Ectomycorrhizal fungal diversity interacts with soil nutrients to predict plant growth despite weak plant-soil feedbacks

Abstract

Background and aims

Plant-soil feedbacks are the result of multiple abiotic and biotic mechanisms. However, few studies have addressed how feedbacks vary based on abiotic context or attempted to identify microbiota responsible for feedbacks. We investigated whether plant-soil feedbacks of an ectomycorrhizal tree (Quercus macrocarpa) varied based on soil nutrient status and whether fungal community composition and diversity could explain feedback patterns.

Methods

We inoculated Q. macrocarpa seedlings with field-sampled soils taken from five soil origins – including heterospecific and conspecific trees and an old field – which were profiled using fungal DNA metabarcoding.

Results

There was a positive home vs. away plant-soil feedback, though feedbacks with individual hosts were not significant regardless of fertilization. Still, hosts harbored distinctive fungal communities that were predictive of plant growth. There was a growth promotive effect of ectomycorrhizal OTU diversity that was weakened with fertilization, suggesting context-dependent relationships between plant growth and a guild of fungal mutualists.

Conclusions

Our results demonstrate that the host-specific accumulation of functionally important soil microbes is not always sufficient to drive species level plant-soil feedbacks. Our data provide support for a role of ECM fungal diversity in mediating plant growth responses, though it is unclear whether this effect was direct or indirect.

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Data Availability

The sequence datasets generated during the current study are available at the NCBI Sequence Read Archive under the BioProject ID: PRJNA486026.

References

  1. Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46

    Google Scholar 

  2. Ángeles-Argáiz RE, Flores-García A, Ulloa M, Garibay-Orijel R (2016) Commercial Sphagnum peat moss is a vector for exotic ectomycorrhizal mushrooms. Biol Invasions 18:89–101

    Google Scholar 

  3. Arnolds E (1991) Decline of ectomycorrhizal fungi in Europe. Agric Ecosyst Environ 35:209–244

    Google Scholar 

  4. Averill C, Dietze MC, Bhatnagar JM (2018) Continental-scale nitrogen pollution is shifting forest mycorrhizal associations and soil carbon stocks. Glob Chang Biol 24:4544–4553

    PubMed  Google Scholar 

  5. Avis PG, Meier IC, Phillips RP (2017) An intact soil core bioassay for cultivating forest ectomycorrhizal fungal communities. . Soil Biological Communities and Ecosystem Resilience. Springer

  6. Baar J, Horton TR, Kretzer A, Bruns TD (1999) Mycorrhizal colonization of Pinus muricata from resistant propagules after a stand-replacing wildfire. New Phytol 143:409–418

    Google Scholar 

  7. Bates D, Maechler M, Bolker B, Walker S (2014) lme4: linear mixed-effects models using Eigen and S4. R package version 10-5 http://www.CRANR-projectorg/package=lme4

  8. Baxter JW, Dighton J (2005) Phosphorus source alters host plant response to ectomycorrhizal diversity. Mycorrhiza 15:513–523

    CAS  PubMed  Google Scholar 

  9. Beckjord PR, Melhuish JH Jr, McIntosh MS, Hacskaylo E (1983) Effects of nitrogen fertilization on growth and ectomycorrhizal formation of Quercus alba, Q. rubra, Q. falcata, and Q. falcata var. pagodifolia. Can J Bot 61:2507–2514

    Google Scholar 

  10. Bennett JA, Maherali H, Reinhart KO, Lekberg Y, Hart MM, Klironomos J (2017) Plant-soil feedbacks and mycorrhizal type influence temperate forest population dynamics. Science 355:181–184

    CAS  PubMed  Google Scholar 

  11. Bethlenfalvay GJ, Bayne HG, Pacovsky RS (1983) Parasitic and mutualistic associations between a mycorrhizal fungus and soybean: the effect of phosphorus on host plant-endophyte interactions. Physiol Plant 57:543–548

    CAS  Google Scholar 

  12. Bever JD (2002) Negative feedback within a mutualism: host–specific growth of mycorrhizal fungi reduces plant benefit. Proc R Soc Lond Ser B Biol Sci 269:2595–2601

    Google Scholar 

  13. Bever JD, Westover KM, Antonovics J (1997) Incorporating the soil community into plant population dynamics: the utility of the feedback approach. J Ecol 85:561–573

    Google Scholar 

  14. Bever JD, Platt TG, Morton ER (2012) Microbial population and community dynamics on plant roots and their feedbacks on plant communities. Annu Rev Microbiol 66:265–283

    CAS  PubMed  PubMed Central  Google Scholar 

  15. Bödeker I, Lindahl BD, Olson Å, Clemmensen KE (2016) Mycorrhizal and saprotrophic fungal guilds compete for the same organic substrates but affect decomposition differently. Funct Ecol 30:1967–1978

    Google Scholar 

  16. Bougher NL, Grove TS, Malajczuk N (1990) Growth and phosphorus acquisition of karri (Eucalyptus diversicolor F. Muell.) seedlings inoculated with ectomycorrhizal fungi in relation to phosphorus supply. New Phytol 114:77–85

    CAS  Google Scholar 

  17. Buwalda J, Goh K (1982) Host-fungus competition for carbon as a cause of growth depressions in vesicular-arbuscular mycorrhizal ryegrass. Soil Biol Biochem 14:103–106

    CAS  Google Scholar 

  18. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Cline ML, Patrick Reid C (1982) Seed source and mycorrhizal fungus effects on growth of containerized Pinus contorta and Pinus ponderosa seedlings. For Sci 28:237–250

    Google Scholar 

  20. Comita LS, Queenborough SA, Murphy SJ, Eck JL, Xu K, Krishnadas M, Beckman N, Zhu Y (2014) Testing predictions of the Janzen–Connell hypothesis: a meta-analysis of experimental evidence for distance-and density-dependent seed and seedling survival. J Ecol 102:845–856

    PubMed  PubMed Central  Google Scholar 

  21. Connell JH (1971) On the role of natural enemies in preventing competitive exclusion in some marine animals and in rain forest trees. In: den Boer PJ, Gradwell GR (eds) Dynamics of populations. Centre for Agricultural Publishing and Documentation, Wageningen

    Google Scholar 

  22. Corrales A, Mangan SA, Turner BL, Dalling JW (2016) An ectomycorrhizal nitrogen economy facilitates monodominance in a neotropical forest. Ecol Lett 19:383–392

    PubMed  Google Scholar 

  23. Cox F, Barsoum N, Lilleskov EA, Bidartondo MI (2010) Nitrogen availability is a primary determinant of conifer mycorrhizas across complex environmental gradients. Ecol Lett 13:1103–1113

    PubMed  Google Scholar 

  24. Cregger M, Veach A, Yang Z, Crouch M, Vilgalys R, Tuskan G, Schadt C (2018) The Populus holobiont: dissecting the effects of plant niches and genotype on the microbiome. Microbiome 6:31

    CAS  PubMed  PubMed Central  Google Scholar 

  25. Davison J, Öpik M, Zobel M, Vasar M, Metsis M, Moora M (2012) Communities of arbuscular mycorrhizal fungi detected in forest soil are spatially heterogeneous but do not vary throughout the growing season. PLoS One 7:e41938

    CAS  PubMed  PubMed Central  Google Scholar 

  26. Dickie I, Reich PB (2005) Ectomycorrhizal fungal communities at forest edges. J Ecol 93:244–255

    Google Scholar 

  27. Dickie IA, Koide RT, Fayish AC (2001) Vesicular–arbuscular mycorrhizal infection of Quercus rubra seedlings. New Phytol 151:257–264

    Google Scholar 

  28. Dickie IA, Dentinger B, Avis PG, McLaughlin DJ, Reich PB (2009) Ectomycorrhizal fungal communities of oak savanna are distinct from forest communities. Mycologia 101:473–483

    CAS  PubMed  Google Scholar 

  29. Dickie IA, Koele N, Blum JD, Gleason JD, McGlone MS (2014) Mycorrhizas in changing ecosystems. Botany 92:149–160

    CAS  Google Scholar 

  30. Duhamel M, Wan J, Bogar LM, Segnitz RM, Duncritts NC, Peay KG (2019) Plant selection initiates alternative successional trajectories in the soil microbial community after disturbance. Ecol Monogr:e01367

  31. Egerton-Warburton L, Allen MF (2001) Endo-and ectomycorrhizas in Quercus agrifolia Nee.(Fagaceae): patterns of root colonization and effects on seedling growth. Mycorrhiza 11:283–290

    CAS  PubMed  Google Scholar 

  32. Glassman SI, Peay KG, Talbot JM, Smith DP, Chung JA, Taylor JW, Vilgalys R, Bruns TD (2015) A continental view of pine-associated ectomycorrhizal fungal spore banks: a quiescent functional guild with a strong biogeographic pattern. New Phytol 205:1619–1631

    CAS  PubMed  Google Scholar 

  33. Graham J, Drouillard D, Hodge N (1996) Carbon economy of sour orange in response to different Glomus spp. Tree Physiol 16:1023–1029

    PubMed  Google Scholar 

  34. Hoffman C, Nelson A, Radulski G (2013) 45-acre forest in Oberlin, Ohio sequesters carbon at an increasing rate, offsetting a small percentage of annual Oberlin College carbon emissions. Unpublished work

  35. Hyatt LA, Rosenberg MS, Howard TG, Bole G, Fang W, Anastasia J, Brown K, Grella R, Hinman K, Kurdziel JP (2003) The distance dependence prediction of the Janzen-Connell hypothesis: a meta-analysis. Oikos 103:590–602

    Google Scholar 

  36. Janzen DH (1970) Herbivores and the number of tree species in tropical forests. Am Nat 104:501–528

    Google Scholar 

  37. Johnson NC (1993) Can fertilization of soil select less mutualistic mycorrhizae? Bull Ecol Soc Am 3:749–757

    Google Scholar 

  38. Johnson NC, Graham JH, Smith F (1997) Functioning of mycorrhizal associations along the mutualism–parasitism continuum. New Phytol 135:575–585

    Google Scholar 

  39. Johnson DJ, Beaulieu WT, Bever JD, Clay K (2012) Conspecific negative density dependence and forest diversity. Science 336:904–907

    CAS  PubMed  Google Scholar 

  40. Jones MD, Durall DM, Cairney JW (2003) Ectomycorrhizal fungal communities in young forest stands regenerating after clearcut logging. New Phytol 157:399–422

    Google Scholar 

  41. Jones MD, Twieg BD, Ward V, Barker J, Durall DM, Simard SW (2010) Functional complementarity of Douglas-fir ectomycorrhizas for extracellular enzyme activity after wildfire or clearcut logging. Funct Ecol 24:1139–1151

    Google Scholar 

  42. Jones FA, Erickson DL, Bernal MA, Bermingham E, Kress WJ, Herre EA, Muller-Landau HC, Turner BL (2011) The roots of diversity: below ground species richness and rooting distributions in a tropical forest revealed by DNA barcodes and inverse modeling. PLoS One 6:e24506

    CAS  PubMed  PubMed Central  Google Scholar 

  43. Jonsson LM, Nilsson MC, Wardle DA, Zackrisson O (2001) Context dependent effects of ectomycorrhizal species richness on tree seedling productivity. Oikos 93:353–364

    Google Scholar 

  44. Karst J, Marczak L, Jones MD, Turkington R (2008) The mutualism–parasitism continuum in ectomycorrhizas: a quantitative assessment using meta-analysis. Ecology 89:1032–1042

    PubMed  Google Scholar 

  45. Kiernan JM, Hendrix JW, Maronek DM (1983) Fertilizer-induced pathogenicity of mycorrhizal fungi to sweetgum seedlings. Soil Biol Biochem 15:257–262

    Google Scholar 

  46. Knoblochová T, Kohout P, Püschel D, Doubková P, Frouz J, Cajthaml T, Kukla J, Vosátka M, Rydlová J (2017) Asymmetric response of root-associated fungal communities of an arbuscular mycorrhizal grass and an ectomycorrhizal tree to their coexistence in primary succession. Mycorrhiza 27:775–789

    PubMed  Google Scholar 

  47. Koide R (1985) The nature of growth depressions in sunflower caused by vesicular–arbuscular mycorrhizal infection. New Phytol 99:449–462

    Google Scholar 

  48. Kõljalg U, Larsson KH, Abarenkov K, Nilsson RH, Alexander IJ, Eberhardt U, Erland S, Høiland K, Kjøller R, Larsson E (2005) UNITE: a database providing web-based methods for the molecular identification of ectomycorrhizal fungi. New Phytol 166:1063–1068

    PubMed  Google Scholar 

  49. Leski T, Aučina A, Skridaila A, Pietras M, Riepšas E, Rudawska M (2010) Ectomycorrhizal community structure of different genotypes of scots pine under forest nursery conditions. Mycorrhiza 20:473–481

    PubMed  Google Scholar 

  50. Liu Y, Yu S, Xie ZP, Staehelin C (2012) Analysis of a negative plant–soil feedback in a subtropical monsoon forest. J Ecol 100:1019–1028

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  52. Mangan SA, Schnitzer SA, Herre EA, Mack KM, Valencia MC, Sanchez EI, Bever JD (2010) Negative plant-soil feedback predicts tree-species relative abundance in a tropical forest. Nature 466:752–755

    CAS  PubMed  Google Scholar 

  53. McCarthy-Neumann S, Ibáñez I (2013) Plant–soil feedback links negative distance dependence and light gradient partitioning during seedling establishment. Ecology 94:780–786

    Google Scholar 

  54. McCarthy-Neumann S, Kobe RK (2010) Conspecific and heterospecific plant–soil feedbacks influence survivorship and growth of temperate tree seedlings. J Ecol 98:408–418

    Google Scholar 

  55. McHugh TA, Gehring CA (2006) Below-ground interactions with arbuscular mycorrhizal shrubs decrease the performance of pinyon pine and the abundance of its ectomycorrhizas. New Phytol 171:171–178

    PubMed  Google Scholar 

  56. Mills KE, Bever JD (1998) Maintenance of diversity within plant communities: soil pathogens as agents of negative feedback. Ecology 79:1595–1601

    Google Scholar 

  57. Mosse B (1973) Plant growth responses to vesicular-arbuscular mycorrizha. New Phytol 72:127–136

    Google Scholar 

  58. Nguyen NH, Song Z, Bates ST, Branco S, Tedersoo L, Menke J, Schilling JS, Kennedy PG (2015) FUNGuild: an open annotation tool for parsing fungal community datasets by ecological guild. Fungal Ecol 20:241–248

    Google Scholar 

  59. Oksanen J, Kindt R, Legendre P, O’Hara B, Simpson G, Solymos P, Stevens MHH, Wagner H (2011) Vegan: community ecology package. R package version 117–11 http://www.CRANR-projectorg/package=vegan

  60. Oliet JA, Salazar JM, Villar R, Robredo E, Valladares F (2011) Fall fertilization of Holm oak affects N and P dynamics, root growth potential, and post-planting phenology and growth. Ann For Sci 68:647–656

    Google Scholar 

  61. Packer A, Clay K (2000) Soil pathogens and spatial patterns of seedling mortality in a temperate tree. Nature 404:278–281

    CAS  PubMed  Google Scholar 

  62. Packer A, Clay K (2004) Development of negative feedback during successive growth cycles of black cherry. Proc R Soc Lond Ser B Biol Sci 271:317–324

    Google Scholar 

  63. Peay KG, Bruns TD (2014) Spore dispersal of basidiomycete fungi at the landscape scale is driven by stochastic and deterministic processes and generates variability in plant–fungal interactions. New Phytol 204:180–191

    PubMed  Google Scholar 

  64. Peay KG, Schubert MG, Nguyen NH, Bruns TD (2012) Measuring ectomycorrhizal fungal dispersal: macroecological patterns driven by microscopic propagules. Mol Ecol 21:4122–4136

    PubMed  Google Scholar 

  65. Pernilla Brinkman E, van der Putten WH, Bakker EJ, Verhoeven KJ (2010) Plant–soil feedback: experimental approaches, statistical analyses and ecological interpretations. J Ecol 98:1063–1073

    Google Scholar 

  66. Phillips RP, Brzostek E, Midgley MG (2013) The mycorrhizal-associated nutrient economy: a new framework for predicting carbon–nutrient couplings in temperate forests. New Phytol 199:41–51

    CAS  PubMed  Google Scholar 

  67. R Core Team R (2019) R: a language and environment for statistical computing. Vienna, Austria

  68. Rinella MJ, Reinhart KO (2018) Toward more robust plant-soil feedback research. Ecology 99:550–556

    PubMed  Google Scholar 

  69. Rutten G, Gómez-Aparicio L (2018) Plant-soil feedbacks and root responses of two Mediterranean oaks along a precipitation gradient. Plant Soil 424:221–231

    CAS  Google Scholar 

  70. Smith LM, Reynolds HL (2015) Plant–soil feedbacks shift from negative to positive with decreasing light in forest understory species. Ecology 96:2523–2532

    PubMed  Google Scholar 

  71. Smith-Ramesh LM, Reynolds HL (2017) The next frontier of plant–soil feedback research: unraveling context dependence across biotic and abiotic gradients. J Veg Sci 28:484–494

    Google Scholar 

  72. Štursová M, Bárta J, Šantrůčková H, Baldrian P (2016) Small-scale spatial heterogeneity of ecosystem properties, microbial community composition and microbial activities in a temperate mountain forest soil. FEMS Microbiol Ecol 92:fiw185

    PubMed  Google Scholar 

  73. Tagu D, Rampant PF, Lapeyrie F, Frey-Klett P, Vion P, Villar M (2001) Variation in the ability to form ectomycorrhizas in the F1 progeny of an interspecific poplar (Populus spp.) cross. Mycorrhiza 10:237–240

    CAS  Google Scholar 

  74. Tammi H, Timonen S, Sen R (2001) Spatiotemporal colonization of Scots pine roots by introduced and indigenous ectomycorrhizal fungi in forest humus and nursery Sphagnum peat microcosms. Can J For Res 31:746–756

    Google Scholar 

  75. Taylor D, Bruns T (1999) Community structure of ectomycorrhizal fungi in a Pinus muricata forest: minimal overlap between the mature forest and resistant propagule communities. Mol Ecol 8:1837–1850

    CAS  PubMed  Google Scholar 

  76. Teste FP, Kardol P, Turner BL, Wardle DA, Zemunik G, Renton M, Laliberté E (2017) Plant-soil feedback and the maintenance of diversity in Mediterranean-climate shrublands. Science 355:173–176

    CAS  PubMed  Google Scholar 

  77. Treseder KK (2004) A meta-analysis of mycorrhizal responses to nitrogen, phosphorus, and atmospheric CO2 in field studies. New Phytol 164:347–355

    Google Scholar 

  78. Uroz S, Calvaruso C, Turpault M-P, Pierrat J-C, Mustin C, Frey-Klett P (2007) Effect of the mycorrhizosphere on the genotypic and metabolic diversity of the bacterial communities involved in mineral weathering in a forest soil. Appl Environ Microbiol 73:3019–3027

    CAS  PubMed  PubMed Central  Google Scholar 

  79. Valliere JM, Allen EB (2016) Interactive effects of nitrogen deposition and drought-stress on plant-soil feedbacks of Artemisia californica seedlings. Plant Soil 403:277–290

    CAS  Google Scholar 

  80. van der Heijden MG, Klironomos JN, Ursic M, Moutoglis P, Streitwolf-Engel R, Boller T, Wiemken A, Sanders IR (1998) Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396:69–72

    Google Scholar 

  81. van der Putten WH, Bardgett RD, Bever JD, Bezemer TM, Casper BB, Fukami T, Kardol P, Klironomos JN, Kulmatiski A, Schweitzer JA, Suding KN, van de Voorde TFJ, Wardle DA (2013) Plant–soil feedbacks: the past, the present and future challenges. J Ecol 101:265–276

    Google Scholar 

  82. van der Putten WH, Bradford MA, Pernilla Brinkman E, van de Voorde TF, Veen G (2016) Where, when and how plant–soil feedback matters in a changing world. Funct Ecol 30:1109–1121

    Google Scholar 

  83. van Strien AJ, Boomsluiter M, Noordeloos ME, Verweij RJ, Kuyper TW (2017) Woodland ectomycorrhizal fungi benefit from large-scale reduction of nitrogen deposition in the Netherlands. J Appl Ecol 55:290–298

    Google Scholar 

  84. Vitousek PM, Mooney HA, Lubchenco J, Melillo JM (1997) Human domination of Earth's ecosystems. Science 277:494–499

    CAS  Google Scholar 

  85. Wagg C, Jansa J, Schmid B, van der Heijden MG (2011) Belowground biodiversity effects of plant symbionts support aboveground productivity. Ecol Lett 14:1001–1009

    PubMed  Google Scholar 

  86. Walker JF, Miller KO Jr, Horton JL (2005) Hyperdiversity of ectomycorrhizal fungus assemblages on oak seedlings in mixed forests in the southern Appalachian Mountains. Mol Ecol 14:829–838

    CAS  PubMed  Google Scholar 

  87. Wickham H (2016) ggplot2: elegant graphics for data analysis. Springer, New York

    Google Scholar 

  88. Zhu K, Woodall CW, Monteiro JV, Clark JS (2015) Prevalence and strength of density-dependent tree recruitment. Ecology 96:2319–2327

    PubMed  Google Scholar 

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Acknowledgements

We would like to thank the staff and faculty of the Oberlin College Biology Department for their support at every step of this project. This research would not have been possible without the help and friendship of Olivia Tsang who helped with plant care and countless other tasks. We thank Sarah McCarthy-Neumann for early feedback on the project and thank Noah Fierer and Rytas Vilgalys for their pre-submission review. We thank the editors and the two anonymous reviewers for their insightful feedback. We also thank the Oberlin Biology Department and Dean’s Office for funding to JN and RL for the experimental and greenhouse work as part of the honors thesis of JN. Funding for the fungal amplicon sequencing and the participation of CS was provided by the Genomic System Sciences Program, U.S. Department of Energy, Office of Science, Biological and Environmental Research, as part of the Plant Microbe Interfaces Scientific Focus Area (http://pmi.ornl.gov). Oak Ridge National Laboratory is managed by UT-Battelle, LLC, for the U.S. Department of Energy under contract DEAC05-00OR22725.

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Correspondence to Jake Nash.

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Nash, J., Laushman, R. & Schadt, C. Ectomycorrhizal fungal diversity interacts with soil nutrients to predict plant growth despite weak plant-soil feedbacks. Plant Soil 453, 445–458 (2020). https://doi.org/10.1007/s11104-020-04616-y

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Keywords

  • Plant-soil feedback
  • Ectomycorrhizal
  • Soil biology
  • Fungal ecology
  • Quercus macrocarpa