Abstract
Aims
Rhizosphere metabolomics can potentially help us to better understand belowground root-environment interactions that are mediated by root exudation in the rhizosphere. The main goals of the present work were to characterize the pattern of maize root exudation in response to straw-derived biochar (BC) addition and chemical nitrogen (N) fertilizer reduction and to explore the underlying mechanisms.
Methods
Two sets of pot experiments were performed independently that involved planting maize in aquic brown soil to which BC was added at dosages of 0 or 5% (w/w, equivalent to 112.5 t ha−1) combined with urea N application at rates of 150 kg ha−1 (100%) or 105 kg ha−1 (70%) for a total of four treatments. Samples containing root exudates were analyzed using nuclear magnetic resonance, and quantitative real-time reverse transcription-PCR (qRT-PCR) was performed to analyze gene expression in maize roots.
Results
The 5% BC addition significantly influenced the global rhizosphere metabolome of the maize seedlings regardless of the N application level, but without BC addition, the rhizosphere metabolome was not significantly affected by a 30% reduction in N. The effects of N reduction on the metabolite profiling of the native root exudates were stronger than those of BC addition and an obvious interaction was observed between BC addition and N reduction. BC addition combined with N reduction significantly changed the levels of some amino acids (e.g., causing a 1.75-fold increase in isoleucine) and organic acids (e.g., causing a 2.16-fold increase in malonate and a 2.15-fold increase in acetate) in the root exudates. Soil environmental factors, including the size of NH4+-N pool and total P content, had a strong positive correlation with rhizosphere metabolome. The decrease in root biomass caused by N reduction was partially mitigated by BC addition, and the expression of ZmMATE1 (for multi-drug and toxic compound extrusion transporter) in root was significantly up-regulated (P < 0.05) by BC addition and N reduction.
Conclusions
Maize roots can reshape their rhizosphere metabolome under BC addition combined with N reduction and its underlying mechanism may involve the synergistic effects of soil environmental factors, root growth, and the expression of transport-associated genes.
This is a preview of subscription content, access via your institution.







References
Adeleke R, Nwangburuka C, Oboirien B (2017) Origins, roles and fate of organic acids in soils: a review. S Afr J Bot 108:393–406. https://doi.org/10.1016/j.sajb.2016.09.002
Akhter A, Hage-ahmed K, Soja G, Steinkellner S (2015) Compost and biochar alter mycorrhization, tomato root exudation, and development of fusarium oxysporum f. sp. lycopersici. Front Plant Sci 6:529–542. https://doi.org/10.3389/fpls.2015.00529
Badri DV, Vivanco JM (2009) Regulation and function of root exudates. Plant Cell Environ 32:666–681. https://doi.org/10.1111/j.1365-3040.2009.01926.x
Baudoin E, Benizri E, Guckert A (2003) Impact of artificial root exudates on the bacterial community structure in bulk soil and maize rhizosphere. Soil Biol Biochem 35:1183–1192. https://doi.org/10.1016/S0038-0717(03)00179-2
Biederman LA, Harpole WS (2013) Biochar and its effects on plant productivity and nutrient cycling: a meta-analysis. GCB Bioenergy 5:202–214. https://doi.org/10.1111/gcbb.12037
Blackwell P, Joseph S, Munroe P, Anawar HM, Storer P, Gilkes RJ, Solaiman ZM (2015) Infuences of biochar and biochar-mineral complex on mycorrhizal colonisation and nutrition of wheat and sorghum. Pedosphere 25:686–695. https://doi.org/10.1016/S1002-0160(15)30049-7
Brencic A, Winans SC (2005) Detection of and response to signals involved in host-microbe interactions by plant-associated bacteria. Microbiol Mol Biol Rev 69:155–194. https://doi.org/10.1128/MMBR.69.1.155-194.2005
Carvalhais LC, Dennis PG, Dmitri F, Fedoseyenko D, Hajirezaei MR, Borriss R, von Wiren N (2011) Root exudation of sugars, amino acids, and organic acids by maize as affected by nitrogen, phosphorus, potassium, and iron deficiency. J Plant Nutr Soil Sci 174:3–11. https://doi.org/10.1002/jpln.201390025
Cheng Y, Cai ZC, Chang SX, Wang J, Zhang JB (2012) Wheat straw and its biochar have contrasting effects on inorganic N retention and N2O production in a cultivated black chernozem. Biol Fertil Soils 48:941–946. https://doi.org/10.1007/s00374-012-0687-0
Coskun D, Britto DT, Shi WM, Kronzucker HJ (2017) How plant root exudates shape the nitrogen cycle. Trends Plant Sci 22:661–673. https://doi.org/10.1016/j.tplants.2017.05.004
De Nobili M, Contin M, Mondini C, Brookes PC (2001) Soil microbial biomass is triggered into activity by trace amounts of substrate. Soil Biol Biochem 33:1163–1170. https://doi.org/10.1016/S0038-0717(01)00020-7
Derrien D, Marol C, Balesdent J (2005) The dynamics of neutral sugars in the rhizosphere of wheat. An approach by 13C pulse-labelling and GC/C/IRMS. Plant Soil 267:243–253. https://doi.org/10.1007/s11104-005-5348-8
Escudero N, Marhuenda-Egea FC, Ibanco-Canete R, Zavala-Gonzalez EA, Lopez-Llorca LV (2014) A metabolomic approach to study the rhizodeposition in the tritrophic interaction: tomato, pochonia chlamydosporia and meloidogyne javanica. Metabolomics 10:788–804. https://doi.org/10.1007/s11306-014-0632-3
Fan TWM, Lane AN, Pedler J, Crowley D, Higashi RM (1997) Comprehensive analysis of organic ligands in whole root exudates using nuclear magnetic resonance and gas chromatography–mass spectrometry. Anal Biochem 251:57–68. https://doi.org/10.1006/abio.1997.2235
Farrar J, Hawes M, Jones D, Lindow S (2003) How roots control the flux of carbon to the rhizosphere. Ecology 84:827–837. https://doi.org/10.1890/0012-9658(2003)084[0827:HRCTFO]2.0.CO;2
Fischer H, Eckhardt KU, Meyer A, Neumann G, Leinweber P, Fischer K, Kuzyakov Y (2010) Rhizodeposition of maize: short-term carbon budget and composition. J Soil Sci Plant Nutr 173:67–79. https://doi.org/10.1002/jpln.200800293
Fisk LM, Barton L, Jones DL, Glanville HC, Murphy DV (2015) Root exudate carbon mitigates nitrogen loss in a semi-arid soil. Soil Biol Biochem 88:380–389. https://doi.org/10.1016/j.soilbio.2015.06.011
Graber ER, Tsechansky L, Gerstl Z, Lew B (2012) High surface area biochar negatively impacts herbicide efficacy. Plant Soil 353:95–106. https://doi.org/10.1007/s11104-011-1012-7
Graber ER, Frenkel O, Jaiswal AK, Elad Y (2014) How may biochar influence severity of diseases caused by soilborne pathogens. Carbon Manage 5:169–183. https://doi.org/10.1080/17583004.2014.913360
Gul S, Whalen JK, Thomas BW, Sachdeva V, Deng H (2015) Physico-chemical properties and micobial responses in biochar-amended soils: mechanisms and future directions. Agric Ecosyst Environ 206:46–59. https://doi.org/10.1016/j.agee.2015.03.015
Guo JH, Liu XJ, Zhang Y, Shen JL, Han WX, Zhang WF, Christie P, Goulding KWT, Vitousek PM, Zhang FS (2010) Significant acidification in major Chinese croplands. Sci 327:1008–1010. https://doi.org/10.1126/science.1182570
Haase S, Neumann G, Kania A, Kuzyakov Y, Römheld V, Kandeler E (2007) Elevation of atmospheric CO2 and N-nutritional status modify nodulation, nodule-carbon supply, and root exudation of Phaseolus vulgaris L. Soil Biol Biochem 39:2208–2221. https://doi.org/10.1016/j.soilbio.2007.03.014
Haichar FE, 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
Haider G, Koyro HW, Azam F, Steffens D, Müller C, Kammann C (2015) Biochar but not humic acid product amendment affected maize yields via improving plant-soil moisture relations. Plant Soil 395:141–157. https://doi.org/10.1007/s11104-014-2294-3
Huang XF, Chaparro JM, Reardon KF, Zhang RF, Shen QR, Vivanco JM (2014) Rhizosphere interactions: root exudates, microbes, and microbial communities. Bot 92:267–275. https://doi.org/10.1139/cjb-2013-0225
Jeffery S, Verheijen FGA, Van DVM, Bastos AC (2011) A quantitative review of the effects of biochar application to soils on crop productivity using meta-analysis. Agric Ecosyst Environ 144:175–187. https://doi.org/10.1016/j.agee.2011.08.015
Jeffery S, Memelink I, Hodgson E, Jones S, Voorde TFJVD, Bezemer TM, Mommer L, van Groenigen JW (2017) Initial biochar effects on plant productivity derive from N fertilization. Plant Soil 415:435–448. https://doi.org/10.1007/s11104-016-3171-z
Jones DL, Brassington DS (1998) Sorption of organic acids in acid soils and its implications in the rhizosphere. Eur J Soil Sci 49:447–455. https://doi.org/10.1046/j.1365-2389.1998.4930447.x
Jones DL, Dennis PG, Owen AG, VanHees PAW (2003) Organic acid behaviour in soils-misconceptions and knowledge gaps. Plant Soil 248:31–41. https://doi.org/10.1023/A:1022304332313
Kant S, Bi YM, Rothstein SJ (2011) Understanding plant response to nitrogen limitation for the improvement of crop nitrogen use efficiency. J Exp Bot 62:1499–1509. https://doi.org/10.1093/jxb/erq297
Kuang Y, Wen D, Zhong C, Zhou G (2003) Root exudates and their roles in phytoremediation. Acta Pharmacol Sin 27:709–717. https://doi.org/10.17521/cjpe.2003.0103
Kuijken RCP, Snel JFH, Heddes MM, Bouwmeester HJ (2015) The importance of a sterile rhizosphere when phenotyping for root exudation. Plant Soil 387:131–142. https://doi.org/10.1007/s11104-014-2283-6
Lee CYC, Pedram EO, Hines AL (1986) Adsorption of oxalic, malonic, and succinic acids on activated carbon. J Chem Eng Data 31:133–136. https://doi.org/10.1021/je00044a001
Lehmann J (2007) Bio-energy in the black. Front Ecol Environ 5:381–387. https://doi.org/10.1890/1540-9295(2007)5[381:BITB]2.0.CO;2
Li B, Fan CH, Zhang H, Chen ZZ, Sun LY, Xiong ZQ (2015) Combined effects of nitrogen fertilization and biochar on the net global warming potential, greenhouse gas intensity and net ecosystem economic budget in intensive vegetable agriculture in southeastern China. Atmos Environ 100:10–19. https://doi.org/10.1016/j.atmosenv.2014.10.034
Luo Q, Wang SY, Sun LN, Wang H (2017) Metabolic profiling of root exudates from two ecotypes of Sedum alfredii treated with Pb based on GC-MS. Sci Rep 7:39878. https://doi.org/10.1038/srep39878
Ma W, Li XX, Li CJ (2011) Modulation of soil particle size and nutrient availability in the maize rhizosheath. Pedosphere 21:483–490. https://doi.org/10.1016/S1002-0160(11)60150-1
Mandal S, Thangarajan R, Bolan NS, Sarkar B, Khan N, Ok YS, Naidu R (2016) Biochar-induced concomitant decrease in ammonia volatilization and increase in nitrogen use efficiency by wheat. Chemosphere 142:120–127. https://doi.org/10.1016/j.chemosphere.2015.04.086
Maron LG, Pineros MA, Guimaraes CT, Magalhaes JV, Pleiman JK, Mao CZ, Shaff J, Belicuas SNJ, Kochian LV (2010) Two functionally distinct members of the MATE (multi-drug and toxic compound extrusion) family of transporters potentially underlie two major aluminum tolerance QTLs in maize. Plant J 61:728–740. https://doi.org/10.1111/j.1365-313X.2009.04103.x
Mehmood K, Li JY, Jiang J, Masud MM, Xu RK (2017) Effect of low energy-consuming biochars in combination with nitrate fertilizer on soil acidity amelioration and maize growth. J Soils Sediments 17:790–799. https://doi.org/10.1007/s11368-015-1219-y
Mete FZ, Mia S, Dijkstra FA, Abuyusuf M, Hossain ASMI (2015) Synergistic effects of biochar and NPK fertilizer on soybean yield in an alkaline soil. Pedosphere 25:713–719. https://doi.org/10.1016/S1002-0160(15)30052-7
Mönchgesang S, Strehmel N, Schmidt S, Westphal L, Taruttis F, Müller E, Herklotz S, Neumann S, Scheel D (2016) Natural variation of root exudates in Arabidopsis thaliana-linking metabolomic and genomic data. Sci Rep 6:29033. https://doi.org/10.1038/srep29033
Nelissen V, Rütting T, Huygens D, Ruysschaert G, Boeckx P (2015) Temporal evolution of biochar’s impact on soil nitrogen processes - a 15N tracing study. GCB Bioenergy 7:635–645. https://doi.org/10.1111/gcbb.12156
Palta JA, Yang JC (2014) Crop root system behaviour and yield preface. Field Crop Res 165:1–4. https://doi.org/10.1016/j.fcr.2014.06.024
Prendergast-Miller MT, Duvalla M, Sohia SP (2014) Biochar–root interactions are mediated by biochar nutrient content and impacts on soil nutrient availability. Eur J Soil Sci 65:173–185. https://doi.org/10.1111/ejss.12079
Proctor C, He YH (2017) Quantifying root extracts and exudates of sedge and shrub in relation to root morphology. Soil Biol Biochem 114:168–180. https://doi.org/10.1016/j.soilbio.2017.07.006
Ramirez KS, Craine JM, Fierer N (2012) Consistent effects of nitrogen amendments on soil microbial communities and processes across biomes. Glob Chang Biol 18:1918–1927. https://doi.org/10.1111/j.1365-2486.2012.02639.x
Rugova A, Puschenreiter M, Koellensperger G, Hann S (2017) Elucidating rhizosphere processes by mass spectrometry- a review. Anal Chim Acta 956:1–13. https://doi.org/10.1016/j.aca.2016.12.44
Solaiman ZM, Anawar HM (2015) Application of biochars for soil constraints: challenges and solutions. Pedosphere 25:631–638. https://doi.org/10.1016/S1002-0160(15)30044-8
Sun CX, Gao XX, Fu JQ, Zhou JH, Wu XF (2015) Metabolic response of maize (Zea mays L.) plants to combined drought and salt stress. Plant Soil 388:99–117. https://doi.org/10.1007/s11104-014-2309-0
Sun CX, Chen X, Cao MM, Li MQ, Zhang YL (2017) Growth and metabolic responses of maize roots to straw biochar application at different rates. Plant Soil 416:1–16. https://doi.org/10.1007/s11104-017-3229-6
Taghizadeh-Toosi A, Clough TJ, Sherlock RR, Condron LM (2012) Biochar adsorbed ammonia is bioavailable. Plant Soil 350:57–69. https://doi.org/10.1007/s11104-011-0870-3
Tiwari S, Singh P, Tiwari R, Meena KK, Yandigeri M, Singh DP, Arora DK (2011) Salt-tolerant rhizobacteria-mediated induced tolerance in wheat (Triticum aestivum) and chemical diversity in rhizosphere enhance plant growth. Biol Fertil Soils 47:907–916. https://doi.org/10.1007/s00374-011-0598-5
Valentinuzzi F, Pii Y, Vigani G, Lehmann M, Cesco S, Mimmo T (2015) Phosphorus and iron deficiencies induce a metabolic reprogramming and affect the exudation traits of the woody plant Fragaria×ananassa. J Exp Bot 66:6483–6495. https://doi.org/10.1093/jxb/erv364
Van Dam NM, Bouwmeester HJ (2016) Metabolomics in the rhizosphere: tapping into belowground chemical communication. Trends Plant Sci 21:256–265. https://doi.org/10.1016/j.tplants.2016.01.008
Van Hees PAW, Jones DL, Finlay R, Godbold DL, Lundstrom US (2005) The carbon we do not see - the impact of low molecular weight compounds on carbon dynamics and respiration in forest soils: a review. Soil Biol Biochem 37:1–13. https://doi.org/10.1016/j.soilbio.2004.06.010
von Wirén N, Lauter FR, Ninnemann O, Gillissen B, Walch-Liu P, Engels C, Jost W, Frommer WB (2000) Differential regulation of three functional ammonium transporter genes by nitrogen in root hairs and by light in leaves of tomato. Plant J 21:167–175. https://doi.org/10.1046/j.1365-313x.2000.00665.x
Zhu SS, Vivanco JM, Manter DK (2016) Nitrogen fertilizer rate affects root exudation, the rhizosphere microbiome and nitrogen-use-efficiency of maize. Appl Soil Ecol 107:324–333. https://doi.org/10.1016/j.apsoil.2016.07.009
Acknowledgements
We thank Dr. Janine A. for his linguistic modification of this paper.
Funding
This study was financially supported by the National Natural Science Foundation of China (No. 31300331), Science and Technology Program of Shenyang City (17-231-1-02), and the Lugu Foundation, P. R. of China.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible editor: Simon Jeffery
Rights and permissions
About this article
Cite this article
Cheng, N., Peng, Y., Kong, Y. et al. Combined effects of biochar addition and nitrogen fertilizer reduction on the rhizosphere metabolomics of maize (Zea mays L.) seedlings. Plant Soil 433, 19–35 (2018). https://doi.org/10.1007/s11104-018-3811-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-018-3811-6
Keywords
- Zea mays L.
- Biochar addition
- Nitrogen fertilizer reduction
- Root exudates
- Rhizosphere metabolomics