The rhizosphere effect on soil gross nitrogen mineralization: A meta-analysis
Dayong Gan, Hui Zeng, Biao Zhu
The rhizosphere effect on soil gross nitrogen mineralization: A meta-analysis
• We performed a meta-analysis to synthesize the rhizosphere effect on soil gross nitrogen mineralization rate.
• It was 81% on average, being significantly higher in woody (than non-woody species) and in ECM associated species (than AM associated species).
• It was positively correlated with the rhizosphere effects on soil C mineralization rate, microbial biomass nitrogen, phenol oxidase activity and root biomass.
• Its variations were mainly controlled by soil microbial variables and plant factors rather than climatic factors.
Rhizosphere effects play crucial roles in determining soil carbon (C) and nitrogen (N) cycling. However, the rhizosphere effect on soil gross nitrogen (N) mineralization (Nmin) has not been quantitatively assessed on the global scale. Here we performed a meta-analysis of compiled data from 24 publications and 37 species to synthesize the rhizosphere effect on soil gross Nmin and its influencing factors. We found that the rhizosphere effect significantly enhanced soil gross Nmin by 81% on average. Such rhizosphere effect was significantly higher in woody species than in non-woody species, and higher in ECM (ectomycorrhizal) associated species than in AM (arbuscular mycorrhizal) associated species. Moreover, the variations of the rhizosphere effect on soil gross Nmin were correlated with those on soil C mineralization, phenol oxidase activity and root biomass rather than with other plant (growth form and mycorrhizal association) and climatic (mean annual temperature and precipitation) factors. These results support the ‘microbial activation’ and ‘microbial N mining’ hypotheses of rhizosphere effects and indicate the coupling of soil C and gross N mineralization in the rhizosphere. Overall, these findings provide novel insights into the rhizosphere effect on soil gross Nmin among plant growth forms and mycorrhizal associations, and improve our mechanistic understanding of soil N dynamics in the rhizosphere.
Rhizosphere effect / Carbon mineralization / Nitrogen mineralization / Microbial biomass / Mycorrhizal association / Plant-soil interaction
[1] |
Bai, E., Li, S.L., Xu, W.H., Li, W., Dai, W.W., Jiang, P., 2013. A meta-analysis of experimental warming effects on terrestrial nitrogen pools and dynamics. New Phytologist 199, 441–451
CrossRef
Google scholar
|
[2] |
Bardgett, R.D., Mommer, L., De Vries, F.T., 2014. Going underground: root traits as drivers of ecosystem processes. Trends in Ecology & Evolution 29, 692–699
CrossRef
Google scholar
|
[3] |
Bergmann, J., Weigelt, A., van der Plas, F., Laughlin, D.C., Kuyper, T.W., Guerrero-Ramirez, N., Valverde-Barrantes, O.J., Bruelheide, H., Freschet, G.T., Iversen, C.M., Kattge, J., McCormack, M.L., Meier, I.C., Rillig, M.C., Roumet, C., Semchenko, M., Sweeney, C.J., van Ruijven, J., York, L.M., Mommer, L., 2020. The fungal collaboration gradient dominates the root economics space in plants. Science Advances 6, eaba3756
CrossRef
Google scholar
|
[4] |
Blaško, R., Högberg, P., Bach, L., Högberg, M., 2013. Relations among soil microbial community composition, nitrogen turnover, and tree growth in N-loaded and previously N-loaded boreal spruce forest. Forest Ecology and Management 302, 319–328
CrossRef
Google scholar
|
[5] |
Booth, M., Stark, J., Rastetter, E., 2005. Controls on nitrogen cycling in terrestrial ecosystems: A synthetic analysis of literature data. Ecological Monographs 75, 139–157
CrossRef
Google scholar
|
[6] |
Brzostek, E.R., Dragoni, D., Brown, Z.A., Phillips, R.P., 2015. Mycorrhizal type determines the magnitude and direction of root-induced changes in decomposition in a temperate forest. New Phytologist 206, 1274–1282
CrossRef
Google scholar
|
[7] |
Brzostek, E.R., Greco, A., Drake, J.E., Finzi, A.C., 2013. Root carbon inputs to the rhizosphere stimulate extracellular enzyme activity and increase nitrogen availability in temperate forest soils. Biogeochemistry 115, 65–76
CrossRef
Google scholar
|
[8] |
Chen, J., Luo, Y.Q., van Groenigen, K.J., Hungate, B.A., Cao, J.J., Zhou, X.H., Wang, R.W., 2018a. A keystone microbial enzyme for nitrogen control of soil carbon storage. Science Advances 4, eaaq1689.
|
[9] |
Chen, X., Ding, Z.J., Tang, M., Zhu, B., 2018b. Greater variations of rhizosphere effects within mycorrhizal group than between mycorrhizal group in a temperate forest. Soil Biology & Biochemistry 126, 237–246
CrossRef
Google scholar
|
[10] |
Cheng, W.X., 1999. Rhizosphere feedback in elevated CO2. Tree Physiology 19, 313–320
CrossRef
Google scholar
|
[11] |
Cheng, W.X., Johnson, D.W., Fu, S.L., 2003. Rhizosphere effects on decomposition: Controls of plant species, phenology, and fertilization. Soil Science Society of America Journal 67, 1418–1427
CrossRef
Google scholar
|
[12] |
Cheng, W.X., Kuzyakov, Y., 2005. Root Effects on Soil Organic Matter Decomposition. In: Zobel, R.W., Wright, S.F., eds. Roots and Soil Management: Interactions between Roots and the Soil, Agronomy Monograph No. 48. ASA-CSSA-SSSA, Madison, WI, pp. 119–143.
|
[13] |
Cheng, W.X., Parton, W.J., Gonzalez-Meler, M.A., Phillips, R., Asao, S., McNickle, G.G., Brzostek, E., Jastrow, J.D., 2014. Synthesis and modeling perspectives of rhizosphere priming. New Phytologist 201, 31–44
CrossRef
Google scholar
|
[14] |
Colin-Belgrand, M., Dambrine, E., Bienaimé, S., Nys, C., Turpault, M.P., 2003. Influence of tree roots on nitrogen mineralization. Scandinavian Journal of Forest Research 18, 260–268.
|
[15] |
Craine, J.M., Morrow, C., Fierer, N., 2007. Microbial nitrogen limitation increases decomposition. Ecology 88, 2105–2113
CrossRef
Google scholar
|
[16] |
Dieleman, W.I.J., Janssens, I.A., 2011. Can publication bias affect ecological research? A case study on soil respiration under elevated CO2. New Phytologist 190, 517–521
CrossRef
Google scholar
|
[17] |
Dijkstra, F.A., Bader, N.E., Johnson, D.W., Cheng, W.X., 2009. Does accelerated soil organic matter decomposition in the presence of plants increase plant N availability? Soil Biology & Biochemistry 41, 1080–1087
CrossRef
Google scholar
|
[18] |
Dijkstra, F.A., Carrillo, Y., Pendall, E., Morgan, J.A., 2013. Rhizosphere priming: a nutrient perspective. Frontiers in Microbiology 4, 216
CrossRef
Google scholar
|
[19] |
Dijkstra, F.A., Cheng, W.X., 2007. Moisture modulates rhizosphere effects on C decomposition in two different soil types. Soil Biology & Biochemistry 39, 2264–2274
CrossRef
Google scholar
|
[20] |
Dijkstra, F.A., Cheng, W.X., Johnson, D.W., 2006. Plant biomass influences rhizosphere priming effects on soil organic matter decomposition in two differently managed soils. Soil Biology & Biochemistry 38, 2519–2526
CrossRef
Google scholar
|
[21] |
Dijkstra, F.A., Zhu, B., Cheng, W.X., 2021. Root effects on soil organic carbon: a double-edged sword. New Phytologist 230, 60–65
CrossRef
Google scholar
|
[22] |
Ding, Z.J., Tang, M., Cheng, W.X., Chen, X., Yin, L.M., Gui, H.C., Zhu, B., 2019. Measuring rhizosphere effects of two tree species in a temperate forest: A comprehensive method comparison. Rhizosphere 10, 100153.
|
[23] |
Feng, J.G., Zhu, B., 2019. A global meta-analysis of soil respiration and its components in response to phosphorus addition. Soil Biology & Biochemistry 135, 38–47
CrossRef
Google scholar
|
[24] |
Feng, J.G., Zhu, B., 2021. Global patterns and associated drivers of priming effect in response to nutrient addition. Soil Biology & Biochemistry 153, 108118
CrossRef
Google scholar
|
[25] |
Finzi, A.C., Abramoff, R.Z., Spiller, K.S., Brzostek, E.R., Darby, B.A., Kramer, M.A., Phillips, R.P., 2015. Rhizosphere processes are quantitatively important components of terrestrial carbon and nutrient cycles. Global Change Biology 21, 2082–2094
CrossRef
Google scholar
|
[26] |
Fontaine, S., Henault, C., Aamor, A., Bdioui, N., Bloor, J., Maire, V., Mary, B., Revaillot, S., Maron, P., 2011. Fungi mediate long term sequestration of carbon and nitrogen in soil through their priming effect. Soil Biology & Biochemistry 43, 86–96
CrossRef
Google scholar
|
[27] |
Frank, D.A., Groffman, P.M., 2009. Plant rhizospheric N processes: what we don’t know and why we should care. Ecology 90, 1512–1519
CrossRef
Google scholar
|
[28] |
Fu, S.L., Cheng, W.X., 2002. Rhizosphere priming effects on the decomposition of soil organic matter in C4 and C3 grassland soils. Plant and Soil 238, 289–294
CrossRef
Google scholar
|
[29] |
Hamer, U., Makeschin, F., 2009. Rhizosphere soil microbial community structure and microbial activity in set-aside and intensively managed arable land. Plant and Soil 316, 57–69
CrossRef
Google scholar
|
[30] |
Han, M.G., Sun, L.J., Gan, D.Y., Fu, L.C., Zhu, B., 2020a. Root functional traits are key determinants of the rhizosphere effect on soil organic matter decomposition across 14 temperate hardwood species. Soil Biology & Biochemistry 151, 108019
CrossRef
Google scholar
|
[31] |
Han, M.G., Zhu, B., 2021. Linking root respiration to chemistry and morphology across species. Global Change Biology 27, 190–201
CrossRef
Google scholar
|
[32] |
Han, Y.F., Feng, J.G., Han, M.G., Zhu, B., 2020b. Responses of arbuscular mycorrhizal fungi to nitrogen addition: A meta-analysis. Global Change Biology 26, 7229–7241
CrossRef
Google scholar
|
[33] |
Hart, S.C., Nason, G.E., Myrold, D.D., Perry, D.A., 1994. Dynamics of gross nitrogen transformations in an old-growth forest: The carbon connection. Ecology 75, 880–891
CrossRef
Google scholar
|
[34] |
Hedges, L.V., Gurevitch, J., Curtis, P.S., 1999. The meta-analysis of response ratios in experimental ecology. Ecology 80, 1150–1156
CrossRef
Google scholar
|
[35] |
Henneron, L., Kardol, P., Wardle, D., Camille, C., Fontaine, S., 2020. Rhizosphere control of soil nitrogen cycling: a key component of plant economic strategies. New Phytologist 228, 1269–1282
CrossRef
Google scholar
|
[36] |
Herman, D.J., Johnson, K.K., Jaeger, C.H., Schwartz, E., Firestone, M.K., 2006. Root influence on nitrogen mineralization and nitrification in Avena barbata rhizosphere soil. Soil Science Society of America Journal 70, 60–66
CrossRef
Google scholar
|
[37] |
Hobbie, S., 1992. Effect of plant species on nutrient cycling. Trends in Ecology & Evolution 7, 336–339
CrossRef
Google scholar
|
[38] |
Holz, M., Aurangojeb, M., Kasimir, Å., Boeckx, P., Kuzyakov, Y., Klemedtsson, L., Rütting, T., 2016. Gross nitrogen dynamics in the mycorrhizosphere of an organic forest soil. Ecosystems (New York, N.Y.) 19, 284–295
CrossRef
Google scholar
|
[39] |
Huo, C.F., Luo, Y.Q., Cheng, W.X., 2017. Rhizosphere priming effect: A meta-analysis. Soil Biology & Biochemistry 111, 78–84
CrossRef
Google scholar
|
[40] |
Jiang, Z.H., Liu, Y.Z., Yang, J.P., Brookes, P.C., Gunina, A., 2021. Rhizosphere priming regulates soil organic carbon and nitrogen mineralization: The significance of abiotic mechanisms. Geoderma 385, 114877
CrossRef
Google scholar
|
[41] |
Jiao, S., Chen, W.M., Wang, J., Du, N.N., Li, Q.P., Wei, G.H., 2018. Soil microbiomes with distinct assemblies through vertical soil profiles drive the cycling of multiple nutrients in reforested ecosystems. Microbiome 6, 146
CrossRef
Google scholar
|
[42] |
Jones, D.L., Hodge, A., Kuzyakov, Y., 2004. Plant and mycorrhizal regulation of rhizodeposition. New Phytologist 163, 459–480
CrossRef
Google scholar
|
[43] |
Keller, A.B., Phillips, R.P., 2019. Leaf litter decay rates differ between mycorrhizal groups in temperate, but not tropical, forests. New Phytologist 222, 556–564
CrossRef
Google scholar
|
[44] |
Koranda, M., Schnecker, J., Kaiser, C., Fuchslueger, L., Kitzler, B., Stange, C.F., Sessitsch, A., Zechmeister-Boltenstern, S., Richter, A., 2011. Microbial processes and community composition in the rhizosphere of European beech–The influence of plant C exudates. Soil Biology & Biochemistry 43, 551–558
CrossRef
Google scholar
|
[45] |
Kuzyakov, Y., 2002. Review: Factors affecting rhizosphere priming effects. Journal of Plant Nutrition and Soil Science 165, 382–396
CrossRef
Google scholar
|
[46] |
Kuzyakov, Y., 2010. Priming effects: interactions between living and dead organic matter. Soil Biology & Biochemistry 42, 1363–1371
CrossRef
Google scholar
|
[47] |
Kuzyakov, Y., Blagodatskaya, E., 2015. Microbial hotspots and hot moments in soil: Concept & review. Soil Biology & Biochemistry 83, 184–199
CrossRef
Google scholar
|
[48] |
Kuzyakov, Y., Xu, X.L., 2013. Competition between roots and microorganisms for nitrogen: mechanisms and ecological relevance. New Phytologist 198, 656–669
CrossRef
Google scholar
|
[49] |
Lebauer, D., Treseder, K., 2008. Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distributed. Ecology 89, 371–379
CrossRef
Google scholar
|
[50] |
Li, X.W., Zhang, C.L., Zhang, B.B., Wu, D., Zhu, D.D., Zhang, W., Ye, Q., Yan, J.H., Fu, J.M., Fang, C.L., Ha, D.L., Fu, S.L., 2021. Nitrogen deposition and increased precipitation interact to affect fine root production and biomass in a temperate forest: Implications for carbon cycling. Science of the Total Environment 765, 144497
CrossRef
Google scholar
|
[51] |
Liao, C.Z., Peng, R.H., Luo, Y.Q., Zhou, X.H., Wu, X.W., Fang, C.M., Chen, J.K., Li, B., 2008. Altered ecosystem carbon and nitrogen cycles by plant invasion: a meta-analysis. New Phytologist 177, 706–714
CrossRef
Google scholar
|
[52] |
Lin, G.G., Guo, D.L., Li, L., Ma, C.E., Zeng, D.H., 2017. Contrasting effects of ectomycorrhizal and arbuscular mycorrhizal tropical tree species on soil nitrogen cycling: the potential mechanisms and corresponding adaptive strategies. Oikos 127, 518–530
CrossRef
Google scholar
|
[53] |
Lindahl, B.D., Tunlid, A., 2015. Ectomycorrhizal fungi – potential organic matter decomposers, yet not saprotrophs. New Phytologist 205, 1443–1447
CrossRef
Google scholar
|
[54] |
Liu, L.L., Wang, X., Lajeunesse, M.J., Miao, G.F., Piao, S.L., Wan, S.Q., Wu, Y.X., Wang, Z.H., Yang, S., Li, P., Deng, M.F., 2016. A cross-biome synthesis of soil respiration and its determinants under simulated precipitation changes. Global Change Biology 22, 1394–1405
CrossRef
Google scholar
|
[55] |
Luo, Y.Q., Zhang, D.Q., Hui, D.F., 2006. Elevated CO2 stimulates net accumulations of carbon and nitrogen in land ecosystems: a meta-analysis. Ecology 87, 53–63.
|
[56] |
Maire, V., Wright, I., Prentice, I., Batjes, N., Bhaskar, R., Bodegom, P., Cornwell, W., Ellsworth, D., Niinemets, Ü., Ordonez, A., Reich, P., Santiago, L., 2015. Global effects of soil and climate on leaf photosynthetic traits and rates: Effects of soil and climate on photosynthetic traits. Global Ecology and Biogeography 24, 706–717
CrossRef
Google scholar
|
[57] |
Meier, I., Pritchard, S., Brzostek, E., McCormack, M., Phillips, R., 2015. The rhizosphere and hyphosphere differ in their impacts on carbon and nitrogen cycling in forests exposed to elevated CO2. New Phytologist 205, 1164–1174
CrossRef
Google scholar
|
[58] |
Mo, C.Y., Jiang, Z.H., Chen, P.F., Cui, H., Yang, J.P., 2021. Microbial metabolic efficiency functions as a mediator to regulate rhizosphere priming effects. Science of the Total Environment 759, 143488
CrossRef
Google scholar
|
[59] |
Murphy, C.J., Baggs, E.M., Morley, N., Wall, D.P., Paterson, E., 2015. Rhizosphere priming can promote mobilisation of N-rich compounds from soil organic matter. Soil Biology & Biochemistry 81, 236–243
CrossRef
Google scholar
|
[60] |
Murphy, D.V., Recous, S., Stockdale, E.A., Fillery, I.R.P., Jensen, L., Hatch, D.J., Goulding, K.W.T., 2003. Gross nitrogen fluxes in soil: theory, measurement and application of 15N pool dilution techniques. Advances in Agronomy 79, 69–118
CrossRef
Google scholar
|
[61] |
Phillips, R.P., Fahey, T.J., 2006. Tree species and mycorrhizal associations influence the magnitude of rhizosphere effects. Ecology 87, 1302–1313
CrossRef
Google scholar
|
[62] |
Pokharel, P., Qi, L., Chang, S.X., 2021. Manure-based biochar decreases heterotrophic respiration and increases gross nitrification rates in rhizosphere soil. Soil Biology & Biochemistry 154, 108147
CrossRef
Google scholar
|
[63] |
Read, D.J., Perez-Moreno, J., 2003. Mycorrhizas and nutrient cycling in ecosystems—a journey towards relevance? New Phytologist 157, 475–492
CrossRef
Google scholar
|
[64] |
Schimel, J., Bennett, J., 2004. Nitrogen mineralization: challenges of a changing paradigm. Ecology 85, 591–602
CrossRef
Google scholar
|
[65] |
Soudzilovskaia, N., Vaessen, S., Barcelo, M., He, J., Rahimlou, S., Abarenkov, K., Brundrett, M., Gomes, S., Merckx, V., Tederesoo, L., 2020. FungalRoot: Global online database of plant mycorrhizal associations. New Phytologist 227, 955–966
CrossRef
Google scholar
|
[66] |
Sun, Y., Xu, X.L., Kuzyakov, Y., 2014. Mechanisms of rhizosphere priming effects and their ecological significance. Acta Phytoecologica Sinica 38, 62–75
CrossRef
Google scholar
|
[67] |
Sun, Y., Zang, H.D., Splettstößer, T., Kumar, A., Xu, X.L., Kuzyakov, Y., Pausch, J., 2021. Plant intraspecific competition and growth stage alter carbon and nitrogen mineralization in the rhizosphere. Plant, Cell & Environment 44, 1231–1242
CrossRef
Google scholar
|
[68] |
Terrer, C., Jackson, R., Prentice, I., Keenan, T., Kaiser, C., Vicca, S., Fisher, J., Reich, P., Stocker, B., Hungate, B., Penuelas, J., McCallum, I., Soudzilovskaia, N., Cernusak, L., Talhelm, A., Van Sundert, K., Piao, S., Newton, P., Hovenden, M., Franklin, O., 2019. Nitrogen and phosphorus constrain the CO2 fertilization of global plant biomass. Nature Climate Change 9, 684–689
CrossRef
Google scholar
|
[69] |
Van Sundert, K., Radujković, D., Cools, N., De Vos, B., Etzold, S., Fernández-Martínez, M., Janssens, I.A., Merilä, P., Peñuelas, J., Sardans, J., Stendahl, J., Terrer, C., Vicca, S., 2020. Towards comparable assessment of the soil nutrient status across scales—Review and development of nutrient metrics. Global Change Biology 26, 392–409
CrossRef
Google scholar
|
[70] |
Viechtbauer, W., 2010. Conducting meta-analyses in R with the metafor package. Journal of Statistical Software 36, 1–48
CrossRef
Google scholar
|
[71] |
Wang, B., Qiu, Y.L., 2006. Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza 16, 299–363
CrossRef
Google scholar
|
[72] |
Weemstra, M., Mommer, L., Visser, E., Ruijven, J., Kuyper, T., Mohren, G.M.J., Sterck, F., 2016. Towards a multidimensional root trait framework: A tree root review. New Phytologist 211, 1159–1169
CrossRef
Google scholar
|
[73] |
Yin, H.J., Wheeler, E., Phillips, R.P., 2014. Root-induced changes in nutrient cycling in forests depend on exudation rates. Soil Biology & Biochemistry 78, 213–221
CrossRef
Google scholar
|
[74] |
Yin, L.M., Dijkstra, F.A., Wang, P., Zhu, B., Cheng, W.X., 2018. Rhizosphere priming effects on soil carbon and nitrogen dynamics among tree species with and without intraspecific competition. New Phytologist 218, 1036–1048
CrossRef
Google scholar
|
[75] |
Zhu, B., Cheng, W.X., 2012. Nodulated soybean enhances rhizosphere priming effects on soil organic matter decomposition more than non-nodulated soybean. Soil Biology & Biochemistry 51, 56–65
CrossRef
Google scholar
|
[76] |
Zhu, B., Gutknecht, J.L.M., Herman, D.J., Keck, D.C., Firestone, M.K., Cheng, W.X., 2014. Rhizosphere priming effects on soil carbon and nitrogen mineralization. Soil Biology & Biochemistry 76, 183–192
CrossRef
Google scholar
|
/
〈 | 〉 |