Abstract
Purpose
Rapid nitrification leads to loss of nitrogen (N) fertilizer in agricultural systems. Plant produced/derived biological nitrification inhibitors (BNIs) are an effective eco-strategy to rein-in soil nitrification to improve crop-N uptake and nitrogen use efficiency (NUE) in production systems. Sorgoleone is the major component of hydrophobic-BNI-activity in sorghum roots. However, the role of genetic differences in sorgoleone production in reducing soil nitrification and N2O emissions are not established.
Methods
Two genetic-stocks of sorghum with high-sorgoleone (HS), and two with low-sorgoleone (LS) production from roots were grown using hydroponics in a plant-growth chamber, in soil in pots in a glasshouse, and in a field experiment. Release of hydrophilic-BNI activity from roots of HS and LS genetic stocks, sorgoleone levels in rhizosphere soils, soil nitrification rates, soil-nitrifier activity and N2O emissions were measured to understand the interplay involving sorgoleone release, hydrophilic-BNI release from roots, soil nitrification, plant growth and N uptake.
Results
HS-producing genetic-stocks showed higher hydrophilic-BNI-capacity compared to LS- producing genetic-stocks. Biomass production and N uptake were significantly higher in HS than in LS genetic-stocks. Glasshouse and field studies suggest that HS genetic stocks had stronger suppressive impact on soil-nitrifier-populations (ammonia-oxidizing archaea and ammonia-oxidizing bacteria), soil-nitrification, and soil-N2O emissions than in LS genetic-stocks.
Conclusion
These results demonstrate that HS sorghum genetic-stocks suppress soil nitrifier activity and can potentially reduce N losses from NO3 − leaching and N2O emissions more effectively than LS genetic-stocks.
Similar content being viewed by others
Data availability
The datasets generated during the current study are available from the corresponding author on reasonable request.
References
Afzal MR, Zhang M, Jin H, Wang G, Zhang M, Ding M, Raza S, Hu J, Zeng H, Gao X, Subbarao GV, Zhu Y (2020) Post-translation regulation of plasma membrane H+-ATPase is involved in the release of biological nitrification inhibitors from sorghum roots. Plant Soil 450:357–372. https://doi.org/10.1007/s11104-020-04511-6
Britto D, Kronzucker H (2002) NH4+ toxicity in higher plants: a critical review. J Plant Physiol 159:567–584. https://doi.org/10.1078/0176-1617-0774
Byrnes RC, Nuñez J, Arenas L, Rao I, Trujillo C, Alvarez C, Arango J, Rasche F, Chirinda N (2017) Biological nitrification inhibition by Brachiaria grasses mitigated soil nitrous emissions from bovine urine patches. Soil Biol Biochem 177:156–163. https://doi.org/10.1016/j.soilbio.2016.12.029
Coskun D, Britto DT, Shi W, Kronzucker HJ (2017) Nitrogen transformations in modern agriculture and role of biological nitrification inhibition. Nat Plants 3:17074. https://doi.org/10.1038/nplants.2017.74
Davidson EA (2009) The contribution of manure and fertilizer nitrogen to atmospheric nitrous oxide since 1860. Nat Geosci 2:659–662. https://doi.org/10.1038/ngeo608
Dayan FE, Rimando AM, Pan Z, Baerson SR, Gimsing AL, Duke SO (2010) Sorgoleone. Phytochem 10:1032–1039. https://doi.org/10.1016/j.phytochem.2010.03.011
Di T, Afzal MR, Yoshihashi T, Deshpande S, Zhu Y, Subbarao GV (2018) Further insights into underlying mechanisms for the release of biological nitrification inhibitors from sorghum roots. Plant Soil 423:99–110. https://doi.org/10.1007/s11104-017-3505-5
Fu Q, Abadie M, Blaud A, Carswell A, Misselbrook T, Clark I, Hirsch P (2020) Effects of urease and nitrification inhibitors on soil N, nitrifier abundance and activity in a sandy loam soil. Biol Fertil Soils 25:185–194. https://doi.org/10.1007/s00374-019-01411-5
Gao X, Wu M, Xu R, Pan R, Kim H, Wang X, Liao H (2014) Root interactions in a maize/soybean intercropping system control soybean soil-borne disease, red crown rot. PLoS ONE 9:e95031. https://doi.org/10.1371/journal.pone.0095031
Gubry-Rangin C, Nicol G, Prosser JI (2020) Archaea rather that bacteria control nitrification in two agricultural acidic soils. FEMS Microbiol Ecol 74:566–574. https://doi.org/10.1111/j.1574-6941.2010.00971.x
Hink L, Gubry-Rangin NGW, Prosser JI (2018) The consequences of niche and physiological differentiation of archaeal and bacterial ammonia oxidisers for nitrous oxide emissions. ISME J 12:1084–1093. https://doi.org/10.1038/s41396-017-0025-5
Hu HW, Xu ZH, He JZ (2014) Ammonia-oxidizing archaea play a predominant role in acid soil nitrification. Adv Agron 125:261–302. https://doi.org/10.1016/B978-0-12-800137-0.00006-6
Ishikawa T, Subbarao GV, Ito O, Okada K (2003) Suppression of nitrification and nitrous oxide emission by tropical grass Brachiaria humidicola. Plant Soil 255:413–419. https://doi.org/10.1007/978-94-017-2923-9_40
Karwat H, Egenolf K, Nuñez J, Rao I, Rasche F, Arango J, Moreta D, Arevalo A, Cadisch G (2018) Low 15N natural abundance in shoot tissue of Brachiaria humidicola is and indicator of reduced N losses due to biological nitrification inhibition (BNI). Front Microbiol 9:2383. https://doi.org/10.3389/fmicb.2018.02383
Karwat H, Sparke M, Fasche F, Arango J, Nuñez J, Rao I, Moreta D, Cadisch G (2019) Nitrate reductase activity in leaves as a plant physiological indicator of in vivo biological nitrification inhibition by Brachiaria humidicola. Plant Physiol Biochem 137:113–120. https://doi.org/10.1016/j.plaphy.2019.02.002
Kaur-Bhambra J, Wardak D, Prosser J, Gubry-Rangin C (2021) Revisiting plant biological nitrification inhibition efficiency using multiple archaeal and bacterial ammonia-oxidising cultures. Biol Fertil Soils. https://doi.org/10.1007/s00374-020-01533-1
Leon A, Subbarao GV, Kishii M, Matsumoto N, Kruseman G (2021) An ex ante life cycle assessment of wheat with high biological nitrification inhibition capacity. Environ Sci Pollut Res. https://doi.org/10.1007/s11356-021-16132-2
Li W, Ma J, Bowatte S, Hoogendoorn C, Hou F (2021a) Evidence of differences in nitrous oxide emissions and biological nitrification inhibition among Elymus grass species. Biol Fertil Soils. https://doi.org/10.1007/s00374-021-01592-y
Li Y, Zhang Y, Chapman SJ, Yao H (2021b) Biological nitrification inhibition by sorghum root exudates impacts ammonia-oxidizing bacteria but not ammonia-oxidizing archaea. Biol Fertil Soils 57:399–407. https://doi.org/10.1007/s00374-020-01538-w
Lu Y, Zhang X, Ma M, Zu W, Kronzucker HJ, Shi W (2021) Syringic acid from rice as a biological nitrification and urease inhibitor and its synergism with 1,9-decanediol. Biol Fertil Soils. https://doi.org/10.1007/s00374-021-01584-y
Maaz TM, Sapkota TB, Eagle AJ, Kantar MB, Bruulsema TW, Majumdar K (2021) Meta-analysis of yield and nitrous oxide outcomes for nitrogen management in agriculture. Glob Chang Biol 27:2342–2360. https://doi.org/10.1111/gcb.15588
Nakamura S, Sarr PS, Takahashi M, Ando Y, Subbarao GV (2020) The contribution of root turnover on biological nitrification inhibition and its impact on the ammonia-oxidizing archaea under brachiaria cultivations. Agronomy 10:1003. https://doi.org/10.3390/agronomy10071003
Nardi P, Laanbroek HJ, Nicol GW, Renella G, Cardinale M, Pietramellara G, Weckwerth W, Trinchera A, Ghatak A, Nannipieri P (2020) Biological nitrification inhibition in the rhizosphere: determining interactions and impact on microbially mediated processes and potential applications. FEMS Microbiol Rev 44:874–908. https://doi.org/10.1093/femsre/fuaa037
O’Sullivan CA, Fillery IRP, Poper MM, Richards RA (2016) Identification of several wheat land races with biological nitrification inhibition capacity. Plant Soil 404:61–74. https://doi.org/10.1007/s11104-016-2822-4
Otaka J, Subbarao GV, Ono H, Yoshihashi T (2021) Biological nitrification inhibition in maize-isolation and identification of hydrophobic inhibitors from root exudates. Biol Fertil Soils. https://doi.org/10.1007/s00374-021-01577-x
Prosser JI, Nicol GW (2012) Archaeal and bacterial ammonia-oxidisers in soil: the quest for niche specialization and differentiation. Trends Microbial 20:523–531. https://doi.org/10.1016/j.tim.2012.08.001
Prosser JI, Hink L, Gubry-Rangin C, Nicol GW (2020) Nitrous oxide production by ammonia oxidizers: Physiological diversity, niche differentiation and potential mitigation strategies. Glob Chang Biol 26:103–118. https://doi.org/10.1111/gcb.14877
Sarr PS, Ando Y, Nakamura S, Deshpande S, Subbarao GV (2020) Sorgoleone release from sorghum roots shapes the composition of nitrifying populations, total bacteria, and archaea and determines the level of nitrification. Biol Fertil Soils 56:145–166. https://doi.org/10.1007/s00374-019-01405-3
Sarr PS, Nakamura S, Ando Y, Iwasaki S, Subbarao GV (2021) Sorgoleone production enhances mycorrhizal association and reduces soil nitrification in sorghum. Rhizosphere 17:100283. https://doi.org/10.1016/j.rhisph.2020.100283
Snider D, Thompson K, Wagner-Riddle C, Spoelstra J, Dunfield K (2015) Molecular techniques and stable isotope ratios at natural abundance give complementary inferences about N2O production pathway in an agricultural soil following a rainfall event. Soil Biol Biochem 88:197–213. https://doi.org/10.1016/j.soilbio.2015.05.021
Stevens CJ (2019) Nitrogen in the environment. Science 363:578–580. https://doi.org/10.1126/science.aav8215
Subbarao GV, Searchinger TD (2021) Opinion: A “more ammonium solution” to mitigate nitrogen pollution and boost crop yields. Proc Natl Acad Sci (PNAS) (USA) 118:e2107576118. https://doi.org/10.1073/pnas.2107576118
Subbarao GV, Ishikawa T, Ito O, Nakahara K, Wang HY, Berry WL (2006a) A bioluminescence assay to detect nitrification inhibitors released from plant roots: a case study with Brachiaria humidicola. Plant Soil 288:101–112. https://doi.org/10.1007/s11104-006-9094-3
Subbarao GV, Ito O, Sahrawat KL, Ishikawa T, Berry WL, Nakahara K, Ishikawa T, Watanabe T, Suenaga K, Rondon M, Rao IM (2006b) Scope and strategies for regulation of nitrification in agricultural systems-challenges and opportunities. Crit Rev Plant Sci 25:303–335. https://doi.org/10.1080/07352680600794232
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. https://doi.org/10.1270/jsbbs.59.529
Subbarao GV, Wang HY, Ito O, Nakahara K, Berry WL (2007b) NH4+ triggers the synthesis and release of biological nitrification inhibition compounds in Brachiara humidicola roots. Plant Soil 290:245–257. https://doi.org/10.1007/s11104-006-9156-6
Subbarao GV, Nakahara K, Hurtodo MP, Ono H, Moreta DE, Salcedo AF, Yoshihashi T, Ishikawa T, Ishitani M, Ohnishi KM, Yoshida M, Rondon M, Rao IM, Lascano CE, Berry WL, Ito O (2009) Evidence for biological nitrification inhibition in Brachiaria pastures. Proc Natl Acad Sci (PNAS) (USA) 106:17302–17307. https://doi.org/10.1073/pnas.0903694106
Subbarao GV, Sahrawat KL, Nakahara K, Ishikawa T, Kudo N, Kishii M, Rao IM, Hash CT, George TS, Srinivasa RP, Nardi P, Bonnett D, Berry WL, Suenage K, Ito O, Lata JC (2012) Biological nitrification inhibition (BNI) – a noval strategy to regulate nitrification in agricultural systems. Adv Agron 114:249–302. https://doi.org/10.1016/B978-0-12-394275-3.00001-8
Subbarao GV, Nakahara K, Ishikawa T, Ono H, Yoshida M, Yoshihashi T, Zhu Y, Zakir H, Deshpande SP, Hash CT, Sahrawat KL (2013) Biological nitrification inhibition (BNI) activity in sorghum and its characterization. Plant Soil 366:243–259. https://doi.org/10.1007/s11104-012-1419-9
Subbarao GV, Yoshihashi T, Worthington M, Nakahara K, Ando Y, Sahrawat KL, Rao IM, Lata JC, Kishii M, Braun HJ (2015) Suppression of soil nitrification by plants. Plant Sci 233:155–164. https://doi.org/10.1016/j.plantsci.2015.01.012
Subbarao GV, Arango J, Masahiro K, Hooper AM, Yoshihashi T, Ando Y, Nakahara K, Deshpande S, Ortiz-Monasterio I, Ishitani M, Peters M, Chirinda N, Wollenberg L, Lata JC, Gerard B, Tobita S, Rao IM, Braum HJ, Kommerell V, Tohme J, Iwanaga M (2017) Genetic mitigation strategies to tackle agricultural GHG emissions: The case for biological nitrification inhibition technology. Plant Sci 262:165–168. https://doi.org/10.1016/j.plantsci.2017.05.004
Subbarao GV, Kishii M, Bozal-Leorri A, Ortiz-Monasterio I, Gao X, Ibba MI, Karwat H, Gonzalez-Moro MB, Gonzalez-Murua C, Yoshihashi T, Tobita S, Kommerell V, Braun HJ, Iwanaga M (2021) Enlisting wild-grass-genes to combat nitrification in wheat farming: a nature-based solution. Proc Natl Acad Sci (PNAS) (USA) 118:e2106595118. https://doi.org/10.1073/pnas.2106595118
Sun L, Lu YF, Yu FW, Kronzucker HJ, Shi WM (2016) Biological nitrification inhibition by rice root exudates and its relationship with nitrogen-use efficiency. New Phytol 212:646–656. https://doi.org/10.1111/nph.14057
Tesfamariam T, Yoshinaga H, Deshpande SP, Rao PS, Sahrawat KL, Ando Y, Nakahara K, Hash CT, Subbarao GV (2014) Biological nitrification inhibition in sorghum: the role of sorgoleone production. Plant Soil 379:325–335. https://doi.org/10.1007/s11104-014-2075-z
Varshney RR, Subbarao GV, Chaturvedi P, Weckwerth (2021) Root exudation of contrasting drought-stressed pearl millet genotypes conveys varying biological nitrification inhibition (BNI) activity. Biol Fertil Soils. https://doi.org/10.1007/s00374-021-01578-w
Vazquez E, Teutscherova N, Dannenmann M, Tochterle P, Butterbach-Bahl K, Pulleman M, Arango J (2020) Gross nitrogen transformations in tropical pasture soils as affected by Urochloa genotypes differing in biological nitrification inhibition (BNI) capacity. Soil Biol Biochem 151:108058. https://doi.org/10.1016/j.soilbio.2020.108058
Villegas D, Arevalo A, Nuñez J, Mazabel J, Subbarao G, Rao I, Vega J, Arango J (2020) Biological nitrification inhibition (BNI): phenotyping of a core germplasm collection of the tropical forage grass Megathyrsus maximus under greenhouse conditions. Front Plant Sci 11:820. https://doi.org/10.3389/fpls.2020.00820
Wang Q, Liu YR, Zhang CJ, Zhang LM, Han LL, Shen JP, He JZ (2017) Responses of soil nitrous oxide production and abundance and composition of associated microbial communities to nitrogen and water amendment. Biol Fertil Soils 53:601–611. https://doi.org/10.1007/s00374-017-1203-3
Yao Z, Pelster D, Liu C, Zheng X, Butterbach-Bahl K (2020) Soil N intensity as a measure to estimate annual N2O and NO fluxes from natural and managed ecosystems. Curr Opin Environ Sustain 47:1–6. https://doi.org/10.1016/j.cosust.2020.03.008
Zakir HAKM, 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 Phytol 180:442–451. https://doi.org/10.1111/j.1469-8137.2008.02576.x
Zeng H, Di T, Zhu Y, Subbarao GV (2016) Transcriptional response of plasma membrane H+ ATPase genes to ammonium nutrition and its functional link to the release of biological nitrification inhibitors from sorghum roots. Plant Soil 398:301–312. https://doi.org/10.1007/s11104-015-2675-2
Zhang LM, Hu HW, Shen JP, He JZ (2012) Ammonia oxidizing archaea have more important role than ammonia-oxidizing bacteria in ammonia oxidation of strongly acid soils. ISME J 6:1032–1045. https://doi.org/10.1038/ismej.2011.168
Zhang M, Zeng H, Afzal MR, Gao X, Li Y, Subbarao GV, Zhu Y (2021) BNI-release mechanisms in plant root system: current status of understanding. Biol Fertil Soils. https://doi.org/10.1007/s00374-021-01568-y
Zhu Y, Zeng HQ, Shen QR, 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 358:131–141. https://doi.org/10.1007/s11104-012-1151-5
Acknowledgements
We would like to appreciate the JIRCAS Visiting Research Fellowship Program, and thank Makoto Yamamoto, Yukiko Ishikawa, Hiroko Aoki, Yoko Koizumi, Raphael Obias Mubanga, Sanae Suzuki, Masami Aoyama for their help with the laboratory and field experiments.
Funding
This work was supported by Japan International Research Center for Agricultural Sciences (JIRCAS) Visiting Research Fellowship Program.
Author information
Authors and Affiliations
Contributions
XG, GVS and TY designed the experiments. XG conducted the experiments. GVS performed biological studies. TY responsible for sorgoleone analysis. PSS conducted amoA gene measurements. KU performed N2O emission measurements. XG and GVS wrote the manuscript. All authors have contributed to the writing of the manuscript.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing interests.
Additional information
Responsible Editor: Richard J. Simpson.
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
11104_2022_5474_MOESM1_ESM.pptx
Fig. S1 The correlation analysis of contrasting BNI genetic-stocks of sorghum between shoot N content and shoot dry weight in hydroponic culture, n = 12. LS genetic-stocks EC670350 and EC670402; HS genetic-stocks EC670311 and IS31861. For correlation analysis: R2 value on asterisk * and ** denoted with p < 0.05 and p < 0.01, respectively (PPTX 125 KB)
Rights and permissions
About this article
Cite this article
Gao, X., Uno, K., Sarr, P.S. et al. High-sorgoleone producing sorghum genetic stocks suppress soil nitrification and N2O emissions better than low-sorgoleone producing genetic stocks. Plant Soil 477, 793–805 (2022). https://doi.org/10.1007/s11104-022-05474-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-022-05474-6