Please wait a minute...
Journal of Integrative Agriculture
Advanced Online Publication | Current Issue | Archive | Adv Search
Legume-cereal intercropping with AMF reduces cadmium bioavailability and enhance land productivity

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

1 The 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 

l 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).

l AMF inoculation synergistically enhances intercropping benefits, improving Cd removal efficiency (MRER>1) and crop resilience through enhanced nutrient uptake and improved rhizosphere soil health.

l 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.

Download:  PDF in ScienceDirect  
Export:  BibTeX | EndNote (RIS)      
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%) versus 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  
Online: 14 July 2025  
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. 2025. Legume-cereal intercropping with AMF reduces cadmium bioavailability and enhance land productivity. Journal of Integrative Agriculture, Doi:10.1016/j.jia.2025.07.017

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. Water, Air, & 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 Journals, 2, 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 Development, 44, 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 Science, 178, 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 Environment, 851, 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 Management, 348, 119284.

Curtright A J, Tiemann L K. 2021. Intercropping increases soil extracellular enzyme activity: A meta-analysis. Agriculture, Ecosystems & 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 phytologist, 84, 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 Plants, 10, 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 Pollution, 307, 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 ONE, 14, e213672.

Johnson J L, Temple K L. 1964. Some variables affecting the measurement of “catalase activity” in soil. Soil Science Society of America Journal, 28, 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 Environment, 800, 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 Safety, 190, 110102.

Khairy M, El-Safty S A, Shenashen M A. 2014. Environmental remediation and monitoring of cadmium. TrAC Trends in Analytical Chemistry, 62, 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 Bulletin, 34, 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 Management, 298, 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 Environment, 571, 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 Ecology, 187, 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 Environment, 599, 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 Regulation, 84, 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 Pollution, 318, 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 Soil, 406, 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 Environment, 874, 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 Agriculture, 102, 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 Chemistry, 55, 1064-1067.

Sun B, Zhao F J, Lombi E, McGrath S P. 2001. Leaching of heavy metals from contaminated soils using EDTA. Environmental Pollution, 113, 111-120.

Tessier A, Campbell P G C, Bisson M. 1979. Sequential extraction procedure for the speciation of particulate trace metals. Analytical Chemistry, 51, 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 Materials, 394, 122505.

Wang Q, Que X. 2013. Phytoremediation-a green approach to environmental clean-up. Chinese Journal of Eco-Agriculture, 21, 261-266.

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. Resources, Conservation and Recycling, 211, 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 Soil, 311, 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 Systems, 94, 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. Agriculture, Ecosystems & Environment, 374, 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 Materials, 406, 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 Research, 184, 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 Phytoremediation, 25, 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 Pollution, 280, 116965.

[1] Runnan Zhou, Sihui Wang, Peiyan Liu, Yifan Cui, Zhenbang Hu, Chunyan Liu, Zhanguo Zhang, Mingliang Yang, Xin Li, Xiaoxia Wu, Qingshan Chen, Ying Zhao. Genome-wide characterization of soybean malate dehydrogenase genes reveals a positive role for GmMDH2 in the salt stress response[J]. >Journal of Integrative Agriculture, 2025, 24(7): 2492-2510.
[2] Dan Lü, Jianxin Li, Xuehai Zhang, Ran Zheng, Aoni Zhang, Jingyun Luo, Bo Tong, Hongbing Luo, Jianbing Yan, Min Deng. Genetic analysis of maize crude fat content by multi-locus genome-wide association study[J]. >Journal of Integrative Agriculture, 2025, 24(7): 2475-2491.
[3] Lihua Xie, Lingling Li, Junhong Xie, Jinbin Wang, Zechariah Effah, Setor Kwami Fudjoe, Muhammad Zahid Mumtaz. A suitable organic fertilizer substitution ratio stabilizes rainfed maize yields and reduces gaseous nitrogen loss in the Loess Plateau, China[J]. >Journal of Integrative Agriculture, 2025, 24(6): 2138-2154.
[4] Chunxiang Li, Yongfeng Song, Yong Zhu, Mengna Cao, Xiao Han, Jinsheng Fan, Zhichao Lü, Yan Xu, Yu Zhou, Xing Zeng, Lin Zhang, Ling Dong, Dequan Sun, Zhenhua Wang, Hong Di. GWAS analysis reveals candidate genes associated with density tolerance (ear leaf structure) in maize (Zea mays L.)[J]. >Journal of Integrative Agriculture, 2025, 24(6): 2046-2062.
[5] Berhane S. Gebregziabher, Shengrui Zhang, Jing Li, Bin Li, Junming Sun. Identification of genomic regions and candidate genes underlying carotenoid accumulation in soybean using next-generation sequen-cing based bulk segregant analysis[J]. >Journal of Integrative Agriculture, 2025, 24(6): 2063-2079.
[6] Qianqian Shi, Xue Han, Xinhao Zhang, Jie Zhang, Qi Fu, Chen Liang, Fangmeng Duan, Honghai Zhao, Wenwen Song. Transcriptome-wide N6-methyladenosine (m6A) profiling of compatible and incompatible responses reveals a nonhost resistance-specific m6A modification involved in soybean–soybean cyst nematode interaction[J]. >Journal of Integrative Agriculture, 2025, 24(5): 1875-1891.
[7] Huairen Zhang, Tauseef Taj Kiani, Huabang Chen, Juan Liu, Xunji Chen. Genome wide association analysis reveals multiple QTLs controlling root development in maize [J]. >Journal of Integrative Agriculture, 2025, 24(5): 1656-1670.
[8] Lanjie Zheng, Qianlong Zhang, Huiying Liu, Xiaoqing Wang, Xiangge Zhang, Zhiwei Hu, Shi Li, Li Ji, Manchun Ji, Yong Gu, Jiaheng Yang, Yong Shi, Yubi Huang, Xu Zheng. Fine mapping and discovery of MIR172e, a candidate gene required for inflorescence development and lower floret abortion in maize ear[J]. >Journal of Integrative Agriculture, 2025, 24(4): 1372-1389.
[9] Dong An, Xingfa Lai, Tianfu Han, Jean Marie Vianney Nsigayehe, Guixin Li, Yuying Shen. Crossing latitude introduction delayed flowering and facilitated dry matter accumulation of soybean as a forage crop[J]. >Journal of Integrative Agriculture, 2025, 24(4): 1436-1447.
[10] Xiaoxia Guo, Wanmao Liu, Yunshan Yang, Guangzhou Liu, Bo Ming, Ruizhi Xie, Keru Wang, Shaokun Li, Peng Hou. Matching the light and nitrogen distributions in the maize canopy to achieve high yield and high radiation use efficiency[J]. >Journal of Integrative Agriculture, 2025, 24(4): 1424-1435.
[11] Yang Wang, Chunhua Mu, Xiangdong Li, Canxing Duan, Jianjun Wang, Xin Lu, Wangshu Li, Zhennan Xu, Shufeng Sun, Ao Zhang, Zhiqiang Zhou, Shenghui Wen, Zhuanfang Hao, Jienan Han, Jianzhou Qu, Wanli Du, Fenghai Li, Jianfeng Weng. A genome-wide association study and transcriptome analysis reveal the genetic basis for the Southern corn rust resistance in maize[J]. >Journal of Integrative Agriculture, 2025, 24(2): 453-466.
[12] Jia Jia, Huan Wang, Ximeng Yang, Bo Chen, Ruqian Wei, Qibin Ma, Yanbo Cheng, Hai Nian. Identification of long InDels through whole genome resequencing to fine map qIF05-1 for seed isoflavone content in soybean (Glycine max L. Merr.) [J]. >Journal of Integrative Agriculture, 2025, 24(1): 85-100.
[13] Xin Dong, Baole Li, Zhenzhen Yan, Ling Guan, Shoubing Huang , Shujun Li, Zhiyun Qi, Ling Tang, Honglin Tian, Zhongjun Fu, Hua Yang. Impacts of high temperature, relative air humidity, and vapor pressure deficit on the seed set of contrasting maize genotypes during flowering[J]. >Journal of Integrative Agriculture, 2024, 23(9): 2955-2969.
[14] Peng Liu, Langlang Ma, Siyi Jian, Yao He, Guangsheng Yuan, Fei Ge, Zhong Chen, Chaoying Zou, Guangtang Pan, Thomas Lübberstedt, Yaou Shen. Population genomic analysis reveals key genetic variations and the driving force for embryonic callus induction capability in maize[J]. >Journal of Integrative Agriculture, 2024, 23(7): 2178-2195.
[15] Hui Chen, Hongxing Chen, Song Zhang, Shengxi Chen, Fulang Cen, Quanzhi Zhao, Xiaoyun Huang, Tengbing He, Zhenran Gao. Comparison of CWSI and Ts-Ta-VIs in moisture monitoring of dryland crops (sorghum and maize) based on UAV remote sensing[J]. >Journal of Integrative Agriculture, 2024, 23(7): 2458-2475.
No Suggested Reading articles found!