Smith FA, Smith SE (1997) Structural diversity in (vesicular)-arbuscular mycorrhizal fungi. New Phytol 137: 373–388
Smith FA, Jakobsen I, Smith SE (2000a) Spatial differences in acquisition of soil phosphate between the arbuscular mycorrhizal fungi S utellospora calospora and Glomus caledonium in symbiosis with Medicago truncatula. New Phytol 147: 357–366
Smith FA, Timonen S, Smith SE (2000b) Mycorrhizas. In: Blom CWPM, Visser EJW (eds) Root ecology. Springer, Berlin Heidelberg New York
Smith SE, Read DJ (1997) Mycorrhizal symbiosis, 2nd edn. Academic Press, London
Smith SE, Rosewarne G, Ayling SM, Dickson S, Schachtman DP, Barker SJ, Reid RJ, Smith FA (1999) Phosphate transfer between vesicular-arbuscular mycorrhizal symbionts: insights from confocal microscopy, microphysiology and molecular studies. In: Lynch JP, Deikman J (eds) Phosphorus in plant biology: regulatory roles in molecular, cellular, organismic and ecosystem processes. American Society of Plant Physiologists, Rockville, pp 111–123
Soberon MJ, Marinez del Rio C (1985) Cheating and taking advantage in mutualistic symbioses. In: Boucher D (ed) The biology of mutualism. Croom Helm, London, pp 192–216
Son CL, Smith SE (1988) Mycorrhizal growth responses: interactions between photon irradiance and phosphorus nutrition. New Phytol 108: 305–314
Staddon PL, Graves JD, Fitter AH (1999) Effect of enhanced atmospheric CO2 on mycorrhizal colonisation and phosphorus inflow in 10 herbaceous species of contrasting growth strategies. Funct Ecol 13: 190–199
Stribley DP, Tinker PB, Rayner JH (1980) Relation of internal phosphorus concentration and plant weight in plants infected by vesicular-arbuscular mycorrhizas. New Phytol 86: 261–266
Thomson BD, Robson AD, Abbott LK (1986) Effects of phosphorus on the formation of mycorrhizas by Gigaspora calospora and Glomus fasciculatum in relation to root carbohydrates. New Phytol 103: 751–765
van der Heijden MGA, Klironomos JN, Ursic M, Moutoglis P, Streitwolf-Engel R, Boller T, Wiemken A, Sanders IR (1998) Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396: 69–72
Wardle DA (1999) Is `sampling effect’ a problem for experiments investigating biodiversity–ecosystem function relationships? Oikos 87: 403–407
Wright DP, Scholes JD, Read DJ (1998) Effects of VA mycorrhizal colonisation on photosynthesis and biomass production of Trifolium repens L. Plant Cell Environ 21: 209–216
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Jakobsen, I., Smith, S.E., Smith, F.A. (2003). Function and Diversity of Arbuscular Mycorrhizae in Carbon and Mineral Nutrition. In: van der Heijden, M.G.A., Sanders, I.R. (eds) Mycorrhizal Ecology. Ecological Studies, vol 157. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-540-38364-2_3
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DOI: https://doi.org/10.1007/978-3-540-38364-2_3
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