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Syringic acid from rice as a biological nitrification and urease inhibitor and its synergism with 1,9-decanediol

Abstract

The type, functions, and mechanisms of biological nitrification inhibitors (BNIs) from rice were investigated using a combination of chemical and molecular techniques, bacterial bioassays, and soil microcosm experiments. We report the discovery of an effective nitrification inhibitor, syringic acid, in the root exudates of rice. Nitrification inhibition activity by syringic acid was verified in both weakly acidic and neutral pure cultures of Nitrosomonas europaea, and was superior to the widely used synthetic nitrification inhibitor, dicyandiamide (DCD). Moreover, syringic acid exhibited a dual inhibitory effect on ammonia monooxygenase (AMO), active in ammonium/ammonia oxidation, and on urease, active in urea hydrolysis. Nitrification inhibition by syringic acid was also demonstrated in a paddy soil system, and the abundance of ammonia-oxidizing bacteria (AOB) and ammonia-oxidizing archaea (AOA) was significantly inhibited under all syringic acid treatments. A synergistic effect of syringic acid and another rice BNI, 1,9-decanediol, on nitrification was found in two pure Nitrosomonas cultures and a paddy soil. Together, our results enhance our understanding of BNI production by rice and enable the design of natural inhibitor formulations that regulate soil N transformation in a concerted manner.

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References

  • Badri DV, Chaparro JM, Zhang RF, Shen QR, Vivanco JM (2013) Application of natural blends of phytochemicals derived from the root exudates of Arabidopsis to the soil reveal that phenolic-related compounds predominantly modulate the soil microbiome. J Biol Chem 288:4502–4512

    CAS  PubMed  PubMed Central  Google Scholar 

  • Baldwin IT, Olson RK, Reiners WA (1983) Protein binding phenolics and the inhibition of nitrification in subalpine balsam fir soils. Soil Biol Biochem 15:419–423

    CAS  Google Scholar 

  • Beeckman F, Motte H, Beeckman T (2018) Nitrification in agricultural soils: impact, actors and mitigation. Curr Opin Biotechnol 50:166–173

    CAS  PubMed  Google Scholar 

  • Castaldi S, Carfora A, Fiorentino A, Natale A, Messere A, Miglietta F, Cotrufo MF (2009) Inhibition of net nitrification activity in a Mediterranean woodland: possible role of chemicals produced by Arbutus unedo. Plant Soil 315:273–283

    CAS  Google Scholar 

  • Cheemanapalli S, Mopuri R, Golla R, Anuradha CM, Chitta SK (2018) Syringic acid (SA) - a review of its occurrence, biosynthesis, pharmacological and industrial importance. Biomed Pharmacother 108:547–557

    Google Scholar 

  • Chen WB, Chen BM, Liao HX, Su JQ, Peng SL (2020) Leaf leachates have the potential to influence soil nitrification via changes in ammonia-oxidizing archaea and bacteria populations. Eur J Soil Sci 71:119–131

    CAS  Google Scholar 

  • Clein JS, Schimel JP (1995) Nitrogen turnover and availability during succession from alder to poplar in Alaskan taiga forests. Soil Biol Biochem 27:743–752

    CAS  Google Scholar 

  • Coskun D, Britto DT, Shi WM, Kronzucker HJ (2017a) How plant root exudates shape the nitrogen cycle. Trends Plant Sci 22:661–673

    CAS  PubMed  Google Scholar 

  • Coskun D, Britto DT, Shi WM, Kronzucker HJ (2017b) Nitrogen transformations in modern agriculture and the role of biological nitrification inhibition. Nat Plants 3:1–10

    Google Scholar 

  • Dey N, Bhattacharjee S (2020) Accumulation of polyphenolic compounds and osmolytes under dehydration stress and their implication in redox regulation in four indigenous aromatic rice cultivars. Rice Sci 27:329–344

    Google Scholar 

  • Duncan EG, O’Sullivan CA, Simonsen AK, Roper MM, Treble K, Whisson K (2016) A composite guanyl thiourea (GTU), dicyandiamide (DCD) inhibitor improves the efficacy of nitrification inhibition in soil. Chemosphere 163:1–5

  • Egenolf K, Verma S, Schone J, Klaiber I, Arango J, Cadisch G, Neumann G, Rasche F (2021) Rhizosphere pH and cation-anion balance determine the exudation of nitrification inhibitor 3-epi-brachialactone suggesting release via secondary transport. Physiol Plant. https://doi.org/10.1111/ppl.13300

  • Fierer N, Schimel JP, Cates RG, Zou JP (2001) Influence of balsam poplar tannin fractions on carbon and nitrogen dynamics in Alaskan taiga floodplain soils. Soil Biol Biochem 33:1827–1839

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Galloway JN, Townsend AR, Erisman JW, Bekunda M, Cai ZC, Freney JR, Martinelli LA, Seitzinger SP, Sutton MA (2008) Transformation of the nitrogen cycle: recent trends, questions, and potential solutions. Science 320:889–892

    CAS  PubMed  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. J Agric Food Chem 55:1385–1388

    CAS  PubMed  Google Scholar 

  • Hattenschwiler S, Vitousek PM (2000) The role of polyphenols in terrestrial ecosystem nutrient cycling. Trends Ecol Evol 15:238–243

    CAS  PubMed  Google Scholar 

  • Jensen K, Revsbech NP, Nielsen LP (1993) Microscale distribution of nitrification activity in sediment determined with a shielded microsensor for nitrate. Appl Environ Microbiol 59:3287–3296

  • Jin ZJ (2004) About the evaluation of drug combination. Acta Pharmacol Sin 25:146–147

    CAS  PubMed  Google Scholar 

  • Karmarkar SV, Tabatabai MA (1991) Effects of biotechnology by-products and organic-acids on nitrification in soils. Biol Fertil Soils 12:165–169

    CAS  Google Scholar 

  • Kaur-Bhambra J, Wardak DLR, Prosser JI, 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

  • Kirk GJD, Kronzucker HJ (2005) The potential for nitrification and nitrate uptake in the rhizospheres of wetland plants: a modelling study. Ann Bot 96:639–646

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kong CH, Li HB, Hu F, Xu XH, Wang P (2006) Allelochemicals released by rice roots and residues in soil. Plant Soil 288:47–56

    CAS  Google Scholar 

  • Kronzucker HJ, Siddiqi MY, Glass ADM (1997) Conifer root discrimination against soil nitrate and the ecology of forest succession. Nature 385:59–61

    CAS  Google Scholar 

  • Kronzucker HJ, Kirk GJD, Siddiqi MY, Glass ADM (1998) Effects of hypoxia on 13NH4+ fluxes in rice roots: kinetics and compartmental analysis. Plant Physiol 116:581–587

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kronzucker HJ, Siddiqi MY, Glass ADM, Kirk GJD (1999) Nitrate-ammonium synergism in rice: a subcellular analysis. Plant Physiol 119:1041–1046

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kronzucker HJ, Siddiqi MY, Glass ADM, Kirk GJD (2000) Comparative kinetic analysis of ammonium and nitrate acquisition by tropical lowland rice: implications for rice cultivation and yield potential. New Phytol 145:471–476

    CAS  PubMed  Google Scholar 

  • Laffite A, Florio A, Andrianarisoa KS, Des Chatelliers CC, Schloter-Hai B, Ndaw SM, Periot C, Schloter M, Zeller B, Poly F, Le Roux X (2020) Biological inhibition of soil nitrification by forest tree species affects Nitrobacter populations. Environ Microbiol 22:1141–1153

    CAS  PubMed  Google Scholar 

  • Li YL, Zhang YL, Hu J, Shen QR (2007) Contribution of nitrification happened in rhizospheric soil growing with different rice cultivars to N nutrition. Biol Fertil Soils 43:417–425

    CAS  Google Scholar 

  • Li YY, Chapman SJ, Nicol GW, Yao HY (2018) Nitrification and nitrifiers in acidic soils. Soil Biol Biochem 116:290–301

    CAS  Google Scholar 

  • Lodhi MAK (1978) Inhibition of nitrifying bacteria, nitrification and mineralization of spoil soils as related to their successional stages. Bull Torrey Bot Club 106:284–289

    Google Scholar 

  • Lu YF, Zhang XN, Jiang JF, Kronzucker HJ, Shen WS, Shi WM (2019) Effects of the biological nitrification inhibitor 1,9-decanediol on nitrification and ammonia oxidizers in three agricultural soils. Soil Biol Biochem 129:48–59

    CAS  Google Scholar 

  • McCarty GW, Bremner JM (1989) Inhibition of nitrification in soils by heterocyclic nitrogen compounds. Biol Fertil Soils 8:204–211

    CAS  Google Scholar 

  • McCarty GW, Bremner JM, Schmidt EL (1991) Effects of phenolic acids on ammonia oxidation by terrestrial autotrophic nitrifying microorganisms. FEMS Microbiol Ecol 85:345–450

    CAS  Google Scholar 

  • McCarty GW (1999) Modes of action of nitrification inhibitors. Biol Fertil Soils 29:1–9

    CAS  Google Scholar 

  • Min J, Sun HJ, Kronzucker HJ, Wang Y, Shi WM (2021) Comprehensive assessment of the effects of nitrification inhibitor application on reactive nitrogen loss in intensive vegetable production systems. Agric Ecosyst Environ 307:107227. https://doi.org/10.1016/j.agee.2020.107227

    CAS  Article  Google Scholar 

  • Mochizuki M, Yamazaki S, Kano K, Ikeda, (2002) Kinetic analysis and mechanistic aspects of autoxidation of catechins. Biochim Biophys Acta Gen Subj 1569:35–44

    CAS  Google Scholar 

  • Nardi P, Akutsu M, Pariasca-Tanaka J, Wissuwa M (2013) Effect of methyl 3-4-hydroxyphenyl propionate, a Sorghum root exudate, on N dynamic, potential nitrification activity and abundance of ammonia-oxidizing bacteria and archaea. Plant Soil 367:627–637

    CAS  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • O’Sullivan CA, Fillery IRP, Roper MM, Richards RA (2016) Identification of several wheat landraces with biological nitrification inhibition capacity. Plant Soil 404:61–74

  • Rice EL, Pancholy SK (1972) Inhibition of nitrification by climax ecosystems. Am J Bot 59:1033–1040

    Google Scholar 

  • Rice EL, Pancholy SK (1973) Inhibition of nitrification by climax ecosystems. II. Additional evidence and possible role of tannins. Am J Bot 60:691–702

    CAS  Google Scholar 

  • Roijers AFM, Tas MM (1964) The determination of urea with p-dimethylaminobenzaldehyde. Clin Chim Acta 9:197–202

    CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Sastry KVH, Moudgal RP, Mohan J, Tyagi JS, Rao GS (2002) Spectrophotometric determination of serum nitrite and nitrate by copper–cadmium alloy. Anal Biochem 306:79–82

  • Schimel JP, Van Cleve K, Cates RG, Clausen TP, Reichardt PB (1996) Effects of balsam poplar (Populus balsamifera) tannins and low molecular weight phenolics on microbial activity in taiga floodplain soil: Implications for changes in N cycling during succession. Can J Bot 74:84–90

    CAS  Google Scholar 

  • Sharma S, Sahu R, Navathe S, Mishra VK, Chand R, Singh PK, Joshi AK, Pandey SP (2018) Natural variation in elicitation of defense-signaling associates to field resistance against the spot blotch disease in bread Wheat (Triticum aestivum L.). Front Plant Sci 9:636

    PubMed  PubMed Central  Google Scholar 

  • Shen T, Stieglmeier M, Dai J, Urich T, Schleper C (2013) Responses of the terrestrial ammonia-oxidizing archaeon Ca. Nitrososphaera viennensis and the ammonia-oxidizing bacterium Nitrosospira multiformis to nitrification inhibitors. FEMS Microbiol Lett 344:121–129

    CAS  PubMed  Google Scholar 

  • Shi C, Sun Y, Zheng ZW, Zhang XR, Song KK, Jia ZY, Chen YF, Yang MC, Liu X, Dong R, Xia XD (2016) Antimicrobial activity of syringic acid against Cronobacter sakazakii and its effect on cell membrane. Food Chem 197:100–106

    CAS  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

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

    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

    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. Proc Natl Acad Sci U S A 106:17302–17307

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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, Braun 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

    CAS  PubMed  Google Scholar 

  • Sun HJ, Zhang HL, Powlson D, Min J, Shi WM (2015) Rice production, nitrous oxide emission and ammonia volatilization as impacted by the nitrification inhibitor 2-chloro-6-(trichloromethyl)-pyridine. Field Crops Res 173:1–7

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

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

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Verhagen FJM, Duyts H, Laanbroek HJ (1992) Competition for ammonium between nitrifying and heterotrophic bacteria in continuously percolated soil columns. Appl Environ Microbiol 58:3303–3311

    CAS  PubMed  PubMed Central  Google Scholar 

  • Vitousek PM, Matson PA, Cleve KV (1989) Nitrogen availability and nitrification during succession: primary, secondary, and old-field seres. Plant Soil 115:229–239

    Google Scholar 

  • Weatherburn MW (1967) Phenol-hypochlorite reaction for determination of ammonia. Anal Chem 39:971–974

    CAS  Google Scholar 

  • Wu E, Liu XY, Zhu XR (1999) The effect of groups in phenolic compounds on inhibition of nitrification in soil. Environ Chem 18:292–403 ((in Chinese))

    Google Scholar 

  • Wu HW, Haig T, Pratley J, Lemerle D, An M (2001) Allelochemicals in wheat (Triticum aestivum L.) Cultivar difference in the exudation of phenolic acids. J Agric Food Chem 49:3742–3745

    CAS  PubMed  Google Scholar 

  • Wu J, Li X, Fang H, Yi YQ, Chen D, Long Y, Gao XX, Wei XY, Chen CYO (2016) Investigation of synergistic mechanism and identification of interaction site of aldose reductase with the combination of gigantol and syringic acid for prevention of diabetic cataract. BMC Complement Altern Med 16:286

    PubMed  PubMed Central  Google Scholar 

  • Wu TL, Qin WX, Alves ME, Fang GD, Sun Q, Cui PX, Liu C, Zhou DM, Wang YJ (2019) Mechanisms of Sb (III) oxidation mediated by low molecular weight phenolic acids. Chem Eng J 356:190–198

    CAS  Google Scholar 

  • Yan XY, Ti CP, Vitousek P, Chen DL, Leip A, Cai ZC, Zhu ZL (2014) Fertilizer nitrogen recovery efficiencies in crop production systems of China with and without consideration of the residual effect of nitrogen. Environ Res Lett 9:095002

    CAS  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Zaman M, Saggar S, Blennerhassett JD, Singh J (2009) Effect of urease and nitrification inhibitors on N transformation, gaseous emissions of ammonia and nitrous oxide, pasture yield and N uptake in grazed pasture system. Soil Biol Biochem 41:1270–1280

    CAS  Google Scholar 

  • 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 acidic soils. ISME J 6:1032–1045

    CAS  PubMed  Google Scholar 

  • Zhang XN, Lu YF, Yang T, Kronzucker HJ, Shi WM (2019) Influencing the release of the biological nitrification inhibitor 1,9-decanediol from rice (Oryza sativa L.) roots. Plant Soil 436:253–265

    CAS  Google Scholar 

  • Zhao M, Zhao HB, Du QJ, Shi YF (2015) Inhibitory Effects of tropical medicinal plant extracts on urea hydrolysis and nitrification in soil: a preliminary study. Hortscience 50:744–749

    CAS  Google Scholar 

  • Zhu YY, 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

    CAS  Google Scholar 

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Funding

This work was supported by grants from the National Natural Science Foundation of China (31761143015, 32072670), the Natural Science Foundation for Excellent Young Scholar of Jiangsu Province of China (BK20190108), the Key Research and Development Program of Shandong Province of China (2019JZZY010701), and the Open Foundation of State Key Laboratory of Soil and Sustainable Agriculture of China (Y812000007).

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Correspondence to Weiming Shi.

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Lu, Y., Zhang, X., Ma, M. et al. Syringic acid from rice as a biological nitrification and urease inhibitor and its synergism with 1,9-decanediol. Biol Fertil Soils 58, 277–289 (2022). https://doi.org/10.1007/s00374-021-01584-y

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Keywords

  • Biological nitrification inhibitor
  • Urease activity
  • Syringic acid
  • Ammonia oxidizer
  • Synergism
  • Rice