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Journal of Integrative Agriculture  2026, Vol. 25 Issue (5): 2109-2120    DOI: 10.1016/j.jia.2025.07.017
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Legume–cereal intercropping with AMF reduces cadmium bioavailability and enhances land productivity

Yanan Yang1, 2, Weizhen Chen1, 3, Zipeng Chen1, Huashou Li1#

1 Guangdong Provincial Key Laboratory of Agricultural & Rural Pollution Abatement and Environmental Safety, College of Natural Resources and Environment, South China Agricultural University, Guangzhou 510642, China

2 Kunpeng Institute of Modern Agriculture at Foshan, Foshan 528200, China

3 Key Laboratory of Yangtze River Water Environment, Ministry of Education/College of Environmental Science and Engineering, Tongji University, Shanghai 200092, China

 Highlights 
● Maize–soybean intercropping reduces grain Cd to safe levels (<0.20 mg kg–1), ensuring compliance with China’s food safety standard (GB2762-2022) while maintaining yield advantages (LER>1).
● AMF inoculation synergistically enhances intercropping benefits, improving Cd removal efficiency (MRER>1) and crop resilience through enhanced nutrient uptake and improved rhizosphere soil health.
A “repair while producing” model demonstrates that strategic crop pairing combined with AMF integration can simultaneously remediate Cd-polluted soils, ensure food safety, and optimize land productivity.
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摘要  

间作体系与丛枝菌根真菌(AMF)接种联合应用,为重金属污染农田提供了一种兼具生态与经济效益的植物修复方案。然而,AMF与间作对镉土壤(Cd)生物有效性的影响尚不明确。本研究通过田间与盆栽试验,探究玉米-大豆间作与AMF接种对作物生长、Cd分配及根际土壤环境的协同效应。田间试验表明:玉米-大豆间作具有显著产量优势,土地当量比(LER)达1.62(普通玉米)与1.64(甜玉米);间作降低大豆各部位镉积累量,其中籽粒镉积累量降低42.8%,同时维持玉米籽粒Cd浓度低于中国食品安全限值(0.20 mg kg-1GB2762-2022);重金属去除当量比(MRER)达1.33-1.38,证实间作在产量与Cd植物提取上的双重优势。盆栽试验表明:AMF接种联合间作体系(IN+A)使玉米增产16.4%,同时显著降低两种作物Cd积累(籽粒浓度符合安全标准);根际分析表明IN+A处理显著改善土壤健康指标:生物有效态Cd降低34.5%pH升高,氧化还原电位(Eh)下降,过氧化氢酶活性提升;接种处理的AMF定殖率较对照组提高2.2-4.3倍。本研究证实:经AMF强化的玉米-大豆间作体系,通过土壤碱化与氧化还原电位下降的协同调控,以及Cd向根系的定向分配,有效降低Cd生物有效性。这种微生物-植物群落协同机制,在保障作物籽粒安全的同时实现土壤Cd稳定,可为污染农田“修复-生产”同步推进提供参考。



Abstract  

The combined implementation of intercropping systems and arbuscular mycorrhizal fungi (AMF) inoculation represents a promising phytoremediation strategy for heavy metal-contaminated farmland, providing both ecological and economic benefits.  However, additional research is necessary to understand the influence of AMF and intercropping on Cd bioavailability.  This study examines the synergistic effects of maize–soybean intercropping and AMF inoculation on crop growth, cadmium (Cd) allocation patterns, and rhizosphere soil dynamics through comprehensive field and pot experiments.  Field trials revealed significant yield advantages in maize–soybean intercropping systems, with land equivalent ratios (LERs) of 1.62 (common maize) and 1.64 (sweet maize).  Intercropping decreased soybean Cd accumulation across all tissues, notably in grains (42.8% reduction), while maintaining maize grain Cd concentrations below China’s food safety threshold (0.20 mg kg–1).  The metal removal equivalent ratio (MRER) achieved 1.33–1.38 in field conditions, validating intercropping’s dual advantage in productivity and Cd phytoextraction.  Pot experiments indicated the AMF-inoculated intercropping system (IN+A) increased maize yield by 16.4% while reducing Cd accumulation in both crops, with grain concentrations meeting safety standards.  Rhizosphere analysis demonstrated IN+A treatment substantially improved soil health indicators: 34.5% reduction in bioavailable Cd, elevated pH, decreased redox potential (Eh), and enhanced catalase activity.  AMF colonization rates were 2.2–4.3 times higher in inoculated treatments (11.5–14.0%) vs. controls (3.2–5.3%).  These results establish that AMF-enhanced legume–cereal intercropping reduces Cd bioavailability through soil alkalinization (pH increase) coupled with redox potential reduction, and metal allocation plasticity redirecting Cd to root tissues.  This interaction between microbial symbiosis and plant community design stabilizes Cd in soils while maintaining crop safety (grain Cd<0.20 mg kg–1), establishing an ecoengineering approach for contaminated farmland remediation.

Keywords:  phytoremediation       cadmium       interplanting       maize       soybean  
Received: 01 April 2025   Accepted: 13 June 2025 Online: 14 July 2025  
Fund: This work was co-funded by the Science and Technology Planning Project of Guangzhou, Guangdong Province, China (202206010176) and the National Key Research and Development Program of China (2020YFC1807805).  
About author:  Yanan Yang, E-mail: muouyingzi@163.com; #Correspondence Huashou Li, Tel: +86-20-85280211, E-mail: lihuashou@scau.edu.cn

Cite this article: 

Yanan Yang, Weizhen Chen, Zipeng Chen, Huashou Li. 2026. Legume–cereal intercropping with AMF reduces cadmium bioavailability and enhances land productivity. Journal of Integrative Agriculture, 25(5): 2109-2120.

Antoniadis V, Shaheen S M, Levizou E, Shahid M, Niazi N K, Vithanage M, Ok Y S, Bolan N, Rinklebe J. 2019. A critical prospective analysis of the potential toxicity of trace element regulation limits in soils worldwide: Are they protective concerning health risk assessment? - A review. Environment International127, 819–847.

Ashraf S, Ali Q, Zahir Z A, Ashraf S, Asghar H N. 2019. Phytoremediation: Environmentally sustainable way for reclamation of heavy metal polluted soils. Environmental Safety174, 714–727.

Awa S H, Hadibarata T. 2020. Removal of heavy metals in contaminated soil by phytoremediation mechanism: A review. WaterAir& Soil Pollution231, 47.

Banerjee A, Sanyal S, Sen S. 2012. Soil phosphatase activity of agricultural land: A possible index of soil fertility. Agricultural Science Research Journals2, 412–419.

Brooker R W, Pakeman R J, Adam E, Banfield-Zanin J A, Bertelsen I, Bickler C, Fog-Petersen J, George D, Newton A C, Rubiales D, Tavoletti S, Villegas-Fernández A M, Karley A J. 2024. Positive effects of intercrop yields in farms from across Europe depend on rainfall, crop composition, and management. Agronomy for Sustainable Development44, 35.

Carvalho M, Brito I, Alho L, Goss M J. 2015. Assessing the progress of colonization by arbuscular mycorrhiza of four plant species under different temperature regimes. Journal of Plant Nutrition and Soil Science178, 515–522.

Chen W Z, Kang Z M, Yang Y N, Li Y S, Qiu R L, Qin J H, Li H S. 2022. Interplanting of rice cultivars with high and low Cd accumulation can achieve the goal of “repairing while producing” in Cd-contaminated soil. Science of the Total Environment851, 158229.

Chen W Z, Li M, Huang P Y, Meng D L, Ying J D, Yang Y N, Qiu R L, Li H S. 2023. The application of mixed stabilizing materials promotes the feasibility of the intercropping system of Gynostemma pentaphyllum/Helianthus annuus L. on arsenic contaminated soil. Journal of Environmental Management348, 119284.

Curtright A J, Tiemann L K. 2021. Intercropping increases soil extracellular enzyme activity: A meta-analysis. AgricultureEcosystems & Environment319, 107489.

Diagne N, Ngom M, Djighaly P I, Fall D, Hocher V, Svistoonoff S. 2020. Roles of arbuscular mycorrhizal fungi on plant growth and performance: Importance in biotic and abiotic stressed regulation. Diversity12, 370.

Frankeberger W T, Johanson J B. 1983. Method of measuring invertase activity in soils. Plant and Soil74, 301–311.

Giovannetti M, Mosse B. 1980. An evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytologist84, 489–500.

Gou F, Van Ittersum M K, Couëdel A, Zhang Y, Wang Y, Van Der Putten P E, Zhang L, Van Der Werf W. 2018. Intercropping with wheat lowers nutrient uptake and biomass accumulation of maize, but increases photosynthetic rate of the ear leaf. AoB Plants10, ply10.

Hao B, Zhang Z, Bao Z, Hao L, Diao F, Li F Y, Guo W. 2022. Claroideoglomus etunicatum affects the structural and functional genes of the rhizosphere microbial community to help maize resist Cd and La stresses. Environmental Pollution307, 119559.

Ingraffia R, Amato G, Frenda A S, Giambalvo D. 2019. Impacts of arbuscular mycorrhizal fungi on nutrient uptake, N2 fixation, N transfer, and growth in a wheat/faba bean intercropping system. PLoS ONE14, e213672.

Johnson J L, Temple K L. 1964. Some variables affecting the measurement of “catalase activity” in soil. Soil Science Society of America Journal28, 207–209.

Kang Z, Gong M, Li Y, Chen W, Yang Y, Qin J, Li H. 2021. Low Cd-accumulating rice intercropping with Sesbania cannabina L. reduces grain Cd while promoting phytoremediation of Cd-contaminated soil. Science of the Total Environment800, 149600.

Kang Z, Zhang W, Qin J, Li S, Yang X, Wei X, Li H. 2020. Yield advantage and cadmium decreasing of rice in intercropping with water spinach under moisture management. Ecotoxicology and Environmental Safety190, 110102.

Khairy M, El-Safty S A, Shenashen M A. 2014. Environmental remediation and monitoring of cadmium. TrAC Trends in Analytical Chemistry62, 56–68.

Lam M H, Tjia A Y, Chan C, Chan W, Lee W. 1997. Speciation study of chromium, copper and nickel in coastal estuarine sediments polluted by domestic and industrial effluents. Marine Pollution Bulletin34, 949–959.

Lei L, Zhu Q, Xu P, Jing Y. 2021. The intercropping and arbuscular mycorrhizal fungus decrease Cd accumulation in upland rice and improve phytoremediation of Cd-contaminated soil by Sphagneticola calendulacea (L.) Pruski. Journal of Environmental Management298, 113516.

Li H, Luo N, Zhang L J, Zhao H M, Li Y W, Cai Q Y, Wong M H, Mo C H. 2016. Do arbuscular mycorrhizal fungi affect cadmium uptake kinetics, subcellular distribution and chemical forms in rice? Science of the Total Environment571, 1183–1190.

Li M, Wang W, Yin H, Chen Y, Ashraf M, Tao H, Li S, Wang W, Yang C, Xiao Y, Zhu L, Xiong Y. 2025. The functional role of arbuscular mycorrhizal fungi in enhancing soil organic carbon stocks and stability in dryland. Soil and Tillage Research 248, 106443.

Li X, Wang Y, Guo P, Zhang Z, Cui X, Hao B, Guo W. 2023. Arbuscular mycorrhizal fungi facilitate Astragalus adsurgens growth and stress tolerance in cadmium and lead contaminated saline soil by regulating rhizosphere bacterial community. Applied Soil Ecology187, 104842.

Luo N, Li X, Chen A Y, Zhang L J, Zhao H M, Xiang L, Cai Q Y, Mo C H, Wong M H, Li H. 2017. Does arbuscular mycorrhizal fungus affect cadmium uptake and chemical forms in rice at different growth stages? Science of the Total Environment599, 1564–1572.

Meena R S, Vijayakumar V, Yadav G S, Mitran T. 2018. Response and interaction of Bradyrhizobium japonicum and arbuscular mycorrhizal fungi in the soybean rhizosphere. Plant Growth Regulation84, 207–223.

Ng C W W, San S P, Wong J T F, Lau S Y. 2023. Intercropping of Pinellia ternata (herbal plant) with Sedum alfredii (Cd-hyperaccumulator) to reduce soil cadmium (Cd) absorption and improve yield. Environmental Pollution318, 120930.

Qiao X, Bei S, Li H, Christie P, Zhang F, Zhang J. 2016. Arbuscular mycorrhizal fungi contribute to overyielding by enhancing crop biomass while suppressing weed biomass in intercropping systems. Plant and Soil406, 173–185.

Rai P K, Sonne C, Kim K H. 2023. Heavy metals and arsenic stress in food crops: Elucidating antioxidative defense mechanisms in hyperaccumulators for food security, agricultural sustainability, and human health. Science of the Total Environment874, 162327.

Song C, Wang W, Gan Y, Wang L, Chang X, Wang Y, Yang W. 2022. Growth promotion ability of phosphate-solubilizing bacteria from the soybean rhizosphere under maize–soybean intercropping systems. Journal of the Science of Food and Agriculture102, 1430–1442.

Subramanian K S, Meranger J C, MacKeen J E. 1983. Graphite furnace atomic absorption spectrometry with matrix modification for determination of cadmium and lead in human urine. Analytical Chemistry55, 1064–1067.

Sun B, Zhao F J, Lombi E, McGrath S P. 2001. Leaching of heavy metals from contaminated soils using EDTA. Environmental Pollution113, 111–120.

Tessier A, Campbell P G C, Bisson M. 1979. Sequential extraction procedure for the speciation of particulate trace metals. Analytical Chemistry51, 844–851.

Wang J, Lu X, Zhang J, Ouyang Y, Wei G, Xiong Y. 2020. Rice intercropping with alligator flag (Thalia dealbata): A novel model to produce safe cereal grains while remediating cadmium contaminated paddy soil. Journal of Hazardous Materials394, 122505.

Wang Q, Que X. 2013. Phytoremediation-a green approach to environmental clean-up. Chinese Journal of Eco-Agriculture21, 261–266. (in Chinese)

Wang W, Chen G, Li M, Chen Y, Wang Y, Tao H, Hou H, Rehman M M U, Ashraf M, Song Y, Kavagi L, Wang B, Xiong Y. 2024. Long-term cereal-legume intercropping accelerates soil organic carbon loss in subsoil of dryland. ResourcesConservation and Recycling211, 107898.

Wang Z, Zhang J, Christie P, Li X. 2008. Influence of inoculation with Glomus mosseae or Acaulospora morrowiae on arsenic uptake and translocation by maize. Plant and Soil311, 235–244.

Wen B, Zhang X, Ren S, Duan Y, Zhang Y, Zhu X, Wang Y, Ma Y, Fang W. 2020. Characteristics of soil nutrients, heavy metals and tea quality in different intercropping patterns. Agroforestry Systems94, 963–974.

Yan Z, Chu J, Nie J, Qu X, Sanchez-Rodriguez A R, Yang Y, Pavinato P S, Zeng Z, Zang H. 2024. Legume-based crop diversification with optimal nitrogen fertilization benefits subsequent wheat yield and soil quality. AgricultureEcosystems & Environment374, 109171.

Yang X, Qin J, Li J, Lai Z, Li H. 2021. Upland rice intercropping with Solanum nigrum inoculated with arbuscular mycorrhizal fungi reduces grain Cd while promoting phytoremediation of Cd-contaminated soil. Journal of Hazardous Materials406, 124325.

Yu Y, Stomph T J, Makowski D, Van der Werf W. 2015. Temporal niche differentiation increases the land equivalent ratio of annual intercrops: A meta-analysis. Field Crops Research184, 133–144.

Zhang R, Huang Y, Liu Y, Liu Q, Zhang L, Li Z, Xu Y, Lin L, Wang L. 2023. Effects of mutual intercropping on cadmium accumulation of Solanum photeinocarpum Nakamura et Odashima and its post-grafting generations. International Journal of Phytoremediation25, 350–358.

Zhang Y, Sun Z, Su Z, Du G, Bai W, Wang Q, Wang R, Nie J, Sun T, Feng C, Zhang Z, Yang N, Zhang X, Evers J B, Van der Werf W, Zhang L. 2022. Root plasticity and interspecific complementarity improve yields and water use efficiency of maize/soybean intercropping in a water-limited condition. Field Crops Research282, 108523.

Zou M M, Zhou S L, Zhou Y J, Jia Z Y, Guo T W, Wang J X. 2021. Cadmium pollution of soil–rice ecosystems in rice cultivation dominated regions in China: A review. Environmental Pollution280, 116965.

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