Skip to main content
Log in

Biological nitrification inhibition in sorghum: the role of sorgoleone production

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Background and aims

Nitrification and denitrification are the two most important processes that contribute to greenhouse gas emission and inefficient use of nitrogen. Suppressing soil nitrification through the release of nitrification inhibitors from roots is a plant function, and termed “Biological Nitrification Inhibition (BNI)”. We report here the role and contribution of sorgoleone release to sorghum-BNI function.

Methods

Three sorghum genotypes (Hybridsorgo, IS41245 and GDLP 34-5-5-3) were evaluated for their capacity to release sorgoleone, which has BNI-activity, in hydroponic and soil culture. Sorgoleone released was measured using HPLC; BNI-activity was determined using a luminescent recombinant Nitrosomonas europaea assay.

Results

Sorgoleone production and BNI-activity release by roots are closely associated (1 μg of sorgoleone is equivalent to 1 ATU activity in assay). Purified sorgoleone inhibited Nitrosomonas activity and suppressed soil nitrification. Sorghum genotypes release varying quantity of sorgoleone; GDLP 34-5-5-3 and Hybridsorgo showed higher capacity for both sorgoleone release and BNI-activity than did IS41245. In soil culture, GDLP 34-5-5-3 released higher quantity of sorgoleone into the rhizosphere, which had higher BNI-activity, and suppressed soil nitrification to a greater extent than did by IS41245.

Conclusions

These results demonstrate genetic differences for sorgoleone release and its functional link with BNI-capacity; there is potential for genetic improvement of sorghum BNI-capacity and deployment of this in low-nitrifying sorghum production systems.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Allison FE (1966) The fate of nitrogen applied to soils. Adv Agron 18:219–258

    Article  CAS  Google Scholar 

  • Alsaadawi IS, Al-Uqaili JK, Alrubeaa AJ, Al-Hadithy SM (1985) Allelopathic suppression of weed and nitrification by selected cultivars of Sorghum bicolor(L.)Moench. J Chem Ecol 12:209–218

    Article  Google Scholar 

  • Anon (1974) Technicon autoanalyzer II. Technicon Industrial Systems, Tarrytown

    Google Scholar 

  • Bertin C, Yang X, Weston LA (2003) The role of root exudates and allelochemicals in the rhizosphere. Plant Soil 256:67–83

    Article  CAS  Google Scholar 

  • Bremner JM, Blackmer AM (1978) Nitrous oxide: emission from soils during nitrification and denitrification of fertilizer nitrogen. Science 199:295–296

    Article  CAS  PubMed  Google Scholar 

  • Chain P, Lamerdin J, Larimer F, Regala W, Lao V, Land M, Hauser L, Hooper A, Klotz M, Norton J et al (2003) Complete genome sequence of the ammonia-oxidizing bacterium and obligate chemolithoautotroph Nitrosomonaseuropaea. J Bacteriol 185:2759–2773

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Czarnota MA, Paul RN, Dayan FE, Nimbal CI, Leslie A, Weston LA (2001) Mode of action, localization of production, chemical nature, and activity of sorgoleone: a potent PSII inhibitor in Sorghum spp. root exudates. Weed Technol 15:813–825

    Article  CAS  Google Scholar 

  • Czarnota MA, Rimando AM, Weston LA (2003) Evaluation of seven sorghum (Sorghum sp.) accessions. J Chem Ecol 29:2073–2083

    Article  CAS  PubMed  Google Scholar 

  • Dayan FE (2006) Factors modulating the levels of the allelo-chemical sorgoleone in Sorghum bicolor. Planta 224:339–346

    Article  CAS  PubMed  Google Scholar 

  • Dayan FE, Howell J, Weidenhamer JD (2009) Dynamic root exudation of sorgoleone and its in plant mechanism of action. J Exp Bot 60:2107–2117

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Gimsing AL, Baelum J, Dayan FE, Locke M, Sejero LH, Jacobsen CS (2009) Mineralization of the allelochemical sorgoleone in soil. Chemosphere 76:1041–1047

    Article  CAS  PubMed  Google Scholar 

  • Hadas A, Hadas A, Sagiv B, Haruvy N (1999) Agricultural practices, soil fertility management modes and resultant nitrogen leaching rates under semi-arid conditions. Agric Water Manag 42:81–95

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Hejl AM, Koster KL (2004) The allelochemical sorgoleone inhibits root H+-ATPase and water uptake. J Chem Ecol 30:2181–2191

    Article  CAS  Google Scholar 

  • Hofstra N, Bouwman AF (2005) Denitrification in agricultural soils: summarizing published data and estimating global annual rates. Nutr Cycl Agroecosyst 72:267–278

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Jones N (2013) Grass gets greener. Nature 501:291

    Article  CAS  PubMed  Google Scholar 

  • Klotz MG, Arp DJ, Chain PS, El-Sheikh AF, Hauser LJ, Hommes NG, Larimer FW, Malfatti SA, Norton JM, Poret-Peterson AT et al (2006) Complete genome sequence of the marine, chemolitho-autotrophic, ammonia oxidizing bacterium Nitrosococcusoceani ATCC 19707. Appl Environ Microbiol 72:6299–6315

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lata JC, Durand J, Lensi R, Abbadie L (1999) Stable coexistence of contrasted nitrification statuses in a wet tropical savanna system. Fun Ecol 13:762–763

    Article  Google Scholar 

  • Lata JC, Degrange V, Raynaud X, Maron PA, Lensi R, Abbadie L (2004) Grass populations control nitrification in savanna soils. Fun Ecol 18:605–611

    Article  Google Scholar 

  • Moore DRE, Waid JS (1971) The influence of washing of living roots on nitrification. Soil Biol Biochem 3:69–83

    Article  CAS  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 181:95–108

    Article  CAS  Google Scholar 

  • Netzly DH, Butler LG (1986) Roots of sorghum exude hydrophobic droplets containing biologically active components. Crop Sci 26:775–778

    Article  CAS  Google Scholar 

  • Nimbal CI, Pedersen JF, Yerkes CN, Weston LA, Weller SC (1996a) Phytotoxicity and distribution of sorgoleone in grain sorghum germplasm. J Agric Food Chem 44:1343–1347

    Article  CAS  Google Scholar 

  • Nimbal CI, Yerkes CN, Weston LA, Weller SC (1996b) Herbicidal activity and site of action of the natural product sorgoleone. Pestic Biochem Physiol 54:73–83

    Article  CAS  Google Scholar 

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

    Google Scholar 

  • Schlesinger WH (2009) On the fate of anthropogenic nitrogen. PNAS (USA) 106:203–208

    Article  CAS  Google Scholar 

  • Shen JP, Zhang LM, Di HJ, He JZ (2012) A review of ammonia-oxidizing bacteria and archaea in Chinese soils. Front Microbiol 3:1–7

    Google Scholar 

  • Smith CW, Frederiksen RA (2000) Sorghum: origin, history, technology, and production. Wiley, New York

    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 Manag 13:296–304

    Article  Google Scholar 

  • Starkenburg SR, Chain PS, Sayavedra-Soto LA, Hauser L, Land ML, Larimer FW, Malfatti SA, Klotz MG, Bottomley PJ, Arp DJ et al (2006) Genome sequence of the chemo-litho autotrophic nitrite-oxidizing bacterium Nitrobacterwinogradskyi Nb-255. Appl Environ Microbiol 72:2050–2063

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Subbarao GV, Ishikawa T, Ito O, Nakahara K, Wang HY, Berry WL (2006) A bioluminescence assay to detect nitrification inhibitors released from plant roots: a case study with Brachiaria humidicola. Plant 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 Soil 294:5–18

    Article  CAS  Google Scholar 

  • Subbarao GV, Wang HY, Ito O, Nakahara K, Berry WL (2007b) NH4 + triggers the synthesis and release of biological nitrification inhibition compounds in Brachiaria humidicola roots. Plant 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 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. PNAS (USA) 106:17302–17307

    Article  CAS  Google Scholar 

  • Subbarao GV, Nakahara K, Ishikawa T, Ono H, Yoshida M, Yoshihashi T, Zhu Y, Zakir HAKM, Deshpande SP et al (2013a) Biological nitrification inhibition (BNI) activity in sorghum and its characterization. Plant Soil 366:243–259

    Article  CAS  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). Ann Bot 112:297–316

    Article  CAS  PubMed  Google Scholar 

  • Subudhi PK, Nguyen HT (2000) Linkage group alignment of sorghum RFLP maps using a RIL mapping population. Genome 43:240–249

    Article  CAS  PubMed  Google Scholar 

  • Treusch AH, Leininger S, Kletzin A, Schuster SC, Klenk HP, Schleper C (2005) Novel genes for nitrite reductase and Amo-related proteins indicate a role of uncultivated mesophilic crenarchaeota in nitrogen cycling. Env Microbiol 7:1985–1995

    Article  CAS  Google Scholar 

  • Uddin MR, Park KW, Kim YK, Park SU, Pyon JY (2010) Enhancing sorgoleone levels in grain sorghum root exudates. J Chem Ecol 36:914–922

    Article  CAS  PubMed  Google Scholar 

  • Walker CB, de la Torre JR, Klotz MG, Urakawa H, Pinel N, Arp DJ, Brochier-Armanet C, Chain PSG, Chan PP, Gollabgir A, Hemp J, Huegler M, Karr EA, Koenneke M, Shin M, Lawton TJ, Lowe T, Martens-Habbena W, Sayavedra-Soto LA, Lang D, Sievert SM, Rosenzweig AC, Manning G, Stahl DA (2010) Nitrosopumilus maritimus genome reveals unique mechanisms for nitrification and autotrophy in globally distributed marine crenarchaea. Proc Natl Acad Sci USA 107(19):8818–8823

    Google Scholar 

  • Weston LA (1996) Utilization of allelopathy for weed management in agroecosystems. Agron J 88:860–866

    Google Scholar 

  • Yang X, Owens TG, Scheffler BE, Weston LA (2004) Manipulation of root hair development and sorgoleone production in sorghum seedlings. J Chem Ecol 30:199–213

    Article  CAS  PubMed  Google Scholar 

  • Zakir H, 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 Phytol 180:442–451

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This research work was supported by JIRCAS fellowship program 2011. This work has been undertaken as part of the CGIAR Research Program on Dryland Cereals.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to G. V. Subbarao.

Additional information

Responsible Editor: Tim Simon George.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Tesfamariam, T., Yoshinaga, H., Deshpande, S.P. et al. Biological nitrification inhibition in sorghum: the role of sorgoleone production. Plant Soil 379, 325–335 (2014). https://doi.org/10.1007/s11104-014-2075-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-014-2075-z

Keywords

Navigation