Abstract
Aims
The understanding of the interactions between N transformations and N uptake by plants in greenhouse soils with large N accumulation is still not clear. The aim is to understand the plant- soil interactions (vegetables) on N transformations with respect to N supply.
Methods
15N tracing studies were conducted in two greenhouse soils to simultaneously quantify soil gross N transformation and plant N uptake rates using the Ntraceplant tool. Results There were significant feedbacks between vegetable N uptake and soil gross N transformation rates in the rhizospheric soil, whether soil N accumulation occurred or not. Plant NO3− uptake rates (UNO3) were higher than the NH4+ uptake rates (UNH4), which is consistent with the NO3−-preference of the vegetable plants studied. While UNH4 was still responsible for 6–49% of total N uptake rates, significantly negative relationships between UNH4 and NH4+ immobilization rate and autotrophic nitrification rate (ONH4) were observed. ONH4 was significantly inhibited in the presence of plants and decreased with time. ONH4 (1.11 mg N kg−1 d−1) was much lower than UNO3 (8.29 mg N kg−1 d−1) in the presence of plants. However, heterotrophic nitrification rate (ONrec), which ranged from 0.10 to 8.11 mg N kg−1 d−1 was significantly stimulated and was responsible for 5–97% of NO3− production in all plant treatments, providing additional NO3− to meet N requirements of plants and microorganisms.
Conclusions
The management of organic N fertilizers should be improved to stimulate inorganic N production via heterotrophic nitrification in greenhouse cultivation.
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References
Albornoz F (2016) Crop responses to nitrogen overfertilization: a review. Sci Hortic 205:79–83. https://doi.org/10.1016/j.scienta.2016.04.026
Bao S (2000) Soil and agricultural chemistry analysis. China agriculture press, Beijing
Biernath C, Fischer H, Kuzyakov Y (2008) Root uptake of N-containing and N-free low molecular weight organic substances by maize: a 14C/15N tracer study. Soil Biol Biochem 40:2237–2245. https://doi.org/10.1016/j.soilbio.2008.04.019
Cao X, Wu L, Ma Q, Jin Q (2015) Advances in studies of absorption and utilization of amino acids by plants: a review. Yingyong Shengtai Xuebao 26
Cao Y, He Z, Zhu T, Zhao F (2021) Organic-C quality as a key driver of microbial nitrogen immobilization in soil: a meta-analysis. Geoderma 383:114–784. https://doi.org/10.1016/j.geoderma.2020.114784
Cheng Y, Wang J, Wang J, Chang SX, Wang S (2017) The quality and quantity of exogenous organic carbon input control microbial NO3− immobilization: a meta-analysis. Soil Biol Biochem 115:357–363. https://doi.org/10.1016/j.soilbio.2017.09.006
Congreves KA, Van Eerd LL (2015) Nitrogen cycling and management in intensive horticultural systems. Nutr Cycl Agroecosyst 102:299–318. https://doi.org/10.1007/s10705-015-9704-7
Cox G, Gibbons J, Wood A, Craigon J, Ramsden S, Crout N (2006) Towards the systematic simplification of mechanistic models. Ecol Model 198:240–246
Cuesta R (2019) Cuesta roble releases 2019 global greenhouse statistics
De Boer W, Kowalchuk GA (2001) Nitrification in acid soils: micro-organisms and mechanisms. Soil Biol Biochem 33:853–866. https://doi.org/10.1016/S0038-0717(00)00247-9
Eylar OR, Schmidt EL (1959) A survey of heterotrophic micro-organisms from soil for ability to form nitrite and nitrate. J Gen Microbiol 20:473–481
Fei C, Zhang S, Liang B, Li J, Jiang L, Xu Y, Ding X (2018) Characteristics and correlation analysis of soil microbial biomass phosphorus in greenhouse vegetable soil with different planting years. Acta Agric Boreali-sinica 33:195
Gioseffi E, Neergaard A, Schjørring JK (2012) Interactions between uptake of amino acids and inorganic nitrogen in wheat plants. Biogeosciences 9:1509–1518
Guo JH, Liu XJ, Zhang Y, Shen JL, Han WX, Zhang WF, Christie P, Goulding K, Vitousek PM, Zhang F (2010) Significant acidification in major Chinese croplands science 327:1008–1010
Haichar FZ, Santaella C, Heulin T, Achouak W (2014) Root exudates mediated interactions belowground. Soil Biol Biochem 77:69–80. https://doi.org/10.1016/j.soilbio.2014.06.017
He X, Chi Q, Cai Z, Cheng Y, Zhang J, Müller C (2020) 15N tracing studies including plant N uptake processes provide new insights on gross N transformations in soil-plant systems. Soil Biol Biochem 141: 107666. doi: https://doi.org/10.1016/j.soilbio.2019.107666
He X, Chi Q, Meng L, Zhao C, He M, Dan X, Huang X, Zhao J, Cai Z, Zhang J, Müller C (2022) Plants with nitrate preference can regulate nitrification to meet their nitrate demand. Soil Biol Biochem 165:108516
He X, Chi Q, Zhao C, Cheng Y, Huang X, Zhao J, Cai Z, Zhang J, Müller C (2021) Plants with an ammonium preference affect soil N transformations to optimize their N acquisition. Soil Biol Biochem 155:108158. https://doi.org/10.1016/j.soilbio.2021.108158
Hill PW, Farrell M, Jones DL (2012) Bigger may be better in soil N cycling: does rapid acquisition of small L-peptides by soil microbes dominate fluxes of protein-derived N in soil? Soil Biol Biochem 48:106–112
Hodge A, Robinson D, Fitter A (2000) Are microorganisms more effective than plants at competing for nitrogen? Trends Plant Sci 5:304–308
Huang XQ, Wen T, Zhang JB, Meng L, Zhu TB, Liu LL, Cai ZC (2015) Control of soil-borne pathogen fusarium oxysporum by biological soil disinfestation with incorporation of various organic matters. Eur J Plant Pathol 143:223–235. https://doi.org/10.1007/s10658-015-0676-x
Hutchinson HB, Miller NHJ (1912) The direct assimilation of inorganic and organic forms of nitrogen by higher plants. J Agric Sci 4:282–302
Inselsbacher E, Umana NH-N, Stange FC, Gorfer M, Schüller E, Ripka K, Zechmeister-Boltenstern S, Hood-Novotny R, Strauss J, Wanek W (2010) Short-term competition between crop plants and soil microbes for inorganic N fertilizer. Soil Biol Biochem 42:360–372
Kielland K (1994) Amino acid absorption by arctic plants: implications for plant nutrition and nitrogen cycling. Ecology 75:2373–2383
Knowles R (1982) Denitrification. Microbiol Rev 46:43–70
Kuzyakov Y, Xu X (2013) Competition between roots and microorganisms for nitrogen: mechanisms and ecological relevance. The New phytologist 198:656–669. https://doi.org/10.1111/nph.12235
Lang E, Jagnow G (1986) Fungi of a forest soil nitrifying at low pH values. FEMS Microbiol Lett 38:257–265. https://doi.org/10.1111/j.1574-6968.1986.tb01736.x
Li J, Liu H, Wang H, Luo J, Zhang X, Liu Z, Zhang Y, Zhai L, Lei Q, Ren T, Li Y, Bashir MA (2018) Managing irrigation and fertilization for the sustainable cultivation of greenhouse vegetables. Agric Water Manag 210:354–363. https://doi.org/10.1016/j.agwat.2018.08.036
Luxhøi J, Nielsen N, Jensen L (2004) Effect of soil heterogeneity on gross nitrogen mineralization measured by 15N-pool dilution techniques. Plant Soil 262:263–275
Müller C, Laughlin RJ, Christie P, Watson CJ (2011) Effects of repeated fertilizer and cattle slurry applications over 38 years on N dynamics in a temperate grassland soil. Soil Biol Biochem 43:1362–1371
Müller C, Rütting T, Kattge J, Laughlin R, Stevens R (2007) Estimation of parameters in complex 15N tracing models by Monte Carlo sampling. Soil Biol Biochem 39:715–726
Meier IC, Finzi AC, Phillips RP (2017) Root exudates increase N availability by stimulating microbial turnover of fast-cycling N pools. Soil Biol Biochem 106:119–128. https://doi.org/10.1016/j.soilbio.2016.12.004
Min J, Lu K, Sun H, Xia L, Zhang H, Shi W (2016) Global warming potential in an intensive vegetable cropping system as affected by crop rotation and nitrogen rate. CLEAN - Soil, Air, Water 44:766–774. https://doi.org/10.1002/clen.201400785
Min J, Sun H, Kronzucker HJ, Wang Y, Shi W (2021) Comprehensive assessment of the effects of nitrification inhibitor application on reactive nitrogen loss in intensive vegetable production systems. Agric Ecosyst Environ 307:107227
Nacry P, Bouguyon E, Gojon A (2013) Nitrogen acquisition by roots: physiological and developmental mechanisms ensuring plant adaptation to a fluctuating resource. Plant Soil 370:1–29. https://doi.org/10.1007/s11104-013-1645-9
Nichols M, Woolley D, Christie C (2001) Effect of oxygen and carbon dioxide concentration in the root zone on the growth of vegetables. International Symposium on Design and Environmental Control of Tropical and Subtropical Greenhouses 578
Padje A, Whiteside MD, Kiers ET (2016) Signals and cues in the evolution of plant–microbe communication. Curr Opin Plant Biol 32:47–52. https://doi.org/10.1016/j.pbi.2016.06.006
Ren T, Christie P, Wang J, Chen Q, Zhang F (2010) Root zone soil nitrogen management to maintain high tomato yields and minimum nitrogen losses to the environment. Sci Hortic 125:25–33. https://doi.org/10.1016/j.scienta.2010.02.014
Schimel JP, Bennett J (2004) Nitrogen mineralization: challenges of a changing paradigm. Ecology 85:591–602
Schmidt EL (1954) Nitrate formation by a soil fungus. Science 119:187–189
Subbarao G, Nakahara K, Ishikawa T, Ono H, Yoshida M, Yoshihashi T, Zhu Y, Zakir H, Deshpande S, Hash C (2013) Biological nitrification inhibition (BNI) activity in sorghum and its characterization. Plant Soil 366:243–259
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
Sun L, Lu Y, Yu F, Kronzucker HJ, Shi W (2016) Biological nitrification inhibition by rice root exudates and its relationship with nitrogen-use efficiency. New Phytol 212:646–656
Sun X, Liang B, Wang J, Cheng Y, Chang SX, Cai Z-C, Müller C, Zhang J-B (2020) Soil N transformation rates are not linked to fertilizer N losses in vegetable soils with high N input. Soil Tillage Res 202:104651. https://doi.org/10.1016/j.still.2020.104651
Ti C, Luo Y, Yan X (2015) Characteristics of nitrogen balance in open-air and greenhouse vegetable cropping systems of China. Environ Sci Pollut Res Int 22:18508–18518. https://doi.org/10.1007/s11356-015-5277-x
Wang J, Chen Z, Xu C, Elrys AS, Shen F, Cheng Y, Chang SX (2021) Organic amendment enhanced microbial nitrate immobilization with negligible denitrification nitrogen loss in an upland soil. Environ Pollut 288:117721. https://doi.org/10.1016/j.envpol.2021.117721
Wang X, Zou C, Gao X, Guan X, Zhang W, Zhang Y, Shi X, Chen X (2018) Nitrous oxide emissions in Chinese vegetable systems: a meta-analysis. Environ Pollut 239:375–383. https://doi.org/10.1016/j.envpol.2018.03.090
Waring BG, Álvarez-Cansino L, Barry KE, Becklund KK, Dale S, Gei MG, Keller AB, Lopez OR, Markesteijn L, Mangan S (2015) Pervasive and strong effects of plants on soil chemistry: a meta-analysis of individual plant ‘Zinke’effects. Proc R Soc B Biol Sci 282:20151001
Zhang J, Cai Z, Müller C (2018) Terrestrial N cycling associated with climate and plant-specific N preferences: a review. Eur J Soil Sci 69:488–501. https://doi.org/10.1111/ejss.12533
Zhang J, Sun W, Zhong W, Cai Z (2014) The substrate is an important factor in controlling the significance of heterotrophic nitrification in acidic forest soils. Soil Biol Biochem 76:143–148. https://doi.org/10.1016/j.soilbio.2014.05.001
Zhang Y, Dai S, Huang X, Zhao Y, Zhao J, Cheng Y, Cai Z, Zhang J (2020) pH-induced changes in fungal abundance and composition affects soil heterotrophic nitrification after 30 days of artificial pH manipulation. Geoderma 366:114255
Zhang Y, Wang J, Dai S, Zhao J, Huang X, Sun Y, Chen J, Cai Z, Zhang J (2019) The effect of C: N ratio on heterotrophic nitrification in acidic soils. Soil Biol Biochem 137:107562
Zhao J, Li Y, Wang B, Huang X, Yang L, Lan T, Zhang J, Cai Z (2017) Comparative soil microbial communities and activities in adjacent Sanqi ginseng monoculture and maize-Sanqi ginseng systems. Appl Soil Ecol 120:89–96. https://doi.org/10.1016/j.apsoil.2017.08.002
Zhou J, Gu B, Schlesinger WH, Ju X (2016) Significant accumulation of nitrate in Chinese semi-humid croplands. Sci Rep 6:1–8
Zhu T, Meng T, Zhang J, Zhong W, Müller C, Cai Z (2015) Fungi-dominant heterotrophic nitrification in a subtropical forest soil of China. J Soils Sediments 15:705–709
Zhu T, Zhang J, Cai Z, Müller C (2011) The N transformation mechanisms for rapid nitrate accumulation in soils under intensive vegetable cultivation. J Soils Sediments 11:1178–1189. https://doi.org/10.1007/s11368-011-0384-x
Acknowledgements
This work was supported by the National Natural Science Foundation of China [grant number 41830642, and U20A20107], the CAS Interdisciplinary Innovation Team project [grant number JCTD-2018-06], and the “Double World-Classes” Development in Geography project. The study was carried out as part of the IAEA funded coordinated research project “Minimizing farming impacts on climate change by enhancing carbon and nitrogen capture and storage in Agro-Ecosystems (D1.50.16)” and was carried out in close collaboration with the German Science Foundation research unit DASIM (FOR 2337).
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Dan, X., Meng, L., He, M. et al. Regulation of nitrogen acquisition in vegetables by different impacts on autotrophic and heterotrophic nitrification. Plant Soil 474, 581–594 (2022). https://doi.org/10.1007/s11104-022-05362-z
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DOI: https://doi.org/10.1007/s11104-022-05362-z