Abstract
Aims
Cereal can stimulate legume N fixation through competition for soil mineral N. In addition, organic acids in the rhizosphere can mobilize external nutrients, which may help nodulation. However, how much NO3− and NH4+ competition and organic acids in the rhizosphere of intercropped crops contribute to N fixation remains unclear and requires study.
Methods
Field and greenhouse experiments were conducted to quantify effects of N competition and organic acids on N fixation in a maize/alfalfa intercropping system.
Results
Intercropping increased nitrogen derived from the atmosphere (%Ndfa), nodules number, and leghemoglobin content by 43.66%, 85.53%, 141.05%, respectively, leading to significantly improved total N uptake and yield, compared to monoculture. The improved %Ndfa was not only due to the depletion of NO3−, but also significantly correlated with the decrease of NO3−/NH4+ ratio and the increase of citric acid in rhizosphere of alfalfa, which could mobilize soluble resources for N fixation under no N addition. Overall, 15.4%–21.5% of N fixed by alfalfa was transferred to associated maize, and the improved N fixation enhanced N transfer.
Conclusions
Our findings provide a mechanism for how root interactions facilitate N fixation, highlighting the importance of NO3−/NH4+ ratio and citric acid in nutrient mobilization for N fixation.
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References
Adu-Gyamfi JJ, Myaka FA, Sakala WD, Odgaard R, Vesterager JM, Høgh-Jensen H (2007) Biological nitrogen fixation and nitrogen and phosphorus budgets in farmer-managed intercrops of maize-pigeonpea in semi-arid southern and eastern Africa. Plant Soil 295:127–136
Baziramakenga R, Simard RR, Leroux GD (1995) Determination of organic acids in soil extracts by ion chromatography. Soil Biol Biochem 27:349–356
Borsani J, Budde CO, Porrini L, Lauxmann MA, Lombardo VA, Murray R, Andreo CS, Drincovich MF, Lara MV (2009) Carbon metabolism of peach fruit after harvest: changes in enzymes involved in organic acid and sugar level modifications. J Exp Bot 60:1823–1837
Carlsson G, Huss-Danell K (2003) Nitrogen fixation in perennial forage legumes in the field. Plant Soil 253:353–372
Chapagain T, Riseman A (2014) Barley-pea intercropping: effects on land productivity, carbon and nitrogen transformations. Field Crop Res 166:18–25
Chapagain T, Riseman A (2015) Nitrogen and carbon transformations, water use efficiency and ecosystem productivity in monocultures and wheat-bean intercropping systems. Nutr Cycl Agroecosyst 101:107–121
Chen PC, Phillips DA (1977) Induction of root nodule senescence by combined nitrogen in Pisum sativum L. Plant Physiol 59:440–442
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
Corre-Hellou G, Crozat Y (2006) Interspecific competition for soil N and its interaction with N2 fixation, leaf expansion and crop growth in pea-barley intercrops. Plant Soil 282:195–208
Fan F, Zhang F, Song Y (2006) Nitrogen fixation of faba bean (Vicia faba L.) interacting with a non-legume in two contrasting intercropping systems. Plant Soil 283:275–286
Fei H, Vessey JK (2003) Involvement of cytokinin in the stimulation of nodulation by low concentrations of ammonium in Pisum sativum. Physiol Plant 118:447–455
Fei H, Vessey JK (2009) Stimulation of nodulation in Medicago truncatula by low concentrations of ammonium: quantitative reverse transcription PCR analysis of selected genes. Physiol Plant 135:317–330
Fujita K, Ofosubudu KG, Ogata S (1992) Biological nitrogen fixation in mixed legume-cereal cropping systems. Plant Soil 141:155–175
Gan Y, Stulen I, van Keulen H, Kuiper PJC (2004) Low concentrations of nitrate and ammonium stimulate nodulation and N2 fixation while inhibiting specific nodulation (nodule DW g−1 root dry weight) and specific N2 fixation (N2 fixed g−1 root dry weight) in soybean. Plant Soil 258:281–292
Graham PH, Vance CP (2000) Nitrogen fixation in perspective: an overview of research and extension needs. Field Crop Res 65:93–106
Gu B, Ju X, Chang J, Ge Y, Vitousekd PM (2015) Integrated reactive nitrogen budgets and future trends in China. Proc Natl Acad Sci USA 112:8792–8797
Guo X, Xiong H, Shen H, Qiu W, Ji C, Zheng Z, Zuo Y (2014) Dynamics in the rhizosphere and iron-uptake gene expression in peanut induced by intercropping with maize: role in improving iron nutrition in peanut. Plant Physiol Biochem 76:36–43
Haichar FEZ, Santaella C, Heulin T, Achouak W (2014) Root exudates mediated interactions belowground. Soil Biol Biochem 77:69–80
Hauggaard-Nielsen H, Ambus P, Jensen ES (2001) Interspecific competition, N use and interference with weeds in pea-barley intercropping. Field Crop Res 70:101–109
Hauggaard-Nielsen H, Gooding M, Ambus P, Corre-Hellou G, Crozat Y, Dahlmann C, Dibet A, von Fragstein P, Pristeri A, Monti M, Jensen ES (2009) Pea-barley intercropping for efficient symbiotic N2-fixation, soil N acquisition and use of other nutrients in European organic cropping systems. Field Crop Res 113:64–71
Herridge DF, Peoples MB, Boddey RM (2008) Global inputs of biological nitrogen fixation in agricultural systems. Plant Soil 311:1–18
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
Jensen ES (1996) Grain yield, symbiotic N2 fixation and interspecific competition for inorganic N in pea-barley intercrops. Plant Soil 182:25–38
Jones DL, Darah PR, Kochian LV (1996) Critical evaluation of organic acid mediated iron dissolution in the rhizosphere and its potential role in root iron uptake. Plant Soil 180:57–66
Latati M, Blavet D, Alkama N (2014) The intercropping cowpea-maize improves soil phosphorus availability and maize yields in an alkaline soil. Plant Soil 385:1–11
Ledgard SF (2001) Nitrogen cycling in low input legume-based agriculture, with emphasis on legume/grass pastures. Plant Soil 228:43–59
Ledgard SF, Steele KW (1992) Biological nitrogen fixation in mixed legume/grass pastures. Plant Soil 141:137–153
Li L, Li SM, Sun JH (2007) Diversity enhances agricultural productivity via rhizosphere phosphorus facilitation on phosphorus-deficient soils. Proc Natl Acad Sci USA 104:11192–11196
Li YY, Yu CB, Xu C, 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
Li B, Li YY, Wu HM (2016) Root exudates drive interspecific facilitation by enhancing nodulation and N2 fixation. Proc Natl Acad Sci USA 113:6496–6501
Mahieu S, Germon F, Aveline A (2009) The influence of water stress on biomass and N accumulation, N partitioning between above and below ground parts and on N rhizodeposition during reproductive growth of pea (Pisum sativum L.). Soil Biol Biochem 41:380–387
Marschner H (1995) Mineral nutrition of higher plants. J Ecol 76:1250
Marschner H, Romheld V (1996) Root-induced changes in the availability of micronutrients in the rhizosphere. In: Waisel Y, Eshel A, Kafkafi U (Eds) Plant roots: the hidden half, 2nd. New York, pp 557–579
Mei PP, Gui LG, Wang P (2012) Maize/faba bean intercropping with rhizobia inoculation enhances productivity and recovery of fertilizer P in a reclaimed desert soil. Field Crop Res 130:19–27
Meng L, Zhang A, Wang F (2015) Arbuscular mycorrhizal fungi and rhizobium facilitate nitrogen uptake and transfer in soybean/maize intercropping system. Front Plant Sci 6:339
Morris R, Garrity D (1993) Resource capture and utilization in intercropping: water. Field Crop Res 34:303–317
Mus F, Crook MB, Garcia K (2016) Symbiotic nitrogen fixation and the challenges to its extension to nonlegumes. Appl Environ Microbiol 82:3698–3710
Neumann A, Schmidtke K, Rauber R (2007) Effects of crop density and tillage system on grain yield and N uptake from soil and atmosphere of sole and intercropped pea and oat. Field Crop Res 100:285–293
Nyfeler D, Huguenin-Elie O, Suter M (2011) Grass-legume mixtures can yield more nitrogen than legume pure stands due to mutual stimulation of nitrogen uptake from symbiotic and non-symbiotic sources. Agr Ecosyst Environ 140:155–163
Pang J, Bansal R, Zhao H (2018) The carboxylate-releasing phosphorus-mobilizing strategy can be proxied by foliar manganese concentration in a large set of chickpea germplasm under low phosphorus supply. New Phytol 219:518–529
Peoples MB, Brockwell J, Hunt JR (2012) Factors affecting the potential contributions of N2 fixation by legumes in Australian pasture systems. Crop Pasture Sci 63:759–786
Pirhofer-Walzl K, Rasmussen J, Høgh-Jensen H (2012) Nitrogen transfer from forage legumes to nine neighbouring plants in a multi-species grassland. Plant Soil 350:71–84
Qiao X, Bei S, Li C (2015) Enhancement of faba bean competitive ability by arbuscular mycorrhizal fungi is highly correlated with dynamic nutrient acquisition by competing wheat. Sci Rep-UK 5:8122
Salvagiotti F, Cassman KG, Specht JE (2008) Nitrogen uptake, fixation and response to fertilizer N in soybeans: a review. Field Crop Res 108:1–13
Schipanski ME, Drinkwater LE, Russelle MP (2010) Understanding the variability in soybean nitrogen fixation across agroecosystems. Plant Soil 329:379–397
Shearer G, Kohl DH (1986) N2-fixation in field settings: estimations based on natural 15N abundance. Funct Plant Boil 13:699–756
Silber A, Yones LB, Dori I (2004) Rhizosphere pH as a result of nitrogen levels and NH4+ /NO3− ratio and its effect on zinc availability and on growth of rice flower (Ozothamnus diosmifolius). Plant Soil 262:205–213
Streeter J, Wong PP (1988) Inhibition of legume nodule formation and N2 fixation by nitrate. Crit Rev Plant Sci 7:1–23
Sun B, Peng Y, Yang H, Li Z, Gao Y, Wang C, Yan Y, Liu Y (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
Thilakarathna MS, Papadopoulos YA, Rodd AV (2016) Nitrogen fixation and transfer of red clover genotypes under legume-grass forage based production systems. Nutr Cycl Agroecosyst 106:233–247
Unkovich M (2012) Nitrogen fixation in Australian dairy systems: review and prospect. Crop Pasture Sci 63:787–804
Vance CP, Uhde-Stone C, Allan DL (2003) Phosphorus acquisition and use: critical adaptations by plants for securing a nonrenewable resource. New Phytol 157:423–447
Vandermeer JH (1989) The ecology of intercropping systems. J Appl Ecol 26:185–188
Vivo A, Andreu JM, De lVS (1989) Leghemoglobin in Lupin plants (Lupinus albus cv Multolupa). Plant Physiol 90:452–457
Wahbi S, Prin Y, Thioulouse J (2016) Impact of wheat/faba bean mixed cropping or rotation systems on soil microbial functionalities. Front Plant Sci 7:1364
Wahla IH, Ahmad R, Ehsanullah Ahmad A, Jabbar A (2009) Competitive functions of components crops in some barley based intercropping systems. Int J Agric Boil 11:69–72
Wang BL, Tang XY, Cheng LY, Zhang AZ, Zhang WH, Zhang FS, Liu JQ, Cao Y, Allan DL, Vance CP, Shen JB (2010) Nitric oxide is involved in phosphorus deficiency-induced cluster-root development and citrate exudation in white lupin. New Phytol 187:1112–1123
West JB, Hillerislambers J, Lee TD (2005) Legume species identity and soil nitrogen supply determine symbiotic nitrogen-fixation responses to elevated atmospheric [CO2]. New Phytol 167:523–530
Xiao Y, Li L, Zhang F (2004) Effect of root contact on interspecific competition and N transfer between wheat and fababean using direct and indirect N techniques. Plant Soil 262:45–54
Yoneyama T, Fujita K, Yoshida T (1986) Variation in natural abundance of 15N among plant parts and in 15N/14N fractionation during N2 fixation in the legume-rhizobia symbiotic system. Plant Cell Physiol 27:791–799
Zhou M, Butterbach-Bahl K (2014) Assessment of nitrate leaching loss on a yield-scaled basis from maize and wheat cropping systems. Plant Soil 374:977–991
Zuo Y, Zhang F, Li X, Cao Y (2000) Studies on the improvement in iron nutrition of peanut by intercropping with maize on a calcareous soil. Plant Soil 220:13–25
Acknowledgments
This work was financially supported by the National Key Basic Research Program of China (2016YFC0500703), the National Natural Science Foundation of China (31670446, 31471945, 31870436, U1803110), and Jilin Special Program for Key Science and Technology Research (Y8D1161001).
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Wang, X., Gao, Y., Zhang, H. et al. Enhancement of rhizosphere citric acid and decrease of NO3−/NH4+ ratio by root interactions facilitate N fixation and transfer. Plant Soil 447, 169–182 (2020). https://doi.org/10.1007/s11104-018-03918-6
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DOI: https://doi.org/10.1007/s11104-018-03918-6