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Identification of several wheat landraces with biological nitrification inhibition capacity

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Abstract

Background and aims

Nitrification is the first step in several pathways that lead to losses of nitrogen from agricultural systems. Biological nitrification inhibition (BNI) refers to the ability of some plant species to release chemicals from their roots that inhibit microbial ammonia oxidation thereby decreasing nitrification rates. BNI has been found in the wheat relative Leymus racemosus but not in Triticum aestivum. The aim of this work was to assess a number of landraces of Triticum aestivum for BNI ability.

Methods

Samples of root exudates and root tissue extracts, collected from hydroponically grown plants, were tested for their impact on nitrification rates when inoculated with pure cultures of two ammonia oxidising bacteria, Nitrosomonas europaea and Nitrosospira multiformis. Pot experiments were then conducted to confirm the results.

Results

The vast majority of the landraces tested caused some level of inhibition. However, of the 96 wheat landraces tested, 26 produced root exudates which caused a statistically significant reduction in nitrification rates of the two ammonia oxidising bacteria. Root exudates from four of the BNI positive landraces were shown to significantly inhibit nitrification rates in a sandy loam soil.

Conclusions

This is the first evidence of significant levels of BNI in Triticum aestivum. The discovery of landraces with BNI ability raises the potential for breeding this trait into modern, elite wheat cultivars.

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References

  • Amberger A (1989) Research on dicyandiamide as a nitrification inhibitor and future outlook. Communications in Soil Science and Plant Analysis 20:1933–1955

  • Arp DJ, Stein LY (2003) Metabolism of inorganic N compounds by ammonia-oxidizing bacteria. Critical Reviews in Biochemistry and Molecular Biology 38:471–495

    Article  CAS  PubMed  Google Scholar 

  • Chen PD, Liu WX, Yuan JH, Wang X, Zhou B, Wang SL, Zhang SZ, Feng YG, Yang BJ, Liu GX, Liu DJ, Qi LL, Zhang P, Friebe B, Gill BS (2005) Development and characterization of wheat- Leymus racemosus translocation lines with resistance to fusarium head blight. Theoretical and Applied Genetics 111:941–948

    Article  PubMed  Google Scholar 

  • Chen DL, Suter HC, Islam A, Edis R (2010) Influence of nitrification inhibitors on nitrification and nitrous oxide (N2O) emission from a clay loam soil fertilized with urea. Soil Biology & Biochemistry 42:660–664

    Article  CAS  Google Scholar 

  • Chen QH, Qi LY, Bi QF, Dai PB, Sun DS, Sun CL, Liu WJ, Lu LL, Ni WZ, Lin XY (2015) Comparative effects of 3,4-dimethylpyrazole phosphate (DMPP) and dicyandiamide (DCD) on ammonia-oxidizing bacteria and archaea in a vegetable soil. Applied Microbiology and Biotechnology 99:477–487

    Article  CAS  PubMed  Google Scholar 

  • Di HJ, Cameron KC, Shen JP, He JZ, Winefield CS (2009a) A lysimeter study of nitrate leaching from grazed grassland as affected by a nitrification inhibitor, dicyandiamide, and relationships with ammonia oxidizing bacteria and archaea. Soil Use and Management 25:454–461

    Article  Google Scholar 

  • Di HJ, Cameron KC, Shen JP, Winefield CS, O’Callaghan M, Bowatte S, He JZ (2009b) Nitrification driven by bacteria and not archaea in nitrogen-rich grassland soils. Nature Geoscience 2:621–624

    Article  CAS  Google Scholar 

  • Di HJ, Cameron KC, Sherlock RR, Shen JP, He JZ, Winefield CS (2010) Nitrous oxide emissions from grazed grassland as affected by a nitrification inhibitor, dicyandiamide, and relationships with ammonia-oxidizing bacteria and archaea. Journal of Soils and Sediments 10:943–954

    Article  CAS  Google Scholar 

  • Erguder TH, Boon N, Wittebolle L, Marzorati M, Verstraete W (2009) Environmental factors shaping the ecological niches of ammonia-oxidizing archaea. Fems Microbiology Reviews 33:855–869

    Article  CAS  PubMed  Google Scholar 

  • Fillery IRP (1999) Monitoring water and nutrient fluxes down the profile: closing the nutrient budget. In: Rengel Z (ed) Mineral nutrition of crops: fundamental mechanisms and implications. Food Products Press, Binghamton, pp 289–325

    Google Scholar 

  • Fillery IRP (2007) Plant-based manipulation of nitrification in soil: a new approach to managing N loss? Plant and Soil 294:1–4

    Article  CAS  Google Scholar 

  • Focht DD, Verstraete W (1977) Biochemical ecology of nitrification and denitrification. Advances in Microbial Ecology 1:134–214

    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 Agricultural and Food Chemistry 55:1385–1388

    Article  CAS  PubMed  Google Scholar 

  • Hu H-W, Xu Z-H, He J-Z (2014) Ammonia-oxidizing archaea play a predominant role in acid soil nitrification. In: DL Sparks (ed) Advances in Agronomy, Vol 125

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

    Article  CAS  Google Scholar 

  • Jia ZJ, Conrad R (2009) Bacteria rather than archaea dominate microbial ammonia oxidation in an agricultural soil. Environmental Microbiology 11:1658–1671

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Leininger 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

    Article  CAS  PubMed  Google Scholar 

  • Liu R, Hayden H, Suter H, He JZ, Chen DL (2015) The effect of nitrification inhibitors in reducing nitrification and the ammonia oxidizer population in three contrasting soils. Journal of Soils and Sediments 15:1113–1118

  • McCarty GW (1999) Modes of action of nitrification inhibitors. Biology and Fertility of Soils 29:1–9

    Article  CAS  Google Scholar 

  • Moreta DE, Arango J, Sotelo M, Vergara D, Rincon A, Ishitani M, Castro A, Miles J, Peters M, Tohme J, Subbarao GV, Rao IM (2014) Biological nitrification inhibition (BNI) in Brachiaria pastures: a novel strategy to improve eco-efficiency of crop-livestock systems and to mitigate climate change. Tropical Grasslands - Forrajes Tropicales. Centro Internacional de Agricultura Tropical (CIAT), Cali

    Google Scholar 

  • Norton JM, Stark JM (2011) Regulation and measurement of nitrification in terrestrial systems. In: Klotz MG (ed) Methods in Enzymology: Research on Nitrification and Related Processes, Vol 486, Part A. Elsevier Academic Press Inc, San Diego, pp 343–368

    Chapter  Google Scholar 

  • O’Sullivan CA, Wakelin SA, Fillery IRP, Roper MM (2013) Factors affecting ammonia-oxidising microorganisms and potential nitrification rates in southern Australian agricultural soils. Soil Research 51:240–252

    Article  Google Scholar 

  • Parkin TB, Hatfield JL (2010) Influence of nitrapyrin on N2O losses from soil receiving fall-applied anhydrous ammonia. Agriculture Ecosystems & Environment 136:81–86

    Article  CAS  Google Scholar 

  • Prosser JI, Nicol GW (2012) Archaeal and bacterial ammonia-oxidisers in soil: the quest for niche specialisation and differentiation. Trends in Microbiology 20:523–531

    Article  CAS  PubMed  Google Scholar 

  • Raun WR, Johnson GV (1999) Improving nitrogen use efficiency for cereal production. Agronomy Journal 91:357–363

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Saari A, Martikainen PJ (2001) Differential inhibition of methane oxidation and nitrification in forest soils by dimethyl sulfoxide (DMSO). Soil Biology & Biochemistry 33:1567–1570

    Article  CAS  Google Scholar 

  • Schleper C, Nicol GW (2010) Ammonia-Oxidising Archaea - Physiology, ecology and evolution. In: Advances in Microbial Physiology, Vol 57. Academic Press Ltd-Elsevier Science Ltd, London, pp 1–41

    Chapter  Google Scholar 

  • Shen JP, Zhang LM, Zhu YG, Zhang JB, He JZ (2008) Abundance and composition of ammonia-oxidizing bacteria and ammonia-oxidizing archaea communities of an alkaline sandy loam. Environmental Microbiology 10:1601–1611

    Article  CAS  PubMed  Google Scholar 

  • Subbarao GV, Ishikawa T, Ito O, Nakahara K, Wang HY, Berry WL (2006) A biolumiuescence assay to detect nitrification inhibitors released from plant roots: a case study with Brachiaria humidicola. Plant and Soil 288:101–112

    Article  CAS  Google Scholar 

  • Subbarao GV, Rondon M, Ito O, Ishikawa T, Rao IM, Nakahara K, Lascano C, Berry WL (2007a) Biological nitrification inhibition (BNI) - is it a widespread phenomenon? Plant and Soil 294:5–18

    Article  CAS  Google Scholar 

  • Subbarao GV, Tomohiro B, Masahiro K, Osamu I, Samejima H, Wang HY, Pearse SJ, Gopalakrishnan S, Nakahara K, Hossain A, Tsujimoto H, Berry WL (2007b) Can biological nitrification inhibition (BNI) genes from perennial Leymus racemosus (Triticeae) combat nitrification in wheat farming? Plant and Soil 299:55–64

    Article  CAS  Google Scholar 

  • Subbarao GV, Wang HY, Ito O, Nakahara K, Berry WL (2007c) NH4 + triggers the synthesis and release of biological nitrification inhibition compounds in Brachiaria humidicola roots. Plant and Soil 290:245–257

    Article  CAS  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 inhibitors of nitrification. Plant and Soil 313:89–99

    Article  CAS  Google Scholar 

  • Subbarao GV, Nakahara K, Hurtado MP, Ono H, Moreta DE, Salcedo AF, Yoshihashi AT, Ishikawa T, Ishitani M, Ohnishi-Kameyama M, Yoshida M, Rondon M, Rao IM, Lascano CE, Berry WL, Ito O (2009) Evidence for biological nitrification inhibition in Brachiaria pastures. Proceedings of the National Academy of Sciences of the United States of America 106:17302–17307

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Suzuki I, Kwok SC, Dular U (1976) Competitive inhibition of ammonia oxidation in Nitrosomonas europaea by methane, carbon monoxide or methanol. Febs Letters 72:117–120

    Article  CAS  PubMed  Google Scholar 

  • Swezey AW, Turner GO (1962) Crop experiments on effect of 2-chloro-6-(trichloromethyl)pyridine for control of nitrification of ammonium and urea fertilizers. Agronomy Journal 54:532–534

    Article  CAS  Google Scholar 

  • Tanaka JP, Nardi P, Wissuwa M (2010) Nitification inhibition activity, a novel trait in root exudates of rice. Ann Bot Plants 2010:plq014

    Google Scholar 

  • Weaver RW, Angle JS, Bottomley BS, Hart SC, Stark JM, Davidson EA, Firestone MK (1994) Nitrogen mineralization, immobilization, and nitrification. In: Methods of Soil Analysis. Part 2. Microbiological and Biochemical Properties, SSSA Book Series. SSSA, Madison

    Google Scholar 

  • White CS (1986) Volatile and water soluble inhibitors of nitrogen mineralisation and nitrification in a Poderosa pine ecosystem. Biology and Fertility of Soils 2:97–104

    Google Scholar 

  • White CS (1988) Nitrification inhibition by monoterpenoids: theoretical mode of action based on molecular structures. Ecology 69:1631–1633

    Article  CAS  Google Scholar 

  • White CS (1991) The role of monoterpenes in soil nitrogen cycling processes in Ponderosa pine: results from laboratory bioassays and field studies. Biogeochemistry 12:43–68

    Article  CAS  Google Scholar 

  • Zakir H, Subbarao GV, Pearse SJ, Gopalakrishnan S, 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 180:442–451

    Article  CAS  PubMed  Google Scholar 

  • Zerulla W, Barth T, Dressel J, Erhardt K, von Locquenghien KH, Pasda G, Radle M, Wissemeier AH (2001) 3,4-Dimethylpyrazole phosphate (DMPP) - a new nitrification inhibitor for agriculture and horticulture - An introduction. Biology and Fertility of Soils 34:79–84

    Article  CAS  Google Scholar 

  • Zou HY, Zhang WT, Feng YY, Liang B (2014) Simultaneous determination of melamine and dicyandiamide in milk by UV spectroscopy coupled with chemometrics. Analytical Methods 6(15):5865–5871

    Article  CAS  Google Scholar 

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Acknowledgements

This work was funded by Bayer CropScience. The authors would like to thank Mrs Karen Treble for the technical assistance that she provided to support these experiments and the staff from the Australian Winter Cereals Collection for making available the seeds of the wheat landraces. We also thank the staff from The Department of Agriculture and Food, Western Australia for allowing access to the Vasse Research Station for soil sampling.

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Correspondence to Cathryn A. O’Sullivan.

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Responsible Editor: Elizabeth M Baggs.

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O’Sullivan, C.A., Fillery, I.R.P., Roper, M.M. et al. Identification of several wheat landraces with biological nitrification inhibition capacity. Plant Soil 404, 61–74 (2016). https://doi.org/10.1007/s11104-016-2822-4

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