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Plant and Soil

, Volume 433, Issue 1–2, pp 127–145 | Cite as

Interactions between soil properties, soil microbes and plants in remnant-grassland and old-field areas: a reciprocal transplant approach

  • Monique E. Smith
  • José M. Facelli
  • Timothy R. Cavagnaro
Regular Article

Abstract

Background and aims

The importance of plant-soil feedback is becoming widely acknowledged; however, how different soil conditions influence these interactions is still relatively unknown. Using soil from a degraded old-field and a remnant grassland, we aimed to explore home-field advantages in plant-soil feedbacks and plant responses to the abiotic and biotic soil conditions. We quantified the soil bacterial and fungal community from these sites and their responses to soil conditions and plant species.

Methods

Sterilized old-field and remnant-grassland soil was inoculated with home or away soil in a reciprocal transplant experiment using a native grass, Rytidosperma auriculatum, and an invasive grass, Avena barbata, as test species. The soil fungal and bacterial communities were characterised using high throughput sequencing.

Results

Plants had a greater growth response to microbes when an inoculant was added to its home soil. However, this relationship is complex, with microbial communities changing in response to the plant species and soil type.

Conclusion

The apparent home-field advantage of the soil microbes shown in this study may restrict the utility of inoculants as a management tool. However, since we inoculated sterile soil, future work should focus on understanding how the inoculated microbial community interacts and competes with resident communities.

Keywords

Bacterial community eDNA Fungal community Invasive annual grass Native perennial grass Old-fields Remnant grasslands Home-field advantage 

Notes

Acknowledgements

We thank Olivia Cousins for providing an internal review, and two anonymous reviewers for advice and helpful comments on a previous version of the manuscript and Dr. Matthew Christmas and Rebecca Stoner for advice and help setting up the experiment. This project was funded by Nature Foundation of South Australia Incorporated, Australian Flora Foundation Incorporated and the Holsworth Wildlife Research Endowment.

Supplementary material

11104_2018_3823_MOESM1_ESM.docx (113.5 mb)
ESM 1 (DOCX 116247 kb)

References

  1. Abraham JK, Corbin JD, D'Antonio CM (2009) California native and exotic perennial grasses differ in their response to soil nitrogen, exotic annual grass density, and order of emergence. Plant Ecol 201:445–456.  https://doi.org/10.1007/s11258-008-9467-1 CrossRefGoogle Scholar
  2. Araujo ASF, Borges CD, Tsai SM, Cesarz S, Eisenhauer N (2014) Soil bacterial diversity in degraded and restored lands of Northeast Brazil. Antonie Van Leeuwenhoek 106:891–899.  https://doi.org/10.1007/s10482-014-0258-5 CrossRefPubMedGoogle Scholar
  3. Ayres E, Steltzer H, Simmons BL, Simpson RT, Steinweg JM, Wallenstein MD, Mellor N, Parton WJ, Moore JC, Wall DH (2009) Home-field advantage accelerates leaf litter decomposition in forests. Soil Biol Biochem 41:606–610.  https://doi.org/10.1016/j.soilbio.2008.12.022 CrossRefGoogle Scholar
  4. Ba L, Facelli E, Facelli JM (2018) Plant-mycorrhizal fungi feedbacks: potential accomplices of Avena barbata’s high invasiveness. Plant Ecol 219:1045–1052.  https://doi.org/10.1007/s11258-018-0857-8 CrossRefGoogle Scholar
  5. Bálint M, Bartha L, O'Hara RB, Olson MS, Otte J, Pfenninger M, Robertson AL, Tiffin P, Schmitt I (2015) Relocation, high-latitude warming and host genetic identity shape the foliar fungal microbiome of poplars. Mol Ecol 24:235–248.  https://doi.org/10.1111/mec.13018 CrossRefPubMedGoogle Scholar
  6. Bálint M, Bahram M, Eren AM, Faust K, Fuhrman JA, Lindahl B, O'Hara RB, Öpik M, Sogin ML, Unterseher M, Tedersoo L (2016) Millions of reads, thousands of taxa: microbial community structure and associations analyzed via marker genes. FEMS Microbiol Rev 40:686–700.  https://doi.org/10.1093/femsre/fuw017 CrossRefPubMedGoogle Scholar
  7. Bates D, Maechler M, Bolker B, Walker S (2014) lme4: linear mixed-effects models using Eigen and S4. R package version 1Google Scholar
  8. Bethlenfalvay G, Brown M, Pacovsky R (1982) Parasitic and mutualistic associations between a mycorrhizal fungus and soybean: development of the host plant. Phytopathology 72:889–893CrossRefGoogle Scholar
  9. 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.  https://doi.org/10.2307/2960528 CrossRefGoogle Scholar
  10. Bever JD, Dickie IA, Facelli E, Facelli JM, Klironomos J, Moora M, Rillig MC, Stock WD, Tibbett M, Zobel M (2010) Rooting theories of plant community ecology in microbial interactions. Trends Ecol Evol 25:468–478.  https://doi.org/10.1016/j.tree.2010.05.004 CrossRefPubMedPubMedCentralGoogle Scholar
  11. 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.  https://doi.org/10.1146/annurev-micro-092611-150107 CrossRefPubMedPubMedCentralGoogle Scholar
  12. Bezemer TM, Lawson CS, Hedlund K, Edwards AR, Brook AJ, Igual JM, Mortimer SR, Van der Putten WH (2006) Plant species and functional group effects on abiotic and microbial soil properties and plant-soil feedback responses in two grasslands. J Ecol 94:893–904.  https://doi.org/10.1111/j.1365-2745.2006.01158.x CrossRefGoogle Scholar
  13. Brinkman EP, Van der Putten WH, Bakker EJ, Verhoeven KJF (2010) Plant-soil feedback: experimental approaches, statistical analyses and ecological interpretations. J Ecol 98:1063–1073.  https://doi.org/10.1111/j.1365-2745.2010.01695.x CrossRefGoogle Scholar
  14. Bruckner A, Heethoff M (2017) A chemo-ecologists' practical guide to compositional data analysis. Chemoecology 27:33–46.  https://doi.org/10.1007/s00049-016-0227-8 CrossRefGoogle Scholar
  15. Bulgarelli D, Garrido-Oter R, Münch PC, Weiman A, Dröge J, Pan Y, McHardy AC, Schulze-Lefert P (2015) Structure and function of the bacterial root microbiota in wild and domesticated barley. Cell Host Microbe 17:392–403.  https://doi.org/10.1016/j.chom.2015.01.011 CrossRefPubMedPubMedCentralGoogle Scholar
  16. Bureau of Meteorology (2017) Climate data: Roseworthy, viewed on 25th November 2017, <http://www.bom.gov.au/climate/data/>
  17. Busse MD, Sanchez FG, Ratcliff AW, Butnor JR, Carter EA, Powers RF (2009) Soil carbon sequestration and changes in fungal and bacterial biomass following incorporation of forest residues. Soil Biol Biochem 41:220–227.  https://doi.org/10.1016/j.soilbio.2008.10.012 CrossRefGoogle Scholar
  18. Callaway RM, Thelen GC, Rodriguez A, Holben WE (2004) Soil biota and exotic plant invasion. Nature 427:731–733.  https://doi.org/10.1038/nature02322 CrossRefPubMedGoogle Scholar
  19. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336.  https://doi.org/10.1038/nmeth.f.303 CrossRefPubMedPubMedCentralGoogle Scholar
  20. Cavagnaro TR (2016) Soil moisture legacy effects: impacts on soil nutrients, plants and mycorrhizal responsiveness. Soil Biol Biochem 95:173–179.  https://doi.org/10.1016/j.soilbio.2015.12.016 CrossRefGoogle Scholar
  21. Chaparro JM, Sheflin AM, Manter DK, Vivanco JM (2012) Manipulating the soil microbiome to increase soil health and plant fertility. Biol Fertil Soils 48:489–499.  https://doi.org/10.1007/s00374-012-0691-4 CrossRefGoogle Scholar
  22. Cramer VA, Hobbs RJ, Standish RJ (2008) What's new about old fileds? Land abandonment and ecosystem assembly. Trends Ecol Evol 23:104–112.  https://doi.org/10.1016/j.tree.2007.10.005 CrossRefPubMedGoogle Scholar
  23. Davidson AM, Jennions M, Nicotra AB (2011) Do invasive species show higher phenotypic plasticity than native species and, if so, is it adaptive? A meta-analysis. Ecol Lett 14:419–431.  https://doi.org/10.1111/j.1461-0248.2011.01596.x CrossRefPubMedGoogle Scholar
  24. DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, Huber T, Dalevi D, Hu P, Andersen GL (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72:5069–5072CrossRefGoogle Scholar
  25. Drenovsky RE, Steenwerth KL, Jackson LE, Scow KM (2010) Land use and climatic factors structure regional patterns in soil microbial communities. Glob Ecol Biogeogr 19:27–39.  https://doi.org/10.1111/j.1466-8238.2009.00486.x CrossRefPubMedPubMedCentralGoogle Scholar
  26. Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461CrossRefGoogle Scholar
  27. Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200CrossRefGoogle Scholar
  28. Emam T (2016) Local soil, but not commercial AMF inoculum, increases native and non-native grass growth at a mine restoration site. Restor Ecol 24:35–44.  https://doi.org/10.1111/rec.12287 CrossRefGoogle Scholar
  29. Facelli JM, Facelli E (1993) Interactions after death - plant litter controls priority effects in a successional plant community. Oecologia 95:277–282.  https://doi.org/10.1007/bf00323500 CrossRefPubMedGoogle Scholar
  30. Fierer N, Strickland MS, Liptzin D, Bradford MA, Cleveland CC (2009) Global patterns in belowground communities. Ecol Lett 12:1238–1249CrossRefGoogle Scholar
  31. Fierer N, Lauber CL, Ramirez KS, Zaneveld J, Bradford MA, Knight R (2012) Comparative metagenomic, phylogenetic and physiological analyses of soil microbial communities across nitrogen gradients. ISME J 6:1007–1017CrossRefGoogle Scholar
  32. Gellie NJC, Mills JG, Breed MF, Lowe AJ (2017) Revegetation rewilds the soil bacterial microbiome of an old field. Mol Ecol 26:2895–2904.  https://doi.org/10.1111/mec.14081 CrossRefPubMedGoogle Scholar
  33. Giovannetti M, Mosse B (1980) Evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytol 84:489–500.  https://doi.org/10.1111/j.1469-8137.1980.tb04556.x CrossRefGoogle Scholar
  34. Graham JH, Leonard RT, Menge JA (1982) Interaction of light-intensity and soil-temperature with phosphorus inhibition of vesicular arbuscular. New Phytol 91:683–690.  https://doi.org/10.1111/j.1469-8137.1982.tb03347.x CrossRefGoogle Scholar
  35. Harris J (2009) Soil microbial communities and restoration ecology: facilitators or followers? Science 325:573–574.  https://doi.org/10.1126/science.1172975 CrossRefPubMedGoogle Scholar
  36. Hawkes CV, Kivlin SN, Du J, Eviner VT (2013) The temporal development and additivity of plant-soil feedback in perennial grasses. Plant Soil 369:141–150.  https://doi.org/10.1007/s11104-012-1557-0 CrossRefGoogle Scholar
  37. Herzberger AJ, Meiners SJ, Towey JB, Butts PA, Armstrong DL (2015) Plant–microbe interactions change along a tallgrass prairie restoration chronosequence. Restor Ecol 23:220–227.  https://doi.org/10.1111/rec.12165 CrossRefGoogle Scholar
  38. Hillebrand H, Bennett DM, Cadotte MW (2008) Consequesnces of dominance: a review of evenness effects on local and regional ecosystem processes. Ecology 89:1510–1520.  https://doi.org/10.1890/07-1053.1 CrossRefPubMedGoogle Scholar
  39. Hoeksema JD, Chaudhary VB, Gehring CA, Johnson NC, Karst J, Koide RT, Pringle A, Zabinski C, Bever JD, Moore JC, Wilson GWT, Klironomos JN, Umbanhowar J (2010) A meta-analysis of context-dependency in plant response to inoculation with mycorrhizal fungi. Ecol Lett 13:394–407.  https://doi.org/10.1111/j.1461-0248.2009.01430.x CrossRefGoogle Scholar
  40. Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biom J 50:346–363.  https://doi.org/10.1002/bimj.200810425 CrossRefGoogle Scholar
  41. Ji B, Gehring CA, Wilson GWT, Miller RM, Flores-Rentería L, Johnson NC (2013) Patterns of diversity and adaptation in Glomeromycota from three prairie grasslands. Mol Ecol 22:2573–2587.  https://doi.org/10.1111/mec.12268 CrossRefPubMedGoogle Scholar
  42. Johnson NC, Wilson GW, Bowker MA, Wilson JA, Miller RM (2010) Resource limitation is a driver of local adaptation in mycorrhizal symbioses. Proc Natl Acad Sci 107:2093–2098CrossRefGoogle Scholar
  43. Jordan NR, Larson DL, Huerd SC (2008) Soil modification by invasive plants: effects on native and invasive species of mixed-grass prairies. Biol Invasions 10:177–190.  https://doi.org/10.1007/s10530-007-9121-1 CrossRefGoogle Scholar
  44. Kardol P, Bezemer TM, van der Putten WH (2006) Temporal variation in plant-soil feedback controls succession. Ecol Lett 9:1080–1088.  https://doi.org/10.1111/j.1461-0248.2006.00953.x CrossRefPubMedGoogle Scholar
  45. Kardol P, Veen GF, Teste FP, Perring MP (2015) Peeking into the black box: a trait-based approach to predicting plant–soil feedback. New Phytol 206:1–4.  https://doi.org/10.1111/nph.13283 CrossRefPubMedGoogle Scholar
  46. Kawecki TJ, Ebert D (2004) Conceptual issues in local adaptation. Ecol Lett 7:1225–1241.  https://doi.org/10.1111/j.1461-0248.2004.00684.x CrossRefGoogle Scholar
  47. Klironomos JN (2002) Feedback with soil biota contributes to plant rarity and invasiveness in communities. Nature 417:67–70.  https://doi.org/10.1038/417067a CrossRefPubMedGoogle Scholar
  48. Koide RT, Li MG (1990) On host regulation of the vesicular arbuscular mycorrhizal symbiosis. New Phytol 114:59–64.  https://doi.org/10.1111/j.1469-8137.1990.tb00373.x CrossRefGoogle Scholar
  49. Kõljalg U, Larsson K-H, Abarenkov K, Nilsson RH, Alexander IJ, Eberhardt U, Erland S, Høiland K, Kjøller R, Larsson E, Pennanen T, Sen R, Taylor AFS, Tedersoo L, Vrålstad T (2005) UNITE: a database providing web-based methods for the molecular identification of ectomycorrhizal fungi. New Phytol 166:1063–1068.  https://doi.org/10.1111/j.1469-8137.2005.01376.x CrossRefPubMedGoogle Scholar
  50. Kulmatiski A, Kardol P (2008) Getting plant—soil feedbacks out of the greenhouse: experimental and conceptual approaches. In: Lüttge U, Beyschlag W, Murata J (eds) Progress in botany. Springer, Berlin HeidelbergGoogle Scholar
  51. Kulmatiski A, Beard KH, Stevens JR, Cobbold SM (2008) Plant-soil feedbacks: a meta-analytical review. Ecol Lett 11:980–992.  https://doi.org/10.1111/j.1461-0248.2008.01209.x CrossRefPubMedGoogle Scholar
  52. Kuzyakov Y, Friedel JK, Stahr K (2000) Review of mechanisms and quantification of priming effects. Soil Biol Biochem 32:1485–1498.  https://doi.org/10.1016/s0038-0717(00)00084-5 CrossRefGoogle Scholar
  53. Lambers H, Mougel C, Jaillard B, Hinsinger P (2009) Plant-microbe-soil interactions in the rhizosphere: an evolutionary perspective. Plant Soil 321:83–115.  https://doi.org/10.1007/s11104-009-0042-x CrossRefGoogle Scholar
  54. Lambert DH, Cole H, Baker DE (1980) Adaptation of vesicular-arbuscular mycorrhizae to edaphic factors. New Phytol 85:513–520.  https://doi.org/10.1111/j.1469-8137.1980.tb00766.x CrossRefGoogle Scholar
  55. Le S, Josse J, Husson F (2008) FactoMineR: an R package for multivariate analysis. J Stat Softw 25:1–18CrossRefGoogle Scholar
  56. Leff JW, Jones SE, Prober SM, Barberan A, Borer ET, Firn JL, Harpole WS, Hobbie SE, Hofmockel KS, Knops JMH, McCulley RL, La Pierre K, Risch AC, Seabloom EW, Schutz M, Steenbock C, Stevens CJ, Fierer N (2015) Consistent responses of soil microbial communities to elevated nutrient inputs in grasslands across the globe. Proc Natl Acad Sci U S A 112:10967–10972.  https://doi.org/10.1073/pnas.1508382112 CrossRefPubMedPubMedCentralGoogle Scholar
  57. Leimu R, Fischer M (2008) A meta-analysis of local adaptation in plants. PLoS One 3:8.  https://doi.org/10.1371/journal.pone.0004010 CrossRefGoogle Scholar
  58. Lekberg Y, Gibbons SM, Rosendahl S, Ramsey PW (2013) Severe plant invasions can increase mycorrhizal fungal abundance and diversity. ISME J 7:1424–1433.  https://doi.org/10.1038/ismej.2013.41 CrossRefPubMedPubMedCentralGoogle Scholar
  59. Lenz TI, Moyle-Croft JL, Facelli JM (2003) Direct and indirect effects of exotic annual grasses on species composition of a south Australian grassland. Austral Ecol 28:23–32.  https://doi.org/10.1046/j.1442-9993.2003.01238.x CrossRefGoogle Scholar
  60. Mangla S, Inderjit CRM (2008) Exotic invasive plant accumulates native soil pathogens which inhibit native plants. J Ecol 96:58–67.  https://doi.org/10.1111/j.1365-2745.2007.01312.x CrossRefGoogle Scholar
  61. McMurdie PJ, Holmes S (2014) Waste not, want not: why rarefying microbiome data is inadmissible. PLoS Comput Biol 10:e1003531CrossRefGoogle Scholar
  62. Miller RE, Gleadow RM, Cavagnaro TR (2014) Age versus stage: does ontogeny modify the effect of phosphorus and arbuscular mycorrhizas on above- and below-ground defence in forage sorghum? Plant Cell Environ 37:929–942.  https://doi.org/10.1111/pce.12209 CrossRefPubMedGoogle Scholar
  63. Mitchell CE, Power AG (2003) Release of invasive plants from fungal and viral pathogens. Nature 421:625–627CrossRefGoogle Scholar
  64. Montalvo AM, Ellstrand NC (2000) Transplantation of the subshrub Lotus scoparius: testing the home-site advantage hypothesis. Conserv Biol 14:1034–1045.  https://doi.org/10.1046/j.1523-1739.2000.99250.x CrossRefGoogle Scholar
  65. Neuenkamp L, Prober SM, Price JN, Zobel M, Standish RJ (2018) Benefits of mycorrhizal inoculation to ecological restoration depend on plant functional type, restoration context and time. Fungal Ecol.  https://doi.org/10.1016/j.funeco.2018.05.004
  66. Ohsowski BM, Klironomos JN, Dunfield KE, Hart MM (2012) The potential of soil amendments for restoring severely disturbed grasslands. Appl Soil Ecol 60:77–83.  https://doi.org/10.1016/j.apsoil.2012.02.006 CrossRefGoogle Scholar
  67. Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O'Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagner H (2017) Vegan: community ecology package. R package version 2.4–3, https://cran.r-project.org/package=vegan
  68. Packer A, Clay K (2000) Soil pathogens and spatial patterns of seedling mortality in a temperate tree. Nature 404:278–281.  https://doi.org/10.1038/35005072 CrossRefPubMedGoogle Scholar
  69. Pregitzer CC, Bailey JK, Hart SC, Schweitzer JA (2010) Soils as agents of selection: feedbacks between plants and soils alter seedling survival and performance. Evol Ecol 24:1045–1059.  https://doi.org/10.1007/s10682-010-9363-8 CrossRefGoogle Scholar
  70. R Core Team (2017) R: a language and environment for statistical computing. In: R Foundation for Statistical Computing, Vienna, AustriaGoogle Scholar
  71. Ramirez KS, Lauber CL, Knight R, Bradford MA, Fierer N (2010) Consistent effects of nitrogen fertilization on soil bacterial communities in contrasting systems. Ecology 91:3463–3470CrossRefGoogle Scholar
  72. Ronsheim ML (2012) The effect of Mycorrhizae on plant growth and reproduction varies with soil phosphorus and developmental stage. Am Midl Nat 167:28–39CrossRefGoogle Scholar
  73. Rosser L (2013) Ecological restoration plan for Para woodlands reserve. Department of Environment, Water and Natural Resources, South Australian Government, Adelaide, AustraliaGoogle Scholar
  74. Rua MA, Antoninka A, Antunes PM, Chaudhary VB, Gehring C, Lamit LJ, Piculell BJ, Bever JD, Zabinski C, Meadow JF, Lajeunesse MJ, Milligan BG, Karst J, Hoeksema JD (2016) Home-field advantage? Evidence of local adaptation among plants, soil, and arbuscular mycorrhizal fungi through meta-analysis. BMC Evol Biol 16:15.  https://doi.org/10.1186/s12862-016-0698-9 CrossRefGoogle Scholar
  75. Skipper HD, Westermann DT (1973) Comparative effects of propylene oxide, sodium azide, and autoclaving on selected soil properties. Soil Biol Biochem 5:409–414.  https://doi.org/10.1016/0038-0717(73)90067-9 CrossRefGoogle Scholar
  76. Smith ME (2018) Interactions between native and exotic plants in the context of grassland restoration and the importance of below-ground processes. University of Adelaide. Faculty of Science. Biological SciencesGoogle Scholar
  77. Smith FA, Smith SE (1981) Mycorrhizal infection and growth of Trifolium subterraneum: use of sterilized soil as a control treatment. New Phytol 88:299–309.  https://doi.org/10.1111/j.1469-8137.1981.tb01726.x CrossRefGoogle Scholar
  78. Smith DS, Schweitzer JA, Turk P, Bailey JK, Hart SC, Shuster SM, Whitham TG (2012) Soil-mediated local adaptation alters seedling survival and performance. Plant Soil 352:243–251CrossRefGoogle Scholar
  79. Smith ME, Delean S, Cavagnaro TR, Facelli JM (2018) Evidence for species-specific plant responses to soil microbial communities from remnant and degraded land provides promise for restoration. Austral Ecol: in press 43:301–308.  https://doi.org/10.1111/aec.12567 CrossRefGoogle Scholar
  80. Son CL, Smith SE (1988) Mycorrhizal growth-responses - interactions between photon irradiance and phosphorus-nutrition. New Phytol 108:305–314.  https://doi.org/10.1111/j.1469-8137.1988.tb04167.x CrossRefGoogle Scholar
  81. Standish RJ, Cramer VA, Hobbs RJ, Kobryn HT (2006) Legacy of land-use evident in soils of Western Australia's wheatbelt. Plant Soil 280:189–207.  https://doi.org/10.1007/s11104-005-2855-6 CrossRefGoogle Scholar
  82. Steenwerth KL, Jackson LE, Calderon FJ, Stromberg MR, Scow KM (2002) Soil microbial community composition and land use history in cultivated and grassland ecosystems of coastal California. Soil Biol Biochem 34:1599–1611.  https://doi.org/10.1016/s0038-0717(02)00144-x CrossRefGoogle Scholar
  83. Stinson KA, Campbell SA, Powell JR, Wolfe BE, Callaway RM, Thelen GC, Hallett SG, Prati D, Klironomos JN (2006) Invasive plant suppresses the growth of native tree seedlings by disrupting belowground mutualisms. PLoS Biol 4:727–731.  https://doi.org/10.1371/journal.pbio.0040140 CrossRefGoogle Scholar
  84. Tilman D (1988) Plant strategies and the dynamics and structure of plant communities. Princeton University PressGoogle Scholar
  85. van der Heijden MGA, Bakker R, Verwaal J, Scheublin TR, Rutten M, van Logtestijn R, Staehelin C (2006) Symbiotic bacteria as a determinant of plant community structure and plant productivity in dune grassland. FEMS Microbiol Ecol 56:178–187.  https://doi.org/10.1111/j.1574-6941.2006.0086.x CrossRefPubMedGoogle Scholar
  86. van der Putten WH, Vet LEM, Harvey JA, Wackers FL (2001) Linking above- and belowground multitrophic interactions of plants, herbivores, pathogens, and their antagonists. Trends Ecol Evol 16:547–554.  https://doi.org/10.1016/s0169-5347(01)02265-0 CrossRefGoogle Scholar
  87. van der Putten WH, Bradford MA, Brinkman EP, van de Voorde TFJ, Veen GF (2016) Where, when and how plant-soil feedback matters in a changing world. Funct Ecol 30:1109–1121.  https://doi.org/10.1111/1365-2435.12657 CrossRefGoogle Scholar
  88. Vierheilig H, Coughlan AP, Wyss U, Piche Y (1998) Ink and vinegar, a simple staining technique for arbuscular-mycorrhizal fungi. Appl Environ Microbiol 64:5004–5007PubMedPubMedCentralGoogle Scholar
  89. Walker J, Reddell P (2007) Retrogressive succession and restoration on old landscapes. In: Walker L, Walker J, Hobbs R (eds) Linking restoration and ecological succession. Springer, New YorkCrossRefGoogle Scholar
  90. Wang Y, Naumann U, Wright ST, Warton DI (2012) Mvabund–an R package for model-based analysis of multivariate abundance data. Methods Ecol Evol 3:471–474CrossRefGoogle Scholar
  91. Warcup J (1957) Chemical and biological aspects of soil sterilization. Soils Fert 20:1–5Google Scholar
  92. Wardle DA (2002) Communities and ecosystems: linking the aboveground and belowground components. Princeton University PressGoogle Scholar
  93. Warton DI, Wright ST, Wang Y (2012) Distance-based multivariate analyses confound location and dispersion effects. Methods Ecol Evol 3:89–101CrossRefGoogle Scholar
  94. Watts-Williams SJ, Cavagnaro TR (2012) Arbuscular mycorrhizas modify tomato responses to soil zinc and phosphorus addition. Biol Fertil Soils 48:285–294.  https://doi.org/10.1007/s00374-011-0621-x CrossRefGoogle Scholar
  95. Weinbaum BS, Allen MF, Allen EB (1996) Survival of Arbuscular Mycorrhizal Fungi following reciprocal transplanting across the Great Basin, USA. Ecol Appl 6:1365–1372.  https://doi.org/10.2307/2269614 CrossRefGoogle Scholar
  96. Weiss S, Xu ZZ, Peddada S, Amir A, Bittinger K, Gonzalez A, Lozupone C, Zaneveld JR, Vázquez-Baeza Y, Birmingham A, Hyde ER, Knight R (2017) Normalization and microbial differential abundance strategies depend upon data characteristics. Microbiome 5:27.  https://doi.org/10.1186/s40168-017-0237-y CrossRefPubMedPubMedCentralGoogle Scholar
  97. Wong MR (2013) Above-and below-ground linkages of semi-arid perennial tussock grasslands. Monash University. Faculty of Science. Biological SciencesGoogle Scholar
  98. Wubs ERJ, van der Putten WH, Bosch M, Bezemer TM (2016) Soil inoculation steers restoration of terrestrial ecosystems. Nat Plants 2:16107.  https://doi.org/10.1038/nplants.2016.107 CrossRefPubMedGoogle Scholar
  99. Yuan X, Knelman JE, Gasarch E, Wang D, Nemergut DR, Seastedt TR (2016) Plant community and soil chemistry responses to long-term nitrogen inputs drive changes in alpine bacterial communities. Ecology 97:1543–1554.  https://doi.org/10.1890/15-1160.1 CrossRefPubMedGoogle Scholar
  100. Zhang J, Kobert K, Flouri T, Stamatakis A (2014) PEAR: a fast and accurate Illumina paired-end reAd mergeR. Bioinformatics 30:614–662CrossRefGoogle Scholar

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© Springer Nature Switzerland AG 2018

Authors and Affiliations

  1. 1.School of Biological Sciences, Benham LaboratoriesUniversity of AdelaideAdelaideAustralia
  2. 2.The Waite Research Institute and The School of Agriculture, Food and WineUniversity of AdelaideAdelaideAustralia

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