[en] Interactions between arbuscular mycorrhizal fungal (AMF) species cocolonizing the same host plant are still little understood in spite of major ecological significance of mycorrhizal symbiosis and widespread occurrence of these fungi in communities rather than alone. Furthermore, shifting the composition of AMF communities has demonstrated consequences for the provision of symbiotic benefits to the host as well as for the qualities of ecosystem services. Therefore, here we addressed the nature and strength of interactions between three different AMF species in all possible two-species combinations on a gradient of inoculation densities. Fungal communities were established in pots with Medicago truncatula plants, and their composition was assessed with taxon-specific real-time PCR markers. Nature of interactions between the fungi was varying from competition to facilitation and was influenced by both the identity and relative abundance of the coinoculated fungi. Plants coinoculated with Claroideoglomus and Rhizophagus grew bigger and contained more phosphorus than with any of these two fungi separately, although these fungi obviously competed for root colonization. On the other hand, plants coinoculated with Gigaspora and Rhizophagus, which facilitated each other's root colonization, grew smaller than with any of these fungi separately. Our results point to as yet little understood complexity of interactions in plant-associated symbiotic fungal communities, which, depending on their composition, can induce significant changes in plant host growth and/or phosphorus acquisition in either direction.
Thonar, Cécile ; Université de Liège - ULiège > Département GxABT > Plant Sciences ; Institute of Agricultural Sciences, ETH Zurich, Eschikon 33, 8315, Lindau, Switzerland, Research Institute for Organic Agriculture (FiBL), Ackerstrasse, 5070, Frick, Switzerland
Frossard, Emmanuel; Institute of Agricultural Sciences, ETH Zurich, 8315 Lindau, Switzerland
Smilauer, Petr; Faculty of Science, University of South Bohemia, 37005 České Budějovice, Czech Republic
Jansa, Jan; Institute of Agricultural Sciences, ETH Zurich, 8315 Lindau, Switzerland ; Institute of Microbiology, Academy of Sciences of the Czech Republic, 14220 Praha 4, Czech Republic
Language :
English
Title :
Competition and facilitation in synthetic communities of arbuscular mycorrhizal fungi.
Czech Science Foundation [CZ] CAS - Czech Academy of Sciences [CZ] ETH Zürich - Swiss Federal Institute of Technology in Zurich [CH]
Funding text :
Financial support by the ETH Zurich
(project no. TH 14/05-3) is gratefully acknowledged. JJ was further
supported by Fellowship J.E. Purkyn e, Czech Science Foundation
(P504121665), Ministry of Education, Youth and Sports
(LK11224) and the long-term development programme RVO
61388971. PS was supported by the project GAJU 04–142/2010/
P. Constructive criticism by Dirk Redecker and five anonymous
reviewers on earlier versions of this paper is highly appreciated
Alkan N, Gadkar V, Yarden O, Kapulnik Y, (2006) Analysis of quantitative interactions between two species of arbuscular mycorrhizal fungi, Glomus mosseae and G. intraradices, by real-time PCR. Applied and Environmental Microbiology, 72, 4192-4199.
Bennett AE, Bever JD, Bowers MD, (2009) Arbuscular mycorrhizal fungal species suppress inducible plant responses and alter defensive strategies following herbivory. Oecologia, 160, 771-779.
Boltz DF, Mellon MG, (1948) Spectrophotometric determination of phosphorus as molybdiphosphoric acid. Analytical Chemistry, 20, 749-751.
Brundrett MC, Piché Y, Peterson RL, (1984) A new method for observing the morphology of vesicular-arbuscular mycorrhizae. Canadian Journal of Botany, 62, 2128-2134.
Clark FE, (1965) The concept of competition in microbial ecology. In: Ecology of Soil-Borne Plant Pathogens (eds, Baker KF, Snyder WC,), pp. 339-347. University of California Press, Berkeley, CA.
Daft MJ, Hogarth BG, (1983) Competitive interactions amongst 4 species of Glomus on maize and onion. Transactions of the British Mycological Society, 80, 339-345.
David-Schwartz R, Gadkar V, Wininger S, et al,. (2003) Isolation of a premycorrhizal infection (pmi2) mutant of tomato, resistant to arbuscular mycorrhizal fungal colonization. Molecular Plant-Microbe Interactions, 16, 382-388.
Dumbrell AJ, Nelson M, Helgason T, Dytham C, Fitter AH, (2010) Idiosyncrasy and overdominance in the structure of natural communities of arbuscular mycorrhizal fungi: is there a role for stochastic processes? Journal of Ecology, 98, 419-428.
Facelli E, Smith SE, Smith FA, (2009) Mycorrhizal symbiosis-overview and new insights into roles of arbuscular mycorrhizas in agro- and natural ecosystems. Australasian Plant Pathology, 38, 338-344.
Feddermann N, Finlay R, Boller T, Elfstrand M, (2010) Functional diversity in arbuscular mycorrhiza-the role of gene expression, phosphorous nutrition and symbiotic efficiency. Fungal Ecology, 3, 1-8.
Fox J, (2008) Applied Regression Analysis and Generalized Linear Models, 2nd edn. Sage Publications, Los Angeles, California.
Frossard E, Sinaj S, (1997) The isotope exchange kinetic technique: a method to describe the availability of inorganic nutrients. Applications to K, P, S and Zn. Isotopes in Environmental and Health Studies, 33, 61-77.
Golubski AJ, (2002) Potential impacts of multiple partners on mycorrhizal community dynamics. Theoretical Population Biology, 62, 47-62.
Hart MM, Reader RJ, Klironomos JN, (2001) Life-history strategies of arbuscular mycorrhizal fungi in relation to their successional dynamics. Mycologia, 93, 1186-1194.
van der Heijden MGA, Klironomos JN, Ursic M, et al,. (1998) Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature, 396, 69-72.
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 Phytologist, 171, 159-170.
Hepper CM, Azcón-Aguilar C, Rosendahl S, Sen R, (1988) Competition between 3 species of Glomus used as spatially separated introduced and indigenous mycorrhizal inocula for leek (Allium porrum L). New Phytologist, 110, 207-215.
Herrera-Medina MJ, Tamayo MI, Vierheilig H, Ocampo JA, Garcia-Garrido JM, (2008) The jasmonic acid signalling pathway restricts the development of the arbuscular mycorrhizal association in tomato. Journal of Plant Growth Regulation, 27, 221-230.
Hoagland D, Arnon D, (1950) The Water-Culture Method for Growing Plants Without Soil. pp. 32. Circular 347, California Agricultural Experimental Station, Berkeley, California.
Holm S, (1979) A simple sequentially rejective multiple test procedure. Scandinavian Journal of Statistics, 6, 65-70.
Jakobsen I, Abbott LK, Robson AD, (1992) External hyphae of vesicular-arbuscular mycorrhizal fungi associated with Trifolium subterraneum L. 1. Spread of hyphae and phosphorus inflow into roots. New Phytologist, 120, 371-380.
Jansa J, Mozafar A, Anken T, et al,. (2002) Diversity and structure of AMF communities as affected by tillage in a temperate soil. Mycorrhiza, 12, 225-234.
Jansa J, Mozafar A, Frossard E, (2003a) Long-distance transport of P and Zn through the hyphae of an arbuscular mycorrhizal fungus in symbiosis with maize. Agronomie, 23, 481-488.
Jansa J, Mozafar A, Kuhn G, et al,. (2003b) Soil tillage affects the community structure of mycorrhizal fungi in maize roots. Ecological Applications, 13, 1164-1176.
Jansa J, Mozafar A, Frossard E, (2005) Phosphorus acquisition strategies within arbuscular mycorrhizal fungal community of a single field site. Plant and Soil, 276, 163-176.
Jansa J, Smith FA, Smith SE, (2008) Are there benefits of simultaneous root colonization by different arbuscular mycorrhizal fungi? New Phytologist, 177, 779-789.
Jansa J, Bukovská P, Gryndler M, (2013) Mycorrhizal hyphae as ecological niche for highly specialized hypersymbionts-or just soil free-riders? Frontiers in Plant Science, 4, 134.
Kiers ET, Duhamel M, Beesetty Y, et al,. (2011) Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science, 333, 880-882.
Klironomos JN, Hart MM, (2002) Colonization of roots by arbuscular mycorrhizal fungi using different sources of inoculum. Mycorrhiza, 12, 181-184.
Koide RT, (2000) Functional complementarity in the arbuscular mycorrhizal symbiosis. New Phytologist, 147, 233-235.
Krüger M, Krüger C, Walker C, Stockinger H, Schüβler A, (2012) Phylogenetic reference data for systematics and phylotaxonomy of arbuscular mycorrhizal fungi from phylum to species level. New Phytologist, 193, 970-984.
Lekberg Y, Koide RT, Rohr JR, Aldrich-Wolfe L, Morton JB, (2007) Role of niche restrictions and dispersal in the composition of arbuscular mycorrhizal fungal communities. Journal of Ecology, 95, 95-105.
Lendenmann M, Thonar C, Barnard R, et al,. (2011) Symbiont identity matters: carbon and phosphorus fluxes between Medicago truncatula and different arbuscular mycorrhizal fungi. Mycorrhiza, 21, 689-702.
Lerat S, Lapointe L, Gutjahr S, Piché Y, Vierheilig H, (2003) Carbon partitioning in a split-root system of arbuscular mycorrhizal plants is fungal and plant species dependent. New Phytologist, 157, 589-595.
Maherali H, Klironomos JN, (2007) Influence of phylogeny on fungal community assembly and ecosystem functioning. Science, 316, 1746-1748.
Maherali H, Klironomos JN, (2012) Phylogenetic and trait-based assembly of arbuscular mycorrhizal fungal communities. PLoS ONE, 7, e36695.
Massoumou M, van Tuinen D, Chatagnier O, et al,. (2007) Medicago truncatula gene responses specific to arbuscular mycorrhiza interactions with different species and genera of Glomeromycota. Mycorrhiza, 17, 223-234.
Mathimaran N, Ruh R, Vullioud P, Frossard E, Jansa J, (2005) Glomus intraradices dominates arbuscular mycorrhizal communities in a heavy textured agricultural soil. Mycorrhiza, 16, 61-66.
McGonigle TP, Miller MH, Evans DG, Fairchild GL, Swan JA, (1990) A new method which gives an objective-measure of colonization of roots by vesicular arbuscular mycorrhizal fungi. New Phytologist, 115, 495-501.
Mummey DL, Antunes PM, Rillig MC, (2009) Arbuscular mycorrhizal fungi pre-inoculant identity determines community composition in roots. Soil Biology and Biochemistry, 41, 1173-1179.
Munkemuller T, de Bello F, Meynard CN, et al,. (2012) From diversity indices to community assembly processes: a test with simulated data. Ecography, 35, 468-480.
Newsham K, Fitter AH, Watkinson AR, (1995) Arbuscular mycorrhiza protect an annual grass from root pathogenic fungi in the field. Journal of Ecology, 83, 991-1000.
Pearson JN, Abbott LK, Jasper DA, (1993) Mediation of competition between 2 colonizing VA mycorrhizal fungi by the host plant. New Phytologist, 123, 93-98.
Pearson JN, Abbott LK, Jasper DA, (1994) Phosphorus, soluble carbohydrates and the competition between 2 arbuscular mycorrhizal fungi colonizing subterranean clover. New Phytologist, 127, 101-106.
Phillips JM, Hayman DS, (1970) Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Transactions of the British Mycological Society, 55, 158-161.
Pinior A, Wyss U, Piché Y, Vierheilig H, (1999) Plants colonized by AM fungi regulate further root colonization by AM fungi through altered root exudation. Canadian Journal of Botany, 77, 891-897.
Pivato B, Mazurier S, Lemanceau P, et al,. (2007) Medicago species affect the community composition of arbuscular mycorrhizal fungi associated with roots. New Phytologist, 176, 197-210.
R Core Team (2013) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. Available from http://www.r-project.org.
Rosendahl S, Matzen HB, (2008) Genetic structure of arbuscular mycorrhizal populations in fallow and cultivated soils. New Phytologist, 179, 1154-1161.
Snaydon RW, (1991) Replacement or additive designs for competition studies. Journal of Applied Ecology, 28, 930-946.
Thonar C, Schnepf A, Frossard E, Roose T, Jansa J, (2011) Traits related to differences in function among three arbuscular mycorrhizal fungi. Plant and Soil, 339, 231-245.
Thonar C, Erb A, Jansa J, (2012) Real-time PCR to quantify composition of arbuscular mycorrhizal fungal communities-marker design, verification, calibration and field validation. Molecular Ecology Resources, 12, 219-232.
van Tuinen D, Jacquot E, Zhao B, Gollotte A, Gianinazzi-Pearson V, (1998) Characterization of root colonization profiles by a microcosm community of arbuscular mycorrhizal fungi using 25S rDNA-targeted nested PCR. Molecular Ecology, 7, 879-887.
Verbruggen E, El Mouden C, Jansa J, et al,. (2012) Spatial structure and interspecific cooperation: theory and an empirical test using the mycorrhizal mutualism. American Naturalist, 179, E133-E146.
Vierheilig H, (2004a) Further root colonization by arbuscular mycorrhizal fungi in already mycorrhizal plants is suppressed after a critical level of root colonization. Journal of Plant Physiology, 161, 339-341.
Vierheilig H, (2004b) Regulatory mechanisms during the plant-arbuscular mycorrhizal fungus interaction. Canadian Journal of Botany, 82, 1166-1176.
Wagg C, Jansa J, Schmid B, van der Heijden MGA, (2011a) Belowground biodiversity effects of plant symbionts support aboveground productivity. Ecology Letters, 14, 1001-1009.
Wagg C, Jansa J, Stadler M, Schmid B, van der Heijden MGA, (2011b) Mycorrhizal fungal identity and diversity relaxes plant-plant competition. Ecology, 92, 1303-1313.
Weigelt A, Jolliffe P, (2003) Indices of plant competition. Journal of Ecology, 91, 707-720.
Wilson JM, (1984) Competition for infection between vesicular arbuscular mycorrhizal fungi. New Phytologist, 97, 427-435.
Wilson JM, Trinick MJ, (1983) Infection development and interactions between vesicular-arbuscular mycorrhizal fungi. New Phytologist, 93, 543-553.
