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Plant and Soil

, Volume 441, Issue 1–2, pp 499–510 | Cite as

Effects of fairy ring fungi on plants and soil in the alpine and temperate grasslands of China

  • Chao Yang
  • Jingjing Li
  • Nan Liu
  • Yingjun ZhangEmail author
Regular Article
  • 188 Downloads

Abstract

Aims

Soil fungi are considered to be key regulators of plant and soil relationships. The fairy rings (FRs) caused by basidiomycete fungi can influence plant productivity and soil nutrient and microbiome composition. We sought to explore the role of FRs in plant communities and soil properties for two types of grasslands in China.

Methods

Plant and soil samples were collected from three concentric zones: outside the ring (OUT), on the ring (ON), and inside the ring (IN). Data were collected on plant productivity, plant diversity, soil properties, and soil bacterial diversity.

Results

We found that FRs significantly improved plant productivity and diversity in both alpine and temperate grasslands. In the alpine grassland, soil water content, pH and bacterial diversity were lower in the ON zone compared to the OUT zone. Likewise, in temperate grasslands, water content was lower in the ON zone compared to both OUT and IN zones. Also, soil pH and bacterial diversity were higher on the ON zone compared to other both zones.

Conclusion

Based on our data, we believe that FR fungi increase plant productivity and diversity, and change the composition of soil bacterial species and diversity. We suggest that the effects of FR fungi on plants included the increase of the soil nutrient content and the effects of FR fungi on soil bacteria included the changes in soil water content and pH value.

Keywords

Fairy rings Saprotrophic fungi Plant-soil relationships Plant diversity Soil properties 

Notes

Acknowledgements

We are grateful to the staff at the National Field Research Station of Grassland Science in Hebei Province, and the Haibei Demonstration Zone of Plateau Modern Ecological Animal Husbandry Science and Technology in Qinghai Province, China for their help with field work. This work was jointly supported by the National Natural Science Foundation of China (31830092) and China Forage and Grass Research System (CARS-35).

Supplementary material

11104_2019_4141_MOESM1_ESM.docx (26 kb)
ESM 1 (DOCX 25 kb)

References

  1. Auge RM (2001) Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza 11:3–42.  https://doi.org/10.1007/s005720100097 CrossRefGoogle Scholar
  2. Bonanomi G, Mingo A, Incerti G, Mazzoleni S, Allegrezza M (2012) Fairy rings caused by a killer fungus foster plant diversity in species-rich grassland. J Veg Sci 23:236–248.  https://doi.org/10.1111/j.1654-1103.2011.01353.x CrossRefGoogle Scholar
  3. Caesar-TonThat TC, Espeland E, Caesar AJ, Sainju UM, Lartey RT, Gaskin JF (2013) Effects of Agaricus lilaceps fairy rings on soil aggregation and microbial community structure in relation to growth stimulation of Western wheatgrass (Pascopyrum smithii) in eastern Montana rangeland. Microb Ecol 66:120–131.  https://doi.org/10.1007/s00248-013-0194-3 CrossRefPubMedGoogle Scholar
  4. Carter MR, Gregorich EG (2008) Soil sampling and methods of analysis, 2nd edn. CRC Press, Boca RatonGoogle Scholar
  5. Delgado-Baquerizo M, Garcia-Palacios P, Milla R, Gallardo A, Maestre FT (2015) Soil characteristics determine soil carbon and nitrogen availability during leaf litter decomposition regardless of litter quality. Soil Biol Biochem 81:134–142.  https://doi.org/10.1016/j.soilbio.2014.11.009 CrossRefGoogle Scholar
  6. Dong WY, Liu EK, Yan CR, Tian J, Zhang HH, Zhang YQ (2017) Impact of no tillage vs. conventional tillage on the soil bacterial community structure in a winter wheat cropping succession in northern China. Eur J Soil Biol 80:35–42.  https://doi.org/10.1016/j.ejsobi.2017.03.001 CrossRefGoogle Scholar
  7. Edwards PJ (1984) The growth of fairy rings of Agaricus-Arvensis and their effect upon grassland vegetation and soil. J Ecol 72:505–513.  https://doi.org/10.2307/2260062 CrossRefGoogle Scholar
  8. Edwards PJ (1988) Effects of the fairy ring fungus Agaricus-Arvensis on nutrient availability in grassland. New Phytol 110:377–381.  https://doi.org/10.1111/j.1469-8137.1988.tb00275.x CrossRefGoogle Scholar
  9. Ehrenfeld JG, Ravit B, Elgersma K (2005) Feedback in the plant-soil system. Annu Rev Environ Resour 30:75–115.  https://doi.org/10.1146/annurev.energy.30.050504.144212 CrossRefGoogle Scholar
  10. Fidanza MA (2007) Characterization of soil properties associated with type-I fairy ring symptoms in turfgrass. Biologia 62:533–536CrossRefGoogle Scholar
  11. Fierer N, Jackson RB (2006) The diversity and biogeography of soil bacterial communities. Proc Natl Acad Sci USA 103:626–631.  https://doi.org/10.1073/pnas.0507535103 CrossRefPubMedGoogle Scholar
  12. Hodge A, Fitter AH (2013) Microbial mediation of plant competition and community structure. Funct Ecol 27:865–875.  https://doi.org/10.1111/1365-2435.12002 CrossRefGoogle Scholar
  13. Hogberg MN, Baath E, Nordgren A, Arnebrant K, Hogberg P (2003) Contrasting effects of nitrogen availability on plant carbon supply to mycorrhizal fungi and saprotrophs - a hypothesis based on field observations in boreal forest. New Phytol 160:225–238CrossRefGoogle Scholar
  14. Jain R, Saxena J, Sharma V (2012) Solubilization of inorganic phosphates by S19 isolated from rhizosphere soil of a semi-arid region. Ann Microbiol 62:725–735CrossRefGoogle Scholar
  15. Lehto T, Zwiazek JJ (2011) Ectomycorrhizas and water relations of trees: a review. Mycorrhiza 21:71–90.  https://doi.org/10.1007/s00572-010-0348-9 CrossRefPubMedGoogle Scholar
  16. Li Y, Zhang Q, Zhang FF, Liu RX, Liu H, Chen F (2015) Analysis of the microbiota of black stain in the primary dentition. Plos One 10:e0137030.  https://doi.org/10.1371/journal.pone.0137030 CrossRefPubMedPubMedCentralGoogle Scholar
  17. Lisboa FJG, Chaer GM, Fernandes MF, Berbara RLL, Madari BE (2014) The match between microbial community structure and soil properties is modulated by land use types and sample origin within an integrated agroecosystem. Soil Biol Biochem 78:97–108.  https://doi.org/10.1016/j.soilbio.2014.07.017 CrossRefGoogle Scholar
  18. Oh SY, Fong JJ, Park MS, Lim YW (2016) Distinctive feature of microbial communities and bacterial functional profiles in Tricholoma matsutake dominant soil. PLoS One 11:e0168573CrossRefPubMedPubMedCentralGoogle Scholar
  19. Peter M (2006) Ectomycorrhizal fungi - fairy rings and the wood-wide web. New Phytol 171:685–687.  https://doi.org/10.1111/j.1469-8137.2006.01856.x CrossRefPubMedGoogle Scholar
  20. Read DJ, Perez-Moreno J (2003) Mycorrhizas and nutrient cycling in ecosystems - a journey towards relevance? New Phytol 157:475–492.  https://doi.org/10.1046/j.1469-8137.2003.00704.x CrossRefGoogle Scholar
  21. Revillini D, Gehring CA, Johnson NC (2016) The role of locally adapted mycorrhizas and rhizobacteria in plant-soil feedback systems. Funct Ecol 30:1086–1098.  https://doi.org/10.1111/1365-2435.12668 CrossRefGoogle Scholar
  22. Rinaudo V, Barberi P, Giovannetti M, van der Heijden MGA (2010) Mycorrhizal fungi suppress aggressive agricultural weeds. Plant Soil 333:7–20.  https://doi.org/10.1007/s11104-009-0202-z CrossRefGoogle Scholar
  23. Rosling A, Suttle KB, Johansson E, Van Hees PAW, Banfield JF (2007) Phosphorous availability influences the dissolution of apatite by soil fungi. Geobiology 5:265–280CrossRefGoogle Scholar
  24. Semchenko M, Leff JW, Lozano YM, Saar S, Davison J, Wilkinson A, Jackson BG, Pritchard WJ, De Long JR, Oakley S, Mason KE, Ostle NJ, Baggs EM, Johnson D, Fierer N, Bardgett RD (2018) Fungal diversity regulates plant-soil feedbacks in temperate grassland. Sci Adv 4:eaau4578.  https://doi.org/10.1126/sciadv.aau4578 CrossRefPubMedPubMedCentralGoogle Scholar
  25. Talbot JM, Bruns TD, Smith DP, Branco S, Glassman SI, Erlandson S, Vilgalys R, Peay KG (2013) Independent roles of ectomycorrhizal and saprotrophic communities in soil organic matter decomposition. Soil Biol Biochem 57:282–291CrossRefGoogle Scholar
  26. Toohey JI (1983) Fungus fairy rings in soil - etiology and chemical ecology. Can Field Nat 97:9–15Google Scholar
  27. Waring BG, Weintraub SR, Sinsabaugh RL (2014) Ecoenzymatic stoichiometry of microbial nutrient acquisition in tropical soils. Biogeochemistry 117:101–113.  https://doi.org/10.1007/s10533-013-9849-x CrossRefGoogle Scholar
  28. Xing R, Yan HY, Gao QB, Zhang FQ, Wang JL, Chen SL (2018) Microbial communities inhabiting the fairy ring of Floccularia luteovirens and isolation of potential mycorrhiza helper bacteria. J Basic Microbiol 58:554–563CrossRefPubMedGoogle Scholar
  29. Xu XL, Ouyang H, Cao GM, Richter A, Wanek W, Kuzyakov Y (2011) Dominant plant species shift their nitrogen uptake patterns in response to nutrient enrichment caused by a fungal fairy in an alpine meadow. Plant Soil 341:495–504.  https://doi.org/10.1007/s11104-010-0662-1 CrossRefGoogle Scholar
  30. Yang C, Li JJ, Zhang FG, Liu N, Zhang YJ (2018a) The optimal Redfield N: P ratio caused by fairy ring fungi stimulates plant productivity in the temperate steppe of China. Fungal Ecol 34:91–98.  https://doi.org/10.1016/j.funeco.2018.05.007 CrossRefGoogle Scholar
  31. Yang C, Zhang FG, Liu N, Hu J, Zhang YJ (2018b) Changes in soil bacterial communities in response to the fairy ring fungus Agaricus gennadii in the temperate steppes of China. Pedobiologia 69:34–40.  https://doi.org/10.1016/j.pedobi.2018.05.002 CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.College of Grassland Science and TechnologyChina Agricultural UniversityBeijingChina
  2. 2.Key Laboratory of Grassland Management and Rational UtilizationMinistry of AgricultureBeijingChina

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