Hostname: page-component-586b7cd67f-gb8f7 Total loading time: 0 Render date: 2024-11-22T17:23:23.197Z Has data issue: false hasContentIssue false

Potential for biological nitrification inhibition to reduce nitrification and N2O emissions in pasture crop–livestock systems

Published online by Cambridge University Press:  06 June 2013

G. V. Subbarao*
Affiliation:
Japan International Research Center for Agricultural Sciences (JIRCAS), 1–1 Ohwashi, Tsukuba, Ibaraki 305-8686, Japan
I. M. Rao
Affiliation:
Centro Internacional de Agricultura Tropical (CIAT), A.A. 6713, Cali, Colombia
K. Nakahara
Affiliation:
Japan International Research Center for Agricultural Sciences (JIRCAS), 1–1 Ohwashi, Tsukuba, Ibaraki 305-8686, Japan
K. L. Sahrawat
Affiliation:
International Crops Research Institute for the Semi-Arid Tropics (ICRISAT), Patancheru, 502 324, Hyderabad, Andhra Pradesh, India
Y. Ando
Affiliation:
Japan International Research Center for Agricultural Sciences (JIRCAS), 1–1 Ohwashi, Tsukuba, Ibaraki 305-8686, Japan
T. Kawashima
Affiliation:
Japan International Research Center for Agricultural Sciences (JIRCAS), 1–1 Ohwashi, Tsukuba, Ibaraki 305-8686, Japan
*
Get access

Abstract

Agriculture and livestock production systems are two major emitters of greenhouse gases. Methane with a GWP (global warming potential) of 21, and nitrous oxide (N2O) with a GWP of 300, are largely emitted from animal production agriculture, where livestock production is based on pasture and feed grains. The principal biological processes involved in N2O emissions are nitrification and denitrification. Biological nitrification inhibition (BNI) is the natural ability of certain plant species to release nitrification inhibitors from their roots that suppress nitrifier activity, thus reducing soil nitrification and N2O emission. Recent methodological developments (e.g. bioluminescence assay to detect BNIs in plant root systems) have led to significant advances in our ability to quantify and characterize the BNI function. Synthesis and release of BNIs from plants is a highly regulated process triggered by the presence of NH4+ in the rhizosphere, which results in the inhibitor being released precisely where the majority of the soil-nitrifier population resides. Among the tropical pasture grasses, the BNI function is strongest (i.e. BNI capacity) in Brachiaria sp. Some feed-grain crops such as sorghum also have significant BNI capacity present in their root systems. The chemical identity of some of these BNIs has now been established, and their mode of inhibitory action on Nitrosomonas has been characterized. The ability of the BNI function in Brachiaria pastures to suppress N2O emissions and soil nitrification potential has been demonstrated; however, its potential role in controlling N2O emissions in agro-pastoral systems is under investigation. Here we present the current status of our understanding on how the BNI functions in Brachiaria pastures and feed-grain crops such as sorghum can be exploited both genetically and, from a production system's perspective, to develop low-nitrifying and low N2O-emitting production systems that would be economically profitable and ecologically sustainable.

Type
Full Paper
Copyright
Copyright © The Animal Consortium 2013 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Alexandratos, N 1999. World food and agriculture: outlook for the medium and longer term. Proceedings of National Academy of Sciences (USA) 96, 59085914.CrossRefGoogle ScholarPubMed
Ashton, I, Miller, WAE, Bowman, WD, Suding, KN 2010. Niche complementarity due to plasticity in resource use: plant partitioning of chemical N forms. Ecology 91, 32523260.Google Scholar
Bending, GD, Lincoln, SD 2000. Inhibition of soil nitrifying bacteria communities and their activities by glucosinolate hydrolysis products. Soil Biology Biochemistry 32, 12611269.Google Scholar
Boudsocq, S, Lata, JC, Mathieu, J, Abbadie, L, Barot, S 2009. Modelling approach to analyse the effects of nitrification inhibition on primary production. Functional Ecology 23, 220230.Google Scholar
Boudsocq, S, Niboyet, A, Lata, JCet al. 2012. Plant preference for ammonium versus nitrate: a neglected determinant of ecosystem functioning? American Naturalist 180, 6069.Google Scholar
Bremner, JM, Blackmer, AM 1978. Nitrous oxide: emission from soils during nitrification of fertilizer nitrogen. Science 199, 295296.Google Scholar
Broadbent, FE, Rauschkolb, RS 1977. Nitrogen fertilization and water pollution. California Agriculture 31, 2425.Google Scholar
Burney, JA, Davis, SJ, Lobell, DB 2010. Greenhouse gas mitigation by agricultural intensification. Proceedings of National Academy of Sciences (USA) 107, 1205212057.Google Scholar
Cassman, KG 1999. Ecological intensification of cereal production systems: yield potential, soil quality and precision agriculture. Proceedings of National Academy of Sciences (USA) 96, 59525959.Google Scholar
Cassman, KG, Pingali, PL 1995. Intensification of irrigated rice systems: learning from the past to meet future challenges. GeoJournal 35, 299305.Google Scholar
Cassman, KG, Dobermann, AR, Walters, DT 2002. Agroecosystems, nitrogen-use efficiency and nitrogen management. Ambio 31, 132140.Google Scholar
Cassman, KG, Dobermann, A, Walters, DT, Yang, H 2003. Meeting cereal demand while protecting natural resources and improving environmental quality. Annual Review Environmental Resources 28, 315358.Google Scholar
Celik, I 2005. Land-use effects on organic matter and physical properties of soil in a southern Mediterranean highland of Turkey. Soil Tillage Research 83, 270277.CrossRefGoogle Scholar
Centner, TJ, Newton, GL 2008. Meeting environmental requirements for the land application of manure. Journal of Animal Science 86, 32283234.Google Scholar
Clark, FE 1962. Losses of nitrogen accompanying nitrification. Transactions International Society of Soil Science IV and V, 173–176.Google Scholar
Cohen, JE, Federoff, NV 1999. Colloquium on plants and population: is there time?. National Academy of Sciences, Washington, DC.Google Scholar
Cooper, AB 1986. Suppression of nitrate formation with an exotic conifer plantation. Plant Soil 93, 383394.Google Scholar
Dalgaard, T, Bienkowski, JF, Bleeker, A, Dragosits, U, Drouet, JL, Durand, P, Frumau, A, Hutchings, NJ, Kedziora, A, Magliulo, V, Olesen, JE, Theobald, MR, Maury, O, Akkal, N, Cellier, P 2012. Farm nitrogen balances in six European landscapes as an indicator for nitrogen losses and basis for improved management. Biogeosciences 9, 53035321.Google Scholar
Dayan, FE, Rimando, AM, Pan, Z, baerson, SR, Gimsing, AL, Duke, SO 2010. Sorgoleone. Phytochemistry 71, 10321039.Google Scholar
Dennis, SJ, Cameron, KC, Di, HJ, Moir, JL, Staples, V, Sills, P, Richards, KG 2012. Reducing nitrate losses from grazed grassland in Ireland using a nitrification inhibitor (DCD). Biology and the Environment 112B, 7989.Google Scholar
Dinnes, DL, Karlen, DL, Jaynes, DB, Kasper, TC, Hatfield, JL, Colvin, TS, Cambardella, CA 2002. Nitrogen management strategies to reduce nitrate leaching in the drained mid-Western soils. Agronomy Journal 94, 153171.Google Scholar
Elliot, ET 1986. Aggregate structure and carbon, nitrogen and phosphorus in native and cultivated soils. Soil Science Society of America Journal 50, 627633.Google Scholar
Food and Agriculture Organization (FAO) 2009. FAOSTAT. http://faostat.fao.org.Google Scholar
Food and Agriculture Organization (FAO) 2012. FAOSTAT. http://apps.fao.org/.Google Scholar
Fertilizer Market Bulletin 2008. FMB Weekly Fertilizer Report. http://fmb-group.co.uk.Google Scholar
Finzi, AC, Norby, RJ, Calfapietra, C, Gallet-Budynek, A, Gielen, B, Holmes, WE, Hoosbeek, MR, Iversen, CM, Jackson, RB, Kubiske, ME 2007. Increases in nitrogen uptake rather than nitrogen-use efficiency support higher rates of temperate forest productivity under elevated CO2. Proceedings of National Academy of Sciences (USA) 104, 1401414019.Google Scholar
Fisher, MJ, Rao, IM, Ayarza, MA, Lascano, CE, Sanz, JI, Thomas, RJ, Vera, RR 1994. Carbon storage by introduced deep-rooted grasses in the South American savannas. Nature 371, 236238.Google Scholar
Galloway, JN, Townsend, AR, Erisman, JW, Bekunda, M, Zai, Z, Freney, JR, Martinelli, LA, Seitzinger, SP, Sutton, MA 2008. Transformation of the nitrogen cycle: recent trends, questions and potential solutions. Science 320, 889892.CrossRefGoogle ScholarPubMed
Giltrap, DL, Singh, J, Saggar, S, Zaman, M 2010. A preliminary study to model the effects of a nitrification inhibitor on nitrous oxide emissions from urine-amended pasture agriculture. Ecosystems and Environment 136, 310317.Google Scholar
Glass, ADM 2003. Nitrogen use efficiency of crop plants: physiological constraints upon nitrogen absorption. Critical Reviews in Plant Sciences 22, 453470.Google Scholar
Gopalakrishnan, S, Subbarao, GV, Nakahara, K, Yoshihashi, T, Ito, O, Maeda, I, Ono, H, Yoshida, M 2007. Nitrification inhibitors from the root tissues of Brachiaria humidicola, a tropical grass. Journal of Agriculture and Food Chemistry 55, 13851388.Google Scholar
Hahn, J, Crutzen, PJ 1982. The role of fixed nitrogen in atmospheric photochemistry. Philosophical Transactions of Royal Society (London) Series B 296, 521541.Google Scholar
Hansen, B, Dalgaard, T, Thorling, L, Sorensen, B, Erlandsen, M 2012. Regional analysis of groundwater nitrate concentrations and trends in Denmark in regard to agricultural influence. Biogeosciences 9, 32773286.Google Scholar
Harrison, K, Bol, AR, Bardgett, RD 2007. Preferences for different nitrogen forms by coexisting plant species and soil microbes: comment. Ecology 88, 989999.Google Scholar
Haynes, RJ, Goh, KM 1978. Ammonium and nitrate nutrition of plants. Biological Reviews 53, 465510.CrossRefGoogle Scholar
Hodge, A, Robinson, D, Fitter, AH 2000. Are microorganisms more effective than plants at competing for nitrogen? Trends in plant science 5, 304308.Google Scholar
Hofstra, N, Bouwman, AF 2005. Denitrification in agricultural soils: summarizing published data and estimating global annual rates. Nutrient Cycling Agro-ecosystems 72, 267278.Google Scholar
Hungate, BA, Dukes, JS, Shaw, MR, Luo, Y, Field, CB 2003. Nitrogen and climate change. Science 302, 15121513.Google Scholar
Iizumi, T, Mizumoto, M, Nakamura, K 1998. A bioluminescence assay using Nitrosomonas europaea for rapid and sensitive detection of nitrification inhibitors. Applied Environmental Microbiology 64, 36563662.Google Scholar
Intergovernmental Panel on Climate Change (IPCC) 2012. Climate change: the physical science basis-summary for policy makers. World Meteorological Organization/United Nations Environ, Prog, Paris.Google Scholar
Jackson, LE, Bowles, TM, Hodson, AK, Lazcano, C 2012. Soil microbial-root and microbial-rhizosphere processes to increase nitrogen availability and retention in agroecosystems. Current opinion in Environmental Sustainability 4, 517522.Google Scholar
Jahangir, MMR, Johnston, P, Khalil, MI, Hennessy, D, Humphreys, J, Fenton, O, Richards, KG 2012. Groundwater: a pathway for terrestrial C and N losses and indirect greenhouse gas emissions. Agriculture Ecosystems and Environment 159, 4048.Google Scholar
Jarvis, SC 1996. Future trends in nitrogen research. Plant Soil 181, 4756.Google Scholar
Kahrl, E, Li, Y, Su, Y, Tenngkeit, T, Walkes, A, Xu, J 2010. Greenhouse gas emissions from nitrogen use in China. Environmental Science Policy 13, 688694.Google Scholar
Khan, SA, Mulvaney, RL, Ellsworth, TR, Boast, CW 2007. The myth of nitrogen fertilization for soil carbon sequestration. Journal of Environmental Quality 36, 18211832.Google Scholar
Kongshaug, G 1998. Energy consumption and greenhouse gas emissions in fertilizer production. IFA Technical Conference, Marrakech, Morocco, 28 September to 1 October 1998.Google Scholar
Kramer, KJ, Moll, HC, Nonhebel, S 1999. Total greenhouse gas emissions related to the Dutch crop production system. Agriculture, Ecosystems and Environment 72, 916.Google Scholar
Kroeze, C 1994. Nitrous oxide and global warming. Science of Total Environment 143, 193209.CrossRefGoogle Scholar
Kuesters, J, Jenssen, T 1998. Selecting the right fertilizer from an environmental life cycle perspective. IFA Technical Conference. Marrakech, Morocco, 28 September to 1 October, 1998.Google Scholar
Lata, JC, Durand, J, Lensi, R, Abbadie, L 1999. Stable coexistence of contrasted nitrification statuses in a wet tropical savanna ecosystem. Functional Ecology 13, 762768.Google Scholar
Lata, JC, Degrange, V, Raynaud, X, Maron, P, Lensi, , Abbadie, L 2004. Grass populations control nitrification in savanna soils. Functional Ecology 18, 605611.CrossRefGoogle Scholar
Leninger, S, Urich, T, Schloter, M, Schwark, L, Qi, J, Nicol, GW, Prosser, JI, Schuster, SC, Schleper, C 2006. Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 442, 806809.Google Scholar
Matson, PA, Naylor, R, Ortiz-Monasterio, I 1998. Integration of environmental, agronomic and economic aspects of fertilizer management. Science 280, 112115.Google Scholar
Matson, PA, McDowell Townsend, AR, Vitousek, PM 1999. The globalization of N deposition: ecosystem consequences in tropical environments. Biogeochemistry 46, 6783.Google Scholar
McCarty, GW 1999. Modes of action of nitrification inhibitors. Biology and Fertility of Soils 29, 19.Google Scholar
Miles, JW, do Valle, CB, Rao, IM, Euclides, VPB 2004. Brachiaria grasses. In ‘Warm-season (C4) grasses (ed. L Moser, B Burson and LE Sollenberger), pp. 745783. ASA-CSSA-SSA, Madison, WI, USA.Google Scholar
Mosier, AR, Duxbury, JM, Freney, JR, Heinemeyer, O, Minami, K 1996. Nitrous oxide emissions from agricultural fields: assessment, measurement and mitigation. Plant Soil 181, 95108.Google Scholar
Mulvaney, RL, Khan, SA, Ellsworth, TR 2009. Synthetic nitrogen fertilizers deplete soil nitrogen: a global dilemma for sustainable cereal production. Journal of Environmental Quality 38, 22952314.Google Scholar
Nasholm, T, Ekblad, A, Nordin, A, Gisler, R, Hosberg, M, Hosberg, P 1998. Boreal forest plants take up organic nitrogen. Nature 392, 914916.Google Scholar
Newbould, P 1989. The use of nitrogen fertilizer in agriculture. Where do we go practically and ecologically? Plant Soil 115, 297311.Google Scholar
Northup, PR, Zengshou, Y, Dahlgren, RA, Vogt, KA 1995. Polyphenol control of nitrogen release from pine litter. Nature 377, 227229.Google Scholar
Paavolainen, L, Kitunen, V, Smolander, A 1998. Inhibition of nitrification in forest soil by monoterpenes. Plant Soil 205, 147154.Google Scholar
Pelletier, N, Tyedmers, P 2010. Forecasting potential global environmental costs of livestock production 2000–2050. Proceedings of National Academy of Sciences (USA) 107, 1837118374.Google Scholar
Peterjohn, WT, Schlesinger, WH 1990. Nitrogen loss from deserts in the south Western United States. Bigeochemistry 10, 6779.Google Scholar
Poudel, DD, Horwath, WR, Lanini, WT 2002. Comparison of soil N availability and leaching potential, crop yields and weeds in organic, low-input and conventional farming systems in northern California. Agriculture Ecosystems and Environment 90, 125137.CrossRefGoogle Scholar
Prasad, R, Power, JF 1995. Nitrification inhibitors for agriculture, health and the environment. Advances in Agronomy 54, 233281.Google Scholar
Prosser, JI 1989. Autotrophic nitrification in bacteria. Advances in Microbial Physiology 30, 125181.CrossRefGoogle ScholarPubMed
Raun, WR, Johnson, GV 1999. Improving nitrogen use efficiency for cereal production. Agronomy Journal 91, 357363.Google Scholar
Rice, E, Pancholy, SK 1972. Inhibition of nitrification by climax ecosystems. American Journal of Botany 59, 10331040.Google Scholar
Rice, E, Pancholy, SK 1974. Inhibition of nitrification by climax ecosystems III. Inhibitors other than tannins. American Journal of Botany 61, 10951103.Google Scholar
Rockstrom, J, Steffen, W, Noone, K, Persson, A, Chapin, FS, Lambin, EF, Lenten, TM, Scheffer, M, Folke, C, Schellnhuber, HJ, Nykvist, B, devit, CA, Hughes, T, vander Luuw, S, Rodhe, H, Sortin, S, Snyder, PK, Costanza, R, Svedin, V, Falkenmark, M, Karlberg, L, Corell, RW, Fabrey, VJ, Hansen, J, Walker, B, Liverman, D, Richardson, K, Crutzen, P, Foley, JA 2009. A safe operating space for humanity. Nature 461, 472475.CrossRefGoogle ScholarPubMed
Ross, XM 1993. Organic matter in tropical soils: current conditions, concerns and prospects for conservation. Progress Physical Geography 17, 265305.Google Scholar
Russell, AE, Cambardella, CA, Laird, DA, Jaynes, DB, Meek, DW 2009. Nitrogen fertilizer effects on soil carbon balances in Midwestern US agricultural systems. Ecological Applications 19, 11021113.Google Scholar
Ruttan, VW 1999. The transition to agricultural sustainability. Proceedings of National Academy of Sciences (USA) 96, 59605967.Google Scholar
Sahrawat, KL 1989. Effects of nitrification inhibitors on nitrogen transformations other than nitrification in soils. Advances in Agronomy 42, 279309.Google Scholar
Salsac, L, Chaillou, S, Morot-Gaudry, J, Lesaint, C 1987. Nitrate and ammonium nutrition in plants. Plant Physiology Biochemistry 25, 805812.Google Scholar
Schafer, A, Victor, DG 1999. Global passenger travel: implications for carbon dioxide emissions. Energy 24, 657679.Google Scholar
Schlesinger, WH 2009. On the fate of anthropogenic nitrogen. Proceedings of National Academy of Sciences (USA) 106, 203208.Google Scholar
Slangen, J, Kerkhoff, P 1984. Nitrification inhibitors in agriculture and horticulture: a literature review. Fertilizer Research 5, 113.Google Scholar
Smart, DR, Bloom, AJ 2001. Wheat leaves emit nitrous oxide during nitrate assimilation. Proceedings of National Academy of Sciences (USA) 98, 78757878.Google Scholar
Smil, V 1999. Nitrogen in crop production: an account of global flows. Global Biogeochemical Cycles 13, 647662.Google Scholar
Smil, V 2001. Enriching the earth: Fritz Haber, Carl Bosch, and the transformation of world food. MIT Press, Cambridge, MA.Google Scholar
Smith, KA, McTaggart, IP, Tsuruta, H 1997. Emissions of N2O and NO associated with nitrogen fertilization in intensive agriculture, and the potential for mitigation. Soil Use Management 13, 296304.Google Scholar
Smits, NAC, Bobbink, R, Laanbrock, HJ, Paalman, AJ, Hefting, MM 2010. Repression of potential nitrification activities by matgrass sward species. Plant Soil 337, 435445.Google Scholar
Smolander, A, Kanerva, S, Adamezyk, B, Kitunen, V 2012. Nitrogen transformations in boreal forest soils – does composition of plant secondary compounds give any explanations? Plant Soil 350, 126.Google Scholar
Socolow, R 1999. Nitrogen management and the future of food: lessons from the management of energy and carbon. Proceedings of National Academy of Sciences (USA) 96, 60016008.Google Scholar
Steinfeld, H, Wassenaar, T 2007. The role of livestock production in carbon and nitrogen cycles. Annual Review of Environmental Resources 32, 271294.Google Scholar
Stelzer, H, Bowman, WD 1998. Differential influence of plant species on soil nitrogen transformations within moist meadow alpine tundra. Ecosystems 1, 464474.Google Scholar
Subbarao, GV, Ito, O, Sahrawat, KL, Berry, WL, Nakahara, K, Ishikawa, T, Watanabe, T, Suenaga, K, Rondon, M, Rao, IM 2006a. Scope and strategies for regulation of nitrification in agricultural systems – challenges and opportunities. Critical Reviews in Plant Sciences 25, 303335.Google Scholar
Subbarao, GV, Ishikawa, T, Ito, O, Nakahara, K, Wang, HY, Berry, WL 2006b. A bioluminescence assay to detect nitrification inhibitors released from plant roots: a case study with Brachiaria humidicola. Plant Soil 288, 101112.Google Scholar
Subbarao, GV, Wang, HY, Ito, O, Nakahara, K, Berry, WL 2007a. NH4+ triggers the synthesis and release of biological nitrification inhibition compounds in Brachiaria humidicola roots. Plant Soil 290, 245257.Google Scholar
Subbarao, GV, Rondon, M, Ito, O, Ishikawa, T, Rao, IM, Nakahara, K, Lascano, C, Berry, WL 2007b. Biological nitrification inhibition (BNI) – is it a widespread phenomenon? Plant Soil 294, 518.Google Scholar
Subbarao, GV, Ban, T, Masahiro, K, Ito, O, Samejima, H, Wang, HY, Pearse, SJ, Gopalakrishnan, S, Nakahara, K, Zakir Hossain, AKM, Tsujimoto, H, Berry, WL 2007c. Can biological nitrification inhibition (BNI) genes from perennial Leymus racemosus (Triticeae) combat nitrification in wheat farming? Plant Soil 299, 5564.Google Scholar
Subbarao, GV, Nakahara, K, Ishikawa, T, Yoshihashi, T, Ito, O, Ono, H, Ohnishi-Kameyama, M, Yoshida, M, Kawano, N, Berry, WL 2008. Free fatty acids from the pasture grass Brachiaria humidicola and one of their methyl esters as indicators of nitrification. Plant Soil 313, 8999.Google Scholar
Subbarao, GV, Nakahara, K, Hurtado, MP, Ono, H, Moreta, DE, Salcedo, AF, Rondon, M, Rao, IM, Lascano, CE, Berry, WL, Ito, O 2009a. Evidence for biological nitrification inhibition in Brachiaria pastures. Proceedings of National Academy of Sciences (USA) 106, 1730217307.Google Scholar
Subbarao, GV, Kishii, M, Nakahara, K, Ishikawa, T, Ban, T, Tsujimoto, H, George, TS, Berry, WL, Hash, CT, Ito, O 2009b. Biological nitrification inhibition (BNI) – is there potential for genetic interventions in the Triticeae? Breeding Science 59, 529545.Google Scholar
Subbarao, GV, Sahrawat, KL, Nakahara, K, Ishikawa, T, Kishii, M, Rao, IM, Hash, CT, George, TS, Srinivasa Rao, P, Nardi, P, Bonnett, D, Berry, W, Suenaga, K, Lata, JC 2012. Biological nitrification inhibition – a novel strategy to regulate nitrification in agricultural systems. Advances in Agronomy 114, 249302.Google Scholar
Subbarao, GV, Nakahara, K, Ishikawa, T, Ono, H, Yoshida, M, Yoshihashi, T, Zhu, Y, Zakir, HAKM, Deshpande, SP, Hash, CT, Sahrawat, KL 2013a. Biological nitrification inhibition (BNI) activity in sorghum and its characterization. Plant Soil 366, 243259.Google Scholar
Subbarao, GV, Sahrawat, KL, Nakahara, K, Rao, IM, Ishitani, M, Hash, CT, Kishii, M, Bonnett, DG, Berry, WL, Lata, JC 2013b. A paradigm shift towards low-nitrifying production systems: the role of biological nitrification inhibition (BNI). Annals of Botany, doi:10.1093/aob/mcs230.Google Scholar
Sutton, MA, Oenema, O, Erisman, JW, Leip, A, van Grinsven, H, Winiwarter, W 2011. Too much of a good thing. Nature 472, 159161.Google Scholar
Taylor, AE, Zeglin, LH, Dooley, S, Myrold, DD, Bottomley, PJ 2010. Evidence for different contributions of archaea and bacteria to the ammonia-oxidizing potential of diverse Oregon soils. Applied Environmental Microbiology 76, 76917698.Google Scholar
Tiessen, H, Cuevas, E, Chacon, P 1994. The role of soil organic matter in sustaining soil fertility. Nature 371, 783785.Google Scholar
Tilman, D, Cassman, KG, Matson, PA, Naylor, R, Polasky, S 2002. Agricultural sustainability and intensive production practices. Nature 418, 671677.CrossRefGoogle ScholarPubMed
Tilman, D, Fargione, J, Wolff, B, Antonio, CD, Dobson, A, Howarth, R, Schindler, D, Schlesinger, WH, Simberloff, D, Swackhamer, D 2001. Forecasting agriculturally driven global environmental change. Science 292, 281284.Google Scholar
Tubiello, FN, Salvatore, M, Rossi, S, Ferrara, A, Fitton, N, Smith, P 2013. The FAOSTAT database of greenhouse gas emissions from agriculture. Environment Research Letters 8, doi:10.1088/1748-9326/8/1/015009.Google Scholar
Turner, RE, Rabalais, NN, Justic, D 2008. Gulf of Mexico hypoxia: alternate states and a legacy. Environmental Science Technology 42, 23232327.Google Scholar
van der Hoek, KW 1998. Nitrogen efficiency in global animal production. Environmental Pollution 102, 127132.Google Scholar
Van Wesemael, B, Paustian, K, Meersmans, J, Goidts, E, Barancikova, G, Easter, M 2010. Agricultural management explains historic changes in regional soil carbon stocks. Proceedings of National Academy of Sciences (USA) 107, 1492614930.Google Scholar
Vitousek, PM, Matson, PA 1984. Mechanisms of nitrogen retention in forest ecosystems: a field experiment. Science 225, 5152.Google Scholar
Vitousek, PM, Howarath, RW 1991. Nitrogen limitation on land and in the sea: how can it occur? Biogeochemistry 13, 87115.Google Scholar
Vitousek, PM, Mooney, HA, Lubchenco, J, Melillo, JM 1997a. Human domination of earth's ecosystems. Science 277, 494499.Google Scholar
Vitousek, PM, Aber, JD, Howarth, W, Likens, GE, Matson, PA, Schindler, DW, Tilman, DG 1997b. Human alteration of the global nitrogen cycle: sources and consequences. Ecological Applications 7, 737750.Google Scholar
Wagner-Riddle, C, Furon, A, McLaughlin, NL, Lee, I, Barbeau, J, Jayasundara, S, Parkin, P, von Bertoldi, P, Warland, J 2007. Intensive measurement of nitrous oxide emissions from a corn-soybean-wheat rotation under two contrasting management systems over 5 years. Global Change Biology 13, 17221736.Google Scholar
White, C 1991. The role of monoterpenes in soil nitrogen cycling processes in ponderosa pine. Biogeochemistry 12, 4368.Google Scholar
Zahn, LM 2007. A boost from wild wheat. Science 318, 171.Google Scholar
Zakir, HAKM, Subbarao, GV, Pearse, SJ, Gopalakrishnan, X, Ito, O, Ishikawa, T, Kawano, N, Nakahara, K, Yoshihashi, T, Ono, H, Yoshida, M 2008. Detection, isolation and characterization of a root-exuded compound, methyl 3-(4-hydroxyphenyl)propionate, responsible for biological nitrification inhibition by sorghum (Sorghum bicolor). New Phytologist 180, 442451.Google Scholar
Zhang, HB, Wang, B, Xu, M 2008. Effects of inorganic fertilizer inputs on grain yields and soil properties in a long-term wheat-corn cropping system in south China. Communications Soil Science Plant Analysis 39, 15831599.Google Scholar
Zhu, Y, Zeng, H, Shen, Q, Ishikawa, T, Subbarao, GV 2012. 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, 131141.Google Scholar