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Nitrogen fertilization altered arbuscular mycorrhizal fungi abundance and soil erosion of paddy fields in the Taihu Lake region of China

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Abstract

Arbuscular mycorrhizal (AM) fungi were of importance in mitigating soil erosion, which was highly influenced by biotic and abiotic factors, such as host plant growth and soil nutrient. To investigate the impact of nitrogen (N) fertilization on seasonal variance in AM colonization and soil erosion, we conducted a field experiment with rice cultivation under four N fertilizer levels (0 kg N ha−1, 270 kg N ha−1, 300 kg N ha−1, and 375 kg N ha−1 plus organic fertilizers) in the Taihu Lake region, China. We investigated AM colonization before rice transplantation, during rice growth, and after rice harvest. We also assessed soil splash erosion of intact soil cores sampled at tillering and after rice harvest. We found that AM colonization (indicated by percentage of root length colonization) varied from 15 to 73%, which was attributed to rice growth, N fertilization, and their interaction. Soil loss due to splash erosion was cut down by organic N fertilizer at tillering, while higher inorganic N fertilization significantly increased soil loss after rice harvest. Additionally, we found significantly negative relationships of AM colonization to soil loss but positive relationships to soil aggregate stability. We highlighted the potential role of AM fungi in decreasing soil erosion and suggested that high N fertilization should be considered carefully when seeking after high yields.

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References

  • Asghari HR, Cavagnaro TR (2012) Arbuscular mycorrhizas reduce nitrogen loss via leaching. PLoS One 7:151-155. https://doi.org/10.1371/journal.pone.0029825

    Article  CAS  Google Scholar 

  • Auge RM (2001) Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza 11:3-42. https://doi.org/10.1007/s005720100097

    Article  Google Scholar 

  • Bakhshandeh S, Corneo PE, Mariotte P, Kertesz MA, Dijkstra FA (2017) Effect of crop rotation on mycorrhizal colonization and wheat yield under different fertilizer treatments. Agric Ecosyst Environ 247:130-136. https://doi.org/10.1016/j.agee.2017.06.027

    Article  Google Scholar 

  • Barthès B, Roose E (2002) Aggregate stability as an indicator of soil susceptibility to runoff and erosion; validation at several levels. Catena 47:133-149

    Article  Google Scholar 

  • Bender SF, Conen F, Van der Heijden MGA (2015) Mycorrhizal effects on nutrient cycling, nutrient leaching and N2O production in experimental grassland. Soil Biol Biochem 80:283-292. https://doi.org/10.1016/j.soilbio.2014.10.016

    Article  CAS  Google Scholar 

  • Borrelli P, Van KO, Meusburger K, Alewell C, Lugato E, Panagos P (2018) A step towards a holistic assessment of soil degradation in Europe: Coupling on-site erosion with sediment transfer and carbon fluxes. Environ Res 168:291-298

    Article  Google Scholar 

  • Bowles TM, Jackson LE, Cavagnaro TR (2017) Mycorrhizal fungi enhance plant nutrient acquisition and modulate nitrogen loss with variable water regimes. Glob Chang Biol 24:e171-e182. https://doi.org/10.1111/gcb.13884

    Article  Google Scholar 

  • Brundrett M, Melville L, Peterson L. (1994) Practical methods in mycorrhiza research. University of Guelph, ON, Canada: Mycologue Publication

  • Bruns TD, Corradi N, Redecker D, Taylor JW, Öpik M (2017) Glomeromycotina: what is a species and why should we care? New Phytol 220:1-5. https://doi.org/10.1111/nph.14913

    Article  Google Scholar 

  • Cabral C, Ravnskov S, Tringovska I, Wollenweber B (2016) Arbuscular mycorrhizal fungi modify nutrient allocation and composition in wheat (Triticum aestivum L.) subjected to heat-stress. Plant Soil 408:385-399. https://doi.org/10.1007/s11104-016-2942-x

    Article  CAS  Google Scholar 

  • Camenzind T et al (2016) Opposing effects of nitrogen versus phosphorus additions on mycorrhizal fungal abundance along an elevational gradient in tropical montane forests. Soil Biol Biochem 94:37-47. https://doi.org/10.1016/j.soilbio.2015.11.011

    Article  CAS  Google Scholar 

  • Cavagnaro TR, Bender SF, Asghari HR, van der Heijden MGA (2015) The role of arbuscular mycorrhizas in reducing soil nutrient loss. Trends Plant Sci 20:283-290. https://doi.org/10.1016/j.tplants.2015.03.004

    Article  CAS  Google Scholar 

  • Cui XC, Hu JL, Lin XG, Wang FY, Chen RR, Wang JH, Zhu JG (2018) Arbuscular mycorrhizal fungi alleviate ozone stress on nitrogen nutrition of field wheat. J Agric Sci Technol 15:1043-1052

    Google Scholar 

  • De La Peña E, Echeverría SR, Van Der Putten WH, Freitas H, Moens M (2006) Mechanism of control of root-feeding nematodes by mycorrhizal fungi in the dune grass Ammophila arenaria. New Phytol 169:829-840

    Article  Google Scholar 

  • Delavaux CS, Smithramesh LM, Kuebbing SE (2017) Beyond nutrients: A meta-analysis of the diverse effects of arbuscular mycorrhizal fungi on plants and soils. Ecology 98:2111-2119

    Article  Google Scholar 

  • Driver JD, Holben WE, Rillig MC (2005) Characterization of glomalin as a hyphal wall component of arbuscular mycorrhizal fungi. Soil Biol Biochem 37:101-106

    Article  CAS  Google Scholar 

  • Falsone G, Bonifacio E, Zanini E (2012) Structure development in aggregates of poorly developed soils through the analysis of the pore system. Catena 95:169-176

    Article  CAS  Google Scholar 

  • Fang H, Li W, Wei S, Jiang C (2014) Seasonal variation of leaf area index (LAI) over paddy rice fields in NE China: Intercomparison of destructive sampling, LAI-2200, digital hemispherical photography (DHP), and AccuPAR methods. Agric For Meteorol 198-199:126-141

    Article  Google Scholar 

  • Gholami L, Sadeghi SHR, Homaee M (2016) Different effects of sheep manure conditioner on runoff and soil loss components in eroded soil. Catena 139:99-104. https://doi.org/10.1016/j.catena.2015.12.011

    Article  CAS  Google Scholar 

  • Giovannetti M, Mosse B (1980) An evaluation of techniques for measuring vesicular-arbuscular infection in roots. New Phytol 84:489-500

    Article  Google Scholar 

  • Hawkes CV, Hartley IP, Ineson P, Fitter AH (2008) Soil temperature affects carbon allocation within arbuscular mycorrhizal networks and carbon transport from plant to fungus. Glob Chang Biol 14:1181-1190. https://doi.org/10.1111/j.1365-2486.2007.01535.x

    Article  Google Scholar 

  • Hodge A, Helgason T, Fitter A (2010) Nutritional ecology of arbuscular mycorrhizal fungi. Fungal Ecol 3:267-273

    Article  Google Scholar 

  • Jakobsen I, Abbott L, Robson A (1992) External hyphae of vesicular—arbuscular mycorrhizal fungi associated with Trifolium subterraneum L. New Phytol 120:509-516

    Article  CAS  Google Scholar 

  • Jiang Y et al (2017) Plants transfer lipids to sustain colonization by mutualistic mycorrhizal and parasitic fungi. Science 356:1172

    Article  CAS  Google Scholar 

  • Johnson NC (2010) Resource stoichiometry elucidates the structure and function of arbuscular mycorrhizas across scales. New Phytol 185:631-647. https://doi.org/10.1111/j.1469-8137.2009.03110.x

    Article  CAS  Google Scholar 

  • Johnson D, Leake JR, Ostle N, Ineson P, Read DJ (2002) In situ (CO2)-C-13 pulse-labelling of upland grassland demonstrates a rapid pathway of carbon flux from arbuscular mycorrhizal mycelia to the soil. New Phytol 153:327-334. https://doi.org/10.1046/j.0028-646X.2001.00316.x

    Article  CAS  Google Scholar 

  • Johnson NC, Wilson GW, Wilson JA, Miller RM, Bowker MA (2015) Mycorrhizal phenotypes and the Law of the Minimum. New Phytol 205:1473-1484

    Article  CAS  Google Scholar 

  • Kervroëdan L, Armand R, Saunier M, Ouvry JF, Faucon MP (2018) Plant functional trait effects on runoff to design herbaceous hedges for soil erosion control. Ecol Eng 118:143-151

    Article  Google Scholar 

  • Kleczewski NM, Herms DA, Bonello P (2011) Nutrient and water availability alter belowground patterns of biomass allocation, carbon partitioning, and ectomycorrhizal abundance in Betula nigra. Trees 26:525-533. https://doi.org/10.1007/s00468-011-0613-3

    Article  Google Scholar 

  • Lehmann A, Rillig MC (2015) Arbuscular mycorrhizal contribution to copper, manganese and iron nutrient concentrations in crops - a meta-analysis. Soil Biol Biochem 81:147-158. https://doi.org/10.1016/j.soilbio.2014.11.013

    Article  CAS  Google Scholar 

  • Lehmann A, Zheng W, Rillig MC (2017) Soil biota contributions to soil aggregation. Nat Ecol Evol 1:1828-1835

    Article  Google Scholar 

  • Leifheit E, Verbruggen E, Rillig M (2015) Arbuscular mycorrhizal fungi reduce decomposition of woody plant litter while increasing soil aggregation. Soil Biol Biochem 81:323-328

    Article  CAS  Google Scholar 

  • Li H, Ye ZH, Chan WF, Chen XW, Wu FY, Wu SC, Wong MH (2011) Can arbuscular mycorrhizal fungi improve grain yield, as uptake and tolerance of rice grown under aerobic conditions? Environ Pollut 159:2537-2545. https://doi.org/10.1016/j.envpol.2011.06.017

    Article  CAS  Google Scholar 

  • Liu Y et al (2012) Direct and indirect influences of 8 yr of nitrogen and phosphorus fertilization on Glomeromycota in an alpine meadow ecosystem. New Phytol 194:523-535. https://doi.org/10.1111/j.1469-8137.2012.04050.x

    Article  CAS  Google Scholar 

  • Louarn J, Carbonne F, Delavault P, Becard G, Rochange S (2012) Reduced germination of Orobanche cumana seeds in the presence of arbuscular mycorrhizal Fungi or their exudates. PLoS One 7:e49273. https://doi.org/10.1371/journal.pone.0049273

    Article  CAS  Google Scholar 

  • Lumini E, Vallino M, Alguacil MM, Romani M, Bianciotto V (2011) Different farming and water regimes in Italian rice fields affect arbuscular mycorrhizal fungal soil communities. Ecol Appl 21:1696-1707

    Article  Google Scholar 

  • Mardhiah U, Caruso T, Gurnell A, Rillig MC (2016) Arbuscular mycorrhizal fungal hyphae reduce soil erosion by surface water flow in a greenhouse experiment. Appl Soil Ecol 99:137-140

    Article  Google Scholar 

  • Miller SP (2000) Arbuscular mycorrhizal colonization of semi-aquatic grasses along a wide hydrologic gradient. New Phytol 145:145-155. https://doi.org/10.1046/j.1469-8137.2000.00566.x

    Article  Google Scholar 

  • Nuccio EE, Hodge A, Pett-Ridge J, Herman DJ, Weber PK, Firestone MK (2013) An arbuscular mycorrhizal fungus significantly modifies the soil bacterial community and nitrogen cycling during litter decomposition. Environ Microbiol 15:1870-1881. https://doi.org/10.1111/1462-2920.12081

    Article  CAS  Google Scholar 

  • Olson KR, Nizeyimana E (1988) Effects of soil erosion on corn yields of seven Illinois soils. J Prod Agric 1:13-19

    Article  Google Scholar 

  • Prosser IP, Dietrich WE, Stevenson J (1995) Flow resistance and sediment transport by concentrated overland flow in a grassland valley. Geomorphology 13:71-86

    Article  Google Scholar 

  • RCoreTeam (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Rillig MC, Field CB, Allen MF (1999) Soil biota responses to long-term atmospheric CO2? Enrichment in two california annual grasslands. Oecologia 119:572-577

    Article  Google Scholar 

  • Rillig MC, Aguilar-Rigueros CA, Camenzind T, Cavagnaro TR, Yang G (2019) Why farmers should manage the arbuscular mycorrhizal symbiosis. New Phytol. https://doi.org/10.1111/nph.15602

  • Sasaki H, Hara T, Ito S, Miura S, Hoque MM, Lieffering M, Kim HY, Okada M, Kobayashi K (2005) Seasonal changes in canopy photosynthesis and respiration, and partitioning of Photosynthate, in Rice (Oryza sativa L.) grown under free-air CO2 enrichment. Plant Cell Physiol 46:1704-1712

    Article  CAS  Google Scholar 

  • Sisaphaithong T et al (2017) Varietal differences in the growth responses of rice to an arbuscular mycorrhizal fungus under natural upland conditions. Plant Signal Behav 12:e1274483. https://doi.org/10.1080/15592324.2016.1274483

    Article  CAS  Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal Symbiosis San Diego. Press, Academic

    Google Scholar 

  • Solaiman MZ, Hirata H (1997) Responses of directly seeded wetland rice to arbuscular mycorrhizal fungi inoculation. J Plant Nutr 20:1479-1487. https://doi.org/10.1080/01904169709365350

    Article  CAS  Google Scholar 

  • Solaiman MZ, Hirata H (1998) Glomus-wetland rice mycorrhizas influenced by nursery inoculation techniques under high fertility soil conditions. Biol Fertil Soils 27:92-96

    Article  Google Scholar 

  • Staddon PL, Ramsey CB, Ostle N, Ineson P, Fitter AH (2003) Rapid turnover of hyphae of mycorrhizal fungi determined by AMS microanalysis of C-14. Science 300:1138-1140. https://doi.org/10.1126/science.1084269

    Article  CAS  Google Scholar 

  • Storer K, Coggan A, Ineson P, Hodge A (2017) Arbuscular mycorrhizal fungi reduce nitrous oxide emissions from N2O hotspots. New Phytol 1-11. https://doi.org/10.1111/nph.14931

  • Thirkell TJ, Charters MD, Elliott AJ, Sait SM, Field KJ (2017) Are mycorrhizal fungi our sustainable saviours? Considerations for achieving food security. J Ecol 105:921-929

    Article  CAS  Google Scholar 

  • Treseder KK (2004) A meta-analysis of mycorrhizal responses to nitrogen, phosphorus, and atmospheric CO2 in field studies. New Phytol 164:347-355. https://doi.org/10.1111/j.1469-8137.2004.01159.x

    Article  Google Scholar 

  • Unger IM, Motavalli PP, Muzika RM (2009) Changes in soil chemical properties with flooding: A field laboratory approach. Agric Ecosyst Environ 131:105-110. https://doi.org/10.1016/j.agee.2008.09.013

    Article  CAS  Google Scholar 

  • van der Heijden MGA (2010) Mycorrhizal fungi reduce nutrient loss from model grassland ecosystems. Ecology 91:1163-1171

    Article  Google Scholar 

  • Vermang J, Demeyer V, Cornelis WM, Gabriels D (2009) Aggregate stability and erosion response to antecedent water content of a loess soil. Soil Sci Soc Am J 73:718-726

    Article  CAS  Google Scholar 

  • 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. Sci Total Environ 593-594:347-356

    Article  CAS  Google Scholar 

  • Wilson GWT, Rice CW, Rillig MC, Springer A, Hartnett DC (2009) Soil aggregation and carbon sequestration are tightly correlated with the abundance of arbuscular mycorrhizal fungi: results from long-term field experiments. Ecol Lett 12:452-461. https://doi.org/10.1111/j.1461-0248.2009.01303.x

    Article  Google Scholar 

  • Wright S, Upadhyaya A (1998) A survey of soils for aggregate stability and glomalin, a glycoprotein produced by hyphae of arbuscular mycorrhizal fungi. Plant Soil 198:97-107

    Article  CAS  Google Scholar 

  • Wu QS, Cao MQ, Zou YN, He XH (2014a) Direct and indirect effects of glomalin, mycorrhizal hyphae, and roots on aggregate stabiliLEty in rhizosphere of trifoliate orange. Sci Rep 4:5823. https://doi.org/10.1038/srep05823

    Article  CAS  Google Scholar 

  • Wu QS, Huang YM, Li Y, Nasrullah HXH (2014b) Contribution of arbuscular mycorrhizas to Glomalin-related soil protein, Soil Organic Carbon and Aggregate Stability in Citrus Rhizosphere. Int J Agric Biol 16:207-212

    CAS  Google Scholar 

  • Wuddivira MN, Stone RJ, Ekwue EI (2009) Clay, organic matter, and wetting effects on splash detachment and aggregate breakdown under intense rainfall. Soil Sci Soc Am J 73:226-232

    Article  CAS  Google Scholar 

  • Xie Y, Yue T (2018) Application of soil erosion models for soil and water conservation. Sci Soil Water Conserv 16:25-37

    Google Scholar 

  • Xu P, Liang LZ, Dong XY, Shen RF (2015) Effect of arbuscular mycorrhizal fungi on aggregate stability of a clay soil inoculating with two different host plants. Acta Agric Scand B Soil Plant 65:23-29. https://doi.org/10.1080/09064710.2014.960887

    Article  CAS  Google Scholar 

  • Yang HS, Dai YJ, Wang XH, Zhang Q, Zhu LQ, Bian XM (2014) Meta-analysis of interactions between arbuscular mycorrhizal Fungi and biotic stressors of plants. Sci World J 746506. https://doi.org/10.1155/2014/746506

  • Zhang S, Wang L, Ma F, Bloomfield KJ, Yang J, Atkin OK (2014) Is resource allocation and grain yield of rice altered by inoculation with arbuscular mycorrhizal fungi? J Plant Ecol 8:436-448

    Article  Google Scholar 

  • Zhang S, Wang L, Ma F, Zhang X, Li Z, Li S, Jiang X (2015a) Can arbuscular mycorrhiza and fertilizer management reduce phosphorus runoff from paddy fields? J Environ Sci 33:211-218

    Article  CAS  Google Scholar 

  • Zhang X, Wang L, Ma F, Shan D (2015b) Effects of Arbuscular Mycorrhizal Fungi on N2O Emissions from Rice Paddies. Water Air Soil Pollut 226:1-10. https://doi.org/10.1007/s11270-015-2493-4

    Article  CAS  Google Scholar 

  • Zhang BB, Chang SX, Anyia AO (2016a) Mycorrhizal inoculation and nitrogen fertilization affect the physiology and growth of spring wheat under two contrasting water regimes. Plant Soil 398:47-57. https://doi.org/10.1007/s11104-015-2635-x

    Article  CAS  Google Scholar 

  • Zhang S, Wang L, Ma F, Zhang X, Fu D (2016b) Reducing nitrogen runoff from paddy fields with arbuscular mycorrhizal fungi under different fertilizer regimes. J Environ Sci 46:92-100

    Article  Google Scholar 

  • Zhang X, Wang L, Ma F, Yang JX, Su M (2017) Effects of arbuscular mycorrhizal fungi inoculation on carbon and nitrogen distribution and grain yield and nutritional quality in rice (Oryza sativa L). J Sci Food Agric 97:2919-2925. https://doi.org/10.1002/jsfa.8129

    Article  CAS  Google Scholar 

  • Zhang S, Lehmann A, Zheng W, You Z, Rillig MC (2019) Arbuscular mycorrhizal fungi increase grain yields: a meta-analysis. New Phytol 222. https://doi.org/10.1111/nph.15570

  • Zhao X, Xie YX, Xiong ZQ, Yan XY, Xing GX, Zhu ZL (2009) Nitrogen fate and environmental consequence in paddy soil under rice-wheat rotation in the Taihu lake region, China. Plant Soil 319:225-234. https://doi.org/10.1007/s11104-008-9865-0

    Article  CAS  Google Scholar 

  • Zhao X, Zhou Y, Min J, Wang SQ, Shi WM, Xing GX (2012) Nitrogen runoff dominates water nitrogen pollution from rice-wheat rotation in the Taihu Lake region of China. Agric Ecosyst Environ 156:1-11. https://doi.org/10.1016/j.agee.2012.04.024

    Article  CAS  Google Scholar 

  • Zhao M et al (2015) Mitigating gaseous nitrogen emissions intensity from a Chinese rice cropping system through an improved management practice aimed to close the yield gap. Agric Ecosyst Environ 203:36-45. https://doi.org/10.1016/j.agee.2015.01.014

    Article  CAS  Google Scholar 

  • Zhu Z et al (2016) Fate of rice shoot and root residues, rhizodeposits, and microbe-assimilated carbon in paddy soil: I. Decomposition and priming effect. Biogeosci Discuss 13:4481-4489

    Article  CAS  Google Scholar 

  • Zhu Y et al (2017) Inoculation of arbuscular mycorrhizal fungi with plastic mulching in rainfed wheat: a promising farming strategy Field. Crop Res 204:229-241. https://doi.org/10.1016/jScr.2016.11.005

    Article  Google Scholar 

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Acknowledgments

We would like to thank Wenfei Yun for help with data collection.

Funding

This work was supported by Natural Science Foundation of Jiangsu Province (grant numbers BK20160689) and National Key Technologies R&D Program of China (2015BAL02B05).

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Zhang, S., Yu, J., Wang, S. et al. Nitrogen fertilization altered arbuscular mycorrhizal fungi abundance and soil erosion of paddy fields in the Taihu Lake region of China. Environ Sci Pollut Res 26, 27987–27998 (2019). https://doi.org/10.1007/s11356-019-06005-0

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