[en] Many studies have scrutinized the nutritional benefits of arbuscular mycorrhizal associations to their host plants, while the carbon (C) balance of the symbiosis has often been neglected. Here, we present quantification of both the C costs and the phosphorus (P) uptake benefits of mycorrhizal association between barrel medic (Medicago truncatula) and three arbuscular mycorrhizal fungal species, namely Glomus intraradices, Glomus claroideum, and Gigaspora margarita. Plant growth, P uptake and C allocation were assessed 7 weeks after sowing by comparing inoculated plants with their non-mycorrhizal counterparts, supplemented with different amounts of P. Isotope tracing ³³P and ¹³C) was used to quantify both the mycorrhizal benefits and the costs, respectively. G. intraradices supported greatest plant P acquisition and incurred high C costs, which lead to similar plant growth benefits as inoculation with G. claroideum, which was less efficient in supporting plant P acquisition, but also required less C. G. margarita imposed large C requirement on the host plant and provided negligible P uptake benefits. However, it did not significantly reduce plant growth due to sink strength stimulation of plant photosynthesis. A simple experimental system such as the one established here should allow quantification of mycorrhizal costs and benefits routinely on a large number of experimental units. This is necessary for rapid progress in assessment of C fluxes between the plants and different mycorrhizal fungi or fungal communities, and for understanding the dynamics between mutualism and parasitism in mycorrhizal symbioses.
Lendenmann, Mark; ETH Zurich, Institute of Agricultural Sciences, Plant Nutrition Group, Eschikon 33, 8315, Lindau, Switzerland
Thonar, Cécile ; Université de Liège - ULiège > Département GxABT > Plant Sciences ; ETH Zurich, Institute of Agricultural Sciences, Plant Nutrition Group, Eschikon 33, 8315, Lindau, Switzerland ; TSBF-CIAT, Tropical Soil Biology and Fertility Institute, c/o ICRAF, UN Avenue, Gigiri, PO Box 30677-00100, Nairobi, Kenya
Barnard, Romain L; ETH Zurich, Institute of Agricultural Sciences, Grassland Science Group, Universitätstrasse 2, 8092, Zürich, Switzerland ; Department of Environmental Science, Policy and Management, University of California, 137 Mulford Hall, Berkeley, CA, 94720, USA
Salmon, Yann; ETH Zurich, Institute of Agricultural Sciences, Grassland Science Group, Universitätstrasse 2, 8092, Zürich, Switzerland ; Institute of Evolutionary Biology and Environmental Studies, University of Zurich, Winterthurerstrasse 190, 8057, Zurich, Switzerland
Werner, Roland A; ETH Zurich, Institute of Agricultural Sciences, Grassland Science Group, Universitätstrasse 2, 8092, Zürich, Switzerland
Frossard, Emmanuel; ETH Zurich, Institute of Agricultural Sciences, Plant Nutrition Group, Eschikon 33, 8315, Lindau, Switzerland
Jansa, Jan; ETH Zurich, Institute of Agricultural Sciences, Plant Nutrition Group, Eschikon 33, 8315, Lindau, Switzerland. jan.jansa@ipw.agrl.ethz.ch
Language :
English
Title :
Symbiont identity matters: carbon and phosphorus fluxes between Medicago truncatula and different arbuscular mycorrhizal fungi.
Acknowledgments We are indebted to Nina Buchmann who enabled us to carry out the carbon isotope composition measurements in her group, and to Annika Lenz for her excellent support at the IRMS. We are very thankful for lab support by Thomas Flura, Ariane Keller, and Cornelia Bühlmann. Funding by the Research Commission of ETH Zurich (project 14/05-3) is gratefully acknowledged. We also thank two anonymous reviewers for constructive criticism, which resulted in improving clarity and quality of the manuscript, and to Angela Erb for the final language check.
Alef K (1995) Estimation of soil respiration. In: Alef K, Nannipieri P (eds) Methods in applied soil microbiology and biochemistry. Academic Press, London, pp 464-467.
Bever JD, Richardson SC, Lawrence BM, Holmes J, Watson M (2009) Preferential allocation to beneficial symbiont with spatial structure maintains mycorrhizal mutualism. Ecol Lett 12: 13-21.
Boddington CL, Dodd JC (1999) Evidence that differences in phosphate metabolism in mycorrhizas formed by species of Glomus and Gigaspora might be related to their life-cycle strategies. New Phytol 142: 531-538.
Brooks PD, Geilmann H, Werner RA, Brand WA (2003) Improved precision of coupled delta 13C and delta 15N measurements from single samples using an elemental analyser/isotope ratio mass spectrometer combination with a post-column 6-port valve and selective CO 2 trapping; improved halide robustness of the combustion reactor using CeO 2. Rapid Commun Mass Sp 17: 1924-1926.
Bryla DR, Eissenstat DM (2005) Respiratory costs of mycorrhizal associations. In: Lambers H, Ribas-Carbo M (eds) Plant respiration: from cell to ecosystem. Springer, Dordrecht, pp 207-224.
Cavagnaro TR, Smith FA, Ayling SM, Smith SE (2003) Growth and phosphorus nutrition of a Paris-type arbuscular mycorrhizal symbiosis. New Phytol 157: 127-134.
Gavito ME, Olsson PA (2003) Allocation of plant carbon to foraging and storage in arbuscular mycorrhizal fungi. FEMS Microbiol Ecol 45: 181-187.
Graham JH, Abbott LK (2000) Wheat responses to aggressive and non-aggressive arbuscular mycorrhizal fungi. Plant Soil 220: 207-218.
Graham JH, Eissenstat DM (1998) Field evidence for the carbon cost of citrus mycorrhizas. New Phytol 140: 103-110.
Grimoldi AA, Kavanová M, Lattanzi FA, Schaufele R, Schnyder H (2006) Arbuscular mycorrhizal colonization on carbon economy in perennial ryegrass: quantification by (CO 2)- 13C/(CO 2)- 12C steady-state labelling and gas exchange. New Phytol 172: 544-553.
Harris D, Porter LK, Paul EA (1997) Continuous flow isotope ratio mass spectrometry of carbon dioxide trapped as strontium carbonate. Comm Soil Sci Plant Anal 28: 747-757.
Heinemeyer A, Ineson P, Ostle N, Fitter AH (2006) Respiration of the external mycelium in the arbuscular mycorrhizal symbiosis shows strong dependence on recent photosynthates and acclimation to temperature. New Phytol 171: 159-170.
Hoagland D, Arnon D (1950) The water-culture method for growing plants without soil. California Agricultural Research Station, Berkeley.
Jabaji-Hare S (1988) Lipid and fatty acid profiles of some vesicular-arbuscular mycorrhizal fungi: contribution to taxonomy. Mycologia 80: 622-629.
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 L. 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 L. 2. Hyphal transport of 32P over defined distances. New Phytol 120: 509-516.
Jansa J, Gryndler M, Matucha M (1999) Comparison of the lipid profiles of arbuscular mycorrhizal (AM) fungi and soil saprophytic fungi. Symbiosis 26: 247-264.
Jansa J, Mozafar A, Anken T, Ruh R, Sanders IR, Frossard E (2002) Diversity and structure of AMF communities as affected by tillage in a temperate soil. Mycorrhiza 12: 225-234.
Jansa J, Mozafar A, Kuhn G, Anken T, Ruh R, Sanders IR, Frossard E (2003) Soil tillage affects the community structure of mycorrhizal fungi in maize roots. Ecol Appl 13: 1164-1176.
Jansa J, Mozafar A, Frossard E (2005) Phosphorus acquisition strategies within arbuscular mycorrhizal fungal community of a single field site. Plant Soil 276: 163-176.
Jansa J, Finlay R, Wallander H, Smith FA, Smith SE (2011) Role of mycorrhizal symbioses in phosphorus cycling. In: Bünemann E, Oberson A, Frossard E (eds) Phosphorus in action - biological processes in soil phosphorus cycling, Soil Biology series 26. Springer, Berlin, pp 137-168.
Johnson D, Leake JR, Read DJ (2002) Transfer of recent photosynthate into mycorrhizal mycelium of an upland grassland: short-term respiratory losses and accumulation of 14C. Soil Biol Biochem 34: 1521-1524.
Jones MD, Smith SE (2004) Exploring functional definitions of mycorrhizas: are mycorrhizas always mutualisms? Can J Bot 82: 1089-1109.
Kaschuk G, Kuyper TW, Leffelaar PA, Hungria M, Giller KE (2009) Are the rates of photosynthesis stimulated by the carbon sink strength of rhizobial and arbuscular mycorrhizal symbioses? Soil Biol Biochem 41: 1233-1244.
Kiers ET, Palmer TM, Ives AR, Bruno JF, Bronstein JL (2010) Mutualisms in a changing world: an evolutionary perspective. Ecol Lett 13: 1459-1474.
Koide R, Elliot G (1989) Cost benefit and efficiency of the vesicular-arbuscular mycorrhizal symbiosis. Funct Ecol 3: 4-7.
Li HY, Smith FA, Dickson S, Holloway RE, Smith SE (2008) Plant growth depressions in arbuscular mycorrhizal symbioses: not just caused by carbon drain? New Phytol 178: 852-862.
Liu JY, Versaw WK, Pumplin N, Gomez SK, Blaylock LA, Harrison MJ (2008) Closely related members of the Medicago truncatula PHT1 phosphate transporter gene family encode phosphate transporters with distinct biochemical activities. J Biol Chem 283: 24673-24681.
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 17: 223-234.
Merryweather J, Fitter A (1998) The arbuscular mycorrhizal fungi of Hyacinthoides non-scripta I. Diversity of fungal taxa. New Phytol 138: 117-129.
Munkvold L, Kjøller R, Vestberg M, Rosendahl S, Jakobsen I (2004) High functional diversity within species of arbuscular mycorrhizal fungi. New Phytol 164: 357-364.
Ohno T, Zibilske LM (1991) Determination of low concentrations of phosphorus in soil extracts using malachite green. Soil Sci Soc Am J 55: 892-895.
Olsson PA, Johnson NC (2005) Tracking carbon from the atmosphere to the rhizosphere. Ecol Lett 8: 1264-1270.
Olsson PA, van Aarle IM, Gavito ME, Bengtson P, Bengtsson G (2005) 13C incorporation into signature fatty acids as an assay for carbon allocation in arbuscular mycorrhiza. Appl Environ Microbiol 71: 2592-2599.
Parniske M (2008) Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat Rev Microbiol 6: 763-775.
Paul EA, Kucey RMN (1981) Carbon flow in plant microbial associations. Science 213: 473-474.
Pearson JN, Jakobsen I (1993) Symbiotic exchange of carbon and phosphorus between cucumber and three arbuscular mycorrhizal fungi. New Phytol 124: 481-488.
Ruehr NK, Offermann CA, Gessler A, Winkler JB, Ferrio JP, Buchmann N, Barnard RL (2009) Drought effects on allocation of recent carbon: from beech leaves to soil CO 2 efflux. New Phytol 184: 950-961.
Saito M (1995) Enzyme activities of the internal hyphae and germinated spores of an arbuscular mycorrhizal fungus, Gigaspora margarita Becker and Hall. New Phytol 129: 425-431.
Smith S, Read D (2008) Mycorrhizal symbiosis. Academic Press, New York.
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 SE, Smith FA, Jakobsen I (2004) Functional diversity in arbuscular mycorrhizal (AM) symbioses: the contribution of the mycorrhizal P uptake pathway is not correlated with mycorrhizal responses in growth or total P uptake. New Phytol 162: 511-524.
Smith FA, Grace EJ, Smith SE (2009) More than a carbon economy: nutrient trade and ecological sustainability in facultative arbuscular mycorrhizal symbioses. New Phytol 182: 347-358.
Thonar C, Schnepf A, Frossard E, Roose T, Jansa J (2011) Traits related to differences in function among three arbuscular mycorrhizal fungi. Plant Soil 339: 231-245.
Toljander JF, Artursson V, Paul LR, Jansson JK, Finlay RD (2006) Attachment of different soil bacteria to arbuscular mycorrhizal fungal extraradical hyphae is determined by hyphal vitality and fungal species. FEMS Microbiol Lett 254: 34-40.
Verbruggen E, Kiers ET (2010) Evolutionary ecology of mycorrhizal functional diversity in agricultural systems. Evol Appl 3: 547-560.
Werner RA, Brand WA (2001) Referencing strategies and techniques in stable isotope ratio analysis. Rapid Commun Mass Sp 15: 501-519.
Werner RA, Bruch BA, Brand WA (1999) ConFlo III - An interface for high precision delta 13C and delta 15N analysis with an extended dynamic range. Rapid Commun Mass Sp 13: 1237-1241.
Wright DP, Read DJ, Scholes JD (1998) Mycorrhizal sink strength influences whole plant carbon balance of Trifolium repens L. Plant Cell Environ 21: 881-891.
