Abstract
Aims
N rhizodeposition plays a vital role in regulating rhizosphere soil N dynamics. However, its effects on the rhizosphere soil N cycle in clonal plants and the underlying mechanism remain unclear.
Methods
15N solutions with different concentrations were injected into young or connected mature ramets of Moso bamboo (Phyllostachys edulis), respectively, in the field, to explore the response of rhizosphere N transformation to N rhizodeposition.
Results
15N injection increased the 15N abundance in the rhizosphere soil of both young and mature ramets, with higher 15N abundance in 20–40-cm layer than that in 0–20-cm layer. Functional genes involved in nitrification and denitrification in the rhizosphere were upregulated when young ramets received low- and medium-N solutions. However, the genes showed diverse responses to high-N treatment in young ramets, with increased abundances of ammonia-oxidizing bacteria and decreased levels of ammonia-oxidizing archaea, comammox, and denitrifiers. In contrast, the functional genes involved in denitrification in the 20–40-cm layer of rhizosphere soil were upregulated by high-N treatment in mature ramets. Additionally, partial-least-squares path modeling revealed 15N abundance in the soil indirectly affected N mineralization, N mineralization directly affected nitrification, and nitrification directly affected denitrification in a positive manner.
Conclusion
The variations of N rhizodeposition and transformation process in both connected ramets is highly consistent in responding to different N treatments, but the nitrifiers and denitrifiers in the deeper rhizosphere soil were more sensitive to N rhizodeposits than those in the upper rhizosphere soil.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Arcand MM, Knight JD, Farrell RE (2013) Estimating belowground nitrogen inputs of pea and canola and their contribution to soil inorganic N pools using 15N labeling. Plant Soil 371:67–80. https://doi.org/10.1007/s11104-013-1626-z
Brookes PC, Landman A, Pruden G, Jenkinson DS (1985) Chloroform fumigation and the release of soil nitrogen: a rapid direct extraction method to measure microbial biomass nitrogen in soil. Soil Biol Biochem 17:837–842. https://doi.org/10.1016/0038-0717(85)90144-0
Brzostek ER, Greco A, Drake JE, Finzi AC (2013) Root carbon inputs to the rhizosphere stimulate extracellular enzyme activity and increase nitrogen availability in temperate forest soils. Biogeochemistry 115:65–76. https://doi.org/10.1007/s10533-012-9818-9
Cao Y, Sun X, Shi Y, Lu C, Miao Y, Chen Z, Han S (2021) Quantitative evidence of underestimated nitrogen rhizodeposition using 15N split-root labeling during spring wheat developmental period. Catena (Amst) 207:105618. https://doi.org/10.1016/j.catena.2021.105618
Cao T, Luo Y, Shi M, Tian X, Kuzyakov Y (2024) Microbial interactions for nutrient acquisition in soil: miners, scavengers, and carriers. Soil Biol Biochem 188:109215. https://doi.org/10.1016/j.soilbio.2023.109215
Chen H, Feng Y, Zhou J, Xu Z, Lian C, Guo Q (2013) Root biomass distribution and seasonal variation of Phyllostachys edulis. Energy Environ Sci 22:1678–1681. (In Chinese). https://doi.org/10.16258/j.cnki.1674-5906.2013.10.006
Chen JS, Li J, Zhang Y, Zong H, Lei NF (2015) Clonal integration ameliorates the carbon accumulation capacity of a stoloniferous herb, Glechoma longituba, growing in heterogenous light conditions by facilitating nitrogen assimilation in the rhizosphere. Ann Bot 115:127–136. https://doi.org/10.1093/aob/mcu207
Coskun D, Britto DT, Shi W, 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
Dimassi B, Mary B, Fontaine S, Perveen N, Revaillot S, Cohan JP (2014) Effect of nutrients availability and long-term tillage on priming effect and soil C mineralization. Soil Biol Biochem 78:332–339. https://doi.org/10.1016/j.soilbio.2014.07.016
Dorich RA, Nelson DW (1983) Direct colorimetric measurement of ammonium in potassium chloride extracts of soils. Soil Sci Soc Am J 47:833–836. https://doi.org/10.2136/sssaj1983.03615995004700040042x
Garcia C, Roldan A, Hernandez T (2005) Ability of different plant species to promote microbiological processes in semiarid soil. Geoderma 124:193–202. https://doi.org/10.1016/j.geoderma.2004.04.013
Gardner M, Peoples M, Condon J, Li G, Conyers M, Dear B (2012) Evaluating the importance of a potential source of error when applying shoot 15N labelling techniques to legumes to quantify the below-ground transfer of nitrogen to other species. In: Proceedings of the 16th Australian Agronomy Conference, Armidale, NSW, Australia
Gasser M, Hammelehle A, Oberson A, Frossard E, Mayer J (2015) Quantitative evidence of overestimated rhizodeposition using 15N leaf-labelling. Soil Biol Biochem 85:10–20. https://doi.org/10.1016/j.soilbio.2015.02.002
Grace JB, Anderson TM, Seabloom EW, Borer ET, Adler PB, Harpole WS, Hautier Y, Hillebrand H, Lind EM, Pärtel M, Bakker JD, Buckley YM, Crawley MJ, Damschen EI, Davies KF, Fay PA, Firn J, Gruner DS, Hector A et al (2016) Integrative modelling reveals mechanisms linking productivity and plant species richness. Nature 529:390–393. https://doi.org/10.1038/nature16524
Hink L, Gubry-Rangin C, Nicol GW, 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
Hupe A, Schulz H, Bruns C, Joergensen RG, Wichern F (2016) Digging in the dirt–inadequacy of belowground plant biomass quantification. Soil Biol Biochem 96:137–144. https://doi.org/10.1016/j.soilbio.2016.01.014
Hupe A, Schulz H, Bruns C, Haase T, Heß J, Dyckmans J, Joergensen RG, Wichern F (2019) Get on your boots: estimating root biomass and rhizodeposition of peas under field conditions reveals the necessity of field experiments. Plant Soil 443:449–462. https://doi.org/10.1007/s11104-019-04238-z
Hütsch BW, Augustin J, Merbach W (2002) Plant rhizodeposition—an important source for carbon turnover in soils. J Plant Nutr Soil Sci 165:397–407. https://doi.org/10.1002/1522-2624(200208)165:4<397::aid-jpln397>3.0.co;2-c
Janzen HH (1990) Deposition of nitrogen into the rhizosphere by wheat roots. Soil Biol Biochem 22:1155–1160. https://doi.org/10.1016/0038-0717(90)90043-Y
Janzen HH, Bruinsma Y (1989) Methodology for the quantification of root and rhizosphere nitrogen dynamics by exposure of shoots to 15N-labelled ammonia. Soil Biol Biochem 21:189–196. https://doi.org/10.1016/0038-0717(89)90094-1
Karhu K, Hilasvuori E, Fritze H, Biasi C, Nykänen H, Liski J, Vanhala P, Heinonsalo J, Pumpanen J (2016) Priming effect increases with depth in a boreal forest soil. Soil Biol Biochem 99:104–107. https://doi.org/10.1016/j.soilbio.2016.05.001
Koch H, van Kessel MA, Lücker S (2019) Complete nitrification: insights into the ecophysiology of comammox Nitrospira. Appl Microbiol Biotechnol 103:177–189. https://doi.org/10.1007/s00253-018-9486-3
Lancaster NA, Bushey JT, Tobias CR, Song B, Vadas TM (2016) Impact of chloride on denitrification potential in roadside wetlands. Environ Pollut 212:216–223. https://doi.org/10.1016/j.envpol.2016.01.068
Li Y, Chen JS, Xue G, Peng Y, Song HX (2018) Effect of clonal integration on nitrogen cycling in rhizosphere of rhizomatous clonal plant, Phyllostachys bissetii, under heterogeneous light. Sci Total Environ 628:594–602. https://doi.org/10.1016/j.scitotenv.2018.02.002
Marschner H (ed) (2011) Marschner’s mineral nutrition of higher plants. Academic press, London. https://doi.org/10.1016/C2009-0-63043-9
Mayer J, Buegger F, Jensen ES, Schloter M, Heß J (2003) Estimating N rhizodeposition of grain legumes using a 15N in situ stem labelling method. Soil Biol Biochem 35:21–28. https://doi.org/10.1016/S0038-0717(02)00212-2
Mayer J, Buegger F, Jensen ES, Schloter M, Heß J (2004) Turnover of grain legume N rhizodeposits and effect of rhizodeposition on the turnover of crop residues. Biol Fertil Soils 39:153–164. https://doi.org/10.1007/s00374-003-0694-2
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
National Forestry and Grassland Administration (2019) Report for Chinese Forest resource (2014–2018). China Forestry Publishing House, Beijing (In Chinese)
Norman RJ, Stucki JW (1981) The determination of nitrate and nitrite in soil extracts by ultraviolet spectrophotometry. Soil Sci Soc Am J 45:347–353. https://doi.org/10.2136/sssaj1981.03615995004500020024x
Paterson E (2003) Importance of rhizodeposition in the coupling of plant and microbial productivity. Eur J Soil Sci 54:741–750. https://doi.org/10.1046/j.1351-0754.2003.0557.x
Paterson E, Gebbing T, Abel C, Sim A, Telfer G (2007) Rhizodeposition shapes rhizosphere microbial community structure in organic soil. New Phytol 173:600–610. https://doi.org/10.1111/j.1469-8137.2006.01931.x
Peixoto L, Elsgaard L, Rasmussen J, Kuzyakov Y, Banfield CC, Dippold MA, Olesen JE (2020) Decreased rhizodeposition, but increased microbial carbon stabilization with soil depth down to 3.6 m. Soil Biol Biochem 150:108008. https://doi.org/10.1016/j.soilbio.2020.108008
Qiu Q, Li M, Mgelwa AS, Hu YL (2023) Divergent mineralization of exogenous organic substrates and their priming effects depending on soil types. Biol Fertil Soils 59:87–101. https://doi.org/10.1007/s00374-022-01682-5
Quinio M, De Waele M, Dessaint F, Biju-Duval L, Buthiot M, Cadet E, Bybee-Finley A, Guillemin J, Cordeau S (2017) Separating the confounding effects of farming practices on weeds and winter wheat production using path modelling. Eur J Agron 82:134–143. https://doi.org/10.1016/j.eja.2016.10.011
Rasmussen J, Eriksen J, Jensen ES, Høgh-Jensen H (2010) Root size fractions of ryegrass and clover contribute differently to C and N inclusion in SOM. Biol Fertil Soils 46:293–297. https://doi.org/10.1007/s00374-009-0430-7
Rasmussen J, Dresbøll DB, Enggrob KL, Peixoto L (2021) A novel 15N vertical split-root method for in situ estimation of N rhizodeposition. Geoderma 383:114782. https://doi.org/10.1016/j.geoderma.2020.114782
Sanchez G (2013) PLS Path Modeling with R Trowchez Editions. Berkeley, 2013. http://www.gastonsanchez.com/PLS Path Modeling with R.pdf
Scandellari F, Tonon G, Thalheimer M, Ceccon C, Gioacchini P, Aber JD, Tagliavini M (2007) Assessing nitrogen fluxes from roots to soil associated to rhizodeposition by apple (Malus domestica) trees. Trees 21:499–505. https://doi.org/10.1007/s00468-007-0141-3
Scandellari F, Ventura M, Gioacchini P, Antisari LV, Tagliavini M (2010) Seasonal pattern of net nitrogen rhizodeposition from peach (Prunus persica (L.) Batsch) trees in soils with different textures. Agric Ecosyst Environ 136:162–168. https://doi.org/10.1016/j.agee.2009.12.017
Shi M, Zhang J, Sun J, Li Q, Lin X, Song X (2022) Unequal nitrogen translocation pattern caused by clonal integration between connected ramets ensures necessary nitrogen supply for young Moso bamboo growth. Environ Exp Bot 200:104900. https://doi.org/10.1016/j.envexpbot.2022.104900
Sindhu MA, Cornfield AH (1967a) Effect of sodium chloride and moisture content on ammonification and nitrification in incubated soil. J Sci Food Agric 18:505–506. https://doi.org/10.1002/jsfa.2740181103
Sindhu MT, Cornfield AH (1967b) Comparative effects of varying levels of chlorides and sulphates of sodium, potassium, calcium, and magnesium on ammonification and nitrification during incubation of soil. Plant Soil 27:468–472. https://doi.org/10.1007/BF01376343
Song X, Peng C, Zhou G, Gu H, Li Q, Zhang C (2016) Dynamic allocation and transfer of non-structural carbohydrates, a possible mechanism for the explosive growth of Moso bamboo (Phyllostachys heterocycla). Sci Rep 6:1–8. https://doi.org/10.1038/srep25908
Song X, Peng C, Ciais P, Li Q, Xiang W, Xiao W, Zhou G, Deng L (2020) Nitrogen addition increased CO2 uptake more than non-CO2 greenhouse gases emissions in a Moso bamboo forest. Sci Adv 6: eaaw5790. https://doi.org/10.1126/sciadv.aaw5790
Su W, Fan S, Zhao J, Cai C (2019) Effects of various fertilization placements on the fate of urea-15N in Moso bamboo forests. For Ecol Manag 453:117632. https://doi.org/10.1016/j.foreco.2019.117632
Wang J, Xu T, Wang Y, Li G, Abdullah I, Zhong Z, Liu J, Zhu W, Wang L, Wang D, Yu FH (2021a) A meta-analysis of effects of physiological integration in clonal plants under homogeneous vs. heterogeneous environments. Funct Ecol 35:578–589. https://doi.org/10.1111/1365-2435.13732
Wang X, Yang Y, Pei K, Zhou J, Peixoto L, Gunina A, Zeng Z, Zang H, Rasmussen J, Kuzyakov Y (2021b) Nitrogen rhizodeposition by legumes and its fate in agroecosystems: a field study and literature review. Land Degrad Dev 32:410–419. https://doi.org/10.1002/ldr.3729
Westerman RL, Tucker TC (1974) Effect of salts and salts plus Nitrogen-15-labeled ammonium chloride on mineralization of soil nitrogen, nitrification, and immobilization. Soil Sci Soc Am J 38:602–605. https://doi.org/10.2136/sssaj1974.03615995003800040024x
Wichern F, Mayer J, Joergensen RG, Müller T (2007) Rhizodeposition of C and N in peas and oats after 13C–15N double labelling under field conditions. Soil Biol Biochem 39:2527–2537. https://doi.org/10.1016/j.soilbio.2007.04.022
Wichern F, Eberhardt E, Mayer J, Joergensen RG, Müller T (2008) Nitrogen rhizodeposition in agricultural crops: methods, estimates and future prospects. Soil Biol Biochem 40:30–48. https://doi.org/10.1016/j.soilbio.2007.08.010
Zang H, Yang X, Feng X, Qian X, Hu Y, Ren C, Zeng Z (2015) Rhizodeposition of nitrogen and carbon by mungbean (Vigna radiata L.) and its contribution to intercropped oats (Avena nuda L.). PLoS One 10:e0121132. https://doi.org/10.1371/journal.pone.0128503
Funding
The authors are grateful for the financial support from the Natural Science Foundation of China (32101493, 31930075, 32125027), and Scientific Research Foundation of Zhejiang A&F University (Nos. 2020FR088; 2022LFR006).
Author information
Authors and Affiliations
Contributions
Man Shi: Conceptualization, Methodology, Investigation, Formal analysis, Data curation, Visualization, Writing – Original Draft Preparation, Funding acquisition. Weiwei Yang: Writing – review & editing. Junbo Zhang & Jilei Sun: Methodology, Investigation. Hangxiang Ji: Investigation, Visualization. Quan Li, Tingting Cao & Zhikang Wang: Writing – review & editing. Chao Zhang: Investigation. Xinzhang Song: Design, Conceptualization, Methodology, Validation, Writing – review & editing, Supervision, Funding acquisition.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no competing interests.
Additional information
Responsible Editor: Paul Bodelier.
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
ESM 1
(DOCX 402 kb)
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Shi, M., Yang, W., Zhang, J. et al. Effects of N rhizodeposition on rhizosphere N transformation in clonal ramets of Moso bamboo forest. Plant Soil (2024). https://doi.org/10.1007/s11104-024-06615-9
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11104-024-06615-9