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
Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46
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
Arnolds E (1991) Decline of ectomycorrhizal fungi in Europe. Agric Ecosyst Environ 35:209–244
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
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
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
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
Baxter JW, Dighton J (2005) Phosphorus source alters host plant response to ectomycorrhizal diversity. Mycorrhiza 15:513–523
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
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
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
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
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
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
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
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
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
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
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
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
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
Corrales A, Mangan SA, Turner BL, Dalling JW (2016) An ectomycorrhizal nitrogen economy facilitates monodominance in a neotropical forest. Ecol Lett 19:383–392
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
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
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
Dickie I, Reich PB (2005) Ectomycorrhizal fungal communities at forest edges. J Ecol 93:244–255
Dickie IA, Koide RT, Fayish AC (2001) Vesicular–arbuscular mycorrhizal infection of Quercus rubra seedlings. New Phytol 151:257–264
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
Dickie IA, Koele N, Blum JD, Gleason JD, McGlone MS (2014) Mycorrhizas in changing ecosystems. Botany 92:149–160
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
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
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
Graham J, Drouillard D, Hodge N (1996) Carbon economy of sour orange in response to different Glomus spp. Tree Physiol 16:1023–1029
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
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
Janzen DH (1970) Herbivores and the number of tree species in tropical forests. Am Nat 104:501–528
Johnson NC (1993) Can fertilization of soil select less mutualistic mycorrhizae? Bull Ecol Soc Am 3:749–757
Johnson NC, Graham JH, Smith F (1997) Functioning of mycorrhizal associations along the mutualism–parasitism continuum. New Phytol 135:575–585
Johnson DJ, Beaulieu WT, Bever JD, Clay K (2012) Conspecific negative density dependence and forest diversity. Science 336:904–907
Jones MD, Durall DM, Cairney JW (2003) Ectomycorrhizal fungal communities in young forest stands regenerating after clearcut logging. New Phytol 157:399–422
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
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
Jonsson LM, Nilsson MC, Wardle DA, Zackrisson O (2001) Context dependent effects of ectomycorrhizal species richness on tree seedling productivity. Oikos 93:353–364
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
Kiernan JM, Hendrix JW, Maronek DM (1983) Fertilizer-induced pathogenicity of mycorrhizal fungi to sweetgum seedlings. Soil Biol Biochem 15:257–262
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
Koide R (1985) The nature of growth depressions in sunflower caused by vesicular–arbuscular mycorrhizal infection. New Phytol 99:449–462
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
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
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
Maherali H, Klironomos JN (2007) Influence of phylogeny on fungal community assembly and ecosystem functioning. Science 316:1746–1748
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
McCarthy-Neumann S, Ibáñez I (2013) Plant–soil feedback links negative distance dependence and light gradient partitioning during seedling establishment. Ecology 94:780–786
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
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
Mills KE, Bever JD (1998) Maintenance of diversity within plant communities: soil pathogens as agents of negative feedback. Ecology 79:1595–1601
Mosse B (1973) Plant growth responses to vesicular-arbuscular mycorrizha. New Phytol 72:127–136
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
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
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
Packer A, Clay K (2000) Soil pathogens and spatial patterns of seedling mortality in a temperate tree. Nature 404:278–281
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
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
Peay KG, Schubert MG, Nguyen NH, Bruns TD (2012) Measuring ectomycorrhizal fungal dispersal: macroecological patterns driven by microscopic propagules. Mol Ecol 21:4122–4136
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
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
R Core Team R (2019) R: a language and environment for statistical computing. Vienna, Austria
Rinella MJ, Reinhart KO (2018) Toward more robust plant-soil feedback research. Ecology 99:550–556
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
Smith LM, Reynolds HL (2015) Plant–soil feedbacks shift from negative to positive with decreasing light in forest understory species. Ecology 96:2523–2532
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
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
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
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
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
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
Treseder KK (2004) A meta-analysis of mycorrhizal responses to nitrogen, phosphorus, and atmospheric CO2 in field studies. New Phytol 164:347–355
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
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
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
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
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
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
Vitousek PM, Mooney HA, Lubchenco J, Melillo JM (1997) Human domination of Earth's ecosystems. Science 277:494–499
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
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
Wickham H (2016) ggplot2: elegant graphics for data analysis. Springer, New York
Zhu K, Woodall CW, Monteiro JV, Clark JS (2015) Prevalence and strength of density-dependent tree recruitment. Ecology 96:2319–2327
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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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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DOI: https://doi.org/10.1007/s11104-020-04616-y