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Nitrogen transformations in modern agriculture and the role of biological nitrification inhibition

Abstract

The nitrogen (N)-use efficiency of agricultural plants is notoriously poor. Globally, about 50% of the N fertilizer applied to cropping systems is not absorbed by plants, but lost to the environment as ammonia (NH3), nitrate (NO3), and nitrous oxide (N2O, a greenhouse gas with 300 times the heat-trapping capacity of carbon dioxide), raising agricultural production costs and contributing to pollution and climate change. These losses are driven by volatilization of NH3 and by a matrix of nitrification and denitrification reactions catalysed by soil microorganisms (chiefly bacteria and archaea). Here, we discuss mitigation of the harmful and wasteful process of agricultural N loss via biological nitrification inhibitors (BNIs) exuded by plant roots. We examine key recent discoveries in the emerging field of BNI research, focusing on BNI compounds and their specificity and transport, and discuss prospects for their role in improving agriculture while reducing its environmental impact.

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Figure 1: Nitrogen budgets of the ‘big three’ crops.
Figure 2: Schematic overview of the fate of nitrogen fertilizers applied to agricultural systems.
Figure 3: BNIs from root exudates and their enzyme targets.
Figure 4: Zonation and mechanisms of BNI root exudation.

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References

  1. Godfray, H. C. J. et al. Food security: the challenge of feeding 9 billion people. Science 327, 812–818 (2010).

    Article  CAS  PubMed  Google Scholar 

  2. Fowler, D. et al. The global nitrogen cycle in the twenty-first century. Phil. Trans. Roy. Soc. B. 368, 20130164 (2013).

    Article  CAS  Google Scholar 

  3. Galloway, J. N. et al. Transformation of the nitrogen cycle: recent trends, questions, and potential solutions. Science 320, 889–892 (2008).

    Article  CAS  PubMed  Google Scholar 

  4. Erisman, J. W., Sutton, M. A., Galloway, J., Klimont, Z. & Winiwarter, W. How a century of ammonia synthesis changed the world. Nat. Geosci. 1, 636–639 (2008).

    Article  CAS  Google Scholar 

  5. Cassman, K. G., Dobermann, A. & Walters, D. T. Agroecosystems, nitrogen-use efficiency, and nitrogen management. Ambio 31, 132–140 (2002).

    Article  PubMed  Google Scholar 

  6. Ladha, J. K., Pathak, H., Krupnik, T. J., Six, J. & van Kessel, C. Efficiency of fertilizer nitrogen in cereal production: retrospects and prospects. Adv. Agron. 87, 85–156 (2005).

  7. Erisman, J. W., Galloway, J., Seitzinger, S., Bleeker, A. & Butterbach-Bahl, K. Reactive nitrogen in the environment and its effect on climate change. Curr. Opin. Environ. Sustain. 3, 281–290 (2011).

    Article  Google Scholar 

  8. Schlesinger, W. H. On the fate of anthropogenic nitrogen. Proc. Natl Acad. Sci. USA 106, 203–208 (2009).

    Article  CAS  PubMed  Google Scholar 

  9. Tilman, D. & Isbell, F. Biodiversity: recovery as nitrogen declines. Nature 528, 336–337 (2015).

    Article  CAS  PubMed  Google Scholar 

  10. Vitousek, P. M. et al. Human alteration of the global nitrogen cycle: sources and consequences. Ecol. Appl. 7, 737–750 (1997).

    Google Scholar 

  11. Townsend, A. R. et al. Human health effects of a changing global nitrogen cycle. Front. Ecol. Environ. 1, 240–246 (2003).

    Article  Google Scholar 

  12. Ravishankara, A. R., Daniel, J. S. & Portmann, R. W. Nitrous oxide (N2O): the dominant ozone-depleting substance emitted in the 21st century. Science 326, 123–125 (2009).

    Article  CAS  PubMed  Google Scholar 

  13. Chen, A. Q. et al. Characteristics of ammonia volatilization on rice grown under different nitrogen application rates and its quantitative predictions in Erhai Lake Watershed, China. Nutr. Cycl. Agroecosys. 101, 139–152 (2015).

    Article  CAS  Google Scholar 

  14. Kowalchuk, G. A. & Stephen, J. R. Ammonia-oxidizing bacteria: a model for molecular microbial ecology. Ann. Rev. Microbiol. 55, 485–529 (2001).

    Article  CAS  Google Scholar 

  15. Daims, H., Lucker, S. & Wagner, M. A new perspective on microbes formerly known as nitrite-oxidizing bacteria. Trends Microbiol. 24, 699–712 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Hayatsu, M., Tago, K. & Saito, M. Various players in the nitrogen cycle: diversity and functions of the microorganisms involved in nitrification and denitrification. Soil Sci. Plant Nutr. 54, 33–45 (2008).

    Article  CAS  Google Scholar 

  17. Prosser, J. I. & Nicol, G. W. Archaeal and bacterial ammonia-oxidisers in soil: the quest for niche specialisation and differentiation. Trends Microbiol. 20, 523–531 (2012).

    Article  CAS  PubMed  Google Scholar 

  18. Daims, H. et al. Complete nitrification by Nitrospira bacteria. Nature 528, 504–509 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. van Kessel, M. et al. Complete nitrification by a single microorganism. Nature 528, 555–559 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Jia, Z. & Conrad, R. Bacteria rather than archaea dominate microbial ammonia oxidation in an agricultural soil. Environ. Microbiol. 11, 1658–1671 (2009).

    Article  CAS  PubMed  Google Scholar 

  21. Leininger, S. et al. Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 442, 806–809 (2006).

    Article  CAS  PubMed  Google Scholar 

  22. Thion, C. E. et al. Plant nitrogen-use strategy as a driver of rhizosphere archaeal and bacterial ammonia oxidiser abundance. FEMS Microbiol. Ecol. 92, fiw091 (2016).

    Article  CAS  PubMed  Google Scholar 

  23. Venter, J. C. et al. Environmental genome shotgun sequencing of the Sargasso Sea. Science 304, 66–74 (2004).

    Article  CAS  PubMed  Google Scholar 

  24. Woese, C. R. & Fox, G. E. Phylogenetic structure of prokaryotic domain – primary kingdoms. Proc. Natl Acad. Sci. USA 74, 5088–5090 (1977).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Hatzenpichler, R. Diversity, physiology, and niche differentiation of ammonia-oxidizing archaea. Appl. Environ. Microbiol. 78, 7501–7510 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Hu, H. W., Xu, Z. H. & He, J. Z. Ammonia-oxidizing archaea play a predominant role in acid soil nitrification. Adv. Agron. 125, 261–302 (2014).

    Article  Google Scholar 

  27. Halvorson, A. D., Snyder, C. S., Blaylock, A. D. & Del Grosso, S. J. Enhanced-efficiency nitrogen fertilizers: potential role in nitrous oxide emission mitigation. Agron. J. 106, 715–722 (2014).

    Article  CAS  Google Scholar 

  28. Pan, B. B., Lam, S. K., Mosier, A., Luo, Y. Q. & Chen, D. L. Ammonia volatilization from synthetic fertilizers and its mitigation strategies: a global synthesis. Agri. Ecosys. Environ. 232, 283–289 (2016).

    Article  CAS  Google Scholar 

  29. Lin, B.-L., Sakoda, A., Shibasaki, R. & Suzuki, M. A modelling approach to global nitrate leaching caused by anthropogenic fertilisation. Water Res. 35, 1961–1968 (2001).

    Article  CAS  PubMed  Google Scholar 

  30. Di, H. J. & Cameron, K. C. Nitrate leaching in temperate agroecosystems: sources, factors and mitigating strategies. Nutr. Cycl. Agroecosys. 64, 237–256 (2002).

    Article  CAS  Google Scholar 

  31. Seitzinger, S. et al. Denitrification across landscapes and waterscapes: a synthesis. Ecol. Appl. 16, 2064–2090 (2006).

    Article  CAS  PubMed  Google Scholar 

  32. Forster, P. et al. in Climate Change 2007: The Physical Science Basis (eds Solomon, S. et. al) ch. 2, 129–234 (Cambridge Univ. Press, 2007).

    Google Scholar 

  33. Linquist, B., van Groenigen, K. J., Adviento-Borbe, M. A., Pittelkow, C. & van Kessel, C. An agronomic assessment of greenhouse gas emissions from major cereal crops. Glob. Change Biol. 18, 194–209 (2012).

    Article  Google Scholar 

  34. Turner, P. A. et al. Indirect nitrous oxide emissions from streams within the US corn belt scale with stream order. Proc. Natl Acad. Sci. USA 112, 9839–9843 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Kool, D. M., Dolfing, J., Wrage, N. & Van Groenigen, J. W. Nitrifier denitrification as a distinct and significant source of nitrous oxide from soil. Soil Biol. Biochem. 43, 174–178 (2011).

    Article  CAS  Google Scholar 

  36. Liu, R. et al. Nitrification is a primary driver of nitrous oxide production in laboratory microcosms from different land-use soils. Front. Microbiol. 7, 1373 (2016).

  37. Reay, D. S. et al. Global agriculture and nitrous oxide emissions. Nat. Clim. Change 2, 410–416 (2012).

    Article  CAS  Google Scholar 

  38. Smith, P. et al. in Climate change 2007: Mitigation: Contribution of Working Group III to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change ( eds Metz, B., Davidson, O. R., Bosch, P. R., Dave, R. & Meyer, L. A. ) Ch. 8, 497–540 (Cambridge Univ. Press, 2007).

    Google Scholar 

  39. Prasad, R. & Power, J. Nitrification inhibitors for agriculture, health, and the environment. Adv. Agron. 54, 233–281 (1995).

    Article  CAS  Google Scholar 

  40. Abalos, D., Jeffery, S., Sanz-Cobena, A., Guardia, G. & Vallejo, A. Meta-analysis of the effect of urease and nitrification inhibitors on crop productivity and nitrogen use efficiency. Agri. Ecosys. Environ. 189, 136–144 (2014).

    Article  CAS  Google Scholar 

  41. Qiu, H., Sun, D., Gunatilake, S. R., She, J. & Mlsna, T. E. Analysis of trace dicyandiamide in stream water using solid phase extraction and liquid chromatography UV spectrometry. J. Environ. Sci. 35, 38–42 (2015).

    Article  CAS  Google Scholar 

  42. Fillery, I. R. Plant-based manipulation of nitrification in soil: a new approach to managing N loss? Plant Soil 294, 1–4 (2007).

    Article  CAS  Google Scholar 

  43. Subbarao, G. V. et al. Scope and strategies for regulation of nitrification in agricultural systems — challenges and opportunities. Crit. Rev. Plant Sci. 25, 303–335 (2006).

    Article  CAS  Google Scholar 

  44. Akiyama, H., Yan, X. & Yagi, K. Evaluation of effectiveness of enhanced-efficiency fertilizers as mitigation options for N2O and NO emissions from agricultural soils: meta-analysis. Glob. Change Biol. 16, 1837–1846 (2010).

    Article  Google Scholar 

  45. Wedin, D. A. & Tilman, D. Species effects on nitrogen cycling: a test with perennial grasses. Oecologia 84, 433–441 (1990).

    Article  PubMed  Google Scholar 

  46. Bardgett, R. D., Mommer, L. & De Vries, F. T. Going underground: root traits as drivers of ecosystem processes. Trends Ecol. Evol. 29, 692–699 (2014).

    Article  PubMed  Google Scholar 

  47. Rice, E. L. & Pancholy, S. K. Inhibition of nitrification by climax ecosystems. III. Inhibitors other than tannins. Am. J. Bot. 61, 1095–1103 (1974).

    Article  CAS  Google Scholar 

  48. Basaraba, J. Influence of vegetable tannins on nitrification in soil. Plant Soil 21, 8–16 (1964).

    Article  Google Scholar 

  49. Subbarao, G. et al. A bioluminescence assay to detect nitrification inhibitors released from plant roots: a case study with Brachiaria humidicola. Plant Soil 288, 101–112 (2006).

    Article  CAS  Google Scholar 

  50. Subbarao, G. V. et al. Evidence for biological nitrification inhibition in Brachiaria pastures. Proc. Natl Acad. Sci. USA 106, 17302–17307 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Rice, E. L. & Pancholy, S. K. Inhibition of nitrification by climax ecosystems. Am. J. Bot. 59, 1033–1040 (1972).

    Article  Google Scholar 

  52. Britto, D. T. & Kronzucker, H. J. Ecological significance and complexity of N-source preference in plants. Ann. Bot. 112, 957–963 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Lata, J. C. et al. Grass populations control nitrification in savanna soils. Funct. Ecol. 18, 605–611 (2004).

    Article  Google Scholar 

  54. Boudsocq, S., Lata, J. C., Mathieu, J., Abbadie, L. & Barot, S. Modelling approach to analyse the effects of nitrification inhibition on primary production. Funct. Ecol. 23, 220–230 (2009).

    Article  Google Scholar 

  55. Sylvester-Bradley, R., Mosquera, D. & Mendez, J. E. Inhibition of nitrate accumulation in tropical grassland soils – effect of nitrogen-fertilization and soil disturbance. J. Soil Sci. 39, 407–416 (1988).

    Article  CAS  Google Scholar 

  56. Ishikawa, T., Subbarao, G. V., Ito, O. & Okada, K. Suppression of nitrification and nitrous oxide emission by the tropical grass Brachiaria humidicola. Plant Soil 255, 413–419 (2003).

    Article  CAS  Google Scholar 

  57. Gopalakrishnan, S. et al. Nitrification inhibitors from the root tissues of Brachiaria humidicola, a tropical grass. J. Agri. Food Chem. 55, 1385–1388 (2007).

    Article  CAS  Google Scholar 

  58. Iizumi, T., Mizumoto, M. & Nakamura, K. A bioluminescence assay using Nitrosomonas europaea for rapid and sensitive detection of nitrification inhibitors. Appl. Environ. Microbiol. 64, 3656–3662 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  59. Nardi, P., Akutsu, M., Pariasca-Tanaka, J. & Wissuwa, M. Effect of methyl 3-4-hydroxyphenyl propionate, a sorghum root exudate, on N dynamic, potential nitrification activity and abundance of ammonia-oxidizing bacteria and archaea. Plant Soil 367, 627–637 (2013).

    Article  CAS  Google Scholar 

  60. Subbarao, G. V. et al. Biological nitrification inhibition (BNI) activity in sorghum and its characterization. Plant Soil 366, 243–259 (2013).

    Article  CAS  Google Scholar 

  61. Zakir, H. et al. Detection, isolation and characterization of a root-exuded compound, methyl 3-(4-hydroxyphenyl) propionate, responsible for biological nitrification inhibition by sorghum (Sorghum bicolor). New Phytol. 180, 442–451 (2008).

    Article  CAS  PubMed  Google Scholar 

  62. Subbarao, G. V. et al. Biological nitrification inhibition (BNI) – is it a widespread phenomenon? Plant Soil 294, 5–18 (2007).

    Article  CAS  Google Scholar 

  63. de Boer, A. H. & de Vries- van Leeuwen, I. J. Fusicoccanes: diterpenes with surprising biological functions. Trends Plant Sci. 17, 360–368 (2012).

    Article  CAS  PubMed  Google Scholar 

  64. Sun, L., Lu, Y. F., Yu, F. W., Kronzucker, H. J. & Shi, W. M. Biological nitrification inhibition by rice root exudates and its relationship with nitrogen-use efficiency. New Phytol. 212, 646–656 (2016).

    Article  CAS  PubMed  Google Scholar 

  65. Subbarao, G. V. et al. Can biological nitrification inhibition (BNI) genes from perennial Leymus racemosus (Triticeae) combat nitrification in wheat farming? Plant Soil 299, 55–64 (2007).

    Article  CAS  Google Scholar 

  66. Subbarao, G. V. et al. Biological nitrification inhibition (BNI) – is there potential for genetic interventions in the Triticeae? Breed. Sci. 59, 529–545 (2009).

    Article  CAS  Google Scholar 

  67. O'sullivan, C. A., Fillery, I. R. P., Roper, M. M. & Richards, R. A. Identification of several wheat landraces with biological nitrification inhibition capacity. Plant Soil 404, 61–74 (2016).

    Article  CAS  Google Scholar 

  68. Tanaka, J. P., Nardi, P. & Wissuwa, M. Nitrification inhibition activity, a novel trait in root exudates of rice. AoB Plants 2010, plq014 (2010).

    Google Scholar 

  69. White, C. S. Nitrification inhibition by monoterpenoids – theoretical mode of action based on molecular structures. Ecology 69, 1631–1633 (1988).

    Article  CAS  Google Scholar 

  70. McConn, M. & Browse, J. The critical requirement for linolenic acid is pollen development, not photosynthesis, in an Arabidopsis mutant. Plant Cell 8, 403–416 (1996).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Dayan, F. E. et al. Sorgoleone. Phytochem. 71, 1032–1039 (2010).

    Article  CAS  Google Scholar 

  72. Kodama, O., Miyakawa, J., Akatsuka, T. & Kiyosawa, S. Sakuranetin, a flavanone phytoalexin from ultraviolet-irradiated rice leaves. Phytochem. 31, 3807–3809 (1992).

    Article  CAS  Google Scholar 

  73. Liu, Y. et al. The nitrification inhibitor methyl 3-(4-hydroxyphenyl) propionate modulates root development by interfering with auxin signaling via the NO/ROS pathway. Plant Physiol. 171, 1686–1703 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. McCarty, G. W. Modes of action of nitrification inhibitors. Biol. Fert. Soils 29, 1–9 (1999).

    Article  CAS  Google Scholar 

  75. Subbarao, G. V., Wang, H. Y., Ito, O., Nakahara, K. & Berry, W. L. NH4+ triggers the synthesis and release of biological nitrification inhibition compounds in Brachiaria humidicola roots. Plant Soil 290, 245–257 (2007).

    Article  CAS  Google Scholar 

  76. Zeng, H. Q., Di, T. J., Zhu, Y. Y. & Subbarao, G. V. Transcriptional response of plasma membrane H+-ATPase genes to ammonium nutrition and its functional link to the release of biological nitrification inhibitors from sorghum roots. Plant Soil 398, 301–312 (2016).

    Article  CAS  Google Scholar 

  77. Zhu, Y. Y., Zeng, H. Q., Shen, Q. R., Ishikawa, T. & Subbarao, G. V. Interplay among NH4+ uptake, rhizosphere pH and plasma membrane H+-ATPase determine the release of BNIs in sorghum roots - possible mechanisms and underlying hypothesis. Plant Soil 358, 125–135 (2012).

    Article  CAS  Google Scholar 

  78. Lima, J. E., Kojima, S., Takahashi, H. & von Wiren, N. Ammonium triggers lateral root branching in Arabidopsis in an AMMONIUM TRANSPORTER1;3-dependent manner. Plant Cell 22, 3621–3633 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Badri, D. V. & Vivanco, J. M. Regulation and function of root exudates. Plant Cell Environ. 32, 666–681 (2009).

    Article  CAS  PubMed  Google Scholar 

  80. Weston, L. A., Ryan, P. R. & Watt, M. Mechanisms for cellular transport and release of allelochemicals from plant roots into the rhizosphere. J. Exp. Bot. 63, 3445–3454 (2012).

    Article  CAS  PubMed  Google Scholar 

  81. Wang, M. Y., Glass, A. D. M., Shaff, J. E. & Kochian, L. V. Ammonium uptake by rice roots (III. Electrophysiology). Plant Physiol. 104, 899–906 (1994).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Britto, D. T., Siddiqi, M. Y., Glass, A. D. M. & Kronzucker, H. J. Futile transmembrane NH4+ cycling: a cellular hypothesis to explain ammonium toxicity in plants. Proc. Natl Acad. Sci. USA 98, 4255–4258 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Subbarao, G. V. et al. Suppression of soil nitrification by plants. Plant Sci. 233, 155–164 (2015).

    Article  CAS  PubMed  Google Scholar 

  84. Marre, E. Fusicoccin: a tool in plant physiology. Ann. Rev. Plant Physiol. Plant Molec. Biol. 30, 273–288 (1979).

    Article  CAS  Google Scholar 

  85. Ullrich-Eberius, C. I., Sanz, A. & Novacky, A. J. Evaluation of arsenate-associated and vanadate-associated changes of electrical membrane potential and phosphate transport in Lemna gibba G1. J. Exp. Bot. 40, 119–128 (1989).

    Article  CAS  Google Scholar 

  86. Cesco, S., Neumann, G., Tomasi, N., Pinton, R. & Weisskopf, L. Release of plant-borne flavonoids into the rhizosphere and their role in plant nutrition. Plant Soil 329, 1–25 (2010).

    Article  CAS  Google Scholar 

  87. Rea, P. A. Plant ATP-binding cassette transporters. Ann. Rev. Plant Biol. 58, 347–375 (2007).

    Article  CAS  Google Scholar 

  88. Ryan, P. R., Delhaize, E. & Jones, D. L. Function and mechanism of organic anion exudation from plant roots. Ann. Rev. Plant Physiol. Plant Molec. Biol. 52, 527–560 (2001).

    Article  CAS  Google Scholar 

  89. Kochian, L. V., Pineros, M. A., Liu, J. P. & Magalhaes, J. V. Plant adaptation to acid soils: the molecular basis for crop aluminum resistance. Ann. Rev. Plant Biol. 66, 571–598 (2015).

    Article  CAS  Google Scholar 

  90. Bashir, K. et al. Rice phenolics efflux transporter 2 (PEZ2) plays an important role in solubilizing apoplasmic iron. Soil Sci. Plant Nutr. 57, 803–812 (2011).

    Article  CAS  Google Scholar 

  91. Walker, T. S., Bais, H. P., Grotewold, E. & Vivanco, J. M. Root exudation and rhizosphere biology. Plant Physiol. 132, 44–51 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Bertin, C., Yang, X. H. & Weston, L. A. The role of root exudates and allelochemicals in the rhizosphere. Plant Soil 256, 67–83 (2003).

    Article  CAS  Google Scholar 

  93. Czarnota, M. A., Paul, R. N., Weston, L. A. & Duke, S. O. Anatomy of sorgoleone-secreting root hairs of Sorghum species. Int. J. Plant Sci. 164, 861–866 (2003).

    Article  Google Scholar 

  94. Moreta, D. E. et al. Biological nitrification inhibition (BNI) in Brachiaria pastures: a novel strategy to improve eco-efficiency of crop-livestock systems and to mitigate climate change. Trop. Grasslands 2, 88–91 (2014).

    Article  Google Scholar 

  95. Palmgren, M. G. et al. Are we ready for back-to-nature crop breeding? Trends Plant Sci. 20, 155–164 (2015).

    Article  CAS  PubMed  Google Scholar 

  96. Oldroyd, G. E. D. & Dixon, R. Biotechnological solutions to the nitrogen problem. Curr. Opin. Biotech. 26, 19–24 (2014).

    Article  CAS  PubMed  Google Scholar 

  97. Ncube, B., Dimes, J. P., Twomlow, S. J., Mupangwa, W. & Giller, K. E. Raising the productivity of smallholder farms under semi-arid conditions by use of small doses of manure and nitrogen: a case of participatory research. Nutr. Cycl. Agroecosys. 77, 53–67 (2007).

    Article  Google Scholar 

  98. Vitousek, P. M. et al. Nutrient imbalances in agricultural development. Science 324, 1519–1520 (2009).

    Article  CAS  PubMed  Google Scholar 

  99. Subbarao, G. V. et al. A paradigm shift towards low-nitrifying production systems: the role of biological nitrification inhibition (BNI). Ann. Bot. 112, 297–316 (2013).

    Article  CAS  PubMed  Google Scholar 

  100. Bloom, A. J. et al. CO2 enrichment inhibits shoot nitrate assimilation in C3 but not C4 plants and slows growth under nitrate in C3 plants. Ecology 93, 355–367 (2012).

    Article  PubMed  Google Scholar 

  101. Britto, D. T. & Kronzucker, H. J. NH4+ toxicity in higher plants: a critical review. J. Plant Physiol. 159, 567–584 (2002).

    Article  CAS  Google Scholar 

  102. Britto, D. T. et al. Potassium and nitrogen poising: physiological changes and biomass gains in rice and barley. Can. J. Plant Sci. 94, 1085–1089 (2014).

    Article  CAS  Google Scholar 

  103. Kirk, G. J. D. & Kronzucker, H. J. The potential for nitrification and nitrate uptake in the rhizosphere of wetland plants: a modelling study. Ann. Bot. 96, 639–646 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. Kronzucker, H. J., Siddiqi, M. Y., Glass, A. D. M. & Kirk, G. J. D. Nitrate-ammonium synergism in rice: a subcellular flux analysis. Plant Physiol. 119, 1041–1045 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Qiao, C. L. et al. How inhibiting nitrification affects nitrogen cycle and reduces environmental impacts of anthropogenic nitrogen input. Glob. Change Biol. 21, 1249–1257 (2015).

    Article  Google Scholar 

  106. Lam, S. K., Suter, H., Mosier, A. R. & Chen, D. Using nitrification inhibitors to mitigate agricultural N2O emission: a double-edged sword? Glob. Change Biol. 23, 485–489 (2016).

    Article  Google Scholar 

  107. Jones, D. L., Hodge, A. & Kuzyakov, Y. Plant and mycorrhizal regulation of rhizodeposition. New Phytol. 163, 459–480 (2004).

    Article  CAS  PubMed  Google Scholar 

  108. Marschner, H. Marschner's Mineral Nutrition of Higher Plants (Academic, 2011)

    Google Scholar 

  109. Winogradsky, S. The method in soil microbiology as illustrated by studies on Azotobacter and the nitrifying organisms. Soil Sci. 40, 59–76 (1935).

    Article  CAS  Google Scholar 

  110. Frijlink, M. J., Abee, T., Laanbroek, H. J., Deboer, W. & Konings, W. N. The bioenergetics of ammonia and hydroxylamine oxidation in Nitrosomonas europaea at acid and alkaline pH. Arch. Microbiol. 157, 194–199 (1992).

    Article  CAS  Google Scholar 

  111. Tarre, S., Shlafman, E., Beliavski, M. & Green, M. Changes in ammonia oxidiser population during transition to low pH in a biofilm reactor starting with Nitrosomonas europaea. Water Sci. Tech. 55, 363–368 (2007).

    Article  CAS  Google Scholar 

  112. Bardon, C. et al. Evidence for biological denitrification inhibition (BDI) by plant secondary metabolites. New Phytol. 204, 620–630 (2014).

    Article  CAS  PubMed  Google Scholar 

  113. Li, Y. L., Kronzucker, H. J. & Shi, W. M. Microprofiling of nitrogen patches in paddy soil: analysis of spatiotemporal nutrient heterogeneity at the microscale. Sci. Rep. 6, 27064 (2016).

  114. Dinsdale, E. A. et al. Functional metagenomic profiling of nine biomes. Nature 452, 629–632 (2008).

    Article  CAS  PubMed  Google Scholar 

  115. Oita, A. et al. Substantial nitrogen pollution embedded in international trade. Nat. Geosci. 9, 111–115 (2016).

    Article  CAS  Google Scholar 

  116. Andrews, M. & Lea, P. J. Our nitrogen ‘footprint’: the need for increased crop nitrogen use efficiency. Ann. Appl. Biol. 163, 165–169 (2013).

    Article  CAS  Google Scholar 

  117. Tesfamariam, T. et al. Biological nitrification inhibition in sorghum: the role of sorgoleone production. Plant Soil 379, 325–335 (2014).

    Article  CAS  Google Scholar 

  118. Subbarao, G. V. et al. Free fatty acids from the pasture grass Brachiaria humidicola and one of their methyl esters as inhibitors of nitrification. Plant Soil 313, 89–99 (2008).

    Article  CAS  Google Scholar 

  119. Ladha, J. K. et al. Global nitrogen budgets in cereals: a 50-year assessment for maize, rice, and wheat production systems. Sci. Rep. 6, 19355 (2016).

  120. Cassman, K. G., Dobermann, A., Walters, D. T. & Yang, H. Meeting cereal demand while protecting natural resources and improving environmental quality. Ann. Rev. Environ. Res. 28, 315–358 (2003).

    Article  Google Scholar 

  121. Bouwman, A. F. et al. A global high-resolution emission inventory for ammonia. Glob. Biogeochem. Cycl. 11, 561–587 (1997).

    Article  CAS  Google Scholar 

  122. Sommer, S. G., Schjoerring, J. K. & Denmead, O. T. Ammonia emission from mineral fertilizers and fertilized crops. Adv. Agron. 82, 557–622 (2004).

    Article  CAS  Google Scholar 

  123. Cai, G. X. et al. Nitrogen losses from fertilizers applied to maize, wheat and rice in the North China Plain. Nutr. Cycl. Agroecosys. 63, 187–195 (2002).

    Article  CAS  Google Scholar 

  124. Zhang, X. L. et al. In situ nitrogen mineralization, nitrification, and ammonia volatilization in maize field fertilized with urea in Huanghuaihai region of northern China. PLoS ONE 10, e0115649 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  125. Cai, Z. C. et al. Methane and nitrous oxide emissions from rice paddy fields as affected by nitrogen fertilisers and water management. Plant Soil 196, 7–14 (1997).

    Article  CAS  Google Scholar 

  126. Ding, W., Cai, Y., Cai, Z., Yagi, K. & Zheng, X. Nitrous oxide emissions from an intensively cultivated maize-wheat rotation soil in the North China Plain. Sci. Tot. Environ. 373, 501–511 (2007).

    Article  CAS  Google Scholar 

  127. Zhang, Y. Y. et al. Emissions of nitrous oxide, nitrogen oxides and ammonia from a maize field in the North China Plain. Atmos. Environ. 45, 2956–2961 (2011).

    Article  CAS  Google Scholar 

  128. Chowdary, V. M., Rao, N. H. & Sarma, P. B. S. A coupled soil water and nitrogen balance model for flooded rice fields in India. Agri. Ecosys. Environ. 103, 425–441 (2004).

    Article  CAS  Google Scholar 

  129. Ghosh, B. C. & Bhat, R. Environmental hazards of nitrogen loading in wetland rice fields. Environ. Poll. 102, 123–126 (1998).

    Article  CAS  Google Scholar 

  130. Tian, Y. H., Yin, B., Yang, L. Z., Yin, S. X. & Zhu, Z. L. Nitrogen runoff and leaching losses during rice-wheat rotations in Taihu Lake Region, China. Pedosphere 17, 445–456 (2007).

    Article  CAS  Google Scholar 

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Acknowledgements

The authors would like to thank the Natural Sciences and Engineering Research Council of Canada (NSERC), the Strategic Priority Research Program (B)—‘Soil-microbial system function and regulation’ of the Chinese Academy of Sciences, and the National Natural Science Foundation of China.

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Correspondence to Herbert J. Kronzucker.

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Coskun, D., Britto, D., Shi, W. et al. Nitrogen transformations in modern agriculture and the role of biological nitrification inhibition. Nature Plants 3, 17074 (2017). https://doi.org/10.1038/nplants.2017.74

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