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A plant–microbe interaction framework explaining nutrient effects on primary production


In most terrestrial ecosystems, plant growth is limited by nitrogen and phosphorus. Adding either nutrient to soil usually affects primary production, but their effects can be positive or negative. Here we provide a general stoichiometric framework for interpreting these contrasting effects. First, we identify nitrogen and phosphorus limitations on plants and soil microorganisms using their respective nitrogen to phosphorus critical ratios. Second, we use these ratios to show how soil microorganisms mediate the response of primary production to limiting and non-limiting nutrient addition along a wide gradient of soil nutrient availability. Using a meta-analysis of 51 factorial nitrogen–phosphorus fertilization experiments conducted across multiple ecosystems, we demonstrate that the response of primary production to nitrogen and phosphorus additions is accurately predicted by our stoichiometric framework. The only pattern that could not be predicted by our original framework suggests that nitrogen has not only a structural function in growing organisms, but also a key role in promoting plant and microbial nutrient acquisition. We conclude that this stoichiometric framework offers the most parsimonious way to interpret contrasting and, until now, unresolved responses of primary production to nutrient addition in terrestrial ecosystems.

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Fig. 1: Concept of nutrient limitation.
Fig. 2: Consequences of differential plant and microbial nutrient limitations.
Fig. 3: Correspondence between the theory and published data.


  1. 1.

    LeBauer, D. S. & Treseder, K. K. Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distributed. Ecology 89, 371–379 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

  2. 2.

    Harpole, W. S. et al. Nutrient co-limitation of primary producer communities. Ecol. Lett. 14, 852–862 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  3. 3.

    Elser, J. J. et al. Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecol. Lett. 10, 1135–1142 (2007).

    Article  Google Scholar 

  4. 4.

    Gorban, A. N., Pokidysheva, L. I., Smirnova, E. V. & Tyukina, T. A. Law of the minimum paradoxes. Bull. Math. Biol. 73, 2013–2044 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  5. 5.

    Danger, M., Daufresne, T., Lucas, F., Pissard, S. & Lacroix, G. Does Liebig’s law of the minimum scale up from species to communities? Oikos 117, 1741–1751 (2008).

    Article  Google Scholar 

  6. 6.

    Marleau, J. N., Guichard, F. & Loreau, M. Emergence of nutrient co-limitation through movement in stoichiometric meta-ecosystems. Ecol. Lett. 18, 1163–1173 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  7. 7.

    Farrior, C. E. et al. Resource limitation in a competitive context determines complex plant responses to experimental resource additions. Ecology 94, 2505–2517 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  8. 8.

    Schmidt, I. K., Michelsen, A. & Jonasson, S. Effects on plant production after addition of labile carbon to arctic/alpine soils. Oecologia 112, 305–313 (1997).

    Article  PubMed  PubMed Central  Google Scholar 

  9. 9.

    Schmidt, I. K., Michelsen, A. & Jonasson, S. Effects of labile soil carbon on nutrient partitioning between an arctic graminoid and microbes. Oecologia 112, 557–565 (1997).

    Article  PubMed  PubMed Central  Google Scholar 

  10. 10.

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

    Article  CAS  Google Scholar 

  11. 11.

    Wild, B. et al. Amino acid production exceeds plant nitrogen demand in Siberian tundra. Environ. Res. Lett. 13, 034002 (2018).

    Article  CAS  Google Scholar 

  12. 12.

    Manzoni, S., Trofymow, J. A., Jackson, R. B. & Porporato, A. Stoichiometric controls on carbon, nitrogen, and phosphorus dynamics in decomposing litter. Ecol. Monogr. 80, 89–106 (2010).

    Article  Google Scholar 

  13. 13.

    Spohn, M. & Kuzyakov, Y. Phosphorus mineralization can be driven by microbial need for carbon. Soil. Biol. Biochem. 61, 69–75 (2013).

    Article  CAS  Google Scholar 

  14. 14.

    Sakala, W. D., Cadisch, G. & Giller, K. E. Interactions between residues of maize and pigeonpea and mineral N fertilizers during decomposition and N-mineralization. Soil. Biol. Biochem. 32, 679–688 (2000).

    Article  CAS  Google Scholar 

  15. 15.

    Chen, Y. et al. Nitrogen mineralization as a result of phosphorus supplementation in long-term phosphate deficient soil. Appl. Soil Ecol. 106, 24–32 (2016).

    Article  Google Scholar 

  16. 16.

    Brundrett, M. C. Mycorrhizal associations and other means of nutrition of vascular plants: understanding the global diversity of host plants by resolving conflicting information and developing reliable means of diagnosis. Plant Soil 320, 37–77 (2009).

    Article  CAS  Google Scholar 

  17. 17.

    Smith, S. E. & Read, D. J. Mycorrhizal Symbiosis 3rd ed (Academic Press, Cambridge, MA, 2010).

  18. 18.

    Franklin, O. et al. Forests trapped in nitrogen limitation—an ecological market perspective on ectomycorrhizal symbiosis. New Phytol. 203, 657–666 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. 19.

    Ågren, G. I., Wetterstedt, J. Å. & Billberger, M. F. K. Nutrient limitation on terrestrial plant-modeling the interaction between nitrogen and phosphorus. New Phytol. 194, 953–960 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. 20.

    Čapek, P., Kotas, P., Manzoni, S. & Šantrůčková, H. Drivers of phosphorus limitation across soil microbial communities. Funct. Ecol. 30, 1705–1713 (2016).

    Article  Google Scholar 

  21. 21.

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

    Article  Google Scholar 

  22. 22.

    Elser, J. J., Fagan, W. F., Kerkhoff, A. J., Swenson, N. G. & Enquist, B. J. Biological stoichiometry of plant production: metabolism, scaling and ecological response to global change. New Phytol. 186, 593–608 (2010).

    Article  CAS  Google Scholar 

  23. 23.

    Ågren, G. I. The C:N/P stoichiometry of autotrophs—theory and observations. Ecol. Lett. 7, 185–191 (2004).

    Article  Google Scholar 

  24. 24.

    Klausmeier, C. A., Litchman, E., Daufresne, T. & Levin, S. A. Optimal nitrogen-to-phosphorus stoichiometry of phytoplankton. Nature 429, 171–174 (2004).

    Article  CAS  Google Scholar 

  25. 25.

    Minden, V. & Kleyer, M. Internal and external regulation of plant organ stoichiometry. Plant Biol. 16, 897–907 (2014).

    Article  CAS  Google Scholar 

  26. 26.

    Cotner, J. B., Makino, W. & Biddanda, B. A. Temperature affects stoichiometry and biochemical composition of Escherichia coli. Microb. Ecol. 52, 26–33 (2006).

    Article  CAS  Google Scholar 

  27. 27.

    Cherif, M. & Loreau, M. When microbes and consumers determine the limiting nutrient of autotrophs: a theoretical analysis. Proc. Biol. Sci. 276, 487–497 (2009).

    Article  Google Scholar 

  28. 28.

    Yan, Z. B. et al. Effects of nitrogen and phosphorus supply on growth rate, leaf stoichiometry, and nutrient resorption of Arabidopsis thaliana. Plant Soil 388, 147–155 (2015).

    Article  CAS  Google Scholar 

  29. 29.

    Makino, W., Cotner, J. B., Sterner, R. W. & Elser, J. J. Are bacteria more like plants or animals? Growth rate and resource dependence of bacterial C: N: P stoichiometry. Funct. Ecol. 17, 121–130 (2003).

    Article  Google Scholar 

  30. 30.

    Yan, J. et al. The mechanism for exclusion of Pinus massoniana during the succession in subtropical forest ecosystems: light competition or stoichiometric homoeostasis? Sci. Rep. 5, 10994 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. 31.

    Hall, E. K. et al. Linking microbial and ecosystem ecology using ecological stoichiometry: a synthesis of conceptual and empirical approaches. Ecosystems 14, 261–273 (2010).

    Article  Google Scholar 

  32. 32.

    Zechmeister-Boltenstern, S. et al. The application of ecological stoichiometry to plant–microbial–soil organic matter transformations. Ecol. Monogr. 85, 133155 (2015).

    Article  Google Scholar 

  33. 33.

    Güsewell, S., Gessner, M. O., Gusewell, S. & Gessner, M. O. N. P. ratios influence litter decomposition and colonization by fungi and bacteria in microcosms. Funct. Ecol. 23, 211–219 (2009).

    Article  Google Scholar 

  34. 34.

    Demoling, F., Figueroa, D. & Baath, E. Comparison of factors limiting bacterial growth in different soils. Soil. Biol. Biochem. 39, 2485–2495 (2007).

    Article  CAS  Google Scholar 

  35. 35.

    Manzoni, S. et al. Environmental and stoichiometric controls on microbial carbon-use efficiency in soils. New Phytol. 196, 79–91 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. 36.

    Sinsabaugh, R. L., Manzoni, S., Moorhead, D. L., Richter, A. & Elser, J. Carbon use efficiency of microbial communities: stoichiometry, methodology and modelling. Ecol. Lett. 16, 930–939 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  37. 37.

    Doi, H. et al. Integrating elements and energy through the metabolic dependencies of gross growth efficiency and the threshold elemental ratio. Oikos 119, 752–765 (2010).

    Article  CAS  Google Scholar 

  38. 38.

    Isaac, M. E., Hinsinger, P. & Harmand, J. M. Nitrogen and phosphorus economy of a legume tree-cereal intercropping system under controlled conditions. Sci. Total Environ. 434, 71–78 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. 39.

    Augusto, L., Delerue, F., Gallet-Budynek, A. & Achat, D. L. Global assessment of limitation to symbiotic nitrogen fixation by phosphorus availability in terrestrial ecosystems using a meta-analysis approach. Global. Biogeochem. Cycles 27, 804–815 (2013).

    Article  CAS  Google Scholar 

  40. 40.

    Diáková, K. et al. Variation in N2 fixation in subarctic tundra in relation to landscape position and nitrogen pools and fluxes. Arctic Antarct. Alp. Res. 48, 111–125 (2016).

    Article  Google Scholar 

  41. 41.

    Šantrůčková, H., Rejmánková, E., Pivničková, B. & Snyder, J. M. Nutrient enrichment in tropical wetlands: shifts from autotrophic to heterotrophic nitrogen fixation. Biogeochemistry 101, 295–310 (2010).

    Article  CAS  Google Scholar 

  42. 42.

    Lagrange, A., L’Huillier, L. & Amir, H. Mycorrhizal status of Cyperaceae from New Caledonian ultramafic soils: effects of phosphorus availability on arbuscular mycorrhizal colonization of Costularia comosa under field conditions. Mycorrhiza 23, 655–661 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  43. 43.

    Koide, R. T., Huenneke, L. F., Hamburg, S. P. & Mooney, H. A. Effects of applications of fungicide, phosphorus and nitrogen on the structure and productivity of an annual serpentine plant community. Funct. Ecol. 2, 335 (1988).

    Article  Google Scholar 

  44. 44.

    Mooshammer, M. et al. Adjustment of microbial nitrogen use efficiency to carbon: nitrogen imbalances regulates soil nitrogen cycling. Nat. Commun. 5, 3694 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. 45.

    Saggar, S., Parfitt, R. L., Salt, G. & Skinner, M. F. Carbon and phosphorus transformations during decomposition of pine forest floor with different phosphorus status. Biol. Fertil. Soils 27, 197–204 (1998).

    Article  CAS  Google Scholar 

  46. 46.

    Dietrich, K., Spohn, M., Villamagua, M. & Oelmann, Y. Nutrient addition affects net and gross mineralization of phosphorus in the organic layer of a tropical montane forest. Biogeochemistry 136, 223–236 (2017).

    Article  CAS  Google Scholar 

  47. 47.

    Nave, L. E., Vance, E. D., Swanston, C. W. & Curtis, P. S. Impacts of elevated N inputs on north temperate forest soil C storage, C/N, and net N-mineralization. Geoderma 153, 231–240 (2009).

    Article  CAS  Google Scholar 

  48. 48.

    Hatch, D. J., Lovell, R. D., Antil, R. S., Jarvis, S. C. & Owen, P. M. Nitrogen mineralization and microbial activity in permanent pastures amended with nitrogen fertilizer or dung. Biol. Fertil. Soils 30, 288–293 (2000).

    Article  Google Scholar 

  49. 49.

    Johnson, D. W., Edwards, N. T. & Todd, D. E. Nitrogen mineralization, immobilization, and nitrification following urea fertilization of a forest soil under field and laboratory conditions. Soil Sci. Soc. Am. J. 44, 610 (1980).

    Article  CAS  Google Scholar 

  50. 50.

    Adams, M. A. & Attiwill, P. M. Patterns of nitrogen mineralization in 23-year old pine forest following nitrogen fertilizing. For. Ecol. Manage. 7, 241–248 (1984).

    Article  Google Scholar 

  51. 51.

    Marklein, A. R. & Houlton, B. Z. Nitrogen inputs accelerate phosphorus cycling rates across a wide variety of terrestrial ecosystems. New Phytol. 193, 696–704 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. 52.

    Feller, I. C., McKee, K. L., Whigham, D. F. & O’Neill, J. P. Nitrogen vs. phosphorus limitation across an ecotonal gradient in a mangrove forest. Biogeochemistry 62, 145–175 (2003).

    Article  CAS  Google Scholar 

  53. 53.

    Keuskamp, J. A., Feller, I. C., Laanbroek, H. J., Verhoeven, J. T. A. & Hefting, M. M. Short- and long-term effects of nutrient enrichment on microbial exoenzyme activity in mangrove peat. Soil. Biol. Biochem. 81, 38–47 (2015).

    Article  CAS  Google Scholar 

  54. 54.

    Watanabe, T., Urayama, M., Shinano, T., Okada, R. & Osaki, M. Application of ionomics to plant and soil in fields under long-term fertilizer trials. + 4, 781 (2015).

    PubMed  PubMed Central  Google Scholar 

  55. 55.

    Chang, Y. et al. Nutrients resorption and stoichiometry characteristics of different-aged plantations of Larix kaempferi in the Qinling Mountains, central China. PLoS ONE 12, e0189424 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. 56.

    Kulaev, I., Vagabov, V. & Kulakovskaya, T. New aspects of inorganic polyphosphate metabolism and function. J. Biosci. Bioeng. 88, 111–129 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. 57.

    Xu, X. et al. Convergence of microbial assimilations of soil carbon, nitrogen, phosphorus, and sulfur in terrestrial ecosystems. Sci. Rep. 5, 17445 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. 58.

    Manzoni, S. et al. Optimal metabolic regulation along resource stoichiometry gradients. Ecol. Lett. 20, 1182–1191 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  59. 59.

    Olde Venterink, H. Productivity increase upon supply of multiple nutrients in fertilization experiments; co-limitation or chemical facilitation? Plant Soil 408, 515–518 (2016).

    Article  CAS  Google Scholar 

  60. 60.

    Bracken, M. E. S. et al. Signatures of nutrient limitation and co-limitation: responses of autotroph internal nutrient concentrations to nitrogen and phosphorus additions. Oikos 124, 113–121 (2015).

    Article  CAS  Google Scholar 

  61. 61.

    Dutta, P. S., Kooi, B. W. & Feudel, U. Multiple resource limitation: nonequilibrium coexistence of species in a competition model using a synthesizing unit. Theor. Ecol. 7, 407–421 (2014).

    Article  Google Scholar 

  62. 62.

    Xu, X. F., Thornton, P. E. & Post, W. M. A global analysis of soil microbial biomass carbon, nitrogen and phosphorus in terrestrial ecosystems. Glob. Ecol. Biogeogr. 22, 737–749 (2013).

    Article  Google Scholar 

  63. 63.

    Wassen, M., Van Der Vliet, R. & Verhoeven, J. Nutrient limitation in the Biebrza fens and floodplain (Poland). ACTA Bot. Neerl. 47, 241–253 (1998).

    Google Scholar 

  64. 64.

    Wright, S. J. et al. Potassium, phosphorus, or nitrogen limit root allocation, tree growth, or litter production in a lowland tropical forest. Ecology 92, 161–1625 (2011).

    Article  Google Scholar 

  65. 65.

    Campo, J. & Vázquez-Yanes, C. Effects of nutrient limitation on above-ground carbon dynamics during tropical dry forest regeneration in Yucatán, Mexico. Ecosystems 7, 311–319 (2004).

    Article  CAS  Google Scholar 

  66. 66.

    Santiago, L. S. et al. Tropical tree seedling growth responses to nitrogen, phosphorus and potassium addition. J. Ecol. 100, 309–316 (2012).

    Article  CAS  Google Scholar 

  67. 67.

    Carpenter, A. T., Moore, J. C., Redente, E. F. & Stark, J. C. Plant community dynamics in a semi-arid ecosystem in relation to nutrient addition following a major disturbance. Plant Soil 126, 91–99 (1990).

    Article  CAS  Google Scholar 

  68. 68.

    Vitousek, P. M., Walker, L. R., Whiteaker, L. D. & Matson, P. A. Nutrient limitations to plant growth during primary succession in Hawaii Volcanoes National Park. Biogeochemistry 23, 197–215 (1993).

    Article  Google Scholar 

  69. 69.

    Batterman, S. A., Wurzburger, N. & Hedin, L. O. Nitrogen and phosphorus interact to control tropical symbiotic N2 fixation: a test in Inga punctata. J. Ecol. 101, 1400–1408 (2013).

    Article  CAS  Google Scholar 

  70. 70.

    Limpens, J., Berendse, F. & Klees, H. How phosphorus availability affects the impact of nitrogen deposition on sphagnum and vascular plants in bogs. Ecosystems 7, 793–804 (2004).

    Article  CAS  Google Scholar 

  71. 71.

    Zamin, T. J., Bret-Harte, M. S. & Grogan, P. Evergreen shrubs dominate responses to experimental summer warming and fertilization in Canadian mesic low arctic tundra. J. Ecol. 102, 749–766 (2014).

    Article  Google Scholar 

  72. 72.

    Lammerts, E. J., Pegtel, D. M., Grootjans, A. P. & van der Veen, A. Nutrient limitation and vegetation changes in a coastal dune slack. J. Veg. Sci. 10, 111–122 (1999).

    Article  Google Scholar 

  73. 73.

    Zhu, F., Lu, X., Mo, J. & EJ, P. Phosphorus limitation on photosynthesis of two dominant understory species in a lowland tropical forest. J. Plant Ecol. 7, 526–534 (2014).

    Article  Google Scholar 

  74. 74.

    Vitousek, P. M. & Farrington, H. Nutrient limitation and soil development: experimental test of a biogeochemical theory. Biogeochemistry 37, 63–75 (1997).

    Article  CAS  Google Scholar 

  75. 75.

    Augustine, D. J., McNaughton, S. J. & Frank, D. A. Feedbacks between soil nutrients and large herbivors in a managed savanna ecosystem. Ecol. Appl. 13, 1325–1337 (2003).

    Article  Google Scholar 

  76. 76.

    Alvarez, R., Santanatoglia, O. J. & Garcia, R. Effect of temperature on soil microbial biomass and its metabolic quotient in situ under different tillage systems. Biol. Fertil. Soils 19, 227–230 (1995).

    Article  Google Scholar 

  77. 77.

    Chen, F. -S., Zeng, D. -H., Fahey, T. J., Yao, C. -Y. & Yu, Z. -Y. Response of leaf anatomy of Chenopodium acuminatum to soil resource availability in a semi-arid grassland. Plant Ecol. 209, 375–382 (2010).

    Article  Google Scholar 

  78. 78.

    Mayor, J. R., Mack, M. C. & Schuur, E. A. G. Decoupled stoichiometric, isotopic, and fungal responses of an ectomycorrhizal black spruce forest to nitrogen and phosphorus additions. Soil. Biol. Biochem. 88, 247–256 (2015).

    Article  CAS  Google Scholar 

  79. 79.

    Van Duren, I. C., Boeye, D. & Grootjans, A. P. Nutrient limitations in an extant and drained poor fen: implications for restoration. Plant Ecol. 133, 91–100 (1997).

    Article  Google Scholar 

  80. 80.

    Haag, R. W. Nutrient limitations to plant production in two tundra communities. Can. J. Bot. 52, 103–116 (1974).

    Article  CAS  Google Scholar 

  81. 81.

    Sundqvist, M. K., Liu, Z., Giesler, R. & Wardle, D. A. Plant and microbial responses to nitrogen and phosphorus addition across an elevational gradient in subarctic tundra. Ecology 95, 1819–1835 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  82. 82.

    van der Hoek, D., van Mierlo Anita, J. E. M. & van Groenendael, J. M. Nutrient limitation and nutrient-driven shifts in plant species composition in a species-rich fen meadow. J. Veg. Sci. 15, 389–396 (2004).

    Article  Google Scholar 

  83. 83.

    Bowman, W. D., Theodose, T. A., Schardt, J. C. & Conant, R. T. Constraints of nutrient availability on primary production in two alpine tundra communities. Ecology 74, 2085–2097 (1993).

    Article  Google Scholar 

  84. 84.

    Davidson, E. A. et al. Nitrogen and phosphorus limitation of biomass growth in a tropical secondary forest. Ecol. Appl. 14, 150–163 (2004).

    Article  Google Scholar 

  85. 85.

    Güsewell, S., Koerselman, W. & Verhoeven, J. T. A. Time-dependent effects of fertilization on plant biomass in floating fens. J. Veg. Sci. 13, 705–718 (2002).

    Article  Google Scholar 

  86. 86.

    Ngai, J. T. & Jefferies, R. L. Nutrient limitation of plant growth and forage quality in Arctic coastal marshes. J. Ecol. 92, 1001–1010 (2004).

    Article  Google Scholar 

  87. 87.

    Potthast, K., Hamer, U. & Makeschin, F. In an Ecuadorian pasture soil the growth of Setaria sphacelata, but not of soil microorganisms, is co-limited by N and P. Appl. Soil Ecol. 62, 103–114 (2012).

    Article  Google Scholar 

  88. 88.

    Johnson, N. C., Wilson, G. W. T., Wilson, J. A., Miller, R. M. & Bowker, M. A. Mycorrhizal phenotypes and the Law of the Minimum. New Phytol. 205, 1473–1484 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. 89.

    Barger, N. N., D’Antonio, C. M., Ghneim, T., Brink, K. & Cuevas, E. Nutrient limitation to primary productivity in a secondary savanna in Venezuela. Biotropica 34, 493 (2002).

    Article  Google Scholar 

  90. 90.

    Soudzilovskaia, N. A., Onipchenko, V. G., Cornelissen, J. H. C. & Aerts, R. Biomass production, N/P ratio and nutrient limitation in a Caucasian alpine tundra plant community. J. Veg. Sci. 16, 399–406 (2005).

    Article  Google Scholar 

  91. 91.

    Gill, R. A. et al. Linking community and ecosystem development on Mount St Helens. Oecologia 148, 312–324 (2006).

    Article  Google Scholar 

  92. 92.

    Craine, J. M., Morrow, C. & Stock, W. D. Nutrient concentration ratios and co-limitation in South African grasslands. New Phytol. 179, 829–836 (2008).

    Article  CAS  Google Scholar 

  93. 93.

    von Oheimb, G. et al. N/P ratio and the nature of nutrient limitation in Calluna-dominated heathlands. Ecosystems 13, 317–327 (2010).

    Article  CAS  Google Scholar 

  94. 94.

    Iversen, C. M., Bridgham, S. D. & Kellogg, L. E. Scaling plant nitrogen use and uptake efficiencies in response to nutrient addition in peatlands. Ecology 91, 693–707 (2010).

    Article  Google Scholar 

  95. 95.

    Laliberté, E. et al. Experimental assessment of nutrient limitation along a 2-million-year dune chronosequence in the south-western Australia biodiversity hotspot. J. Ecol. 100, 631–642 (2012).

    Article  CAS  Google Scholar 

  96. 96.

    Onipchenko, V. G. et al. Alpine plant functional group responses to fertiliser addition depend on abiotic regime and community composition. Plant Soil 357, 103–115 (2012).

    Article  CAS  Google Scholar 

  97. 97.

    Fisher, J. B. et al. Nutrient limitation in rainforests and cloud forests along a 3,000-m elevation gradient in the Peruvian Andes. Oecologia. 172, 889–902 (2013).

    Article  Google Scholar 

  98. 98.

    Cusell, C., Kooijman, A. & Lamers, L. P. M. Nitrogen or phosphorus limitation in rich fens? Edaphic differences explain contrasting results in vegetation development after fertilization. Plant Soil 384, 153–168 (2014).

    Article  CAS  Google Scholar 

  99. 99.

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

    Article  CAS  Google Scholar 

  100. 100.

    Tischer, A. et al. Above- and below-ground linkages of a nitrogen and phosphorus co-limited tropical mountain pasture system—responses to nutrient enrichment. Plant Soil 391, 333–352 (2015).

    Article  CAS  Google Scholar 

  101. 101.

    He, M. & Dijkstra, F. A. Phosphorus addition enhances loss of nitrogen in a phosphorus-poor soil. Soil. Biol. Biochem. 82, 99–106 (2015).

    Article  CAS  Google Scholar 

  102. 102.

    Chen, F. -S. et al. Nitrogen and phosphorus additions alter nutrient dynamics but not resorption efficiencies of Chinese fir leaves and twigs differing in age. Tree. Physiol. 35, 1106–1117 (2015).

    Article  CAS  Google Scholar 

  103. 103.

    Alvarez-Clare, S. & Mack, M. C. Do foliar, litter, and root nitrogen and phosphorus concentrations reflect nutrient limitation in a lowland tropical wet forest? PLoS ONE 10, e0123796 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. 104.

    Homeier, J. et al. Tropical Andean forests are highly susceptible to nutrient inputs—rapid effects of experimental N and P addition to an Ecuadorian montane forest. PLoS ONE 7, e47128 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. 105.

    Dai, X., Ouyang, Z., Li, Y. & Wang, H. Variation in yield gap induced by nitrogen, phosphorus and potassium fertilizer in North China Plain. PLoS ONE 8, e82147 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. 106.

    R Development Core Team, R. & R Core Team. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. 1, 409 (2014).

  107. 107.

    Poisot, T. The digitize package: extracting numerical data from scatterplots. R J. 3, 25–26 (2011).

    Article  Google Scholar 

  108. 108.

    Maherali, H., Oberle, B., Stevens, P. F., Cornwell, W. K. & McGlinn, D. J. Mutualism persistence and abandonment during the evolution of the mycorrhizal symbiosis. Am. Nat. 188, E113–E125 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  109. 109.

    Viechtbauer, W. Conducting meta-analyses in R with the metafor. J. Stat. Softw. 36, 1–48 (2010).

    Article  Google Scholar 

  110. 110.

    Del Re, A. C. & Hoyt, W. T. MAd: meta-analysis with mean differences v.0.8-2 (CRAN, 2014);

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This study was supported by the International Program CryoCARB (MSM 7E10073—CryoCARB, Austrian Science Fund (FWF): I370-B17, German Federal Ministry of Education and Research (03F0616A)), project no. GA17-15229S and the SoWa Research Infrastructure funded by MEYS CZ grants LM2015075 and EF16_013/0001782—SoWa Ecosystems Research. S.M. acknowledges support from the Swedish Research Councils, Formas (2015-468) and VR (2016-04146) and the Bolin Centre for Climate Research. J.B., T.U. and H.S. were also supported by Czech Science Foundation project no. 16-18453 S. G.H. acknowledges the Joint Partnership Initiative project COUP and the Swedish Research Council grant no. E0689701 and the project CryoN funded by Academy of Finland (no. 132045). P.C. would also like to thank TES program of the U.S. Department of Energy (DOE) Office of Science, Biological and Environmental Research (BER) for partial support at Pacific Northwest National Laboratory (PNNL). PNNL is operated by Battelle for DOE. X. Xu kindly shared his dataset on microbial biomass elemental composition. We also thank N. Hess and B. Bond-Lamberty for comments and language corrections to this manuscript.

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P.C. collected data for meta-analysis and wrote the manuscript. P.C., S.M. and H.S. developed the conceptual framework. Other co-authors conducted a thorough critical review of the manuscript and contributed to manuscript writing.

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Correspondence to Petr Čapek.

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Supplementary information

Supplementary Table 1

List of studies used in the meta-analysis with corresponding variables extracted from each study (ecosystem type, measured plant characteristic, soil N/P and C/N ratio, microbial critical N/P and C/N ratio, plant critical N/P ratio and dominant plant–microbe relationship).

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Statistical meta-analysis

Step-by-step statistical meta-analysis with detailed additional information.

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Čapek, P., Manzoni, S., Kaštovská, E. et al. A plant–microbe interaction framework explaining nutrient effects on primary production. Nat Ecol Evol 2, 1588–1596 (2018).

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