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Arbuscular common mycorrhizal networks mediate intra- and interspecific interactions of two prairie grasses

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Abstract

Arbuscular mycorrhizal fungi form extensive common mycorrhizal networks (CMNs) that may interconnect neighboring root systems of the same or different plant species, thereby potentially influencing the distribution of limiting mineral nutrients among plants. We examined how CMNs affected intra- and interspecific interactions within and between populations of Andropogon gerardii, a highly mycorrhiza dependent, dominant prairie grass and Elymus canadensis, a moderately dependent, subordinate prairie species. We grew A. gerardii and E. canadensis alone and intermixed in microcosms, with individual root systems isolated, but either interconnected by CMNs or with CMNs severed weekly. CMNs, which provided access to a large soil volume, improved survival of both A. gerardii and E. canadensis, but intensified intraspecific competition for A. gerardii. When mixed with E. canadensis, A. gerardii overyielded aboveground biomass in the presence of intact CMNs but not when CMNs were severed, suggesting that A. gerardii with intact CMNs most benefitted from weaker interspecific than intraspecific interactions across CMNs. CMNs improved manganese uptake by both species, with the largest plants receiving the most manganese. Enhanced growth in consequence of improved mineral nutrition led to large E. canadensis in intact CMNs experiencing water-stress, as indicated by 13C isotope abundance. Our findings suggest that in prairie plant communities, CMNs may influence mineral nutrient distribution, water relations, within-species size hierarchies, and between-species interactions.

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References

  • Al-Karaki GN, Clark R (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 

  • Allsopp N, Stock WD (1992) Density dependent interactions between VA mycorrhizal fungi and even-aged seedlings of two perennial Fabaceae species. Oecolgia 91:281–287

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Bever JD et al (2010) Rooting theories of plant community ecology in microbial interactions. Trends Ecol Evolution 25:468–478. https://doi.org/10.1016/j.tree.2010.05.004

    Article  Google Scholar 

  • Cahill JF Jr, Casper BB (2000) Investigating the relationship between neighbor root biomass and belowground competition: field evidence for symmetric competition belowground. Oikos 90:311–320

    Article  Google Scholar 

  • Chiariello N, Hickman JC, Mooney HA (1982) Endomycorrhizal role for interspecific transfer of phosphorus in a community of annual plants. Science 217:941–943

    Article  CAS  PubMed  Google Scholar 

  • Fellbaum CR, Mensah JA, Cloos AJ, Strahan GE, Pfeffer PE, Kiers ET, Bücking H (2014) Fungal nutrient allocation in common mycorrhizal networks is regulated by the carbon source strength of individual host plants. New Phytol 203:646–656. https://doi.org/10.1111/nph.12827

    Article  CAS  PubMed  Google Scholar 

  • Firbank L, Watkinson A, Grace J, Tilman D (1990) On the effects of competition: from monocultures to mixtures. In: Grace J (ed) Perspectives on Plant Competition, Academic Press, San Diego, pp 165–192

  • Hammer EC, Pallon J, Wallander H, Olsson PA (2011) Tit for tat? A mycorrhizal fungus accumulates phosphorus under low plant carbon availability. FEMS Microbiol Ecol 76:236–244. https://doi.org/10.1111/j.1574-6941.2011.01043.x

    Article  CAS  PubMed  Google Scholar 

  • Hartnett DC, Hetrick BAD, Wilson GWT (1993) Mycorrhizal influence on intra- and interspecific neighbour interactions among co-occurring prairie grasses. J Ecol 81:787–795

    Article  Google Scholar 

  • Hartnett DC, Samenus RJ, Fischer LE, Hetrick BAD (1994) Plant demographic responses to mycorrhizal symbiosis in tallgrass prairie. Oecolgia 99:21–26. https://doi.org/10.1007/bf00317079

    Article  CAS  Google Scholar 

  • He X, Critchley C, Bledsoe C (2003) Nitrogen transfer within and between plants through common mycorrhizal networks (CMNs). CRC Crit Rev Plant Sci 22:531–567. https://doi.org/10.1080/07352680390253520

    Article  Google Scholar 

  • Hetrick BAD, Wilson GWT, Hartnett DC (1989) Relationship between mycorrhizal dependence and competitive ability of 2 tallgrass prairie grasses. Can J Bot-Revue Canadienne De Botanique 67:2608–2615

    Google Scholar 

  • Hetrick BAD, Wilson GWT, Todd TC (1990) Differential responses of C3 and C4 grasses to mycorrhizal symbiosis, phosphorus fertilization, and soil microorganisms. Can J Bot 68:461–467. https://doi.org/10.1139/b90-061

    Article  Google Scholar 

  • Jakobsen I, Hammer EC (2015) Nutrient dynamics in arbuscular mycorrhizal networks. Nutrient Dynamics in Arbuscular Mycorrhizal Networks. In: Horton TR (ed) Mycorrhizal Networks. Springer, Dordrecht, pp 91–131

  • Janos DP (2007) Plant responsiveness to mycorrhizas differs from dependence upon mycorrhizas. Mycorrhiza 17:75–91. https://doi.org/10.1007/s00572-006-0094-1

    Article  PubMed  Google Scholar 

  • Kiers ET et al (2011) Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science 333:880–882. https://doi.org/10.1126/science.1208473

    Article  CAS  PubMed  Google Scholar 

  • Lehmann A, Rillig MC (2015) Arbuscular mycorrhizal contribution to copper, manganese and iron nutrient concentrations in crops—a meta-analysis. Soil Biol Biochem 81:147–158

    Article  CAS  Google Scholar 

  • Lekberg Y, Hammer EC, Olsson PA (2010) Plants as resource islands and storage units—adopting the mycocentric view of arbuscular mycorrhizal networks. FEMS Microbiol Ecol 74:336–345. https://doi.org/10.1111/j.1574-6941.2010.00956.x

    Article  CAS  PubMed  Google Scholar 

  • 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 Phytol 115:495–501. https://doi.org/10.1111/j.1469-8137.1990.tb00476.x

    Article  Google Scholar 

  • Merrild MP, Ambus P, Rosendahl S, Jakobsen I (2013) Common arbuscular mycorrhizal networks amplify competition for phosphorus between seedlings and established plants. New Phytol 200:229–240. https://doi.org/10.1111/nph.12351

    Article  CAS  PubMed  Google Scholar 

  • Miller SL, Allen EB (1992) Mycorrhizae, nutrient translocation, and interactions between plants. In: Allen MF (ed) Mycorrhizal functioning. Chapman & Hall, New York, pp 301–332

    Google Scholar 

  • Moora M, Zobel M (1996) Effect of arbuscular mycorrhiza on inter-and intraspecific competition of two grassland species. Oecologia 108:79–84

    Article  PubMed  Google Scholar 

  • Olsson PA, Rahm J, Aliasgharzad N (2010) Carbon dynamics in mycorrhizal symbioses is linked to carbon costs and phosphorus benefits. FEMS Microbiol Ecol 72:125–131. https://doi.org/10.1111/j.1574-6941.2009.00833.x

    Article  PubMed  Google Scholar 

  • Ricklefs RE (1979) Ecology. Chiron Press, New York

    Google Scholar 

  • Schroeder-Moreno MS, Janos DP (2008) Intra- and inter-specific density affects plant growth responses to arbuscular mycorrhizas. Botany 86:1180–1193. https://doi.org/10.1139/b08-080

    Article  Google Scholar 

  • Schüßler A, Walker C (2010) The Glomeromycota: a species list with new families and new genera. The Royal Botanic Garden Kew, Botanische Staatssammlung Munich, and Oregon State University, p 19

  • Simard SW, Durall DM (2004) Mycorrhizal networks: a review of their extent, function, and importance. Can J Bot 82:1140–1165. https://doi.org/10.1139/b04-116

    Article  CAS  Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic, Cambridge

    Google Scholar 

  • Smith MD, Hartnett DC, Wilson GWT (1999) Interacting influence of mycorrhizal symbiosis and competition on plant diversity in tallgrass prairie. Oecologia 121:574–582. https://doi.org/10.1007/s004420050964

    Article  CAS  PubMed  Google Scholar 

  • Tisdall J (1991) Fungal hyphae and structural stability of soil. Soil Res 29:729–743. https://doi.org/10.1071/SR9910729

    Article  Google Scholar 

  • Vandermeer J (1981) The interference production principle: an ecological theory for agriculture. Bioscience 31:361–364. https://doi.org/10.2307/1308400

    Article  Google Scholar 

  • Walder F, van der Heijden MGA (2015) Regulation of resource exchange in the arbuscular mycorrhizal symbiosis. Nat Plants. https://doi.org/10.1038/NPLANTS.2015.159

  • Walder F, Niemann H, Natarajan M, Lehmann M, Boller T, Wiemken A (2012) Mycorrhizal networks: common goods of plants shared under unequal terms of trade. Plant Physiol 159:789–797

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weaver JE, Fitzpatrick T (1934) The prairie. Ecol Monogr:112–295

  • Weiner J (1985) Size hierachies in experimental populations of annual plants. Ecology 66:743–752

    Article  Google Scholar 

  • Weiner J (1988) The influence of competition on plant reproduction In: Plant reproductive ecology, Oxford University Press, New York, pp 228–245

  • Weiner J (1990) Asymmetric competition in plant populations. Trees 5:360–364

    CAS  Google Scholar 

  • Weiner J, Solbrig OT (1984) The meaning and measurement of size hierarchies in plant populations. Oecologia 61:334–336

    Article  PubMed  Google Scholar 

  • Weiner J, Thomas SC (1986) Size variability and competition in plant monocultures. Oikos 47:211–222

    Article  Google Scholar 

  • Weiner J, Wright DB, Castro S (1997) Symmetry of below-ground competition between Kochia scoparia individuals. Oikos 79:85–91

    Article  Google Scholar 

  • Weremijewicz J, Janos DP (2013) Common mycorrhizal networks amplify size inequality in Andropogon gerardii monocultures. New Phytol 198:203–213. https://doi.org/10.1111/nph.12125

    Article  CAS  PubMed  Google Scholar 

  • Weremijewicz J, Seto K (2016) Mycorrhizas influence functional traits of two tallgrass prairie species. Ecol Evol. https://doi.org/10.1002/ece3.2129

  • Weremijewicz J, Sternberg LDSLO, Janos DP (2016) Common mycorrhizal networks amplify competition by preferential mineral nutrient allocation to large host plants. New Phytol 212(2):461–471

    Article  CAS  PubMed  Google Scholar 

  • West HM (1996) Influence of arbuscular mycorrhizal infection on competition between Holcus lanatus and Dactylis glomerata. J Ecol 84:429–438. https://doi.org/10.2307/2261204

    Article  Google Scholar 

  • Yachandra VK, Sauer K, Klein MP (1996) Manganese cluster in photosynthesis: where plants oxidize water to dioxygen. Chem Rev 96:2927–2950

    Article  CAS  PubMed  Google Scholar 

  • Zeileis A, Kleiber C (2014) ineq: Measuring inequality, concentration, and poverty. https://CRAN.Rproject.org/package=ineq. Accessed 26 May 2015

  • 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

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Ms. Alison R. Lincoln and Richmond Heights Middle School for allowing us to conduct this experiment with the enthusiastic assistance of AgriScience Magnet students, and for providing glasshouse space. We thank Jennifer Velasquez for assistance in maintaining and harvesting the experiment, Michael Amaranthus (Mycorrhizal Applications) for providing mycorrhizal inoculum, and two anonymous reviewers for their helpful suggestions.

Funding

This study was funded by a National Science Foundation Doctoral Dissertation Improvement Grant (DEB-1401677).

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Correspondence to Joanna Weremijewicz.

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All data are presented in the manuscript as tables and figures. Data are available from Open Science Framework DOI 10.17605/OSF.IO/FAPJN.

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Weremijewicz, J., da Silveira Lobo O’Reilly Sternberg, L. & Janos, D.P. Arbuscular common mycorrhizal networks mediate intra- and interspecific interactions of two prairie grasses. Mycorrhiza 28, 71–83 (2018). https://doi.org/10.1007/s00572-017-0801-0

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