A paradigm shift towards low-nitrifying production systems: The role of biological nitrification inhibition (BNI)

Annals of Botany

Volumn 112, Issue 2, 2013, Pages 297-316

  Subbarao, G V ^a   Sahrawat, K L ^b   Nakahara, K ^a   Rao, I M ^c   Ishitani, M ^c   Hash, C T ^d   Kishii, M ^e   Bonnett, D G ^f   Berry, W L ^g   Lata, J C ^h  

^a JAPAN INTERNATIONAL RESEARCH CENTER FOR AGRICULTURAL SCIENCES   (Japan)

^b INTERNATIONAL CROPS RESEARCH INSTITUTE FOR THE SEMI ARID TROPICS ICRISAT   (India)

^c INTERNATIONAL CENTER FOR TROPICAL AGRICULTURE CIAT   (Colombia)

^d ICRISAT Sahelian Center   (Niger)

^e YOKOHAMA CITY UNIVERSITY   (Japan)

^f INTERNATIONAL MAIZE AND WHEAT IMPROVEMENT CENTER CIMMYT   (Mexico)

^g UNIVERSITY OF CALIFORNIA   (United States)

^h ECOLE NORMALE SUPÉRIEURE   (France)

Author keywords

ammonia mono oxygenase; AMO; biological nitrification inhibition; BNI; BNI capacity; brachialactone; fatty acids; HAO; high nitrifying production systems; hydroxylamine oxidoreductase; low nitrifying production systems; nitrate leaching; nitrification; Nitrosomonas; nitrous oxide emissions; sustainability; synthetic nitrification inhibitors

Indexed keywords

FATTY ACID; FERTILIZER; HYDROXYLAMINE OXIDASE; LACTONE; NITROGEN; QUATERNARY AMMONIUM DERIVATIVE;

AMMONIUM; BIOASSAY; BIOENGINEERING; ECOSYSTEM HEALTH; EMISSION; FATTY ACID; FORAGE; GENETIC VARIATION; GRASS; INHIBITION; INHIBITOR; LEACHING; NITRIFICATION; NITROGEN CYCLE; NITROUS OXIDE; NUTRIENT USE EFFICIENCY; PARADIGM SHIFT; PHYSIOLOGY; SUSTAINABILITY;

AGRICULTURE; AMMONIA MONO-OXYGENASE; AMO; BIOLOGICAL NITRIFICATION INHIBITION; BNI; BNI CAPACITY; BRACHIALACTONE; BRACHIARIA; CHEMISTRY; CROP; DRUG EFFECT; ECOSYSTEM; HAO; HIGH-NITRIFYING PRODUCTION SYSTEMS; LOW-NITRIFYING PRODUCTION SYSTEMS; METABOLISM; NITRATE LEACHING; NITRIFICATION; NITROSOMONAS; NITROUS OXIDE EMISSIONS; PLANT ROOT; REVIEW; SOIL; SORGHUM; SUSTAINABILITY; SYNTHETIC NITRIFICATION INHIBITORS; WHEAT;

AMMONIA MONO-OXYGENASE; AMO; BIOLOGICAL NITRIFICATION INHIBITION; BNI; BNI CAPACITY; BRACHIALACTONE; FATTY ACIDS; HAO; HIGH-NITRIFYING PRODUCTION SYSTEMS; HYDROXYLAMINE OXIDOREDUCTASE; LOW-NITRIFYING PRODUCTION SYSTEMS; NITRATE LEACHING; NITRIFICATION; NITROSOMONAS; NITROUS OXIDE EMISSIONS; SUSTAINABILITY; SYNTHETIC NITRIFICATION INHIBITORS;

AGRICULTURE; BRACHIARIA; CROPS, AGRICULTURAL; ECOSYSTEM; FERTILIZERS; LACTONES; NITRIFICATION; NITROGEN; NITROSOMONAS; PLANT ROOTS; QUATERNARY AMMONIUM COMPOUNDS; SOIL; SORGHUM; TRITICUM;

EID: 84880304843     PISSN: 03057364     EISSN: 10958290     Source Type: Journal    
DOI: 10.1093/aob/mcs230     Document Type: Review

References (220)

1. 15N-glycine differ among dominant exotic and subordinate native grasses from a California oak wood-land. Environmental and Experimental Botany 65:205-209.
2. Akiyama K, Hayashi H. 2006. Strigolatones:chemical signals for fungal symbionts and parasitic weeds in plant roots. Annals of Botany 97:925-931.
3. Ashton I, Miller WAE, Bowman WD, Suding KN. 2010. Niche complementarity due to plasticity in resource use:plant partitioning of chemical N forms. Ecology 91:3252-3260.
4. Awad A, Sato D, Kusumoto D, Kamioka H, Takeuchi Y, Yoneyama K. 2006. Characterization of strigolactones, germination stimulants for the root parasitic plants Striga and Orobanche produced by maize, millet and sorghum. Plant Growth Regulation 48:221-227.
5. Baerson SR, Dayan FE, Rimando AM, et al. 2007. A functional genomics investigation of allelochemical biosynthesis in Sorghum bicolor root hairs. Journal of Biological Chemistry 283:3231-3247.
6. Baldwin IT, Olson RK, Reiners WA. 1983. Protein binding phenolics and the inhibition of nitrification in subalpine balsam-fir soils. Soil Biology Biochemistry 15:419-423.
7. Barker AV, Mills HA. 1980. Ammonium and nitrate nutrition of horticultural crops. Horticultural Review 2:395-423.
8. Barot S, Ugolini A, Brikci B. 2007. When do soil decomposers and ecosystem engineers enhance plant production? Functional Biology 21:1-10.
9. Basaraba J. 1964. Influence of vegetable tannins on nitrification in soil. Plant Soil 21:8-16.
10. Bate GC. 1981. Nitrogen cycling in savanna ecosystems. Ecological Bulletin 33:463-475.
11. Bellamy PH, Loveland PJ, Bradley RI, Murray R, Lark RM, Kirk GJD. 2005. Carbon losses from all soils across England and Wales 1978-2003. Nature 437:245-248.
12. Bending GD, Lincoln SD. 2000. Inhibition of soil nitrifying bacteria communities and their activities by glucosinolate hydrolysis products. Soil Biology and Biochemistry 32:1261-1269.
13. 2. Geochimica et Cosmochimica Acta 70:5653-5664.
14. Bertin C, Yang X, Weston LA. 2003. The role of root exudates and allelo-chemicals in the rhizosphere. Plant and Soil 256:67-83.
15. 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 23:220-230.
16. Boudsocq S, Barot S, Loeuille N. 2011. Evolution of nutrient acquisition:when adaptation fills the gap between contrasting ecological theories. Proceedings of the Royal Society B:Biological Sciences 278:449-457.
17. Boudsocq S, Niboyet A, Lata JC, et al. 2012. Plant preference for ammonium versus nitrate:A neglected determinant of ecosystem functioning? American Naturalist 180:60-69.
18. Bouwmeester HJ, Roux C, Lopez-Raez JA, Bécard G. 2007. Rhizosphere communication of plants, parasitic plants and AM fungi. Trends in Plant Science 12:224-230.
19. Bremner JM, Blackmer AM. 1978. Nitrous oxide:emission from soils during nitrification and denitrification of fertilizer nitrogen. Science 199:295-296.
20. Bremner JM, Mc Carty GW. 1988. Effects of terpenoids on nitrification in soil. Soil Science Society of America Journal 52:1630-1633.
21. Bremner JM, Breitenbeck GA, Blackmer AM. 1981. Effect of nitrapyrin on emission of nitrous oxide from soils fertilized with anhydrous ammonia. Geophysical Research Letters 8:353-356.
22. + cycling:A cellular hypothesis to explain ammonium tox-icity in plants. Proceedings of the National Academy of Sciences, USA 98:4255-4258.
23. Broadbent FE, Rauschkolb RS. 1977. Nitrogen fertilization and water pollution. California Agriculture 31:24-25.
24. Brown PJ, Rooney WL, Franks C, Kresovich S. 2008. Efficient mapping of plant height quantitative trait loci in a sorghum association population with introgressed dwarfing genes. Genetics 180:629-637.
25. Burford JR, Sahrawat KL. eds. 1989. Management of Vertisols for improved agricultural production:Proceedings of an IBSRAM inaugural workshop, 18-22 February 1985, ICRISAT Center, Patancheru, India, ICRISAT, Patancheru 502 324, Andhra Pradesh, India.
26. Burney JA, Davis SJ, Lobell DB. 2010. Greenhouse gas mitigation by agricultural intensification. Proceedings of National Academy of Sciences, USA 107:12052-12057.
27. Buso GSC, Bliss FA. 1988. Variability among lettuce cultivars grown at two levels of available phosphorus. Plant and Soil 111:67-73.
28. Canfield DE, Glazer AN, Falkowski PG. 2010. The evolution and future of earth's nitrogen cycle. Science 330:192-196.
29. Casa AM, Pressoir G, Brown PJ, et al. 2008. Community resources and strategies for association mapping in sorghum. Crop Science 48:30-40.
30. Castaldi S, Carfora A, Fiorentino A, et al. 2009. Inhibition of net nitrification activity in a Mediterranean woodland:possible role of chemicals produced by Arbutus unedo. Plant and Soil 315:273-283.
31. Celik I. 2005. Land-use effects on organic matter and physical properties of soil in a southern Mediterranean highland of Turkey. Soil Tillage Research 83:270-277.
32. Chang M, Netzly DH, Butler LG, Lynn DG. 1986. Chemical regulation of distance:characterization of the first natural host germination stimulant for Striga asiatica. Journal of the American Chemical Society 108:7858-7860.
33. Clark FE. 1962. Losses of nitrogen accompanying nitrification. Transactions of the International Society of Soil Science IV and V:173-176.
34. Clark FE, Beard WE, Smith DH. 1960. Dissimilar nitrifying capacities of soils in relation to losses of applied nitrogen. Proceedings of the Soil Science Society of America 24:50-54.
35. Cook CE, Whichard LP, Wall ME, et al. 1972. Germination stimulants II. The structure of strigol, a potent seed germination stimulant for witch-weed (Striga lutea Lour.). Journal of the American Chemistry Society 94:6198-6199.
36. Cook D, Rimado AM, Clemente TE, et al. 2010. Alkylresorcinol synthases expressed in Sorghum bicolor root hairs play an essential role in the biosynthesis of the allelopathic benzoquinone sorgoleone. The Plant Cell 22:867-887.
37. Cooper AB. 1986. Suppression of nitrate formation with an exotic conifer plantation. Plant and Soil 93:383-394.
38. Crutzen PJ, Ehhalt DH. 1977. Effects of nitrogen fertilizers and combustion on the stratospheric ozone layer. Ambio 6:112-116.
39. Dansgaard W, Johnsen SJ, Clausen HB, et al. 1993. Evidence for general instability of past climate from a 250-kyr ice-core record. Nature 364:218-220.
40. Davis J, Haglund C. 1999. Life cycle inventory (LCI) of fertilizer production. Fertilizer products used in Sweden and Western Europe. SIK-Report No. 654. Master's Thesis, Chalmers University of Technology, Sweden.
41. De Cicco J, Fung F. 2006. Global warming on the road:The climate impact of America's automobiles. www.environmentaldefense.org
42. Dinnes DL, Karlen DL, Jaynes DB, et al. 2002. Nitrogen management strategies to reduce nitrate leaching in tile drained Mid-Western soils. Agronomy Journal 94:153-171.
43. Donaldson JM, Henderson GS. 1990a. Nitrification potential of secondary succession upland oak forests:1. Mineralization and nitrification during laboratory incubations. Soil Science Society of America Journal 54:892-897.
44. Donaldson JM, Henderson GS. 1990b. Nitrification potential of secondary succession upland oak forests II. Regulation of ammonium-oxidizing bacteria populations. Soil Science Society of America Journal 54:898-902.
45. Ejeta G. 2007. Breeding for Striga resistance in sorghum:exploitation of an intricate host-parasite biology. Crop Science 47(suppl 3):S216-S227.
46. Elliott ET. 1986. Aggregate structure and carbon, nitrogen and phosphorus in native and cultivated soils. Soil Science Society of America Journal 50:627-633.
47. Elshire RJ, Glaubitz JC, Sun Q, et al. 2011. A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLo S One 6:e19379. http://dx.doi.org/10.1371/journal.pone.0019379.
48. Endo TR. 2007. The gametocidal chromosome as a tool for chromosome manipulation in wheat. Chromosome Research 15:67-75.
49. Erickson A, Ramsewak RS, Smucker AJ, Nair MGJ. 2000. Nitrification inhibitors from the roots of Leucaena leucocephala. Journal of Agricultural and Food Chemistry 48:6174-6177
50. FAO. 2011. FAOSTAT Database-Agriculture production. Rome:Food and Agriculture Organization of the United Nations.
51. Fenwick GR, Heaney RK, Mullin WJ. 1983. Glucosinolates and their breakdown products in food and food plants. In:Furia TE. ed. Critical reviews in food science and nutrition. Boca Raon, FL:CRC Press, 123-201.
52. Fillery IRP. 2007. Plant-based manipulation of nitrification in soil:A new approach to managing N loss? Plant and Soil 294:1-4.
53. 2. Proceedings of National Academy of Sciences, USA 104:14014-14019.
54. Fisher MJ, Rao IM, Ayarza MA, et al. 1994. Carbon storage by introduced deep-rooted grasses in the South American savannas. Nature 371:236-238.
55. Foley JA, Defries R, Asner GP, et al. 2005. Global consequences of land use. Science 309:570-574.
56. Frank DA, Groffman PM. 2009. Plant rhizosphere N processes:what we don't know and why we should care. Ecology 90:1512-1519.
57. Friebe B, Jiang J, Raupp WJ, Mc Intosh RA, Gill BS. 1996. Characterization of wheat-alien translocations conferring resistance to diseases and pest:current status. Euphytica 91:59-87.
58. Galloway JN, Townsend AR, Erisman JW, et al. 2008. Transformation of the nitrogen cycle:recent trends, questions and potential solutions. Science 320:889-892.
59. Glass ADM. 2003. Nitrogen use efficiency of crop plants:physiological constraints upon nitrogen absorption. Critical Reviews in Plant Sciences 22:453-470.
60. Gomez-Roldan V, Fermas S, Brewer PB, et al. 2008. Strigolactone inhibition of shoot branching. Nature 455:189-194.
61. Gopalakrishnan S, Subbarao GV, Nakahara K, et al. 2007. Nitrification inhibitors from the root tissues of Brachiaria humidicola, a tropical grass. Journal of Agricultural and Food Chemistry 55:1385-1388.
62. Gopalakrishnan S, Watanabe T, Pearse SJ, Ito O, Hossain ZAKM, Subbarao GV. 2009. Biological nitrification inhibition (BNI) by Brachiaria humidicola roots varies with soil type and inhibits nitrifying bacteria, but not other major soil microorganisms. Soil Science and Plant Nutrition 55:725-733.
63. Guthrie TT, Bomke AA. 1980. Nitrification inhibition by N-Serve and ATC in soils with varying texture. Soil Science Society of America Journal 44:314-320.
64. Hari P, Kulmala L. eds. 2008. Boreal forest and climate change. New York:Springer.
65. Harrison K, Bol AR, Bardgett RD. 2007. Preferences for different nitrogen forms by coexisting plant species and soil microbes:comment. Ecology 88:989-999.
66. Hart SC, Stark JM, Davidson EA, Firestone MK. 1994. Nitrogen mineralization, immobilization and nitrification. In:Weaver RW, Angle JS, Bottomley BS. eds. Methods of soil analysis, Part 2. Microbiological and biochemical properties. Madison, WI:Soil Science Society of America, 985-1018.
67. Hauck C, Muller S, Schilknecht H. 1992. A germination stimulant for parasitic flowering plants from Sorghum bicolor, a genuine host plant. Journal of Plant Physiology 139:474-478.
68. Haussmann BIG, Hess DE, Omanya GO, et al. 2004. Genomic regions influencing resistance to the parasitic weed Striga hermonthica in two re-combinant inbred populations of sorghum. Theoretical and Applied Genetics 109:1005-1016.
69. Hawkes CV, Wren IF, Herman DJ, Firestone MK. 2005. Plant invasion alters nitrogen cycling by modifying the soil nitrifying community. Ecology Letters 8:976-985.
70. Haynes RJ, Goh KM. 1978. Ammonium and nitrate nutrition of plants. Biological Reviews 53:465-510.
71. Hendrickson LL, Keeney DR, Walsh LM, Liegel EA. 1978. Evaluation of nitrapyrin as a means of improving N use efficiency in irrigated sands. Agronomy Journal 70:699-708.
72. Hess DE, Ejeta G, Butler LG. 1992. Selecting sorghum genotypes expressing a quantitative biosynthetic trait that confers resistance to Striga. Phytochemistry 31:493-497.
73. Hewins DB, Hyatt LA. 2009. Flexible N uptake and assimilation mechanisms may assist biological invasion by Alliaria petiolata. Biological Invasions 12:2639-2647.
74. Hodge A, Robinson D, Fitter AH. 2000. Are microorganisms more effective than plants at competing for nitrogen? Trends in Plant Science 5:304-308.
75. Hofstra N, Bouwman AF. 2005. Denitrification in agricultural soils:summarizing published data and estimating global annual rates. Nutrient Cycling Agroecosystems 72:267-278.
76. Houlton BZ, Sigman DM, Schuur EAG, Hedin LO. 2007. A climate-driven switch in plant nitrogen acquisition within tropical forest communities. Proceedings of National Academy of Sciences, USA 104:8902-8906.
77. Huber DM, Warren HL, Nelson DW, Tsai CY. 1977. Nitrification inhibitors-new tools for food production. Bioscience 27:523-529.
78. Hungate BA, Dukes JS, Shaw MR, Luo Y, Field CB. 2003. Nitrogen and climate change. Science 302:1512-1513.
79. Iizumi T, Mizumoto M, Nakamura K. 1998. A bioluminescence assay using Nitrosomonas europaea for rapid and sensitive detection of nitrification inhibitors. Applied and Environmental Microbiology 64:3656-3662
80. IPCC (Intergovernmental Panel on Climate Change). 1996. Revised IPCC guidelines for national greenhouse gas inventories:reference manual. London:IPCC
81. IPCC (Intergovernmental Panel on Climate Change). 2007. Climate change:The physical science basis-summary for policy makers. Paris:World Meteorological Organization/United Nations Environmental Program
82. IPCC (Intergovernmental Panel on Climate Change). 2012. Fifth assessment report (AR5). XXXV/Doc. 7. Geneva, Switzerland.
83. Ishikawa T, Subbarao GV, Ito O, Okada K. 2003. Suppression of nitrification and nitrous oxide emission by the tropical grass Brachiaria humidi-cola. Plant and Soil 255:413-419.
84. Islam AKMR, Shepherd KW, Sparrow DHB. 1975. Addition of individual barley chromosomes to wheat. In:Gaul H, Thiemig VK. eds. Proceedings of 3rd international barley genetics symposium. Munich, Germany, 260-270.
85. Jarvis SC. 1996. Future trends in nitrogen research. Plant and Soil 181:47-56.
86. Jordan CF, Todd RL, Escalante G. 1979. Nitrogen conservation in a tropical rain forest. Oecologia 39:123-128.
87. Ju XT, Xing GX, Chen XP, et al. 2009. Reducing environmental risk by improving N management in intensive Chinese agricultural systems. Proceedings of National Academy of Sciences, USA 106:3041-3046.
88. Kahrl E, Li Y, Su Y, Tenngkeit T, Walkes A, Xu J. 2010. Greenhouse gas emissions from nitrogen use in China. Environmental Science Policy 13:688-694.
89. Kramer KJ, Moll HC, Nonhebel S. 1999. Total greenhouse gas emissions related to the Dutch crop production system. Agriculture, Ecosystems and Environment 72:9-16.
90. Kongshaug G. 1998. Energy consumption and greenhouse gas emissions in fertilizer production. IFA Technical Conference, Marrakech, Morocco, 28 September to 1 October, 1998.
91. 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.
92. Kielland K. 2001. Short-circuiting the nitrogen cycle:ecophysiological strategies of nitrogen uptake in plants from marginal environments. In:Ae N, Arihara J, Okada, Srinivasan A. eds. Plant nutrient acquisition:new perspectives, Vol. 17. Tokyo:Springer-Verlag, 376-398.
93. Kishii M. 2011. Production of five Leymus racemosus chromosome transloca-tion lines. e WIS 111:11-13.
94. Kishii M, Yamada T, Sasakuma T, Tsujimoto H. 2004. Production of wheat-Leymus racemosus chromosome addition lines. Theoretical and Applied Genetics 109:255-260.
95. Kroeze C. 1994. Nitrous oxide and global warming. Science Total Environment 143:193-209.
96. Lata JC. 1999. Interactions between microbial processes, nutrient cycle and grass cover functioning:study of soil nitrification under the Gramineae Hyparrhenia diplandra in a wet tropical savanna of Ivory Coast. Ph D Thesis, University of Paris VI, Paris, France.
97. Lata JC, Durand J, Lensi R, Abbadie L. 1999. Stable coexistence of contrasted nitrification statuses in a wet tropical savanna ecosystem. Functional Ecology 13:762-768.
98. Lata JC, Guillaume K, Degrange V, Abbadie L, Lensi R. 2000. Relationships between root density of the African grass Hyparrhenia diplandra and nitrification at the decimetric scale:an inhibition-stimulation balance hypothesis. Proceedings of the Royal Society B:Biological Sciences 267:595-600.
99. Lata JC, Degrange V, Raynaud X, Maron PA, Lensi R, Abbadie L. 2004. Grass populations control nitrification in savanna soils. Functional Ecology 18:605-611.
100. Liao M, Fillery IRP, Palta JA. 2004. Early vigorous growth is a major factor influencing nitrogen uptake in wheat. Functional Plant Biology 31:121-129.
101. Likens GE, Bormann FH, Johnson NM. 1969. Nitrification:importance to nutrient losses from a cutover forested ecosystem. Science 163:1205-1206.
102. Lodhi MAK. 1979. Inhibition of nitrifying bacteria, nitrification and mineralization in spoil soil as related to their successional stages. Bulletin of the Torrey Botanical Club 106:284-289.
103. Lodhi MAK. 1982. Additional evidence of inhibition of nitrifiers and possible cycling of inhibitors produced by selected plants in a climax community. Bulletin of the Torrey Botanical Club 109:199-204.
104. Leninger S, Urich T, Schloter M, et al. 2006. Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 442:806-809.
105. Lukaszewski AJ. 2000. Manipulation of the 1RS.1BL translocation in wheat by induced homoeologous recombination. Crop Science 40:216-225.
106. Magill AH, Aber JD, Benston GM, et al. 2000. Long-term nitrogen additions and nitrogen saturation in two temperate forests. Ecosystems 3:238-253.
107. Maire V, Gross N, da Silveira Pontes L, Picon-Cochard C, Soussana JF. 2009. Trade-off between root nitrogen acquisition and shoot nitrogen utilization across 13 co-occurring pasture grass species. Functional Ecology 23:668-679.
108. Manske GG, Ortiz-Monasterio JI, van Grinkel M, Rajaram S, Molina E, Vlek PLG. 2000. Traits associated with improved P-uptake efficiency in CIMMYT's semi-dwarf spring bread wheat grown on an acid Andisol in Mexico. Plant and Soil 221:189-204.
109. Matson PA, Mc Dowell Townsend AR, Vitousek PM. 1999. The globalization of N deposition:ecosystem consequences in tropical environments. Biogeochemistry 46:67-83.
110. Mc Carty GW. 1999. Modes of action of nitrification inhibitors. Biology and Fertility of Soils 29:1-9.
111. Meiklejohn J. 1968. Numbers of nitrifying bacteria in some Rhodesian soils under natural grass and improved pastures. Journal of Applied Ecology 5:291-300.
112. 4) grasses. Madison, WI:ASA-CSSA-SSA, 745-783.
113. Montagnini F, Haines B, Swank W. 1989. Factors controlling nitrification in soils of early successional and oak/hickory forest in the southern Appalachians. Forest Ecology and Management 26:77-94.
114. Moore DRE, Waid JS. 1971. The influence of washings of living roots on nitrification. Soil Biology and Biochemistry 3:69-83.
115. Mosier AR, Duxbury JM, Freney JR, Heinmeyer O, Minami K. 1996. Nitrous oxide emissions from agricultural fields:assessment, measurement and mitigation. Plant and Soil 181:95-108.
116. Mouquet N, Moore JL, Loreau M. 2002. Plant species richness and community productivity:why the mechanism that promotes coexistence matters. Ecology Letters 5:56-65.
117. Munns R, Hare RA, James RA, Rebetzke GJ. 2000. Genetic variation for improving the salt tolerance of durum wheat. Australian Journal of Agricultural Research 51:69-74.
118. Munro PE. 1966a. Inhibition of nitrifiers by grass root extracts. Journal of Applied Ecology 3:231-238.
119. Munro PE. 1966b. Inhibition of nitrite-oxidizers by roots of grass. Journal of Applied Ecology 3:227-229.
120. Muromtsev GS, Voblikova VD, Kobrina NS, Koreneva VM, Krasnopolskaya LM, Sadovskaya VL. 1994. Occurrence of fusicoc-canes in plants and fungi. Journal of Plant Growth Regulation 13:39-49.
121. Nasholm T, Ekblad A, Nordin A, Gisler R, Hosberg M, Hosberg P. 1998. Boreal forest plants take up organic nitrogen. Nature 392:914-916.
122. Netzly DH, Riopel JL, Ejeta G, Butler LG. 1988. Germination stimulants of witchweed (Striga asiatica) from hydrophobic root exudates of sorghum (Sorghum bicolor). Weed Science 36:441-446.
123. Newbould P. 1989. The use of nitrogen fertilizer in agriculture. Where do we go practically and ecologically? Plant and Soil 115:297-311.
124. Nimbal CI, Pedersen JF, Yerkes CN, Weston LA, Weller SC. 1996. Phytotoxicity and distribution of sorgoleone in grain sorghum. Journal of Agricultural and Food Chemistry 44:1343-1347.
125. Northup PR, Zengshou Y, Dahlgren RA, Vogt KA. 1995. Polyphenol control of nitrogen release from pine litter. Nature 377:227-229.
126. Paavolainen L, Kitunen V, Smolander A. 1998. Inhibition of nitrification in forest soil by monoterpenes. Plant and Soil 205:147-154.
127. 9, 12, 15 fatty acid isolated from Sorghum bicolor root hairs. Journal of Biological Chemistry 282:4326-4335.
128. Patyk A. 1996. Balance of energy consumption and emissions of fertilizer production and supply. Reprints from the International Conference of Life Cycle Assessment in Agriculture, Food and Non-Food Agro-Industry and Forestry:Achievements and Prospects. Brussels, Belgium, 4-5 April, 1996, 73-87.
129. Peterjohn WT, Schlesinger WH. 1990. Nitrogen loss from deserts in the South Western United States. Biogeochemistry 10:67-79.
130. Petit JR, Jouzel J, Raynaud D, et al. 1999. Climate and atmospheric history of the past 420, 000 years from the Vostok ice core, Antarctica. Nature 399:429-436.
131. Philippot L, Hallin S. 2011. Towards food, feed and energy crops mitigating climate change. Trends in Plant Science 16:476-480.
132. 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 90:125-137.
133. Pratt PF, Adriano DC. 1973. Nitrate concentrations in the unsaturated zone beneath irrigated fields in southern California. Soil Science Society of America Proceedings 37:321-322.
134. Purchase BS. 1974. Evaluation of the claim that grass root exudates inhibit nitrification. Plant and Soil 41:527-539.
135. Qi LL, Wang SL, Chen PD, Liu DJ, Friebe B, Gill BS. 1997. Molecular cytogenetic analysis of Leymus racemosus chromosomes added to wheat. Theoretical and Applied Genetics 95:1084-1091.
136. Raaijmakers JM, Paulitz TC, Steinberg C, Alabouvette C, Moenne-Loccoz Y. 2009. The rhizosphere:A playground and battle-field for soil borne pathogens and beneficial microorganisms. Plant and Soil 321:341-361.
137. Ramu P, Deshpande SP, Senthilvel S, et al. 2010. In-silico mapping of important genes and markers available in public domain for efficient sorghum breeding. Molecular Breeding 26:409-418.
138. Rao IM, Kerridge PC, Macedo M. 1996. Adaptation to low fertility acid soils and nutritional requirements of Brachiaria. In:Miles JW, Maas BL, do Valle CB. eds. The biology, agronomy and improvement of Brachiaria. Cali, Colombia:CIAT, 53-71.
139. Raun WR, Johnson GV. 1999. Improving nitrogen use efficiency for cereal production. Agronomy Journal 91:357-363.
140. Raynaud X. 2010. Soil properties are key determinants for the development of exudates gradients in a rhizosphere simulation model. Soil Biology and Biochemistry 42:210-219.
141. Rengel Z, Marschner P. 2005. Nutrient availability and management in the rhizosphere:exploiting genotypic differences. New Phytologist 168:305-312.
142. Rice E, Pancholy SK. 1972. Inhibition of nitrification by climax ecosystems. American Journal of Botany 59:1033-1040.
143. Rice E, Pancholy SK. 1973. Inhibition of nitrification by climax ecosystems II. Additional evidence and possible role of tannins. American Journal of Botany 60:691-702.
144. Rice E, Pancholy SK. 1974. Inhibition of nitrification by climax ecosystems III. Inhibitors other than tannins. American Journal of Botany 61:1095-1103.
145. Rich PJ, Ejeta G. 2007. Biology of host-parasite interactions in Striga species. In:Ejeta G, Gressl J. eds. Integrating new technologies for Striga control:Towards ending the witch-hunt. Singapore:World Scientific Publishing Company PTE LTD, 19-32.
146. Rioual P, Andrieu-Ponel V, Rietti-Shati M, et al. 2001. High-resolution record of climate stability in France during the last interglacial period. Nature 413:293-296.
147. Robinson GP. 1963. Nitrification in a New Zealand grassland soil. Plant and Soil 2:173-183.
148. Robertson GP. 1982a. Nitrification in forested ecosystem. Philosophical Transactions of the Royal Society B:Biological Sciences. 296:445-457.
149. Robertson GP. 1982b. Factors regulating nitrification in primary and secondary succession. Ecology 63:1561-1573.
150. Rodgers GA. 1986. Nitrification inhibitors in agriculture. Journal of Environmental Science and Health A21:701-722.
151. Rockstrom J, Steffen W, Noone K, et al. 2009. A safe operating space for humanity. Nature 461:472-475.
152. Ross SM. 1993. Organic matter in tropical soils:current conditions, concerns and prospects for conservation. Progress in Physical Geography 17:265-305.
153. Rossiter-Rachor NA, Setterfield SA, Douglas MM, Hutley LB, Cook GD, Schmidt S. 2009. Invasive Andropogon gayanus (gamba grass) is an ecosystem transformer of nitrogen relations in Australian savanna. Ecological Applications 19:1546-1560.
154. Sahrawat KL. 1981. Comparison of karanjin with other nitrification inhibitors for retardation of nitrification of urea N in soil. Plant and Soil 59:494-498.
155. Sahrawat KL. 1982. Nitrification in some tropical soils. Plant and Soil 65:281-286.
156. Sahrawat KL. 1989. Effects of nitrification inhibitors on nitrogen transformations other than nitrification in soils. Advances in Agronomy 42:279-309.
157. Sahrawat KL. 1996. Nitrification inhibitors with emphasis on natural products and the persistence of fertilizer nitrogen in the soil. Nitrogen Economy in Tropical Soils 69:379-388.
158. Sahrawat KL. 2008. Factors affecting nitrification in soils. Communications in Soil Sciences and Plant Analysis 39:1436-1446.
159. Sahrawat KL, Keeney DR. 1985. Perspectives for research on development of nitrification inhibitors. Communications in Soil Science and Plant Analysis 16:517-524.
160. Sahrawat KL, Mukerjee SK. 1977. Nitrification inhibitors 1. Studies with Karanjin, a furanoflavonoid from karanja (Pongamia glabra) seeds. Plant and Soil 47:27-36.
161. Sahrawat KL, Mukerjee SK, Gulati KC. 1977. Nitrification inhibitors II. Studies with furano compounds. Plant and Soil 47:687-691.
162. Salsac L, Chaillou S, Morot-Gaudry J, Lesaint C. 1987. Nitrate and ammonium nutrition in plants. Plant Physiology and Biochemistry 25:805-812.
163. Satish K, Gutema Z, Grenier C, Rich PJ, Ejeta G. 2011. Molecular tagging and validation of microsatellite markers linked to the low germination stimulant gene (lgs) for Striga resistance in sorghum [Sorghum bicolor (L.) Moench]. Theoretical and Applied Genetics. 124:989-1003.
164. Schafer A, Victor DG. 1999. Global passenger travel:implications for carbon dioxide emissions. Energy 24:657-679.
165. Schimel JP, Bennett J. 2004. Nitrogen mineralization:challenges of a changing paradigm. Ecology 85:591-602.
166. Schlesinger WH. 2009. On the fate of anthropogenic nitrogen. Proceedings of National Academy of Sciences, USA 106:203-208.
167. Sears ER. 1977. Induced mutant with homoeologous pairing in common wheat. Canadian Journal of Genetics and Cytology 19:585-593.
168. Sears ER. 1993. Use of radiation to transfer alien chromosome segments to wheat. Crop Science 33:897-901.
169. Shaviv A, Mikkelsen RL. 1993. Controlled-release fertilizers to increase efficiency of nutrient use and minimize environmental degradation-A review. Fertilizer Research 35:1-12.
170. Shoji S, Kanno H. 1994. Use of polyolefin-coated fertilizers for increasing fertilizer efficiency and reducing nitrate leaching and nitrous-oxide emissions. Fertilizer Research 39:147-152.
171. Siame BA, Weerasuriya Y, Wood K, Ejeta G, Buttler LG. 1993. Isolation of strigol, a germination stimulant for Striga asiatica from host plants. Journal of Agricultural and Food Chemistry 41:1486-1491.
172. Singh RP, Hodson DP, Jin Y, et al. 2006. Current status, likely migration and strategies to mitigate the threat to wheat production from race Ug99 (TTKS) of stem rust pathogen. CAB Reviews 54:1-13.
173. Slangen J, Kerkhoff P. 1984. Nitrification inhibitors in agriculture and horticulture:A literature review. Fertilizer Research 5:1-76.
174. Smart DR, Bloom AJ. 2001. Wheat leaves emit nitrous oxide during nitrate assimilation. Proceedings of National Academy of Sciences, USA 98:7875-7878.
175. 2O and NO associated with nitrogen fertilization in intensive agriculture, and the potential for mitigation. Soil Use Management 13:296-304.
176. Smith P, Martino D, Cai Z, et al. 2007. Agriculture. In:Metz B, Davidson OR, Bosch PR, Dave R, Meyer LA. eds, Climate change 2007:mitigation. Contribution of working group III to the fourth assessment report of the Intergovernmental Panel on Climate Change. Cambridge:Cambridge University Press, 497-540.
177. Smits NAC, Bobbink R, Laanbrock HJ, Paalman AJ, Hefting MM. 2010a. Repression of potential nitrification activities by matgrass sward species. Plant and Soil 337:435-445.
178. Smits NAC, Hefting MM, Kamst-van Agterveld MP, Laanbroek HJ, Paalman AJ, Bobbink R. 2010b. Nitrification along a grassland gradient:inhibition found in matgrass swards. Soil Biology and Biochemistry 42:635-641.
179. Smolander A, Priha O, Paavolainen L, Steer J, Malkonen E. 1998. Nitrogen and carbon transformation before and after clear-cutting in repeatedly N-fertilized and limed forest soils. Soil Biology and Biochemistry 30:477-490.
180. 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 and Soil 350:1-26.
181. Sommer K, Mertz M, Rossig K. 1976. Stickstoff zu weizen mit ammonium-nitrificiden, mitteilung 2:Proteingehalte, proteinfraktionen und backfahig-keit. Landwirtschaftliche Forschung 29:161-169.
182. Steltzer H, Bowman WD. 1998. Differential influence of plant species on soil nitrogen transformations within moist meadow alpine tundra. Ecosystems 1:464-474.
183. Stienstra AW, Klein Gunnewiek P, Laanbroek HJ. 1994. Repression of nitrification in soils under a climax grassland vegetation. FEMS Microbiological Ecology 14:45-52.
184. Stokstad E. 2007. Deadly wheat fungus threatens world's breadbaskets. Science 315:1786-1787.
185. Subbarao GV, Ito O, Sahrawat KL, et al. 2006a. Scope and strategies for regulation of nitrification in agricultural systems-challenges and opportunities. Critical Reviews in Plant Sciences 25:303-335.
186. 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 and Soil 288:101-112.
187. + triggers the synthesis and release of biological nitrification inhibition compounds in Brachiaria humidicola roots. Plant and Soil 290:245-257.
188. Subbarao GV, Rondon M, Ito O, et al. 2007b. Biological nitrification inhibition (BNI)-is it a widespread phenomenon? Plant and Soil 294:5-18.
189. Subbarao GV, Ban T, Masahiro K, et al. 2007c. Can biological nitrification inhibition (BNI) genes from perennial Leymus racemosus (Triticeae) combat nitrification in wheat farming? Plant and Soil 299:55-64.
190. Subbarao GV, Nakahara K, Ishikawa T, et al. 2008. Free fatty acids from the pasture grass Brachiaria humidicola and one of their methyl esters as inhibitors of nitrification. Plant and Soil 313:89-99.
191. Subbarao GV, Nakahara K, Hurtado MP, et al. 2009a. Evidence for biological nitrification inhibition in Brachiaria pastures. Proceedings of National Academy of Sciences, USA 106:17302-17307.
192. Subbarao GV, Kishii M, Nakahara K, et al. 2009b. Biological nitrification inhibition (BNI)-is there potential for genetic interventions in the Triticeae? Breeding Science 59:529-545.
193. Subbarao GV, Hossain AKMZ, Nakahara K, et al. 2009c. Biological nitrification inhibition (BNI) potential in sorghum. In:The Proceedings of the International Plant Nutrition Colloquium XVI. Department of Plant Sciences, UC Davis, 2009 UC Davis, CA. (E-journal article:http://repositories.cdlib.org/cgi/ viewcontent.cgi/article=1175&context=jpnc/xvi).
194. Subbarao GV, Sahrawat KL, Nakahara K, et al. 2012a. Biological nitrification inhibition-A novel strategy to regulate nitrification in agricultural systems. Advances in Agronomy 114:249-302.
195. Subbarao GV, Nakahara K, Ishikawa T, et al. 2012b. Biological nitrification inhibition (BNI) activity in sorghum and its characterization. Plant and Soil. http://dx.doi.org/10.1007/s11104-012-1419-9.
196. Sutton MA, Oenema O, Erisman JW, Leip A, van Grinsven H, Winiwarter W. 2011. Too much of a good thing. Nature 472:159-161.
197. Sylvester-Bradley R, Mosquera D, Mendez JE. 1988. Inhibition of nitrate accumulation in tropical grassland soils:effects of nitrogen fertilization and soil disturbance. Journal of Soil Science 39:407-416.
198. 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 76:7691-7698.
199. Tiessen H, Cuevas E, Chacon P. 1994. The role of soil organic matter in sustaining soil fertility. Nature 371:783-785.
200. Tilman D, Fargione J, Wolff B, et al. 2001. Forecasting agriculturally driven global environmental change. Science 292:281-284.
201. Tilman D, Cassman KG, Matson PA, Naylor R, Polasky S. 2002. Agricultural sustainability and intensive production practices. Nature 418:671-677.
202. Toyomasu T, Tsukahara M, Kaneko A, et al. 2007. Fusicoccins are bio-synthesized by an unusual chimera diterpene synthase in fungi. Proceedings of National Academy of Sciences, USA 104:3084-3088.
203. 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 107:14926-14930.
204. Vitousek PM, Howarath RW. 1991. Nitrogen limitation on land and in the sea:how can it occur? Biogeochemistry 13:87-115.
205. Vitousek PM, Matson PA. 1984. Mechanisms of nitrogen retention in forest ecosystems:A field experiment. Science 225:51-52.
206. Vitousek PM, Aber JD, Howarth W, et al. 1997. Human alteration of the global nitrogen cycle:sources and consequences. Ecological Applications 7:737-750.
207. Walker TS, Bais HP, Grotewold E, Vivanco JM. 2003. Root exudation and rhizosphere biology. Plant Physiology 132:44-51.
208. Weigelt A, Bol R, Bardgett RD. 2005. Preferential uptake of soil nitrogen forms by grassland species. Oecologia 142:627-635.
209. 4) oxidation during 3 years of repeated applications in field experiments. Nutrient Cycling in Agroecosystems 60:57-64.
210. White C. 1991. The role of monoterpenes in soil nitrogen cycling processes in ponderosa pine. Biogeochemistry 12:43-68.
211. Woldendorp JW, Laanbroek HJ. 1989. Activity of nitrifiers in relation to nitrogen nutrition of plants in natural ecosystems. Plant and Soil 115:217-228.
212. Wolt JD. 2004. A meta-evaluation of nitrapyrin agronomic and environmental effectiveness with emphasis on corn production in the mid-Western USA. Nutrient Cycling in Agroecosystems 69:23-41.
213. Xie X, Yoneyama K, Kusumoto D, et al. 2008. Sorgomol germination stimulant for root parasitic plants, produced by Sorghum bicolor. Tetrahedron Letters 49:2066-2068.
214. Yoneyama K, Xie X, Kusumoto D, et al. 2007. Nitrogen deficiency as well as phosphorus deficiency in sorghum promotes the production and exudation of 5-deoxystrigol, the host recognition signal for arbuscular mycorrhizal fungi and root parasites. Planta 227:125-132.
215. Yoneyama K, Awad AA, Xie X, Yoneyama K, Takeuchi Y. 2010. Strigolactones as germination stimulants for root parasitic plants. Plant and Cell Physiology 51:1095-1103.
216. Zahn LM. 2007. A boost from wild wheat. Science 318:171.
217. Zakir HAKM, Subbarao GV, Pearse SJ, et al. 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 180:442-451.
218. Zerulla W, Barth T, Dressel J, et al. 2001. 3, 4-Dimethylpyrazole phosphate (DMPP)-A new nitrification inhibitor for agriculture and horticulture. Biology and Fertility of Soils 34:79-84.
219. +-ATPase determine the release of BNIs in sorghum roots-possible mechanisms and underlying hypothesis. Plant and Soil 358:131-141.
220. Zvomuya F, Rosen CJ, Russelle MP, Gupta SC. 2003. Nitrate leaching and nitrogen recovery following application of polyefincoated urea to potato. Journal of Environmental Quality 32:480-489.