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Soil Microbe-Mediated N:P Stoichiometric Effects on Solidago canadensis Performance Depend on Nutrient Levels

  • Plant Microbe Interactions
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Abstract

Both soil microbes and soil N:P ratios can affect plant growth, but it is unclear whether they can interact to alter plant growth and whether such an interactive effect depends on nutrient levels. Here, we tested the hypothesis that soil microbes can ameliorate the negative effects of nutrient imbalance caused by low or high N:P ratios on plant growth and that such an ameliorative effect of soil microbes depends on nutrient supply levels. We grew individuals of six populations of the clonal plant Solidago canadensis at three N:P ratios (low (1.7), intermediate (15), and high (135)), under two nutrient levels (low versus high) and in the presence versus absence of soil microbes. The presence of soil microbes significantly increased biomass of S. canadensis at all three N:P ratios and under both nutrient levels. Under the low-nutrient level, biomass, height, and leaf number of S. canadensis did not differ significantly among the three N:P ratio treatments in the absence of soil microbes, but they were higher at the high than at the low and the intermediate N:P ratio in the presence of soil microbes. Under the high-nutrient level, by contrast, biomass, height, and leaf number of S. canadensis were significantly higher at the low than at the high and the intermediate N:P ratio in the absence of soil microbes, but increased with increasing the N:P ratio in the presence of soil microbes. In the presence of soil microbes, number of ramets (asexual individuals) and the accumulation of N and P in plants were significantly higher at the high than at the low and the intermediate N:P ratio under both nutrient levels, whereas in the absence of soil microbes, they did not differ significantly among the three N:P ratio regardless of the nutrient levels. Our results provide empirical evidence that soil microbes can alter effects of N:P ratios on plant performance and that such an effect depends on nutrient availability. Soil microbes may, therefore, play a role in modulating ecosystem functions such as productivity and carbon and nutrient cycling via modulating nutrient imbalance caused by low and high N:P ratios.

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After acceptance, all data will be deposited at Dryad Digital Repository.

References

  1. Elser JJ, Andersen T, Baron JS, Bergström A-K, Jansson M, Kyle M, Nydick KR, Steger L et al (2009) Shifts in lake N: P stoichiometry and nutrient limitation driven by atmospheric nitrogen deposition. Science 326:835–837

    Article  CAS  PubMed  Google Scholar 

  2. Peñuelas J, Poulter B, Sardans J, Ciais P, van der Velde M, Bopp L, Boucher O, Godderis Y et al (2013) Human-induced nitrogen–phosphorus imbalances alter natural and managed ecosystems across the globe. Nat Commun 4:2934

    Article  PubMed  Google Scholar 

  3. Yuan ZY, Chen HYH (2015) Decoupling of nitrogen and phosphorus in terrestrial plants associated with global changes. Nat Clim Chang 5:465

    Article  CAS  Google Scholar 

  4. Zheng M, Zhou Z, Luo Y, Zhao P, Mo J (2019) Global pattern and controls of biological nitrogen fixation under nutrient enrichment: a meta-analysis. Glob Change Biol 25:3018–3030

    Article  Google Scholar 

  5. Song M-H, Yu F-H, Ouyang H, Cao G-M, Xu X-L, Cornelissen JHC (2012) Different inter-annual responses to availability and form of nitrogen explain species coexistence in an alpine meadow community after release from grazing. Glob Change Biol 18:3100–3111

    Article  Google Scholar 

  6. Pingali PL (2012) Green revolution: impacts, limits, and the path ahead. Proc Natl Acad Sci 109:12302–12308

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Galloway JN, Townsend AR, Erisman JW, Bekunda M, Cai Z, Freney JR, Martinelli LA, Seitzinger SP et al (2008) Transformation of the nitrogen cycle: recent trends, questions, and potential solutions. Science 320:889–892

    Article  CAS  PubMed  Google Scholar 

  8. He CE, Wang X, Liu X, Fangmeier A, Christie P, Zhang F (2010) Nitrogen deposition and its contribution to nutrient inputs to intensively managed agricultural ecosystems. Ecol Appl 20:80–90

    Article  PubMed  Google Scholar 

  9. Vitousek P, Aber J, Howarth R, Likens G, Matson P, Schindler D, Schlesinger W, Tilman D (1997) Human alteration of the global nitrogen cycle: sources and consequences. Ecol Appl 7:737–750

    Google Scholar 

  10. Vitousek PM, Porder S, Houlton BZ, Chadwick OA (2010) Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen–phosphorus interactions. Ecol Appl 20:5–15

    Article  PubMed  Google Scholar 

  11. Zhan S, Wang YZ, Z., Li W, Bai Y, (2017) Nitrogen enrichment alters plant N:P stoichiometry and intensifies phosphorus limitation in a steppe ecosystem. Environ Exp Bot 134:21–32

    Article  CAS  Google Scholar 

  12. Yang Q, Carrillo J, Jin H, Shang L, Hovick SM, Nijjer S, Gabler CA, Li B et al (2013) Plant–soil biota interactions of an invasive species in its native and introduced ranges: implications for invasion success. Soil Biol Biochem 65:78–85

    Article  CAS  Google Scholar 

  13. Čapek P, Manzoni S, Kaštovská E, Wild B, Diáková K, Bárta J, Schnecker J, Biasi C et al (2018) A plant–microbe interaction framework explaining nutrient effects on primary production. Nat Ecol Evol 2:1588–1596

    Article  PubMed  Google Scholar 

  14. Jones DL, Magthab EA, Gleeson DB, Hill PW, Sánchez-Rodríguez AR, Roberts P, Ge T, Murphy DV (2018) Microbial competition for nitrogen and carbon is as intense in the subsoil as in the topsoil. Soil Biol Biochem 117:72–82

    Article  CAS  Google Scholar 

  15. Kuzyakov Y, Xu XL (2013) Competition between roots and microorganisms for nitrogen: mechanisms and ecological relevance. New Phytol 198:656–669

    Article  CAS  PubMed  Google Scholar 

  16. Davidson EA, Howarth RW (2007) Nutrients in synergy. Nature 449:1000–1001

    Article  CAS  PubMed  Google Scholar 

  17. Xia J, Wan S (2008) Global response patterns of terrestrial plant species to nitrogen addition. New Phytol 179:428–439

    Article  CAS  PubMed  Google Scholar 

  18. Yan Z, Tian D, Han W, Tang Z, Fang J (2017) An assessment on the uncertainty of the nitrogen to phosphorus ratio as a threshold for nutrient limitation in plants. Ann Bot 120:937–942

    Article  PubMed  PubMed Central  Google Scholar 

  19. LeBauer DS, Treseder KK (2008) Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distributed. Ecology 89:371–379

    Article  PubMed  Google Scholar 

  20. Fujita Y, de Ruiter PC, Wassen MJ, Heil GWJP, Soil, (2010) Time-dependent, species-specific effects of N:P stoichiometry on grassland plant growth. Plant Soil 334:99–112

    Article  CAS  Google Scholar 

  21. Güsewell S (2004) N:P ratios in terrestrial plants: variation and functional significance. New Phytol 164:243–266

    Article  PubMed  Google Scholar 

  22. Harpole WS, Ngai JT, Cleland EE, Seabloom EW, Borer ET, Bracken MES, Elser JJ, Gruner DS et al (2011) Nutrient co-limitation of primary producer communities. Ecol Lett 14:852–862

    Article  PubMed  Google Scholar 

  23. Song M-H, Yu F-H (2015) Reduced compensatory effects explain the nitrogen-mediated reduction in stability of an alpine meadow on the Tibetan Plateau. New Phytol 207:70–77

    Article  PubMed  Google Scholar 

  24. Güsewell S (2005) High nitrogen : phosphorus ratios reduce nutrient retention and second-year growth of wetland sedges. New Phytol 166:537–550

    Article  PubMed  Google Scholar 

  25. Xu X, Thornton PE, Post WM (2013) A global analysis of soil microbial biomass carbon, nitrogen and phosphorus in terrestrial ecosystems. Glob Ecol Biogeogr 22:737–749

    Article  Google Scholar 

  26. Koerselman W, Meuleman AFM (1996) The vegetation N:P ratio: a new tool to detect the nature of nutrient limitation. J Appl Ecol 33:1441–1450

    Article  Google Scholar 

  27. Yang Y, Pan J, Han B-P, Naselli-Flores L (2020) The effects of absolute and relative nutrient concentrations (N/P) on phytoplankton in a subtropical reservoir. Ecological Indicators 115:106466

    Article  CAS  Google Scholar 

  28. Güsewell S, Bollens U (2003) Composition of plant species mixtures grown at various N:P ratios and levels of nutrient supply. Basic Appl Ecol 4:453–466

    Article  Google Scholar 

  29. Fay PA, Prober SM, Harpole WS, Knops JM, Bakker JD, Borer ET, Lind EM, MacDougall AS et al (2015) Grassland productivity limited by multiple nutrients. Nat Plants 1:15080

    Article  CAS  PubMed  Google Scholar 

  30. Güsewell S (2005) Responses of wetland graminoids to the relative supply of nitrogen and phosphorus. Plant Ecol 176:35–55

    Article  Google Scholar 

  31. Güsewell S, Koerselman W (2002) Variation in nitrogen and phosphorus concentrations of wetland plants. Perspectives in Plant Ecology, Evolution and Systematics 5:37–61

    Article  Google Scholar 

  32. Lenton TM, Klausmeier CA (2007) Biotic stoichiometric controls on the deep ocean N:P ratio. Biogeosciences 4:353–367

    Article  CAS  Google Scholar 

  33. Richardson AE, Barea J-M, McNeill AM, Prigent-Combaret C (2009) Acquisition of phosphorus and nitrogen in the rhizosphere and plant growth promotion by microorganisms. Plant Soil 321:305–339

    Article  CAS  Google Scholar 

  34. Hestrin R, Hammer EC, Mueller CW, Lehmann J (2019) Synergies between mycorrhizal fungi and soil microbial communities increase plant nitrogen acquisition. Commun Biol 2:233

    Article  PubMed  PubMed Central  Google Scholar 

  35. in’t Zandt D, van den Brink A, de Kroon H, Visser EJW (2019) Plant-soil feedback is shut down when nutrients come to town. Plant Soil 439:541–551

    Article  Google Scholar 

  36. Zhang CB, Wang J, Qian BY, Li WH (2009) Effects of the invader Solidago canadensis on soil properties. Appl Soil Ecol 43:163–169

    Article  CAS  Google Scholar 

  37. Li J, Du L, Guan W, Yu F-H, van Kleunen M (2016) Latitudinal and longitudinal clines of phenotypic plasticity in the invasive herb Solidago canadensis in China. Oecologia 182:755–764

    Article  PubMed  Google Scholar 

  38. Jin H, Yuan Y, Gao F, Oduor AMO, Li J (2020) The invasive plant Solidago canadensis exhibits partial local adaptation to low salinity at germination but not at later life-history stages. Am J Bot 107:1–8

    Article  Google Scholar 

  39. Jizhong W, Ayub MOO, Robin P, Beilei W, Luxi C, Beifen Y, Yu F-H, Junmin L (2019) Can polyploidy confer invasive plants with a wider climatic tolerance? A test using Solidago canadensis. Ecol Evol 10:5617–5630

    Google Scholar 

  40. Adomako MO, Ning L, Tang M, Du D-L, van Kleunen M, Yu F-H (2019) Diversity- and density-mediated allelopathic effects of resident plant communities on invasion by an exotic plant. Plant Soil 440:581–592

    Article  CAS  Google Scholar 

  41. Li YZ, Yin X, Wei W, Yang EY, Hang Y, Tian ZH, Da LJ (2010) Inhibition of local plant Phragmites communis on the invasive plant Solidago canadensis. Acta Ecol Sin 30:6881–6891

    Google Scholar 

  42. Ye X-Q, Yan Y-N, Wu M, Yu F-H (2019) High capacity of nutrient accumulation by invasive Solidago canadensis in a coastal grassland. Front Plant Sci 10:575

    Article  PubMed  PubMed Central  Google Scholar 

  43. Rasmussen PU, Bennett AE, Tack AJM (2020) The impact of elevated temperature and drought on the ecology and evolution of plant–soil microbe interactions. J Ecol 108:337–352

    Article  Google Scholar 

  44. Wubs ERJ, van der Putten WH, Mortimer SR, Korthals GW, Duyts H, Wagenaar R, Bezemer TM (2019) Single introductions of soil biota and plants generate long-term legacies in soil and plant community assembly. Ecol Lett 22:1145–1151

    Article  PubMed  PubMed Central  Google Scholar 

  45. Whitaker BK, Bauer JT, Bever JD, Clay K (2017) Negative plant-phyllosphere feedbacks in native Asteraceae hosts – a novel extension of the plant-soil feedback framework. Ecol Lett 20:1064–1073

    Article  PubMed  Google Scholar 

  46. Zhang H, Chang R, Guo X, Liang X, Wang R, Liu J (2017) Shifts in growth and competitive dominance of the invasive plant Alternanthera philoxeroides under different nitrogen and phosphorus supply. Environ Exp Bot 135:118–125

    Article  CAS  Google Scholar 

  47. Pinheiro J, Bates D, DebRoy S, Sarkar D (2007) nlme: linear and nonlinear mixed effects models. R package

  48. Bates D (2011) Mixed Models in R Using the lme4 Package. Part 5: generalized linear mixed models. University of Wisconsin, Madison, WI, USA

  49. Powell M (2009) The BOBYQA algorithm for bound constrained optimization without derivatives. Technical Report, Department of Applied Mathematics and Theoretical Physics

  50. Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biom J 50:346–363

    Article  PubMed  Google Scholar 

  51. R Core Team (2020) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  52. RStudio Team (2015) Integrated development environment for R. RStudio Inc, Boston, MA

    Google Scholar 

  53. Kuzyakov Y (2010) Priming effects: interactions between living and dead organic matter. Soil Biol Biochem 42:1363–1371

    Article  CAS  Google Scholar 

  54. Leigh J, Hodge A, Fitter AH (2009) Arbuscular mycorrhizal fungi can transfer substantial amounts of nitrogen to their host plant from organic material. New Phytol 181:199–207

    Article  CAS  PubMed  Google Scholar 

  55. Rousk K, Michelsen A, Rousk J (2016) Microbial control of soil organic matter mineralization responses to labile carbon in subarctic climate change treatments. Glob Change Biol 22:4150–4161

    Article  Google Scholar 

  56. Biere A, Bennett AE (2013) Three-way interactions between plants, microbes and insects. Funct Ecol 27:567–573

    Article  Google Scholar 

  57. Larimer AL, Bever JD, Clay K (2010) The interactive effects of plant microbial symbionts: a review and meta-analysis. Symbiosis 51:139–148

    Article  Google Scholar 

  58. Porter SS, Bantay R, Friel CA, Garoutte A, Gdanetz K, Ibarreta K, Moore BM, Shetty P et al (2020) Beneficial microbes ameliorate abiotic and biotic sources of stress on plants. Funct Ecol 00:1–12

    Google Scholar 

  59. Craine JM, Jackson RD (2010) Plant nitrogen and phosphorus limitation in 98 North American grassland soils. Plant Soil 334:73–84

    Article  CAS  Google Scholar 

  60. Gotelli NJ, Ellison AM (2002) Nitrogen deposition and extinction risk in the northern pitcher plant, Sarracenia purpurea. Ecology 83:2758–2765

    Article  Google Scholar 

  61. Sardans J, Rivas-Ubach A, Peñuelas J (2012) The C:N:P stoichiometry of organisms and ecosystems in a changing world: a review and perspectives. Perspect Plant Ecol Evol Syst 14:33–47

    Article  Google Scholar 

  62. Carter TS, Clark CM, Fenn ME, Jovan S, Perakis SS, Riddell J, Schaberg PG, Greaver TL et al (2017) Mechanisms of nitrogen deposition effects on temperate forest lichens and trees. Ecosphere 8:e01717

    Article  Google Scholar 

  63. Cheng Y, Wang J, Ge Z, Zhang J, Cai Y, Chang SX, Cai Z, Chen HYH (2020) Background nitrogen deposition controls the effects of experimental nitrogen addition on soil gross N transformations in forest ecosystems. Biogeochemistry 151:335–341

    Article  CAS  Google Scholar 

  64. Stevens CJ, David TI, Storkey J (2018) Atmospheric nitrogen deposition in terrestrial ecosystems: its impact on plant communities and consequences across trophic levels. Funct Ecol 32:1757–1769

    Article  Google Scholar 

  65. Moreira H, Pereira SIA, Vega A, Castro PML, Marques APGC (2020) Synergistic effects of arbuscular mycorrhizal fungi and plant growth-promoting bacteria benefit maize growth under increasing soil salinity. J Environ Manag 257:109982

    Article  CAS  Google Scholar 

  66. Cavagnaro TR, Jackson LE, Six J, Ferris H, Goyal S, Asami D, Scow KM (2006) Arbuscular mycorrhizas, microbial communities, nutrient availability, and soil aggregates in organic tomato production. Plant Soil 282:209–225

    Article  CAS  Google Scholar 

  67. Grman E, Robinson TMP (2013) Resource availability and imbalance affect plant–mycorrhizal interactions: a field test of three hypotheses. Ecology 94:62–71

    Article  PubMed  Google Scholar 

  68. Adomako MO, Xue W, Tang M, Du D-L, Yu F-H (2020) Synergistic effects of soil microbes on Solidago canadensis depend on water and nutrient availability. Microb Ecol 80:837–845

    Article  CAS  PubMed  Google Scholar 

  69. Johnson NC (2010) Resource stoichiometry elucidates the structure and function of arbuscular mycorrhizas across scales. New Phytol 185:631–647

    Article  CAS  PubMed  Google Scholar 

  70. Lin C, Lin W, Chen S, Peng J, Guo J, Yang Y (2019) Phosphorus addition accelerates fine root decomposition by stimulating extracellular enzyme activity in a subtropical natural evergreen broad-leaved forest. Eur J Forest Res 138:917–928

    Article  CAS  Google Scholar 

  71. Shane MW, Lambers H (2005) Cluster roots: a curiosity in context. Plant Soil 274:101–125

    Article  CAS  Google Scholar 

  72. Shane MW, Lambers H (2005) Manganese accumulation in leaves of Hakea prostrata (Proteaceae) and the significance of cluster roots for micronutrient uptake as dependent on phosphorus supply. Physiol Plant 124:441–450

    Article  CAS  Google Scholar 

  73. Zhang D, Wang C, Li X, Yang X, Zhao L, Liu L, Zhu C, Li R (2018) Linking plant ecological stoichiometry with soil nutrient and bacterial communities in apple orchards. Appl Soil Ecol 126:1–10

    Article  Google Scholar 

  74. Zhang H, Goll DS, Wang Y-P, Ciais P, Wieder WR, Abramoff R, Huang Y, Guenet B et al (2020) Microbial dynamics and soil physicochemical properties explain large-scale variations in soil organic carbon. Glob Change Biol 26:2668–2685

    Article  Google Scholar 

  75. Xi N, Bloor JMG, Wang Y, Chu C (2019) Contribution of conspecific soil microorganisms to tree seedling light responses: insights from two tropical species with contrasting shade tolerance. Environ Exp Bot 166:103826

    Article  CAS  Google Scholar 

  76. Allison SD, Vitousek PM (2005) Responses of extracellular enzymes to simple and complex nutrient inputs. Soil Biol Biochem 37:937–944

    Article  CAS  Google Scholar 

  77. Jin L, Gu Y, Xiao M, Chen J, Li B (2004) The history of Solidago canadensis invasion and the development of its mycorrhizal associations in newly-reclaimed land. Funct Plant Biol 31

  78. Dong L-J, He W-M (2019) The relative contributions of climate, soil, diversity and interactions to leaf trait variation and spectrum of invasive Solidago canadensis. BMC Ecol 19:24

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We thank Dr. Ayub M.O. Oduor for providing the seeds of Solidago canadensis, help with data analysis, and comments on an early version of the manuscript.

Funding

This work was supported by the Ten-Thousand-Talent Program of Zhejiang Province (2018R52016), the National Natural Science Foundation of China (31870610), and the Joint Fund of Zhejiang Provincial Natural Science Foundation (LTZ20C030001).

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Conceptualization: Michael Opoku Adomako; methodology: Michael Opoku Adomako and Fei-Hai Yu; formal analysis and investigation: Michael Opoku Adomako; writing—original draft preparation: Michael Opoku Adomako; writing—review and editing: Fei-Hai Yu, Wei Xue, and Dao-Lin Du; funding acquisition: Fei-Hai Yu; resources: Fei-Hai Yu; Supervision: Fei-Hai Yu and Dao-Lin Du.

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Correspondence to Fei-Hai Yu.

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Adomako, M.O., Xue, W., Du, DL. et al. Soil Microbe-Mediated N:P Stoichiometric Effects on Solidago canadensis Performance Depend on Nutrient Levels . Microb Ecol 83, 960–970 (2022). https://doi.org/10.1007/s00248-021-01814-8

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