Role of arbuscular mycorrhizal fungi in cadmium tolerance in rice (Oryza sativa L): a meta-analysis

Main Article Content

Ximei Li
Ruiyong Jing
Liyan Wang
Nan Wu
Zhenhua Guo


absorption, bacteria, rice, pollution, soil


Rice is an important agricultural product consumed globally. Rice polluted by cadmium (Cd) poses serious health risks. Numerous studies have shown that arbuscular mycorrhizal fungi (AMF) decrease Cd concentrations in the grain, shoots, and roots of rice. However, one study showed that AMF increased the root Cd concentration in rice. Therefore, a meta-analysis of the contribution of AMF to rice Cd tolerance became necessary. This meta-analysis was conducted to analyze the role of AMF in Cd tolerance in rice by searching the following databases: ProQuest, PubMed, Scopus, and ScienceDirect. A total of 571 studies were found, of which nine studies and 25 datasets were used in the meta-analysis. The period of inclusion of research reports was from January 1992 to April 2022. The results showed that with the addition of Rhizophagus irregularis, Cd concentration in the roots was higher than in the control group, although the overall Cd concentration in the plant was reduced. Four species of AMF reduced Cd concentration in rice shoots and grain tissues. These AMF species increased the biomass of rice root and shoot tissues; however, they did not affect grain biomass. AMF decreased the transfer factor (TF), and the TF of Glomus versiforme (12.99%) was significantly lower than the other three AMF types. We proposed that Cd could be enriched in rice roots, and the transfer of Cd to the grain could be inhibited. At the time of grain harvesting, rice roots are removed from the soil, thus removing Cd from the soil. This operation can efficiently improve both land-bearing capacity and soil without affecting rice yield. Thus, Cd was enriched in rice roots, and the potential for Cd transfer to the grain was inhibited due to the decreased TF. The future research must focus on how R. irregularis could improve the HMA3 gene expression in rice root, and prevents the transportation of Cd from the roots to shoots.

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Cantamessa, S., Massa, N., Gamalero, E. and Berta, G., 2020. Phytoremediation of a highly arsenic polluted site, using Pteris vittata L. and arbuscular mycorrhizal fungi. Plants (Basel) 9(9): 1211. 10.3390/plants9091211

Chen, X.W., Wu, L., Luo, N., Mo, C.H., Wong, M.H. and Li, H., 2019. Arbuscular mycorrhizal fungi and the associated bacterial community influence the uptake of cadmium in rice. Geoderma 337: 749–757. 10.1016/j.geoderma.2018.10.029

Chen, X., Zhang, Z., Gu, M., Li, H., Shohag, M.J.I., Shen, F., et al. 2020. Combined use of arbuscular mycorrhizal fungus and selenium fertilizer shapes microbial community structure and enhances organic selenium accumulation in rice grain. Science of the Total Environment 748: 141166. 10.1016/j.scitotenv.2020.141166

Eslami, M., Mashak, Z., Heshmati, A., Shokrzadeh, M. and Mozaffari Nejad, A.S., 2015. Determination of aflatoxin B1 levels in Iranian rice by ELISA method. Toxin Reviews 34(3): 125–128. 10.3109/15569543.2015.1074925

Gao, M.Y., Chen, X.W., Huang, W.X., Wu, L., Yu, Z.S., Xiang, L., et al. 2021. Cell wall modification induced by an arbuscular mycorrhizal fungus enhanced cadmium fixation in rice root. Journal of Hazardous Materials 416: 125894. 10.1016/j.jhazmat.2021.125894

Guo, Z., Islam, M.S., Liu, D., Liu, G., Lv, L., Yang, Y., et al. 2018. Differential effects of follistatin on porcine oocyte competence and cumulus cell gene expression in vitro. Reproduction in Domestic Animals 53(1): 3–10. 10.1111/rda.13035

Guo, Z., Lv, L., Liu, D., He, X., Wang, W., Feng, Y., et al. 2022. A global meta-analysis of animal manure application and soil microbial ecology based on random control treatments. PLoS One 17(1): e0262139. 10.1371/journal.pone.0262139

He, G., Liu, X. and Cui, Z., 2021. Achieving global food security by focusing on nitrogen efficiency potentials and local production. Global Food Security 29: 100536. 10.1016/j.gfs.2021.100536

Huang, X., An, G., Zhu, S., Wang, L. and Ma, F., 2018. Can Cd translocation in Oryza sativa L. be attenuated by arbuscular mycorrhizal fungi in the presence of EDTA? Environmental Science and Pollution Research (ESPR) 25(10): 9380–9390. 10.1007/s11356-017-1157-x

Huang, Y., Wang, L., Wang, W., Li, T., He, Z. and Yang, X., 2019. Current status of agricultural soil pollution by heavy metals in China: a meta-analysis. Science of the Total Environment 651(Pt 2): 3034–3042. 10.1016/j.scitotenv.2018.10.185

Jaffre, T., Pillon, Y., Thomine, S. and Merlot, S., 2013. The metal hyperaccumulators from New Caledonia can broaden our understanding of nickel accumulation in plants. Frontiers in Plant Science 4: 279. 10.3389/fpls.2013.00279

Jiang, Y., Luan, L., Hu, K., Liu, M., Chen, Z., Geisen, S., et al. 2020. Trophic interactions as determinants of the arbuscular mycorrhizal fungal community with cascading plant-promoting consequences. Microbiome 8(1): 142. 10.1186/s40168-020-00918-6

Kloppholz, S., Kuhn, H. and Requena, N., 2011. A secreted fungal effector of Glomus intraradices promotes symbiotic biotrophy. Current Biology 21(14): 1204–1209. 10.1016/j.cub.2011.06.044

Kobayashi, Y., Maeda, T., Yamaguchi, K., Kameoka, H., Tanaka, S., Ezawa, T., et al. 2018. The genome of Rhizophagus clarus HR1 reveals a common genetic basis for auxotrophy among arbuscular mycorrhizal fungi. BMC Genomics 19(1): 465. 10.1186/s12864-018-4853-0

Kumar, S., Prasad, S., Yadav, K.K., Shrivastava, M., Gupta, N., Nagar, S., et al. 2019. Hazardous heavy metals contamination of vegetables and food chain: role of sustainable remediation approaches—a review. Environmental Research 179(Pt A): 108792. 10.1016/j.envres.2019.108792

Lei, L.L., Zhu, Q.Y., Xu, P.X. and Jing, Y.X., 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. 10.1016/j.jenvman.2021.113516

Li, H., Chen, X.W., Wu, L., Luo, N., Huang, W.X., Mo, C.H., et al. 2020. Effects of arbuscular mycorrhizal fungi on redox homeostasis of rice under Cd stress. Plant and Soil 455(1): 121–138. 10.1007/s11104-020-04678-y

Li, H., Gao, M.Y., Mo, C.H., Wong, M.H., Chen, X.W. and Wang, J.J., 2022. Potential use of arbuscular mycorrhizal fungi for simultaneous mitigation of arsenic and cadmium accumulation in rice. Journal of Experimental Botany 73(1): 50–67. 10.1093/jxb/erab444

Li, H., Luo, N., Zhang, L.J., Zhao, H.M., Li, Y.W., Cai, Q.Y., et al. 2016. Do arbuscular mycorrhizal fungi affect cadmium uptake kinetics, subcellular distribution and chemical forms in rice? Science of the Total Environment 571: 1183–1190. 10.1016/j.scitotenv.2016.07.124

Luo, J.S., Huang, J., Zeng, D.L., Peng, J.S., Zhang, G.B., Ma, H.L., et al. 2018. A defensin-like protein drives cadmium efflux and allocation in rice. Nature Communications 9(1): 645. 10.1038/s41467-018-03088-0

Luo, N., Li, X., Chen, A.Y., Zhang, L.J., Zhao, H.M., Xiang, L., et al. 2017. Does arbuscular mycorrhizal fungus affect cadmium uptake and chemical forms in rice at different growth stages? Science of the Total Environment 599–600: 1564–1572. 10.1016/j.scitotenv.2017.05.047

Ma, S., Wang, Z., Guo, X., Wang, F., Huang, J., Sun, B., et al. 2021. Sourdough improves the quality of whole-wheat flour products: mechanisms and challenges—a review. Food Chemistry 360: 130038. 10.1016/j.foodchem.2021.130038

Maillard, E. and Angers, D.A., 2014. Animal manure application and soil organic carbon stocks: a meta-analysis. Global Change Biology 20(2): 666–679. 10.1111/gcb.12438

Majeed, A., Niaz, A., Rizwan, M., Imran, M., Alsahli, A.A., Alyemeni, M.N., et al. 2021. Effects of biochar, farm manure, and pressmud on mineral nutrients and cadmium availability to wheat (Triticum aestivum L.) in Cd-contaminated soil. Physiologia Plantarum 173(1): 191–200. 10.1111/ppl.13348

Malar, C.M., Kruger, M., Kruger, C., Wang, Y., Stajich, J.E., Keller, J., et al. 2021. The genome of Geosiphon pyriformis reveals ancestral traits linked to the emergence of the arbuscular mycorrhizal symbiosis. Current Biology 31(7): 1570–1577 e1574. 10.1016/j.cub.2021.01.058

Martin, F.M., Uroz, S. and Barker, D.G., 2017. Ancestral alliances: plant mutualistic symbioses with fungi and bacteria. Science 356(6340): eaad4501. 10.1126/science.aad4501

Morin, E., Miyauchi, S., San Clemente, H., Chen, E.C.H., Pelin, A., de la Providencia, I., et al. 2019. Comparative genomics of Rhizophagus irregularis, R. cerebriforme, R. diaphanus and Gigaspora rosea highlights specific genetic features in glomeromycotina. New Phytologist 222(3): 1584–1598. 10.1111/nph.15687

Orlowska, E., Przybylowicz, W., Orlowski, D., Turnau, K. and Mesjasz-Przybylowicz, J., 2011. The effect of mycorrhiza on the growth and elemental composition of Ni-hyperaccumulating plant Berkheya coddii Roessler. Environmental Pollution 159(12): 3730–3738. 10.1016/j.envpol.2011.07.008

Pan, J., Cao, S., Xu, G., Rehman, M., Li, X., Luo, D., et al. 2022. Comprehensive analysis reveals the underlying mechanism of arbuscular mycorrhizal fungi in kenaf cadmium stress alleviation. Chemosphere 314: 137566. 10.2139/ssrn.4267813

Sarmast, E., Fallah, A.A., Jafari, T. and Mousavi Khaneghah, A., 2021. Occurrence and fate of mycotoxins in cereals and cereal-based products: a narrative review of systematic reviews and meta-analyses studies. Current Opinion in Food Science 39: 68–75. 10.1016/j.cofs.2020.12.013

Snelders, N.C., Rovenich, H., Petti, G.C., Rocafort, M., van den Berg, G.C.M., Vorholt, J.A., et al. 2020. Microbiome manipulation by a soil-borne fungal plant pathogen using effector proteins. Nature Plants 6(11): 1365–1374. 10.1038/s41477-020-00799-5

Sun, X., Chen, W., Ivanov, S., MacLean, A.M., Wight, H., Ramaraj, T., et al. 2019. Genome and evolution of the arbuscular mycorrhizal fungus Diversispora epigaea (formerly Glomus versiforme) and its bacterial endosymbionts. New Phytologist 221(3): 1556–1573. 10.1111/nph.15472

Tang, L., Dong, J., Qu, M., Lv, Q., Zhang, L., Peng, C., et al. 2022. Knockout of OsNRAMP5 enhances rice tolerance to cadmium toxicity in response to varying external cadmium concentrations via distinct mechanisms. Science of the Total Environment 832: 155006. 10.1016/j.scitotenv.2022.155006

Tang, L., Mao, B., Li, Y., Lv, Q., Zhang, L., Chen, C., et al. 2017. Knockout of OsNramp5 using the CRISPR/Cas9 system produces low Cd-accumulating indica rice without compromising yield. Scientific Reports, 7(1): 14438. 10.1038/s41598-017-14832-9

Tisarum, R., Theerawitaya, C., Samphumphuang, T., Polispitak, K., Thongpoem, P., Singh, H.P., et al. 2020. Alleviation of salt stress in upland rice (Oryza sativa L. ssp. indica cv. leum pua) using arbuscular mycorrhizal fungi inoculation. Frontiers in Plant Science 11: 348. 10.3389/fpls.2020.00348

Uraguchi, S., Kamiya, T., Clemens, S. and Fujiwara, T., 2014. Characterization of OsLCT1, a cadmium transporter from indica rice (Oryza sativa). Physiologia Plantarum 151(3): 339–347. 10.1111/ppl.12189

Vallino, M., Fiorilli, V. and Bonfante, P., 2014. Rice flooding negatively impacts root branching and arbuscular mycorrhizal colonization, but not fungal viability. Plant, Cell & Environment 37(3): 557–572. 10.1111/pce.12177

Venice, F., Ghignone, S., Salvioli di Fossalunga, A., Amselem, J., Novero, M., Xianan, X., et al. 2020. At the nexus of three kingdoms: the genome of the mycorrhizal fungus Gigaspora margarita provides insights into plant, endobacterial and fungal interactions. Environmental Microbiology 22(1): 122–141. 10.1111/1462-2920.14827

Wang, H.Q., Xuan, W., Huang, X.Y., Mao, C. and Zhao, F.J., 2021. Cadmium inhibits lateral root emergence in rice by disrupting OsPIN-mediated auxin distribution and the protective effect of Os HMA3. Plant & Cell Physiology 62(1): 166–177. 10.1093/pcp/pcaa150

Wang, P., Yamaji, N., Inoue, K., Mochida, K. and Ma, J.F., 2020. Plastic transport systems of rice for mineral elements in response to diverse soil environmental changes. New Phytologist 226(1): 156–169. 10.1111/nph.16335

Xiao, W., Ye, X., Zhu, Z., Zhang, Q., Zhao, S., Chen, D., et al. 2020. Evaluation of cadmium (Cd) transfer from paddy soil to rice (Oryza sativa L.) using DGT in comparison with conventional chemical methods: derivation of models to predict Cd accumulation in rice grains. Environmental Science and Pollution Research (ESPR) 27(13): 14953–14962. 10.1007/s11356-020-07976-1

Yamaji, N., Xia, J., Mitani-Ueno, N., Yokosho, K. and Feng Ma, J., 2013. Preferential delivery of zinc to developing tissues in rice is mediated by P-type heavy metal ATPase OsHMA2. Plant Physiology 162(2): 927–939. 10.1104/pp.113.216564

Yan, H., Xu, W., Xie, J., Gao, Y., Wu, L., Sun, L., et al. 2019. Variation of a major facilitator superfamily gene contributes to differential cadmium accumulation between rice subspecies. Nature Communications 10(1): 2562. 10.1038/s41467-019-10544-y

Yang, X., Qin, J., Li, J., Lai, Z. and 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. 10.1016/j.jhazmat.2020.124325

Yildirir, G., Sperschneider, J., Malar, C.M., Chen, E.C.H., Iwasaki, W., Cornell, C., et al. 2022. Long reads and Hi-C sequencing illuminate the two-compartment genome of the model arbuscular mycorrhizal symbiont Rhizophagus irregularis. New Phytologist 233(3): 1097–1107. 10.1111/nph.17842

Yu, Z., Zhao, X., Liang, X., Li, Z., Wang, L., He, Y., et al. 2022. Arbuscular mycorrhizal fungi reduce cadmium leaching from sand columns by reducing availability and enhancing uptake by maize roots. Journal of Fungi (Basel), 8(8):866. 10.3390/jof8080866

Zhang, X.-H., Lin, A.-J., Gao, Y.-L., Reid, R.J., Wong, M.-H. and Zhu, Y.-G., 2009. Arbuscular mycorrhizal colonisation increases copper binding capacity of root cell walls of Oryza sativa L. and reduces copper uptake. Soil Biology and Biochemistry 41(5): 930–935. 10.1016/j.soilbio.2008.08.011

Zhang, L., Zhou, J., George, T.S., Limpens, E. and Feng, G., 2022. Arbuscular mycorrhizal fungi conducting the hyphosphere bacterial orchestra. Trends in Plant Science 27(4): 402–411. 10.1016/j.tplants.2021.10.008

Zhou, X., Cao, Q., Orfila, C., Zhao, J. and Zhang, L., 2021. Systematic review and meta-analysis on the effects of Astaxanthin on human skin ageing. Nutrients 13(9):2917. 10.3390/nu13092917

Zhou, J., Chai, X., Zhang, L., George, T.S., Wang, F. and Feng, G., 2020. Different arbuscular mycorrhizal fungi cocolonizing on a single plant root system recruit distinct microbiomes. mSystems (ASM Journals) 5(6): e00929-20. 10.1128/mSystems.00929-20

Zhou, M., Li, X., Liu, X., Mi, Y., Fu, Z., Zhang, R., et al. 2022. Effects of antimony on rice growth and its existing forms in rice under arbuscular mycorrhizal fungi environment. Frontiers in Microbiology 13: 814323. 10.3389/fmicb.2022.814323

Zhu, H., Chen, C., Xu, C., Zhu, Q. and Huang, D., 2016. Effects of soil acidification and liming on the phytoavailability of cadmium in paddy soils of central subtropical China. Environmental Pollution 219: 99–106. 10.1016/j.envpol.2016.10.043

Zhu, Q., Xu, P., Lei, L. and Jing, Y., 2022. Transcriptome analysis reveals decreased accumulation and toxicity of Cd in upland rice inoculated with arbuscular mycorrhizal fungi. Applied Soil Ecology 177: 104501. 10.1016/j.apsoil.2022.104501