Abstract
This study aims to investigate the role of arbuscular mycorrhizal (AM) symbiosis in reducing N loss from paddy fields, using two rice lines: a mycorrhiza-defective rice line (non-mycorrhizal) and its mycorrhizal progenitor. Two rice lines were grown in the presence of an AM fungal isolate. In this study, N loss of runoff, leaching, N2O emission, and NH3 volatilization were measured, and in addition, N uptake of rice, soil aggregates, and plant available N concentration of soil. The results obtained suggest that N loss via runoff, leaching, NH3 volatilization, and N2O emission of mycorrhizal rice was 11%, 8%, 6%, and 1%, lower than that of non-mycorrhizal rice, respectively. Meanwhile, mycorrhizal rice has higher biomass and plant N uptake. Our study shows that the AM symbiosis contributes to the sustainability of rice production by reducing N loss, enhancing soil aggregation and increasing plant N uptake.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data Availability
All data generated or analyzed during this study are included in this published article.
References
Asghari, H. R., & Cavagnaro, T. R. (2011). Arbuscular mycorrhizas enhance plant interception of leached nutrients. Functional Plant Biology, 38, 219–226. https://doi.org/10.1071/fp10180
Asghari, H. R., & Cavagnaro, T. R. (2012). Arbuscular mycorrhizas reduce nitrogen loss via leaching. Public Library of Science, 7, 151–155. https://doi.org/10.1371/journal.pone.0029825
Bavel, C. (1950). Mean weight-diameter of soil aggregates as a statistical index of aggregation. Soil Science Society of America, Proceedings, 14, 20–23. https://doi.org/10.2136/sssaj1950.036159950014000c0005x
Bender, S. F., Conen, F., & Van der Heijden, M. G. A. (2015). Mycorrhizal effects on nutrient cycling, nutrient leaching and N2O production in experimental grassland. Soil Biology & Biochemistry, 80, 283–292. https://doi.org/10.1016/j.soilbio.2014.10.016
Bender, S. F., Plantenga, F., Neftel, A., Jocher, M., Oberholzer, H. R., Köhl, L., Giles, M., Daniell, T. J., & Heijden, M. G. V. D. (2014). Symbiotic relationships between soil fungi and plants reduce N2O emissions from soil. Isme Journal, 8, 1336–1345. https://doi.org/10.1038/ismej.2013.224
Cao, Y., Tian, Y., Yin, B., & Zhu, Z. (2013). Assessment of ammonia volatilization from paddy fields under crop management practices aimed to increase grain yield and N efficiency. Field Crops Research, 147, 23–31. https://doi.org/10.1016/j.fcr.2013.03.015
Cavagnaro, T. R., Barrios-Masias, F. H., & Jackson, L. E. (2012). Arbuscular mycorrhizas and their role in plant growth, nitrogen interception and soil gas efflux in an organic production system. Plant and Soil, 353, 181–194. https://doi.org/10.1007/s11104-011-1021-6
Cavagnaro, T. R., Bender, S. F., Asghari, H. R., & van der Heijden, M. G. A. (2015). The role of arbuscular mycorrhizas in reducing soil nutrient loss. Trends in Plant Science, 20, 283–290. https://doi.org/10.1016/j.tplants.2015.03.004
Cavagnaro, T. R., Jackson, L. E., Six, J., Ferris, H., Goyal, S., Asami, D., & Scow, K. M. (2006). Arbuscular mycorrhizas, microbial communities, nutrient availability, and soil aggregates in organic tomato production. Plant and Soil, 282, 209–225. https://doi.org/10.1007/s11104-005-5847-7
Chen, X., Cui, Z., Fan, M., Vitousek, P., Zhao, M., Ma, W., Wang, Z., Zhang, W., Yan, X., & Yang, J. (2014). Producing more grain with lower environmental costs. Nature, 514, 486–489. https://doi.org/10.1038/nature13609
Ciais P. Sabine C. Bala G. Bopp L. Brovkin V. Al. E. House J.I (2013) Carbon and other biogeochemical cycles: climate change 2013: The physical science basis. Contribution of working group I to the fifth assessment report of the intergovernmental panel on climate change. Cambridge: Cambridge University Press. 465–570
Corkidi, L., Merhaut, D. J., Allen, E. B., Downer, J., Bohn, J., & Evans, M. (2011). Effects of mycorrhizal colonization on nitrogen and phosphorus leaching from nursery containers. Hortscience, 46, 1472–1479. https://doi.org/10.21273/hortsci.46.11.1472
Cui, Z., Vitousek, P. M., Zhang, F., & Chen, X. (2016). Strengthening agronomy research for food security and environmental quality. Environmental Science and Technology, 50, 1639–1641. https://doi.org/10.1021/acs.est.6b00267
Erisman, J. W., Sutton, M. A., Galloway, J., Klimont, Z., & Winiwarter, W. (2008). How a century of ammonia synthesis changed the world. Nature Geoscience, 1, 636–639. https://doi.org/10.1038/ngeo325
Giovannetti, M., & Mosse, B. (2010). An evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytologist, 84, 489–500. https://doi.org/10.1111/j.1469-8137.1980.tb04556.x
Gon, H. D. V. D., & Bleeker, A. (2005). Indirect N2O emission due to atmospheric N deposition for the Netherlands. Atmospheric Environment, 39, 5827–5838. https://doi.org/10.1016/j.atmosenv.2005.06.019
Hodge, A., & Storer, K. (2015). Arbuscular mycorrhiza and nitrogen: Implications for individual plants through to ecosystems. Plant and Soil, 386, 1–19. https://doi.org/10.1007/s11104-014-2162-1
Jiang, Y., Wang, W., Xie, Q., Liu, N., Liu, L., Wang, D., Zhang, X., Yang, C., Chen, X., Tang, D., et al. (2017). Plants transfer lipids to sustain colonization by mutualistic mycorrhizal and parasitic fungi. Science, 356, 1172–1175. https://doi.org/10.1126/science.aam9970
van der Köhl, L., & Heijden, M. G. (2016). Arbuscular mycorrhizal fungal species differ in their effect on nutrient leaching. Soil Biology and Biochemistry, 94, 191–199. https://doi.org/10.1016/j.soilbio.2015.11.019
Kemper, W. D., & Rosenau, R. C. (1986). Aggregate stability and size distribution. Methods of Soil Analysis, 1, 425–442. https://doi.org/10.2136/sssabookser5.1.2ed.c17
Lam, S. K., Suter, H., Mosier, A. R., & Chen, D. L. (2017). Using nitrification inhibitors to mitigate agricultural N2O emission: A double-edged sword? Global Change Biology, 23, 485–489. https://doi.org/10.1111/gcb.13338
Lehmann, A., & Rillig, M. C. (2015). Arbuscular mycorrhizal contribution to copper, manganese and iron nutrient concentrations in crops - A meta-analysis. Soil Biology & Biochemistry, 81, 147–158. https://doi.org/10.1016/j.soilbio.2014.11.013
Lehmann, A., Veresoglou, S. D., Leifheit, E. F., & Rillig, M. C. (2014). Arbuscular mycorrhizal influence on zinc nutrition in crop plants - A meta-analysis. Soil Biology & Biochemistry, 69, 123–131. https://doi.org/10.1016/j.soilbio.2013.11.001
Lehmann, A., Zheng, W., & Rillig, M. C. (2017). Soil biota contributions to soil aggregation. Nature Ecology & Evolution, 1, 1828–1835. https://doi.org/10.1038/s41559-017-0344-y
Lehrsch, GA., Kincaid, D. (2006) Sprinkler droplet energy effects on soil penetraition resistance and aggregate stability and size distribution. Soil Science 171(6) 435–447. https://doi.org/10.1097/01.ss.0000227361.36922.ad
Leifheit, E., Verbruggen, E., & Rillig, M. C. (2015). Arbuscular mycorrhizal fungi reduce decomposition of woody plant litter while increasing soil aggregation. Soil Biology and Biochemistry, 81, 323–328. https://doi.org/10.1016/j.soilbio.2014.12.003
Leifheit, E. F., Veresoglou, S. D., Lehmann, A., Morris, E. K., & Rillig, M. C. (2014). Multiple factors influence the role of arbuscular mycorrhizal fungi in soil aggregation-A meta-analysis. Plant and Soil, 374, 523–537. https://doi.org/10.1007/s11104-013-1899-2
Lewis, W. M., Wurtsbaugh, W. A., & Paerl, H. W. (2011). Rationale for control of anthropogenic nitrogen and phosphorus to reduce eutrophication of inland waters. Environmental Science and Technology, 45, 10300–10305. https://doi.org/10.1021/es202401p
Rillig, M. C., Ramsey, P. W., Gannon, J. E., Mummey, D. L., Gadkar, V., & Kapulnik, Y. (2008). Suitability of mycorrhiza-defective mutant/wildtype plant pairs (Solanum lycopersicum L. cv Micro-Tom) to address questions in mycorrhizal soil ecology. Plant and Soil, 308, 267–275. https://doi.org/10.1007/s11104-008-9629-x
Sik, Y. K., Kyu, C. J., Gwon, S. J., & Young Cho, J. (2006). Concentration profile of nitrogen and phosphorus in leachate of a paddy plot during the rice cultivation period in southern Korea. Communications in Soil Science and Plant Analysis, 37, 1957–1972. https://doi.org/10.1080/00103620600767306
Springmann, M., Clark, M., Mason-D’Croz, D., Wiebe, K., Bodirsky, B. L., de Lassaletta, L., Vries, W., Vermeulen, S. J., Herrero, M., Carlson, K. M., et al. (2018). Options for keeping the food system within environmental limits. Nature, 562, 519–525. https://doi.org/10.1038/s41586-018-0594-0
Storer, K., Coggan, A., Ineson, P., & Hodge, A. (2017). Arbuscular mycorrhizal fungi reduce nitrous oxide emissions from N2O hotspots. New Phytologist, 220, 1285–1295. https://doi.org/10.1111/nph.14931
van der Heijden, M. G. A. (2010). Mycorrhizal fungi reduce nutrient loss from model grassland ecosystems. Ecology, 91, 1163–1171. https://doi.org/10.1890/09-0336.1
Wang, H., Zhang, D., Zhang, Y., Zhai, L., Yin, B., Zhou, F., Geng, Y., Pan, J., Luo, J., Gu, B., et al. (2018). Ammonia emissions from paddy fields are underestimated in China. Environmental Pollution, 235, 482–488. https://doi.org/10.1016/j.envpol.2017.12.103
Wang, J., Wang, D., Zhang, G., Wang, Y., Wang, C., Teng, Y., & Christie, P. (2014a). Nitrogen and phosphorus leaching losses from intensively managed paddy fields with straw retention. Agricultural Water Management, 141, 66–73. https://doi.org/10.1016/j.agwat.2014.04.008
Wang, Y., Cheng, S., Fang, H., Yu, G., Xu, M., Dang, X., Li, L., & Lei, W. (2014b). Simulated nitrogen deposition reduces CH4 uptake and increases N2O emission from a subtropical plantation forest soil in southern China. Public Library of Science., 9, e93571. https://doi.org/10.1371/journal.pone.0093571
Wang, S., Shan, J., Xia, Y., Tang, Q., Xia, L., Lin, J., & Yan, X. (2017). Different effects of biochar and a nitrification inhibitor application on paddy soil denitrification: A field experiment over two consecutive rice-growing seasons. Science of the Total Environment, 593, 347–356. https://doi.org/10.1016/j.scitotenv.2017.03.159
Whiteside, M. D., Garcia, M. O., & Treseder, K. K. (2012). Amino acid uptake in arbuscular mycorrhizal plants. Public Library of Science, 7(10), e47643. https://doi.org/10.1371/journal.pone.0047643
Wu, Y., Li, T., & Yang, L. (2012). Mechanisms of removing pollutants from aqueous solutions by microorganisms and their aggregates: A review. Bioresource Technology., 107, 10–18. https://doi.org/10.1016/j.biortech.2011.12.088
Wu, Y., Liu, J., Shen, R., & Fu, B. (2017). Mitigation of nonpoint source pollution in rural areas: From control to synergies of multi ecosystem services. Science of the Total Environment, 607–608, 1376–1380. https://doi.org/10.1016/j.scitotenv.2017.07.105
Xu, J., Peng, S., Yang, S., & Wang, W. (2012). Ammonia volatilization losses from a rice paddy with different irrigation and nitrogen managements. Agricultural Water Management, 104, 184–192. https://doi.org/10.1016/j.agwat.2011.12.013
Xue, Z., Li, W., Fang, M., & Dan, S. (2015). Effects of arbuscular mycorrhizal fungi on N2O emissions from rice paddies. Water Air & Soil Pollution, 226, 1–10. https://doi.org/10.1007/s11270-015-2493-4
Yoshinaga, I., Miura, A., Hitomi, T., Hamada, K., & Shiratani, E. (2007). Runoff nitrogen from a large sized paddy field during a crop period. Agricultural Water Management, 87, 217–222. https://doi.org/10.1016/j.agwat.2006.06.020
Zhang, S., Lehmann, A., Zheng, W., You, Z., & Rillig, M. C. (2019). Arbuscular mycorrhizal fungi increase grain yields: A meta-analysis. New Phytologist, 222, 543–555. https://doi.org/10.1111/nph.15570
Zhang, S., Wang, L., Ma, F., Zhang, X., & Fu, D. (2016). Reducing nitrogen runoff from paddy fields with arbuscular mycorrhizal fungi under different fertilizer regimes. Journal of Environment Sciences, 46, 92–100. https://doi.org/10.1016/j.jes.2015.12.024
Zhang, S. G., Yun, X., Xia, W., & Y. You Z,. (2020a). Arbuscular mycorrhiza contributes to the control of phosphorus loss in paddy fields. Plant and Soil, 447, 623–636. https://doi.org/10.1007/s11104-019-04394-2
Zhang, S., You, Z., Guo, X., Yun, W., Xia, Y., & Rillig, M. C. (2020b). Suitability of mycorrhiza-defective rice and its progenitor for studies on the control of nitrogen loss in paddy fields via arbuscular mycorrhiza. Frontiers in Microbiology, 186, 1–14. https://doi.org/10.3389/fmicb.2020.00186
Zhang, X., Dong, W., Sun, J., Feng, F., Deng, Y., He, Z., Giles, E. D. O., & Wang, E. (2015a). The receptor kinase CERK1 has dual functions in symbiosis and immunity signalling. Plant Journal, 81, 258–267. https://doi.org/10.1111/tpj.12723
Zhang, X., Wang, L., Ma, F., & Shan, D. (2015b). Effects of arbuscular mycorrhizal fungi on N2O emissions from rice paddies. Water Air and Soil Pollution, 226, 1–10. https://doi.org/10.1007/s11270-015-2493-4
Zhao, X., Xie, Y., Xiong, Z., Yan, X., Xing, G., & Zhu, Z. (2009). Nitrogen fate and environmental consequence in paddy soil under rice-wheat rotation in the Taihu lake region, China. Plant and Soil, 319, 225–234. https://doi.org/10.1007/s11104-008-9865-0
Acknowledgements
We thank Miao He for helping with data collection, Haiyang Xu for designing the microcosm, Ertao Wang for providing the plant and AM fungal isolate, and Xiaowei Wang for the inoculum production.
Funding
This work was supported by the Natural Science Foundation of Jiangsu Province (grant no. BK20160689) and the Postgraduate Research & Practice Innovation Program of Jiangsu Province (JSCX19_0351).
Author information
Authors and Affiliations
Contributions
SZ, analyzed the data, wrote the first manuscript, and modified it; WY, YX, and SW, performed the experiments, collected the samples, and collected the data; YZ and MR, designed the experiment, revised the manuscript, and modified the language. All the authors discussed the results and commented on the manuscript.
Corresponding author
Ethics declarations
Conflict of Interest
The authors declare no competing interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Zhang, S., Yun, W., Xia, Y. et al. Arbuscular Mycorrhiza Reduced Nitrogen Loss via Runoff, Leaching, and Emission of N2O and NH3 from Microcosms of Paddy Fields. Water Air Soil Pollut 233, 11 (2022). https://doi.org/10.1007/s11270-021-05429-0
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11270-021-05429-0