Abstract
Aims
Mycorrhizae and root exudates have been considered the two important pathways for nitrogen (N) transfer from legume to non-legume plants. The present study aimed to investigate contribution of the relative importance of arbuscular mycorrhizal fungi and root exudates in short-term N transfer.
Methods
A field experiment was conducted to explore N transfer from alfalfa to maize under two different N application levels using 15N leaf labeling.
Results
N transfer amount ranged from 7 to 10 mg N plant−1 from alfalfa to maize and significantly decreased (by 11%–22%) with N fertilizer application. Intercropping of 4 rows of maize and 6 rows of alfalfa with 30 cm intra-row spacing (IMA43) was the optimal intercropping mode, which increased N transfer, total N uptake and yield by 18%, 15% and 11%, respectively. The relative importance of arbuscular mycorrhizal fungi and root exudates on N transfer was dependent on soil N availability. Under no N addition, hyphal length density (HLD) of rhizosphere soil explained the largest significant amount (50%) of the variability in N transfer and crop yield. However, root exudates explained 77% of the variability in N transfer and crop yields with N fertilizer application.
Conclusions
Our findings highlighted that N transfer is reliant more on arbuscular mycorrhizal fungi than root exudates in N-deficient soil, whereas root exudates play a more important role in N-fertilized soil.
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References
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
Baziramakenga R, Simard RR, Leroux GD (1995) Determination of organic acids in soil extracts by ion chromatography. Soil Biol Biochem 27:349–356. https://doi.org/10.1016/0038-0717(94)00178-4
Chapagain T, Riseman A (2014) Barley–pea intercropping: Effects on land productivity, carbon and nitrogen transformations. Field Crop Res 166:18–25. https://doi.org/10.1016/j.fcr.2014.06.014
Chu GX, Shen QR, Cao JL (2004) Nitrogen fixation and N transfer from peanut to rice cultivated in aerobic soil in an intercropping system and its effect on soil N fertility. Plant Soil 263:17–27. https://doi.org/10.1023/B:PLSO.0000047722.49160.9e
Clifford PE, Marshall C, Sagar GR (1973) An examination of the value of 14CO2 urea as a source of 14CO2 for studies of assimilate distribution. Ann Bot 37:37–44. https://doi.org/10.1093/oxfordjournals.aob.a084679
Duchicela J, Sullivan TS, Bontti E, Bever JD (2013) Soil aggregate stability increase is strongly related to fungal community succession along an abandoned agriculture field chronosequence in the Bolivian Altiplano. J Appl Ecol 50:1266–1273. https://doi.org/10.1111/1365-2664.12130
Fan FL, Zhang FS, Song YN, Sun J, Bao XG, Guo TW, Li L (2006) Nitrogen fixation of faba bean (Vicia faba L.) interacting with a non-legume in two contrasting intercropping systems. Plant Soil 283:275–286. https://doi.org/10.1007/s11104-006-0019-y
Farnham DE, George JR (1993) Dinitrogen fixation and nitrogen transfer among red clover cultivars. Can J Plant Sci 73:1047–1054. https://doi.org/10.4141/cjps93-136
Fustec J, Lesuffleur F, Mahieu S, Cliquet JB (2010) Nitrogen rhizodeposition of legumes. A review. Agron Sustain Dev 30:57–66. https://doi.org/10.1051/agro/2009003
Gao Y, Wu PT, Zhao XN, Wang ZK (2014) Growth, yield, and nitrogen use in the wheat/maize intercropping system in an arid region of northwestern China. Field Crop Res 167:19–30. https://doi.org/10.1016/j.fcr.2014.07.003
Geng, ZC, Dai W (editors) (2011) Soil science. Part 3: Soil texture and structure. Science Press, Beijing, pp 80–84
Grassini P, Eskridge KM, Cassman KG (2013) Distinguishing between yield advances and yield plateaus in historical crop production trends. Nat Commun 4:2918. https://doi.org/10.1038/ncomms3918
Gylfadóttir T, Helgadóttir Á, Høgh-Jensen H (2007) Consequences of including adapted white clover in northern European grassland: transfer and deposition of nitrogen. Plant Soil 297:93–104. https://doi.org/10.1007/s11104-007-9323-4
Hauggaard-Nielsen H, Gooding M, Ambus P, Corre-Hellou G, Crozat Y, Dahlmann C, Dibet A, von Fragstein P, Pristeri A, Monti M (2009) Pea–barley intercropping and short-term subsequent crop effects across European organic cropping conditions. Nutr Cycl Agroecosyst 85:141–155. https://doi.org/10.1007/s10705-009-9254-y
He XH, Critchley C, Bledsoe C (2003) Nitrogen transfer within and between plants through common mycorrhizal networks (CMNs). Crit Rev Plant Sci 22:531–567. https://doi.org/10.1080/713608315
Hobbie JE, Hobbie EA (2006) 15N in symbiotic fungi and plants estimates nitrogen and carbon flux rates in Arctic tundra. Ecology 87:816–822. https://doi.org/10.1890/0012-9658(2006)87[816:NISFAP]2.0.CO;2
Høgh-Jensen H (2006) The nitrogen transfer between plants: an important but difficult flux to quantify. Plant Soil 282:1–5. https://doi.org/10.1007/s11104-005-2613-9
Jakobsen I, Abbott LK, Robson AD (2010) External hyphae of vesicular-arbuscular mycorrhizal fungi associated with Trifolium subterraneum L. New Phytol 120:371–380. https://doi.org/10.1111/j.1469-8137.1992.tb01077.x
Jalonen R, Nygren P, Sierra J (2009) Transfer of nitrogen from a tropical legume tree to an associated fodder grass via root exudation and common mycelial networks. Plant Cell Environ 32:1366–1376. https://doi.org/10.1111/j.1365-3040.2009.02004.x
Jensen ES (1996) Barley uptake of N deposited in the rhizosphere of associated field pea. Soil Biol Biochem 28:159–168. https://doi.org/10.1016/0038-0717(95)00134-4
Johansen A, Jensen ES (1996) Transfer of N and P from intact or decomposing roots of pea to barley interconnected by an arbuscular mycorrhizal fungus. Soil Biol Biochem 28:73–81. https://doi.org/10.1016/0038-0717(95)00117-4
Khan DF, Peoples MB, Chalk PM, Herridge DF (2002) Quantifying below-ground nitrogen of legumes 2. A comparison of 15N and non-isotopic methods. Plant Soil 239:277–289. https://doi.org/10.1023/A:1015066323050
Kou L, Guo DL, Yang H, Gao WL, Li SG (2015) Growth, morphological traits and mycorrhizal colonization of fine roots respond differently to nitrogen addition in a slash pine plantation in subtropical China. Plant Soil 391:207–218. https://doi.org/10.1007/s11104-015-2420-x
Lambers H, Shane MW, Cramer MD, Pearse SJ, Veneklaas EJ (2006) Root structure and functioning for efficient acquisition of phosphorus: Matching morphological and physiological traits. Ann Bot 98:693–713. https://doi.org/10.1093/aob/mcl114
Latati M, Blavet D, Alkama N, Laoufi H, Drevon JJ, Gérard F, Pansu M, Ounane SM (2014) The intercropping cowpea-maize improves soil phosphorus availability and maize yields in an alkaline soil. Plant Soil 385:181–191. https://doi.org/10.1007/s11104-014-2214-6
Ledgard SF, Freney JR, Simpson JR (1985) Assessing nitrogen transfer from legumes to associated grasses. Soil Biol Biochem 17:575–577. https://doi.org/10.1016/0038-0717(85)90028-8
Li L, Li SM, Sun JH, Zhou LL, Bao XG, Zhang HG, Zhang FS (2007) Diversity enhances agricultural productivity via rhizosphere phosphorus facilitation on phosphorus-deficient soils. Proc Natl Acad Sci 104:11192–11196. https://doi.org/10.1073/pnas.0704591104
Li YY, Yu CB, Cheng XY, Li CJ, Sun JH, Zhang FS, Lambers H, Li L (2009) Intercropping alleviates the inhibitory effect of N fertilization on nodulation and symbiotic N2 fixation of faba bean. Plant Soil 323:295–308. https://doi.org/10.1007/s11104-009-9938-8
Marty C, Pornon A, Escaravage N, Winterton P, Lamaze T (2009) Complex interactions between a legume and two grasses in a subalpine meadow. Am J Bot 96:1814–1820. https://doi.org/10.3732/ajb.0800405
Meng LB, Zhang AY, Wang F, Han XG, Wang DJ, Li SM (2015) Arbuscular mycorrhizal fungi and rhizobium facilitate nitrogen uptake and transfer in soybean/maize intercropping system. Front Plant Sci 6:339. https://doi.org/10.3389/fpls.2015.00339
Montesinos-Navarro A, Verdú M, Querejeta JI, Sortibrán L, Valiente-Banuet A (2016) Soil fungi promote nitrogen transfer among plants involved in long-lasting facilitative interactions. Perspect Plant Ecol Evol Syst 18:45–51. https://doi.org/10.1016/j.ppees.2016.01.004
Page AL (1982) Methods of soil analysis. Part 2. Chemical and microbiological properties. American Society of Agronomy; Soil Science Society of America, Madison, WI, USA
Palta JA, Fillery IR, Mathews EL, Turner NC (1991) Leaf feeding of 15N urea for labelling wheat with nitrogen. Aust J Plant Physio 18:627–636. https://doi.org/10.1071/PP9910627
Paula RR, Bouillet JP, Ocheuze Trivelin PC, Zeller B, Leonardo de Moraes Gonçalves J, Nouvellon Y, Bouvet JM, Plassard C, Laclau JP (2015) Evidence of short-term belowground transfer of nitrogen from Acacia mangium to Eucalyptus grandis trees in a tropical planted forest. Soil Biol Biochem 91:99–108. https://doi.org/10.1016/j.soilbio.2015.08.017
Phillips JM, Hayman DS (1970) Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Br Mycol Soc 55:158–161. https://doi.org/10.1016/S0007-1536(70)80110-3
Pirhofer-Walzl K, Rasmussen J, Høgh-Jensen H, Eriksen J, Søegaard K, Rasmussen J (2012) Nitrogen transfer from forage legumes to nine neighbouring plants in a multi-species grassland. Plant Soil 350:71–84. https://doi.org/10.1007/s11104-011-0882-z
Qiao X, Bei SK, Li CJ, Dong Y, Li HG, Christie P, Zhang FS, Zhang JL (2015) Enhancement of faba bean competitive ability by arbuscular mycorrhizal fungi is highly correlated with dynamic nutrient acquisition by competing wheat. Sci Rep 5: 8122. http://www.nature.com/doifinder/10.1038/srep08122
Rao AV, Giller KE (1993) Nitrogen fixation and its transfer from Leucaena to grass using 15N. For Ecol Manag 61:221–227. https://doi.org/10.1016/0378-1127(93)90203-y
Rasmussen J, Gylfadóttir T, Loges R, Eriksen J, Helgadóttir Á (2013) Spatial and temporal variation in N transfer in grass–white clover mixtures at three Northern European field sites. Soil Biol Biochem 57:654–662. https://doi.org/10.1016/j.soilbio.2012.07.004
Rochester IJ, Peoples MB, Constable GA, Gault RR (1998) Faba beans and other legumes add nitrogen to irrigated cotton cropping systems. Aust J Exp Agric 38:253–260. https://doi.org/10.1071/EA97132
Russelle MP, Allan DL, Gourley CJP (1994) Direct assessment of symbiotically fixed nitrogen in the rhizosphere of alfalfa. Plant Soil 159:233–243. https://doi.org/10.1007/bf00009286
Spohn M, Ermak A, Kuzyakov Y (2013) Microbial gross organic phosphorus mineralization can be stimulated by root exudates-A 33P isotopic dilution study. Soil Biol Biochem 65:254–263. https://doi.org/10.1016/j.soilbio.2013.05.028
Sun BR, Gao YZ, Yang HJ, Zhang HL, Wang XY, Li ZJ (2019) Performance of alfalfa rather than maize stimulates system phosphorus uptake and overyielding of maize/alfalfa intercropping via changes in soil water balance and root morphology and distribution in a light chernozemic soil. Plant Soil 439:145–161. https://doi.org/10.1007/s11104-018-3888-y
Sun BR, Peng Y, Yang HY, Li ZJ, Gao YZ, Wang C, Yan YL, Liu YM (2014) Alfalfa (Medicago sativa L.)/maize (Zea mays L.) intercropping provides a feasible way to improve yield and economic incomes in farming and pastoral areas of northeast China. PLoS One 9:e110556. https://doi.org/10.1371/journal.pone.0110556
Thilakarathna RMMS, McElroy MS, Chapagain T, Papadopoulos YA, Raizada MN (2016) Belowground nitrogen transfer from legumes to non-legumes under managed herbaceous cropping systems. A review Agron Sustain Dev 36:58. https://doi.org/10.1007/s13593-016-0396-4
Veneklaas EJ, Stevens J, Cawthray GR, Turner S, Grigg AM, Lambers H (2003) Chickpea and white lupin rhizosphere carboxylates vary with soil properties and enhance phosphorus uptake. Plant Soil 248:187–197. https://doi.org/10.1023/A:1022367312851
Wahbi S, Maghraoui T, Hafidi M, Sanguin H, Oufdou K, Prin Y, Duponnois R, Galiana A (2016) Enhanced transfer of biologically fixed N from faba bean to intercropped wheat through mycorrhizal symbiosis. Appl Soil Ecol 107:91–98. https://doi.org/10.1016/j.apsoil.2016.05.008
Walker TS, Bais HP, Grotewold E, Vivanco JM (2003) Root exudation and rhizosphere biology. Plant Physiol 132:44–51. https://doi.org/10.1104/pp.102.019661
Wang XY, Gao YZ, Zhang HL, Shao ZQ, Sun BR, Gao Q (2019) Enhancement of rhizosphere citric acid and decrease of NO3−/NH4+ ratio by root interactions facilitate N fixation and transfer. Plant Soil. https://doi.org/10.1007/s11104-018-03918-6
Willey RW, Rao MR (1980) A competitive ratio for quantifying competition between intercrops. Exp Agric 16:117–125. https://doi.org/10.1017/S0014479700010802
Zhang GG, Yang ZB, Dong ST (2011) Interspecific competitiveness affects the total biomass yield in an alfalfa and corn intercropping system. Field Crop Res 124:66–73. https://doi.org/10.1016/j.fcr.2011.06.006
Zhang GG, Zhang CY, Yang ZB, Dong ST (2013) Root distribution and N acquisition in an alfalfa and corn intercropping system. J Agric Sci 5:128–142. https://doi.org/10.5539/jas.v5n9p128
Acknowledgments
We are grateful to Professor Zed Rengel for invaluable advice and English improvement on the manuscript. This work was financially supported by the National Natural Science Foundation of China (31670446, 31471945, 31870436, U1803110), Human Resources and Social Security Department of Jilin Province (2016-28), Key Science and Technology Development Program of Jilin Province (20180201073NY), the National Key Basic Research Program of China (2016YFC0500703), and Ministry of Ecological Environment Biodiversity Observation and Assessment Project (8-2-5-11-2).
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Zhang, H., Wang, X., Gao, Y. et al. Short-term N transfer from alfalfa to maize is dependent more on arbuscular mycorrhizal fungi than root exudates in N deficient soil. Plant Soil 446, 23–41 (2020). https://doi.org/10.1007/s11104-019-04333-1
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DOI: https://doi.org/10.1007/s11104-019-04333-1