Abstract
Using a recombinant luminescent Nitrosomonas europaea assay to quantify biological nitrification inhibition (BNI), we found that a wild relative of wheat (Leymus racemosus (Lam.) Tzvelev) had a high BNI capacity and releases about 20 times more BNI compounds (about 30 ATU g−1 root dry weight 24 h−1) than Triticum aestivum L. (cultivated wheat). The root exudate from cultivated wheat has no inhibitory effect on nitrification when applied to soil; however, the root exudate from L. racemous suppressed \( {\text{NO}}^{ - }_{3} \) formation and kept more than 90% of the soil’s inorganic-N in the \( {\text{NH}}^{ + }_{4} \)-form for 60 days. The high-BNI capacity of L. racemosus is mostly associated with chromosome Lr#n. Two other chromosomes Lr#J, and Lr#I also have an influence on BNI production. Tolerance of L. racemosus to \( {\text{NH}}^{ + }_{4} \) is controlled by chromosome 7Lr#1-1. Sustained release of BNI compounds occurred only in the presence of \( {\text{NH}}^{ + }_{4} \) in the root environment. Given the level of BNI production expressed in DALr#n and assuming normal plant growth, we estimated that nearly 87,500,000 ATU of BNI activity ha−1 day−1 could be released in a field of vigorously growing wheat; this amounts to the equivalent of the inhibitory effect from the application of 52.5 g of the synthetic nitrification inhibitor nitrapyrin (one AT unit of BNI activity is equivalent to 0.6 μg of nitrapyrin). At this rate of BNI production it would take only 19 days for a BNI-enabled wheat crop to produce the inhibitory power of a standard commercial application of nitrapyrin, 1 kg ha−1. The synthetic nitrification inhibitor, dicyandiamide, blocked specifically the AMO (ammonia monooxygenase) pathway, while the BNI from L. racemosus blocked the HAO (hydroxylamine oxidoreductase) pathway in Nitrosomonas. Here we report the first finding of high production of BNI in a wild relative of any cereal and its successful introduction and expression in cultivated wheat. These results demonstrate the potential for empowering the new generation of wheat cultivars with high-BNI capacity to control nitrification in wheat-production systems.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Anonymous (1974) Technicon Autoanalyzer II, Technicon Industrial Systems, Tarrytown
Belser LW, Schmidt EL (1981) Inhibiting effect of nitrapyrin on three genera of ammonia oxidizing nitrifiers. Appl Environ Microbiol 41:819–821
Britto DT, Kronzucker HJ (2002) \( {\text{NH}}^{ + }_{4} \) toxicity in higher plants: a critical review. J Plant Physiol 159:567–584
Chen P, Liu W, Yuan J, Wang X, Zhou B, Wang S, Zhang S, Feng Y, Yang B, Liu G, Liu D, Qi L, Zhang P, Friebe B, Gill BS (2005) Development and characterization of wheat-Leymus racemosus translocation lines with resistance to Fusarium head blight. Theor Appl Genet 111:941–948
Friebe B, Jiang J, Gill BS, Dyck PL (1993) Radiation-induced non-homologous wheat-Agropyron intermedium chromosome translocations conferring resistance to leaf rust. Theor Appl Genet 86:141–149
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. J Agric Food Chem 55:1385–1388
Hughes TD, Welch LF (1970) 2-Chloro-6(trichloromethyl) pyridine as a nitrification inhibitor for anhydrous ammonia applied in different seasons. Agron J 62:821–824
Ishikawa T, Subbarao GV, Ito O, Okada K (2003) Suppression of nitrification and nitrous oxide emission by the tropical grass Brachiaria humidicola. Plant Soil 255:413–419
Kishii M, Wang RRC, Tsujimoto H (2003) Characteristics and behavior of the chromosomes of Leymus mollis and L. racemosus (Triticeae, Poaceae) during mitosis and meiosis. Chomosom Res 11:741–748
Kishii M, Yamada T, Sasakuma T, Tsujimoto H (2004) Production of wheat-Leymus racemosus chromosome addition lines. Theor Appl Genet 109:255–260
Lata JC, Degrange V, Raynaud X, Maron PA, Lensi R, Abbadie I (2004) Grass population control nitrification in Savanna soils. Funct Ecol 13:762–763
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 442:806–809
Litchfield MD (1967) The automated analysis of nitrite and nitrate in blood. Analyst 92:132–136
McCarty GW (1999) Modes of action of nitrification inhibitors. Biol Fertil Soils 29:1–9
Mosier AR, Duxbury JM, Freney JR, Heinemeyer O, Minami K (1996) Nitrous oxide emissions from agricultural fields: assessment, measurement, and mitigation. Plant Soil 181:95–108
Norton JM, Alzerreca JJ, Suwa Y, Klotz MG (2002) Diversity of ammonia monooxygenase operon in autotrophic ammonia oxidizing bacteria. Arch Microbiol 177:139–149
Oliver RE, Cai X, Xu SS, Chen X, Stack RW (2005) Wheat-alien species derivatives: A novel source of resistance to Fusarium head blight in wheat. Crop Sci 45:1353–1360
Powell SJ, Prosser JI (1986) Effect of copper on inhibition by nitrapyrin of growth of Nitrosomonas europaea. Curr Microbiol 14:177–179
Qi LL, Wang SL, Chen PD, Liu DJ, Friebe B, Gill BS (1997) Molecular cytogenetic analysis of Leymus racemosus chromosomes added to wheat. Theor Appl Genet 95:1084–1091
Savin R, Hall AJ, Satorre EH (1994) Testing the root growth subroutine of the CERES-Wheat model for two cultivars of different cycle length. Field Crops Res 38:125–133
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. Crit Rev Plant Sci 25:303–335
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 288:101–112
Subbarao GV, Wang HY, Ito O, Nakahara K, Berry WL (2007a) \( {\text{NH}}^{ + }_{4} \) triggers the synthesis and release of biological nitrification inhibition compounds in Brachiaria humidicola roots. Plant Soil 290:245–257
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 294:5–18
Subbarao GV, Ishikawa T, Nakahara K, Ito O, Rondon M, Rao IM, Lascano C (2007c) Characterization of biological nitrification inhibition (BNI) capacity in Brachiaria humidicola. JIRCAS Work Rep 51:99–106
Subbarao GV, Rondon M, Rao IM, Ishikawa T, Ito O, Hurtado MP, Amezquita E, Barrios E, Lascano C (2007d) Field evaluation of the phenomenon of nitrification inhibition by Brachiaria humidicola and other tropical grasses. JIRCAS Work Rep 51:107–112
Varley JA (1966) Automated method for the determination of nitrogen, phosphorus and potassium in plant material. Analyst 91:119–126
Ward BB, Courtney KJ, Langenheim JH (1997) Inhibition of Nitrosomonas europaea by monoterpenes from coastal redwood (Sequoia sempervirens) in whole-cell studies. J Chem Ecol 23:2583–2598
Acknowledgements
We wish to acknowledge the support from the Government of Japan through the Japan-CIMMYT FHB collaborative research project. We are particularly grateful to Dr. Masa Iwanaga, the director general of CIMMYT for providing guidance, inspiration and encouragement during the drafting of this manuscript.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible Editor: Hans Lambers.
Rights and permissions
About this article
Cite this article
Subbarao, G.V., Tomohiro, B., Masahiro, K. et al. Can biological nitrification inhibition (BNI) genes from perennial Leymus racemosus (Triticeae) combat nitrification in wheat farming?. Plant Soil 299, 55–64 (2007). https://doi.org/10.1007/s11104-007-9360-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-007-9360-z