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Mycorrhiza

, Volume 29, Issue 2, pp 127–139 | Cite as

Abiotic contexts consistently influence mycorrhiza functioning independently of the composition of synthetic arbuscular mycorrhizal fungal communities

  • Alena VoříškováEmail author
  • Jan Jansa
  • David Püschel
  • Miroslav Vosátka
  • Petr Šmilauer
  • Martina Janoušková
Original Article
  • 221 Downloads

Abstract

The relationship between mycorrhiza functioning and composition of arbuscular mycorrhizal (AM) fungal communities is an important but experimentally still rather little explored topic. The main aim of this study was thus to link magnitude of plant benefits from AM symbiosis in different abiotic contexts with quantitative changes in AM fungal community composition. A synthetic AM fungal community inoculated to the model host plant Medicago truncatula was exposed to four different abiotic contexts, namely drought, elevated phosphorus availability, and shading, as compared to standard cultivation conditions, for two cultivation cycles. Growth and phosphorus uptake of the host plants was evaluated along with the quantitative composition of the synthetic AM fungal community. Abiotic context consistently influenced mycorrhiza functioning in terms of plant benefits, and the effects were clearly linked to the P requirement of non-inoculated control plants. In contrast, the abiotic context only had a small and transient effect on the quantitative AM fungal community composition. Our findings suggest no relationship between the degree of mutualism in AM symbiosis and the relative abundances of AM fungal species in communities in our simplified model system. The observed progressive dominance of one AM fungal species indicates an important role of different growth rates of AM fungal species for the establishment of AM fungal communities in simplified systems such as agroecosystems.

Keywords

Pre-conditioning Mycorrhizal functioning Community qPCR Phosphorus Medicago truncatula 

Notes

Acknowledgements

The study was supported by the Czech Science Foundation (project GA15-05466S) and by long-term research development programs RVO 67985939 and RVO 61388971.

Author’s contribution

MJ, JJ, DP, and MV designed the study. AV and DP performed the research. AV and PŠ analyzed data. PŠ contributed new models. AV wrote the paper with a substantial contribution from MJ, JJ, DP, and MV.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

572_2018_878_MOESM1_ESM.pdf (31 kb)
ESM 1 (PDF 31 kb)
572_2018_878_MOESM2_ESM.pdf (235 kb)
ESM 2 (PDF 235 kb)

References

  1. 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. Appl Environ Microbiol 72:4192–4199.  https://doi.org/10.1128/AEM.02889-05 CrossRefGoogle Scholar
  2. Allen MF (2007) Mycorrhizal fungi: highways for water and nutrients in arid soils. Vadose Zo J 6:291.  https://doi.org/10.2136/vzj2006.0068 CrossRefGoogle Scholar
  3. Allen MF (2011) Linking water and nutrients through the vadose zone: a fungal interface between the soil and plant systems. J Arid Land 3:155–163.  https://doi.org/10.3724/SP.J.1227.2011.00155 CrossRefGoogle Scholar
  4. Augé RM (2001) Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza 11:3–42.  https://doi.org/10.1007/s005720100097 CrossRefGoogle Scholar
  5. Barrett G, Campbell CD, Hodge A (2014) The direct response of the external mycelium of arbuscular mycorrhizal fungi to temperature and the implications for nutrient transfer. Soil Biol Biochem 78:109–117.  https://doi.org/10.1016/j.soilbio.2014.07.025 CrossRefGoogle Scholar
  6. Boddington CL, Dodd JC (2000) The effect of agricultural practices on the development of indigenous arbuscular mycorrhizal fungi. II Studies in experimental microcosms. Plant Soil 218:145–157.  https://doi.org/10.1023/A:1014911318284 CrossRefGoogle Scholar
  7. Chagnon PC, Bradley RL, Maherali H, Klironomos JN (2013) A trait-based framework to understand life history of mycorrhizal fungi. Trends Plant Sci 18:484–491.  https://doi.org/10.1016/j.tplants.2013.05.001 CrossRefGoogle Scholar
  8. Cho K, Toler H, Lee J, Ownley B, Stutz JC, Moore JL, Augé RM (2006) Mycorrhizal symbiosis and response of sorghum plants to combined drought and salinity stresses. J Plant Physiol 163:517–528.  https://doi.org/10.1016/j.jplph.2005.05.003 CrossRefGoogle Scholar
  9. Doubková P, Suda J, Sudová R (2012) The symbiosis with arbuscular mycorrhizal fungi contributes to plant tolerance to serpentine edaphic stress. Soil Biol Biochem 44:56–64.  https://doi.org/10.1016/j.soilbio.2011.09.011 CrossRefGoogle Scholar
  10. 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? J Ecol 98:419–428.  https://doi.org/10.1111/j.1365-2745.2009.01622.x CrossRefGoogle Scholar
  11. Engelmoer DJP, Behm JE, Kiers ET (2014) Intense competition between arbuscular mycorrhizal mutualists in an in vitro root microbiome negatively affects total fungal abundance. Mol Ecol 23:1584–1593.  https://doi.org/10.1111/mec.12451 CrossRefGoogle Scholar
  12. Fitter AH, Gilligan CA, Hollingworth K, Kleczkowski A, Twyman RM, Pitchford JW (2005) Biodiversity and ecosystem function in soil. Funct Ecol 19:369–377.  https://doi.org/10.1111/j.1365-2435.2005.00969.x CrossRefGoogle Scholar
  13. Gehring CA, Mueller RC, Haskins KE, Rubiw TK, Whitham TG (2014) Convergence in mycorrhizal fungal communities due to drought, plant competition, parasitism, and susceptibility to herbivory: consequences for fungi and host plants. Front Microbiol 5:1–9.  https://doi.org/10.3389/fmicb.2014.00306 CrossRefGoogle Scholar
  14. Hart MM, Reader RJ (2002) Taxonomic basis for variation in the colonization strategy of arbuscular mycorrhizal fungi. New Phytol 153:335–344.  https://doi.org/10.1046/j.0028-646X.2001.00312.x CrossRefGoogle Scholar
  15. Jackman, S. (2017) pscl: classes and methods for R developed in the Political Science Computational Laboratory. United States Studies Centre, University of Sydney. Sydney, New South Wales, Australia. R package version 15.2. https://github.com/atahk/pscl/. Accessed 21 April 2017
  16. Janoušková M, Krak K, Wagg C, Štorchová H, Caklová P, Vosátka M (2013) Effects of inoculum additions in the presence of a preestablished arbuscular mycorrhizal fungal community. Appl Environ Microbiol 79:6507–6515.  https://doi.org/10.1128/AEM.02135-13 CrossRefGoogle Scholar
  17. Janoušková M, Krak K, Vosátka M, Püschel D, Štorchová H (2017) Inoculation effects on root-colonizing arbuscular mycorrhizal fungal communities spread beyond directly inoculated plants. PLoS One 12:e0181525.  https://doi.org/10.1371/journal.pone.0181525 CrossRefGoogle Scholar
  18. Jansa J, Smith FA, Smith SE (2008) Are there benefits of simultaneous root colonization by different arbuscular mycorrhizal fungi? New Phytol 177:779–789.  https://doi.org/10.1111/j.1469-8137.2007.02294.x CrossRefGoogle Scholar
  19. 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 Biol, vol 26. Springer, Heidelberg, pp 137–168.  https://doi.org/10.1007/978-3-642-15271-9_6 CrossRefGoogle Scholar
  20. Ji B, Bever JD (2016) Plant preferential allocation and fungal reward decline with soil phosphorus: implications for mycorrhizal mutualism. Ecosphere 7:1–11.  https://doi.org/10.1002/ecs2.1256 CrossRefGoogle Scholar
  21. Ji B, Gehring CA, Wilson GWT, Miller RM, Flores-Rentería L, Johnson NC (2013) Patterns of diversity and adaptation in Glomeromycota from three prairie grasslands. Mol Ecol 22:2573–2587.  https://doi.org/10.1111/mec.12268 CrossRefGoogle Scholar
  22. Johnson NC (1993) Can fertilization of soil select less mutualistic mycorrhizae? Ecol Appl 3:749–757.  https://doi.org/10.2307/1942106 CrossRefGoogle Scholar
  23. Johnson NC, Graham JH, Smith FA (1997) Functioning of mycorrhizas along the mutualism parasitism continuum. New Phytol 135:1–12.  https://doi.org/10.1046/j.1469-8137.1997.00729.x CrossRefGoogle Scholar
  24. Johnson D, Vandenkoornhuyse PJ, Leake JR, Gilbert L, Booth RE, Grime JP, Young JPW, Read DJ (2004) Plant communities affect arbuscular mycorrhizal fungal diversity and community composition in grassland microcosms. New Phytol 161:503–515.  https://doi.org/10.1046/j.1469-8137.2003.00938.x CrossRefGoogle Scholar
  25. Johnson NC, Wilson GWT, Wilson JA, Miller RM, Bowker MA (2015) Mycorrhizal phenotypes and the law of the minimum. New Phytol 205:1473–1484.  https://doi.org/10.1111/nph.13172 CrossRefGoogle Scholar
  26. 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.  https://doi.org/10.1016/j.soilbio.2009.03.005 CrossRefGoogle Scholar
  27. Kiers ET, van der Heijden MGA (2006) Mutualistic stability in the arbuscular mycorrhizal symbiosis: exploring hypotheses of evolutionary cooperation. Ecology 87:1627–1636.  https://doi.org/10.1002/ecm.1283 CrossRefGoogle Scholar
  28. Klironomos JN, Hart MM (2002) Colonization of roots by arbuscular mycorrhizal fungi using different sources of inoculum. Mycorrhiza 12:181–184.  https://doi.org/10.1007/s00572-002-0169-6 CrossRefGoogle Scholar
  29. Klironomos JN, Hart MM, Gurney JE, Moutoglis P (2001) Interspecific differences in the tolerance of arbuscular mycorrhizal fungi to freezing and drying. Can J Bot 79:1161–1166.  https://doi.org/10.1139/cjb-79-10-1161 Google Scholar
  30. Knegt B, Jansa J, Franken O, Engelmoer DJP, Werner GDA, Bücking H, Kiers ET (2016) Host plant quality mediates competition between arbuscular mycorrhizal fungi. Fungal Ecol 20:233–240.  https://doi.org/10.1016/j.funeco.2014.09.011 CrossRefGoogle Scholar
  31. Koerselman W, Meuleman AFM (1996) The vegetation N : P ratio : a new tool to detect the nature of nutrient limitation. J Appl Ecol 33:1441–1450.  https://doi.org/10.2307/2404783 CrossRefGoogle Scholar
  32. Konvalinková T, Jansa J (2016) Lights off for arbuscular mycorrhiza: on its symbiotic functioning under light deprivation. Front Plant Sci 7:1–11.  https://doi.org/10.3389/fpls.2016.00782 CrossRefGoogle Scholar
  33. Konvalinková T, Püschel D, Janoušková M, Gryndler M, Jansa J (2015) Duration and intensity of shade differentially affects mycorrhizal growth- and phosphorus uptake responses of Medicago truncatula. Front Plant Sci 6(65).  https://doi.org/10.3389/fpls.2015.00065
  34. Koske RE, Gemma JN (1989) A modified procedure for staining roots to detect VA mycorrhizas. Mycol Res 92:486–488.  https://doi.org/10.1016/S0953-7562(89)80195-9 CrossRefGoogle Scholar
  35. Krak K, Janoušková M, Caklová P, Vosátka M, Štorchová H (2012) Intraradical dynamics of two coexisting isolates of the arbuscular mycorrhizal fungus Glomus intraradices sensu lato as estimated by real-time PCR of mitochondrial DNA. Appl Environ Microbiol 78:3630–3637.  https://doi.org/10.1128/AEM.00035-12 CrossRefGoogle Scholar
  36. Lau JA, Lennon JT (2012) Rapid responses of soil microorganisms improve plant fitness in novel environments. Proc Natl Acad Sci 109:14058–14062.  https://doi.org/10.1073/pnas.1202319109 CrossRefGoogle Scholar
  37. McGonigle TP, Evans DG, Miller MH (1990) Effect of degree of soil disturbance on mycorrhizal colonization and phosphorus absorption by maize in growth chamber and field experiments. New Phytol 116:629–636CrossRefGoogle Scholar
  38. Millar NS, Bennett AE (2016) Stressed-out symbiotes: hypotheses for the influence of abiotic stress on arbuscular mycorrhizal fungi. Oecologia 182:625–641.  https://doi.org/10.1007/s00442-016-3673-7 CrossRefGoogle Scholar
  39. Mummey DL, Antunes PM, Rillig MC (2009) Arbuscular mycorrhizal fungi pre-inoculant identity determines community composition in roots. Soil Biol Biochem 41:1173–1179.  https://doi.org/10.1016/j.soilbio.2009.02.027 CrossRefGoogle Scholar
  40. Oehl F, Schneider D, Sieverding E, Burga CA (2011) Succession of arbuscular mycorrhizal communities in the foreland of the retreating Morteratsch glacier in the Central Alps. Pedobiologia (Jena) 54:321–331.  https://doi.org/10.1016/j.pedobi.2011.07.006 CrossRefGoogle Scholar
  41. Ohno T, Zibilske LM (1991) Determination of low concentrations of phosphorus insoil extracts using malachite green. Soil Sci Soc Am J 55:892–895.  https://doi.org/10.2136/sssaj1991.03615995005500030046x CrossRefGoogle Scholar
  42. Öpik M, Moora M, Zobel M, Saks U, Wheatley R, Wright F, Daniell T (2008) High diversity of arbuscular mycorrhizal fungi in a boreal herb-rich coniferous forest. New Phytol 179:867–876.  https://doi.org/10.1111/j.1469-8137.2008.02515.x CrossRefGoogle Scholar
  43. Powell JR, Parrent JL, Hart MM, Klironomos JH, Rillig MC, Maherali H (2009) Phylogenetic trait conservatism and the evolution of functional trade-offs in arbuscular mycorrhizal fungi. Proc R Soc B Biol Sci 276:4237–4245.  https://doi.org/10.1098/rspb.2009.1015 CrossRefGoogle Scholar
  44. Püschel D, Janoušková M, Hujslová M, Slavíková R, Gryndlerová H, Jansa J (2016) Plant-fungus competition for nitrogen erases mycorrhizal growth benefits of Andropogon gerardii under limited nitrogen supply. Ecol Evol 6:4332–4346.  https://doi.org/10.1002/ece3.2207 CrossRefGoogle Scholar
  45. Püschel D, Janoušková M, Voříšková A, Gryndlerová H, Vosátka M, Jansa J (2017) Arbuscular mycorrhiza stimulates biological nitrogen fixation in two Medicago spp. through improved phosphorus acquisition. Front Plant Sci 8(380).  https://doi.org/10.3389/fpls.2017.00390
  46. Řezáčová V, Zemková L, Beskid O, Püschel D, Konvalinková T, Hujslová M, Slavíková R, Jansa J (2018) Little cross-feeding of the mycorrhizal networks shared between C3-Panicum bisulcatum and C4-Panicum maximum under different temperature regimes. Front Plant Sci 9:1–16.  https://doi.org/10.3389/fpls.2018.00449 CrossRefGoogle Scholar
  47. Ruiz-Lozano JM (2003) Arbuscular mycorrhizal symbiosis and alleviation of osmotic stress. New perspectives for molecular studies. Mycorrhiza 13:309–317.  https://doi.org/10.1007/s00572-003-0237-6 CrossRefGoogle Scholar
  48. Rydlová J, Vosátka M (2003) Effect of Glomus intraradices isolated from Pb-contaminated soil on Pb uptake by Agrostis capillaris is changed by its cultivation in a metal-free substrate. Folia Geobot 38:155–165.  https://doi.org/10.1007/bf02803148 CrossRefGoogle Scholar
  49. Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic Press, LondonGoogle Scholar
  50. Symanczik S, Courty PE, Boller T, Wiemken A, Al-Yahya’ei MN (2015) Impact of water regimes on an experimental community of four desert arbuscular mycorrhizal fungal (AMF) species, as affected by the introduction of a non-native AMF species. Mycorrhiza 25:639–647.  https://doi.org/10.1007/s00572-015-0638-3 CrossRefGoogle Scholar
  51. Tedersoo L, Sánchez-Ramírez S, Kõljalg U, Bahram M, Döring M, Schigel D, May T, Ryberg M, Abarenkov K (2018) High-level classification of the fungi and a tool for evolutionary ecological analyses. Fungal Divers 90:135–159.  https://doi.org/10.1007/s13225-018-0401-0 CrossRefGoogle Scholar
  52. Thonar C, Frossard E, Smilauer P, Jansa J (2014) Competition and facilitation in synthetic communities of arbuscular mycorrhizal fungi. Mol Ecol 23:733–746.  https://doi.org/10.1111/mec.12625 CrossRefGoogle Scholar
  53. Verbruggen E, Kiers ET (2010) Evolutionary ecology of mycorrhizal functional diversity in agricultural systems. Evol Appl 3:547–560.  https://doi.org/10.1111/j.1752-4571.2010.00145.x CrossRefGoogle Scholar
  54. Voříšková A, Jansa J, Püschel D, Krüger M, Cajthaml T, Vosátka M, Janoušková M (2017) Real-time PCR quantification of arbuscular mycorrhizal fungi: does the use of nuclear or mitochondrial markers make a difference? Mycorrhiza 27:577–585.  https://doi.org/10.1007/s00572-017-0777-9 CrossRefGoogle Scholar
  55. Wang Y, Naumann U, Wright ST, Warton DI (2012) Mvabund—an R package for model-based analysis of multivariate abundance data. Methods Ecol Evol 3:471–474.  https://doi.org/10.1111/j.2041-210X.2012.00190.x CrossRefGoogle Scholar
  56. Zeileis A, Kleiber C, Jackman S, Wien W (2008) Regression models for count data in R. J Stat Softw 27:1–25.  https://doi.org/10.1093/jpepsy/jsn055 Google Scholar
  57. Zheng C, Ji B, Zhang J, Zhang F, Bever JD (2015) Shading decreases plant carbon preferential allocation towards the most beneficial mycorrhizal mutualist. New Phytol 205:361–368.  https://doi.org/10.1111/nph.13025 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Institute of BotanyThe Czech Academy of SciencesPrůhoniceCzech Republic
  2. 2.Department of Experimental Plant Biology, Faculty of ScienceCharles UniversityPragueCzech Republic
  3. 3.Institute of MicrobiologyThe Czech Academy of SciencesPragueCzech Republic
  4. 4.Department of Ecosystem Biology, Faculty of ScienceUniversity of South BohemiaČeské BudějoviceCzech Republic

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