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Nutrient limitation drives response of Calamagrostis epigejos to arbuscular mycorrhiza in primary succession

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Abstract

Little is known about the functioning of arbuscular mycorrhizal (AM) symbiosis over the course of primary succession, where soil, host plants, and AM fungal communities all undergo significant changes. Over the course of succession at the studied post-mining site, plant cover changes from an herbaceous community to the closed canopy of a deciduous forest. Calamagrostis epigejos (Poaceae) is a common denominator at all stages, and it dominates among AM host species. Its growth response to AM fungi was studied at four distinctive stages of natural succession: 12, 20, 30, and 50 years of age, each represented by three spatially separated sites. Soils obtained from all 12 studied sites were γ-sterilized and used in a greenhouse experiment in which C. epigejos plants were (1) inoculated with a respective community of native AM fungi, (2) inoculated with reference AM fungal isolates from laboratory collection, or (3) cultivated without AM fungi. AM fungi strongly boosted plant growth during the first two stages but not during the latter two, where the effect was neutral or even negative. While plant phosphorus (P) uptake was generally increased by AM fungi, no contribution of mycorrhizae to nitrogen (N) uptake was recorded. Based on N:P in plant biomass, we related the turn from a positive to a neutral/negative effect of AM fungi on plant growth, observed along the chronosequence, to a shift in relative P and N availability. No functional differences were found between native and reference inocula, yet root colonization by the native AM fungi decreased relative to the reference inoculum in the later succession stages, thereby indicating shifts in the composition of AM fungal communities reflected in different functional characteristics of their members.

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References

  • Al-Karaki GN, Clark RB (1999) Varied rates of mycorrhizal inoculum on growth and nutrient acquisition by barley grown with drought stress. J Plant Nutr 22:1775–1784

    Article  CAS  Google Scholar 

  • Atul-Nayyar A, Hamel C, Hanson K, Germida J (2009) The arbuscular mycorrhizal symbiosis links N mineralization to plant demand. Mycorrhiza 19:239–246

    Article  CAS  PubMed  Google Scholar 

  • Augé RM (2001) Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza 11:3–42

    Article  Google Scholar 

  • Azcón R, Ambrosano E, Charest C (2003) Nutrient acquisition in mycorrhizal lettuce plants under different phosphorus and nitrogen concentration. Plant Sci 165:1137–1145

    Article  Google Scholar 

  • Becklin KM, Pallo ML, Galen C (2012) Willows indirectly reduce arbuscular mycorrhizal fungal colonization in understorey communities. J Ecol 100:343–351

    Article  Google Scholar 

  • Brady NC, Weil R (2008) The nature and properties of soil. Prentice Hall, Upper Saddle River

    Google Scholar 

  • Cakan H, Karatas C (2006) Interactions between mycorrhizal colonization and plant life forms along the successional gradient of coastal sand dunes in the eastern Mediterranean. Turkey Ecol Res 21:301–310

    Article  Google Scholar 

  • Chagnon P-L, Bradley RL, Maherali H, Klironomos JN (2013) A trait-based framework to understand life history of mycorrhizal fungi. Trends Plant Sci 18:484–491

    Article  CAS  PubMed  Google Scholar 

  • Clapperton MJ, Reid DM (1992) A relationship between plant-growth and increasing VA mycorrhizal inoculum density. New Phytol 120:227–234

    Article  Google Scholar 

  • Corrêa A, Cruz C, Perez-Tienda J, Ferrol N (2014) Shedding light onto nutrient responses of arbuscular mycorrhizal plants: nutrient interactions may lead to unpredicted outcomes of the symbiosis. Plant Sci 221:29–41

    Article  PubMed  Google Scholar 

  • Corrêa A, Cruz C, Ferrol N (2015) Nitrogen and carbon/nitrogen dynamics in arbuscular mycorrhiza: the great unknown. Mycorrhiza 25:499–515

    Article  PubMed  Google Scholar 

  • da Silva DKA, de Souza RG, Velez BAD, da Silva GA, Oehl F, Maia LC (2015) Communities of arbuscular mycorrhizal fungi on a vegetation gradient in tropical coastal dunes. Appl Soil Ecol 96:7–17

    Article  Google Scholar 

  • Doubková P, Kohout P, Sudová R (2013) Soil nutritional status, not inoculum identity, primarily determines the effect of arbuscular mycorrhizal fungi on the growth of Knautia arvensis plants. Mycorrhiza 23:561–572

    Article  PubMed  Google Scholar 

  • Dugassa GD, von Alten H, Schonbeck F (1996) Effects of arbuscular mycorrhiza (AM) on health of Linum usitatissimum L. infected by fungal pathogens. Plant Soil 185:173–182

    Article  CAS  Google Scholar 

  • Frouz J, Nováková A (2005) Development of soil microbial properties in topsoil layer during spontaneous succession in heaps after brown coal mining in relation to humus microstructure development. Geoderma 129:54–64

    Article  Google Scholar 

  • Frouz J, Elhottová D, Kuráž V, Šourková M (2006) Effects of soil macrofauna on other soil biota and soil formation in reclaimed and unreclaimed post mining sites: results of a field microcosm experiment. Appl Soil Ecol 33:308–320

    Article  Google Scholar 

  • Frouz J et al (2008) Interactions between soil development, vegetation and soil fauna during spontaneous succession in post mining sites. Eur J Soil Biol 44:109–121

    Article  Google Scholar 

  • Fujiyoshi M, Kagawa A, Nakatsubo T, Masuzawa T (2006) Effects of arbuscular mycorrhizal fungi and soil developmental stages on herbaceous plants growing in the early stage of primary succession on Mount Fuji. Ecol Res 21:278–284

    Article  Google Scholar 

  • Gange AC, Ayres RL (1999) On the relation between arbuscular mycorrhizal colonization and plant ‛benefit’. Oikos 87:615–621

    Article  Google Scholar 

  • Gerdemann JW, Nicolson TH (1963) Spores of mycorrhizal Endogone species extracted from soil by wet sieving and decanting. Trans Br Mycol Soc 46:235–244

    Article  Google Scholar 

  • Giovannetti M, Mosse B (1980) Evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytol 84:489–500

    Article  Google Scholar 

  • Grimoldi AA, Kavanova M, Lattanzi FA, Schaufele R, Schnyder H (2006) Arbuscular mycorrhizal colonization on carbon economy in perennial ryegrass: quantification by (CO2)-C-13/(CO2)-C-12 steady-state labelling and gas exchange. New Phytol 172:544–553

    Article  CAS  PubMed  Google Scholar 

  • Harner MJ, Mummey DL, Stanford JA, Rillig MC (2010) Arbuscular mycorrhizal fungi enhance spotted knapweed growth across a riparian chronosequence. Biol Invasions 12:1481–1490

    Article  Google Scholar 

  • Harte J, Kinzig AP (1993) Mutualism and competition between plants and decomposers—implications for nutrient allocation in ecosystems. Am Nat 141:829–846

    Article  CAS  PubMed  Google Scholar 

  • Hawkins HJ, George E (1999) Effect of plant nitrogen status on the contribution of arbuscular mycorrhizal hyphae to plant nitrogen uptake. Physiol Plant 105:694–700

    Article  CAS  Google Scholar 

  • Hawkins HJ, George E (2001) Reduced N-15-nitrogen transport through arbuscular mycorrhizal hyphae to Triticum aestivum L. supplied with ammonium vs. nitrate nutrition. Ann Bot 87:303–311

    Article  CAS  Google Scholar 

  • Heinemeyer A, Ridgway KP, Edwards EJ, Benham DG, Young JPW, Fitter AH (2004) Impact of soil warming and shading on colonization and community structure of arbuscular mycorrhizal fungi in roots of a native grassland community. Glob Chang Biol 10:52–64

    Article  Google Scholar 

  • Hodge A, Fitter AH (2010) Substantial nitrogen acquisition by arbuscular mycorrhizal fungi from organic material has implications for N cycling. Proc Natl Acad Sci U S A 107:13754–13759

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hodge A, Helgason T, Fitter AH (2010) Nutritional ecology of arbuscular mycorrhizal fungi. Fungal Ecol 3:267–273

    Article  Google Scholar 

  • Hoeksema JD et al (2010) A meta-analysis of context-dependency in plant response to inoculation with mycorrhizal fungi. Ecol Lett 13:394–407

    Article  PubMed  Google Scholar 

  • Ibijbijen J, Urquiaga S, Ismaili M, Alves BJR, Boddey RM (1996) Effect of arbuscular mycorrhizal fungi on growth, mineral nutrition and nitrogen fixation of three varieties of common beans (Phaseolus vulgaris). New Phytol 134:353–360

    Article  CAS  Google Scholar 

  • Jakobsen I, Rosendahl L (1990) Carbon flow into soil and external hyphae from roots of mycorrhizal cucumber plants. New Phytol 115:77–83

    Article  Google Scholar 

  • Janos DP (2007) Plant responsiveness to mycorrhizas differs from dependence upon mycorrhizas. Mycorrhiza 17:75–91

    Article  PubMed  Google Scholar 

  • Johansen A (1999) Depletion of soil mineral N by roots of Cucumis sativus L. colonized or not by arbuscular mycorrhizal fungi. Plant Soil 209:119–127

    Article  CAS  Google Scholar 

  • Johnson NC (2010) Resource stoichiometry elucidates the structure and function of arbuscular mycorrhizas across scales. New Phytol 185:631–647

    Article  CAS  PubMed  Google Scholar 

  • Johnson NC, Graham JH, Smith FA (1997) Functioning of mycorrhizal associations along the mutualism-parasitism continuum. New Phytol 135:575–586

    Article  Google Scholar 

  • Johnson NC, Wilson GWT, Bowker MA, Wilson JA, Miller RM (2010) Resource limitation is a driver of local adaptation in mycorrhizal symbioses. Proc Natl Acad Sci U S A 107:2093–2098

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Johnson NC, Wilson GWT, Wilson JA, Miller RM, Bowker MA (2015) Mycorrhizal phenotypes and the law of the minimum. New Phytol 205:1473–1484

    Article  CAS  PubMed  Google Scholar 

  • Klironomos JN (2003) Variation in plant response to native and exotic arbuscular mycorrhizal fungi. Ecology 84:2292–2301

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Koide RT (1991) Nutrient supply, nutrient demand and plant-response to mycorrhizal infection. New Phytol 117:365–386

    Article  CAS  Google Scholar 

  • Kopáček J, Hejzlar J (1995) Semi-micro determination of total phosphorus in soils, sediments, and organic materials—a simplified perchloric-acid digestion procedure. Commun Soil Sci Plant Anal 26:1935–1946

    Article  Google Scholar 

  • Koske RE, Gemma JN (1989) A modified procedure for staining roots to detect VA mycorrhizas. Mycol Res 92:486–505

    Article  Google Scholar 

  • Koske RE, Gemma JN (1997) Mycorrhizae and succession in plantings of beachgrass in sand dunes. Am J Bot 84:118–130

    Article  Google Scholar 

  • Lavelle P et al (1997) Soil function in a changing world: the role of invertebrate ecosystem engineers. Eur J Soil Biol 33:159–193

    CAS  Google Scholar 

  • Lindahl BO, Taylor AFS, Finlay RD (2002) Defining nutritional constraints on carbon cycling in boreal forests—towards a less ‛phytocentric’ perspective. Plant Soil 242:123–135

    Article  CAS  Google Scholar 

  • Maherali H, Klironomos JN (2007) Influence of phylogeny on fungal community assembly and ecosystem functioning. Science 316:1746–1748

    Article  CAS  PubMed  Google Scholar 

  • Martinez-García LB, Richardson SJ, Tylianakis JM, Peltzer DA, Dickie IA (2015) Host identity is a dominant driver of mycorrhizal fungal community composition during ecosystem development. New Phytol 205:1565–1576

    Article  PubMed  Google Scholar 

  • Marulanda A, Azcon R, Ruiz-Lozano JM (2003) Contribution of six arbuscular mycorrhizal fungal isolates to water uptake by Lactuca sativa plants under drought stress. Physiol Plant 119:526–533

    Article  CAS  Google Scholar 

  • Oba H, Shinozaki N, Oyaizu H, Tawaraya K, Wagatsuma T, Barraquio WL, Saito M (2004) Arbuscular mycorrhizal fungal communities associated with some pioneer plants in the Lahar area of Mt Pinatubo, Philippines. Soil Sci Plant Nutr 50:1195–1203

    Article  Google Scholar 

  • 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 54:321–331

    Article  Google Scholar 

  • Pánková H, Münzbergová Z, Rydlová J, Vosátka M (2014) Co-adaptation of plants and communities of arbuscular mycorrhizal fungi to their soil conditions. Folia Geobotanica 49:521–540

    Article  Google Scholar 

  • Pezzani F, Montana C, Guevara R (2006) Associations between arbuscular mycorrhizal fungi and grasses in the successional context of a two-phase mosaic in the Chihuahuan Desert. Mycorrhiza 16:285–295

    Article  PubMed  Google Scholar 

  • Piotrowski JS, Morford SL, Rillig MC (2008) Inhibition of colonization by a native arbuscular mycorrhizal fungal community via Populus trichocarpa litter, litter extract, and soluble phenolic compounds. Soil Biol Biochem 40:709–717

    Article  CAS  Google Scholar 

  • 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. Ecology and Evolution. doi:10.1002/ece3.2207

  • Rondina ABL, Lescano LEAM, Alves RD, Matsuura EM, Nogueira MA, Zangaro W (2014) Arbuscular mycorrhizas increase survival, precocity and flowering of herbaceous and shrubby species of early stages of tropical succession in pot cultivation. J Trop Ecol 30:599–614

    Article  Google Scholar 

  • Rydlová J, Vosátka M (2001) Associations of dominant plant species with arbuscular mycorrhizal fungi during vegetation development on coal mine spoil banks. Folia Geobotanica 36:85–97

    Article  Google Scholar 

  • Sharma D, Kapoor R, Bhatnagar AK (2009) Differential growth response of Curculigo orchioides to native arbuscular mycorrhizal fungal (AMF) communities varying in number and fungal components. Eur J Soil Biol 45:328–333

    Article  Google Scholar 

  • Sikes BA, Maherali HZ, Klironomos JN (2012) Arbuscular mycorrhizal fungal communities change among three stages of primary sand dune succession but do not alter plant growth. Oikos 121:1791–1800

    Article  Google Scholar 

  • Sikes BA, Maherali H, Klironomos JN (2014) Mycorrhizal fungal growth responds to soil characteristics, but not host plant identity, during a primary lacustrine dune succession. Mycorrhiza 24:219–226

    Article  PubMed  Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis. Academic Press, Cambridge

    Google Scholar 

  • Sylvia DM, Neal LH (1990) Nitrogen affects the phosphorus response of Va Mycorrhiza. New Phytol 115:303–310

    Article  CAS  Google Scholar 

  • Trouvelot A, Kough JL, Gianinazzi-Pearson V (1986) Mesure du taux de mycorhization VA d’un systeme radiculaire. Recherche de methodes d’estimation ayant une signification fonctionnelle. In: Gianinazzi-Pearson V, Gianinazzi S (eds) Physiological and genetical aspects of mycorrhizae. INRA, Paris, pp 217–221

    Google Scholar 

  • Uibopuu A, Moora M, Opik M, Zobel M (2012) Temperate forest understorey species performance is altered by local arbuscular mycorrhizal fungal communities from stands of different successional stages. Plant Soil 356:331–339

    Article  CAS  Google Scholar 

  • Valentine AJ, Osborne BA, Mitchell DT (2001) Interactions between phosphorus supply and total nutrient availability on mycorrhizal colonization, growth and photosynthesis of cucumber. Sci Hortic 88:177–189

    Article  CAS  Google Scholar 

  • van der Heijden MGA, Scheublin TR (2007) Functional traits in mycorrhizal ecology: their use for predicting the impact of arbuscular mycorrhizal fungal communities on plant growth and ecosystem functioning. New Phytol 174:244–250

    Article  PubMed  Google Scholar 

  • Vindušková O, Sebag D, Cailleau G, Brus J, Frouz J (2015) Methodological comparison for quantitative analysis of fossil and recently derived carbon in mine soils with high content of aliphatic kerogen. Org Geochem 89–90:14–22

    Article  Google Scholar 

  • Wardle DA, Bardgett RD, Klironomos JN, Setala H, van der Putten WH, Wall DH (2004) Ecological linkages between above ground and below ground biota. Science 304:1629–1633

    Article  CAS  PubMed  Google Scholar 

  • Wu BY, Isobe K, Ishii R (2004) Arbuscular mycorrhizal colonization of the dominant plant species in primary successional volcanic deserts on the Southeast slope of Mount Fuji. Mycorrhiza 14:391–395

    Article  PubMed  Google Scholar 

  • Wu BY, Hogetsu T, Isobe K, Ishii R (2007) Community structure of arbuscular mycorrhizal fungi in a primary successional volcanic desert on the southeast slope of Mount Fuji. Mycorrhiza 17:495–506

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We are grateful to Hana Šimáčková from the Laboratory of Environmental Chemistry and Soil Analysis, Institute for Environmental Studies, Charles University in Prague, and Hana Strusková from the Analytical Laboratory of the Institute of Botany, Czech Academy of Sciences, who performed chemical analyses of the soil and plant biomass. Financial support was provided by the Czech Science Foundation (grant GA13-10377S) and the long-term research development project RVO 67985939.

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Authors and Affiliations

  1. Institute of Botany of the Czech Academy of Sciences, 252 43, Průhonice, Czech Republic

    Jana Rydlová, David Püschel & Martina Janoušková

  2. Department of Experimental Plant Biology, Faculty of Sciences, Charles University, Viničná 5, 128 00, Praha 2, Czech Republic

    Magdalena Dostálová

  3. Institute for Environmental Studies, Faculty of Sciences, Charles University, Benátská 2, 128 00, Praha 2, Czech Republic

    Jan Frouz

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  1. Jana Rydlová
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Correspondence to Jana Rydlová.

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Rydlová, J., Püschel, D., Dostálová, M. et al. Nutrient limitation drives response of Calamagrostis epigejos to arbuscular mycorrhiza in primary succession. Mycorrhiza 26, 757–767 (2016). https://doi.org/10.1007/s00572-016-0712-5

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