Abstract
Background and aims
Maize/legume intercrop** leads to overyielding and maintains soil nutrients. Rhizobium inoculation in maize/legume intercrop** enhances soil nitrogen; however, its effects on overyielding and other soil nutrients in long-term intercrop** systems is not well understood.
Methods
We conducted a split-split-plot experiment with three factors in northwest China since 2009. The main plot treatments were without or with rhizobium inoculation in faba bean (-Rhizobium, +Rhizobium), while the sub-plot treatments were five nitrogen-application rates and the sub-sub-plot treatments were crop** system (monocultures of faba bean, maize and faba bean/maize intercrop**). During 2018-2020, we measured the yield, soil nutrients in the 0-20 cm topsoil, calculated biodiversity effects, and quantified interspecific interaction of intercrop** using the relative interaction index.
Results
The grain yields in intercrop** with treatments of -Rhizobium and + Rhizobium increased by 8.9% and 32%, respectively, compared with the corresponding weighted means of monocultures. Rhizobium inoculation increased the land-equivalent ratio at high nitrogen application. The combination of rhizobium inoculation and nitrogen application significantly enhanced the complementarity effect and relative interaction index of maize. With rhizobium inoculation, intercrop** increased the soil Olsen P concentration by 13.9-59.9%, compared with the corresponding weighted means of monocultures which may be associated with interspecific facilitation, indicated by relative interaction index of maize.
Conclusions
Our study shows that rhizobium inoculation increased yield advantages and soil Olsen P concentration via enhanced interspecific facilitation of faba bean on maize in the intercrop** system. Rhizobium inoculation can be used as an efficient strategy to enhance the benefits of intercrop**, especially in low-fertility soil.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Abbreviations
- -Rhizobium:
-
Without rhizobium inoculation treatment
- +Rhizobium:
-
Rhizobium inoculation treatment
- Cs:
-
Crop** system
- LER:
-
Land-equivalent ratio
- RII:
-
Relative interaction index
- RIIfaba bean :
-
RII calculated based on the aboveground biomass of faba bean
- RIImaize :
-
RII calculated based on the aboveground biomass of maize
- SE:
-
Selection effect
- CE:
-
Complementarity effect
References
Alarcon-Segura V, Grass I, Breustedt G, Rohlfs M, Tscharntke T (2022) Strip intercrop** of wheat and oilseed rape enhances biodiversity and biological pest control in a conventionally managed farm scenario. J Appl Ecol 59:1513–1523. https://doi.org/10.1111/1365-2664.14161
Armas C, Ordiales R, Pugnaire FI (2004) Measuring plant interactions: a new comparative index. Ecology 85:2682–2686. https://doi.org/10.1890/03-0650
Brooker RW, Bennett AE, Cong WF, Daniell TJ, George TS, Hallett PD, Hawes C, Iannetta PPM, Jones HG, Karley AJ, Li L, McKenzie BM, Pakeman RJ, Paterson E, Schob C, Shen JB, Squire G, Watson CA, Zhang CC et al (2015) Improving intercrop**: a synthesis of research in agronomy, plant physiology and ecology. New Phytol 206:107–117. https://doi.org/10.1111/nph.13132
Chai Q, Nemecek T, Liang C, Zhao C, Yu AZ, Coulter JA, Wang YF, Hu FL, Wang L, Siddique KHM, Gan YT (2021) Integrated farming with intercrop** increases food production while reducing environmental footprint. Proc Natl Acad Sci U S A 118:12. https://doi.org/10.1073/pnas.2106382118
Chen X, Chen HYH, Chang SX (2022) Meta-analysis shows that plant mixtures increase soil phosphorus availability and plant productivity in diverse ecosystems. Nat Ecol Evol 6:1112–1121. https://doi.org/10.1038/s41559-022-01794-z
Crippa M, Solazzo E, Guizzardi D, Monforti-Ferrario F, Tubiello FN, Leip A (2021) Food systems are responsible for a third of global anthropogenic GHG emissions. Nat Food 2:198–209. https://doi.org/10.1038/s43016-021-00225-9
Dakora FD, Phillips DA (2002) Root exudates as mediators of mineral acquisition in low-nutrient environments. Plant Soil 245:35–47. https://doi.org/10.1023/a:1020809400075
Dong QQ, Zhao XH, Zhou DY, Liu ZH, Shi XL, Yuan Y, Jia PY, Liu YY, Song PH, Wang XG, Jiang CJ, Liu XB, Zhang H, Zhong C, Guo F, Wan SB, Yu HQ, Zhang Z (2022) Maize and peanut intercrop** improves the nitrogen accumulation and yield per plant of maize by promoting the secretion of flavonoids and abundance of Bradyrhizobium in rhizosphere. Front Plant Sci 13:16. https://doi.org/10.3389/fpls.2022.957336
Dybzinski R, Fargione JE, Zak DR, Fornara D, Tilman D (2008) Soil fertility increases with plant species diversity in a long-term biodiversity experiment. Oecologia 158:85–93. https://doi.org/10.1007/s00442-008-1123-x
Furey GN, Tilman D (2021) Plant biodiversity and the regeneration of soil fertility. Proc Natl Acad Sci U S A 118:8. https://doi.org/10.1073/pnas.2111321118
Hu HY, Li H, Hao MM, Ren YN, Zhang MK, Liu RY, Zhang Y, Li G, Chen JS, Ning TY, Kuzyakov Y (2021) Nitrogen fixation and crop productivity enhancements co-driven by intercrop root exudates and key rhizosphere bacteria. J Appl Ecol 58:2243–2255. https://doi.org/10.1111/1365-2664.13964
Jiang FY, Zhang L, Zhou JC, George TS, Feng G (2021) Arbuscular mycorrhizal fungi enhance mineralisation of organic phosphorus by carrying bacteria along their extraradical hyphae. New Phytol 230:304–315. https://doi.org/10.1111/nph.17081
Laborde D, Martin W, Swinnen J, Vos R (2020) COVID-19 risks to global food security. Science 369:500–502. https://doi.org/10.1126/science.abc4765
Larimer AL, Clay K, Bever JD (2014) Synergism and context dependency of interactions between arbuscular mycorrhizal fungi and rhizobia with a prairie legume. Ecology 95:1045–1054. https://doi.org/10.1890/13-0025.1
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 U S A 104:11192–11196. https://doi.org/10.1073/pnas.0704591104
Li L, Tilman D, Lambers H, Zhang FS (2014) Plant diversity and overyielding: insights from belowground facilitation of intercrop** in agriculture. New Phytol 203:63–69. https://doi.org/10.1111/nph.12778
Li B, Li YY, Wu HM, Zhang FF, Li CJ, Li XX, Lambers H, Li L (2016) Root exudates drive interspecific facilitation by enhancing nodulation and N-2 fixation. Proc Natl Acad Sci U S A 113:6496–6501. https://doi.org/10.1073/pnas.1523580113
Li CJ, Hoffland E, Kuyper TW, Yu Y, Zhang CC, Li HG, Zhang FS, van der Werf W (2020) Syndromes of production in intercrop** impact yield gains. Nat Plants 6:653–660. https://doi.org/10.1038/s41477-020-0680-9
Li XF, Wang ZG, Bao XG, Sun JH, Yang SC, Wang P, Wang CB, Wu JP, Liu XR, Tian XL, Wang Y, Li JP, Wang Y, **. Nat Sustain 4:943–950. https://doi.org/10.1038/s41893-021-00767-7
Loreau M, Hector A (2001) Partitioning selection and complementarity in biodiversity experiments. Nature 412:72–76. https://doi.org/10.1038/35083573
Ma H, Zhou J, Ge J, Nie J, Zhao J, Xue Z, Hu Y, Yang Y, Peixoto L, Zang H, Zeng Z (2022) Intercrop** improves soil ecosystem multifunctionality through enhanced available nutrients but depends on regional factors. Plant Soil 480:71–84. https://doi.org/10.1007/s11104-022-05554-7
Mahmoud R, Casadebaig P, Hilgert N, Alletto L, Freschet GT, de Mazancourt C, Gaudio N (2022) Species choice and N fertilization influence yield gains through complementarity and selection effects in cereal-legume intercrops. Agron Sustain Dev 42:12. https://doi.org/10.1007/s13593-022-00754-y
Mei PP, Gui LG, Wang P, Huang JC, Long HY, Christie P, Li L (2012) Maize/faba bean intercrop** with rhizobia inoculation enhances productivity and recovery of fertilizer P in a reclaimed desert soil. Field Crop Res 130:19–27. https://doi.org/10.1016/j.fcr.2012.02.007
Mei PP, Wang P, Yang H, Gui LG, Christie P, Li L (2021) Maize/faba bean intercrop** with rhizobial inoculation in a reclaimed desert soil enhances productivity and symbiotic N-2 fixation and reduces apparent N losses. Soil Tillage Res 213:11. https://doi.org/10.1016/j.still.2021.105154
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 intercrop** system. Front Plant Sci 6:10. https://doi.org/10.3389/fpls.2015.00339
Mudare S, Kanomanyanga J, Jiao XQ, Mabasa S, Lamichhane JR, **g JY, Cong WF (2022) Yield and fertilizer benefits of maize/grain legume intercrop** in China and Africa: a meta-analysis. Agron Sustain Dev 42:81. https://doi.org/10.1007/s13593-022-00816-1
Pinheiro, Bates D, Team RC (2022) nlme: linear and nonlinear mixed effects models. R package version 31-160
Richardson AE, Barea JM, McNeill AM, Prigent-Combaret C (2009) Acquisition of phosphorus and nitrogen in the rhizosphere and plant growth promotion by microorganisms. Plant Soil 321:305–339. https://doi.org/10.1007/s11104-009-9895-2
Rillig MC, Mummey DL (2006) Mycorrhizas and soil structure. New Phytol 171:41–53. https://doi.org/10.1111/j.1469-8137.2006.01750.x
Sardans J, Peñuelas J (2015) Potassium: a neglected nutrient in global change. Glob Ecol Biogeogr 24:261–275. https://doi.org/10.1111/geb.12259
Sulieman S, Tran L-SP (2015) Phosphorus homeostasis in legume nodules as an adaptive strategy to phosphorus deficiency. Plant Sci 239:36–43. https://doi.org/10.1016/j.plantsci.2015.06.018
Tang C, Hinsinger P, Drevon JJ, Jaillard B (2001) Phosphorus deficiency impairs early nodule functioning and enhances proton release in roots of Medicago truncatula L. Ann Bot 88:131–138. https://doi.org/10.1006/anbo.2001.1440
Tang XY, Placella SA, Daydé F, Bernard L, Robin A, Journet EP, Justes E, Hinsinger P (2016) Phosphorus availability and microbial community in the rhizosphere of intercropped cereal and legume along a P-fertilizer gradient. Plant Soil 407:119–134. https://doi.org/10.1007/s11104-016-2949-3
Tian XL, Wang CB, Bao XG, Wang P, Li XF, Yang SC, Ding GC, Christie P, Li L (2019) Crop diversity facilitates soil aggregation in relation to soil microbial community composition driven by intercrop**. Plant Soil 436:173–192. https://doi.org/10.1007/s11104-018-03924-8
Tilman D, Lehman CL, Thomson KT (1997) Plant diversity and ecosystem productivity: theoretical considerations. Proc Natl Acad Sci U S A 94:1857–1861. https://doi.org/10.1073/pnas.94.5.1857
Tilman D, Reich PB, Knops J, Wedin D, Mielke T, Lehman C (2001) Diversity and productivity in a long-term grassland experiment. Science 294:843–845. https://doi.org/10.1126/science.1060391
Vandermeer JH (1989) The ecology of intercrop**. Cambridge University Press, Cambridge
Vogel E, Donat MG, Alexander LV, Meinshausen M, Ray DK, Karoly D, Meinshausen N, Frieler K (2019) The effects of climate extremes on global agricultural yields. Environ Res Lett 14:12. https://doi.org/10.1088/1748-9326/ab154b
Wang ZG, ** X, Bao XG, Li XF, Zhao JH, Sun JH, Christie P, Li L (2014) Intercrop** enhances productivity and maintains the most soil fertility properties relative to sole crop**. PLoS One 9:e113984. https://doi.org/10.1371/journal.pone.0113984
Wang XH, Zhao C, Muller C, Wang CZ, Ciais P, Janssens I, Penuelas J, Asseng S, Li T, Elliott J, Huang Y, Li L, Piao S (2020a) Emergent constraint on crop yield response to warmer temperature from field experiments. Nat Sustain 3:908–916. https://doi.org/10.1038/s41893-020-0569-7
Wang XY, Gao YZ, Zhang HL, Shao ZQ, Sun BR, Gao Q (2020b) Enhancement of rhizosphere citric acid and decrease of NO3-/NH4+ ratio by root interactions facilitate N fixation and transfer. Plant Soil 447:169–182. https://doi.org/10.1007/s11104-018-03918-6
Williams DR, Clark M, Buchanan GM, Ficetola GF, Rondinini C, Tilman D (2020) Proactive conservation to prevent habitat losses to agricultural expansion. Nat Sustain. https://doi.org/10.1038/s41893-020-00656-5
Xue R, Wang C, Zhao L, Sun B, Wang B (2022) Agricultural intensification weakens the soil health index and stability of microbial networks. Agric Ecosyst Environ 339:108118. https://doi.org/10.1016/j.agee.2022.108118
Yang H, Zhang W, Li L (2021) Intercrop**: feed more people and build more sustainable agroecosystems. Front Agric Sci Eng 8: 373-386. https://doi.org/10.15302/J-FASE-2021398
Yu R-P, Lambers H, Callaway RM, Wright AJ, Li L (2021) Belowground facilitation and trait matching: two or three to tango? Trends Plant Sci 26:1227–1235. https://doi.org/10.1016/j.tplants.2021.07.014
Zemunik G, Turner BL, Lambers H, Laliberté E (2015) Diversity of plant nutrient-acquisition strategies increases during long-term ecosystem development. Nat Plants 1:15050. https://doi.org/10.1038/nplants.2015.50
Zhang WP, Jia X, Damgaard C, Morris EC, Bai YY, Pan S, Wang GX (2013) The interplay between above- and below-ground plant-plant interactions along an environmental gradient: insights from two-layer zone-of-influence models. Oikos 122:1147–1156. https://doi.org/10.1111/j.1600-0706.2012.20877.x
Zhang WP, Jia X, Wang GX (2017) Facilitation among plants can accelerate density-dependent mortality and steepen self-thinning lines in stressful environments. Oikos 126:1197–1207. https://doi.org/10.1111/oik.03983
Zhang H, Wang X, Gao Y, Sun B (2020a) 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. https://doi.org/10.1007/s11104-019-04333-1
Zhang R, Mu Y, Li X, Li S, Sang P, Wang X, Wu H, Xu N (2020b) Response of the arbuscular mycorrhizal fungi diversity and community in maize and soybean rhizosphere soil and roots to intercrop** systems with different nitrogen application rates. Sci Total Environ 740:139810. https://doi.org/10.1016/j.scitotenv.2020.139810
Zhang L, Chu Q, Zhou J, Rengel Z, Feng G (2021a) Soil phosphorus availability determines the preference for direct or mycorrhizal phosphorus uptake pathway in maize. Geoderma 403:115261. https://doi.org/10.1016/j.geoderma.2021.115261
Zhang WP, Gao SN, Li ZX, Xu HS, Yang H, Yang X, Fan HX, Su Y, Fornara D, Li L (2021b) Shifts from complementarity to selection effects maintain high productivity in maize/legume intercrop** systems. J Appl Ecol 58:2603–2613. https://doi.org/10.1111/1365-2664.13989
Zhang WP, Fornara D, Yang H, Yu R-P, Callaway RM, Li L (2023) Plant litter strengthens positive biodiversity-ecosystem functioning relationships over time. Trends Ecol Evol 38:473–484. https://doi.org/10.1016/j.tree.2022.12.008
Zheng C, Ji B, Zhang J, Zhang F, Bever JD (2015) Shading decreases plant carbon preferential allocation towards the most beneficial mycorrhizal mutualist. New Phytol 205:361–368. https://doi.org/10.1111/nph.13025
Zhou XY, Lu G, Xu ZC, Yan XQ, Khu ST, Yang JF, Zhao J (2023) Influence of Russia-Ukraine war on the global energy and food security. Resour Conserv Recycl 188:12. https://doi.org/10.1016/j.resconrec.2022.106657
Zhu SG, Cheng ZG, Batool A, Wang YB, Wang J, Zhou R, Khan A, Zhu S-Y, Yang Y-M, Wang W, Zhu H, Wang BZ, Tao HY, ** system. Ecol Indic 139:108901. https://doi.org/10.1016/j.ecolind.2022.108901
Zhu SG, Zhu H, Zhou R, Zhang W, Wang W, Zhou YN, Wang BZ, Yang YM, Wang J, Tao HY, **ong YC (2023) Intercrop overyielding weakened by high inputs: global meta-analysis with experimental validation. Agric Ecosyst Environ 342:11. https://doi.org/10.1016/j.agee.2022.108239
Funding
This work was financially supported by National Key Research and Development Program of China (2022YFD1900200), National Natural Science Foundation of China (32130067, 31430014).
Author information
Authors and Affiliations
Contributions
Long Li designed and guided the experiments. Jun Mao, ** Wang, Chuan-Lin **ao and **g-Ru He contributed to the field management and sampling. Jun Mao performed the experiments and wrote the first draft of the manuscript. **-Pu Wu, Wei-** Zhang, Hans Lambers and Long Li commented on previous versions of the manuscript and revised the manuscript.
Corresponding author
Ethics declarations
The authors have no relevant financial or non-financial interests to disclose.
Additional information
Responsible Editor: Andrew Fletcher.
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
ESM 1
(DOCX 1176 kb)
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Mao, J., Wang, P., **. Plant Soil (2023). https://doi.org/10.1007/s11104-023-06425-5
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11104-023-06425-5