The roles and performance of arbuscular mycorrhizal fungi in intercropping systems

Highlights

• Metabolic and non-metabolic benefits of AM fungi under intercropping were reviewed.

• Changes of AM fungi themselves respond to intercropping practices were summarized.

• Mechanistic understanding the synergy between intercropping and AM fungi is needed.

• It’s valuable to harness AM fungal benefits for maximizing intercropping production.

Abstract

Intercropping, which gains productivity and ecological benefits through plant facilitative interactions, is a practice often associated with sustainable agriculture. In such systems, arbuscular mycorrhizal (AM) fungi and the hyphal networks play key roles in plant facilitation by promoting connectivity, mediating interplant transfer of metabolic resources, and managing weeds, pathogens, and contaminants. This review states that the symmetrically or unsymmetrically delivered resources via AM fungi are imperative to maintain facilitative interactions between intercrops. In addition, the responses of AM fungi to intercropping are also discussed, including changes in abundance, diversity, community composition and colonization level. Although general proliferations in AM fungi via intercropping have been shown, the plant hosts and neighbors may exert different influences on AM fungi. Therefore, further research is needed in quantifying the mediating role of AM fungi on outputs of intercropping systems, clarifying the driving forces, and exploring the causation between these processes and the changes in AM fungi themselves. To conclude, the integration with AM fungi extends the understanding of key soil biological processes driving plant facilitation and will guide efforts to optimizing intercropping systems.

Graphical abstract

Keywords

Agriculture sustainability / Contaminant / Mycorrhizal networks / Pathogen / Plant facilitation / Weed

References

[1] Achatz, M., Rillig, M.C., 2014. Arbuscular mycorrhizal fungal hyphae enhance transport of the allelochemical juglone in the field. Soil Biology & Biochemistry 78, 76–82

[2] Arantes, A.C.C., Cotta, S.R., da Conceicao, P.M., Meneghin, S.P., Martinelli, R., Prospero, A.G., Boaretto, R.M., Andreote, F.D., Mattos, D., de Azevedo, F.A., 2020. Implication of Urochloa spp. intercropping and conservation agriculture on soil microbiological quality and yield of Tahiti acid lime in long term orchard experiment. Agriculture 10, 491

[3] Babikova, Z., Gilbert, L., Bruce, T.J.A., Birkett, M., Caulfield, J.C., Woodcock, C., Pickett, J.A., Johnson, D., 2013. Underground signals carried through common mycelial networks warn neighbouring plants of aphid attack. Ecology Letters 16, 835–843

[4] Bahadur, A., Jin, Z., Long, X., Jiang, S., Zhang, Q., Pan, J., Liu, Y., Feng, H., 2019. Arbuscular mycorrhizal fungi alter plant interspecific interaction under nitrogen fertilization. European Journal of Soil Biology 93, 103094

[5] Bainard, L.D., Klironomos, J.N., Gordon, A.M., 2011. Arbuscular mycorrhizal fungi in tree-based intercropping systems: A review of their abundance and diversity. Pedobiologia 54, 57–61

[6] Bainard, L.D., Koch, A.M., Gordon, A.M., Klironomos, J.N., 2012. Temporal and compositional differences of arbuscular mycorrhizal fungal communities in conventional monocropping and tree-based intercropping systems. Soil Biology & Biochemistry 45, 172–180

[7] Barea, J.M., Werner, D., Azcon-Guilar, C., Azcon, R., 2005. Interactions of arbuscular mycorrhiza and nitrogen- fixing symbiosis in sustainable agriculture. In: Werner, D., Newton, W.E. (eds.), Nitrogen Fixation in Agriculture, Forestry, Ecology, and the Environment. Dordrecht: Springer, 199–222.

[8] Barto, E.K., Hilker, M., Muller, F., Mohney, B.K., Weidenhamer, J.D., Rillig, M.C., 2011. The fungal fast lane: Common mycorrhizal networks extend bioactive zones of allelochemicals in soils. PLoS One 6, e27195

[9] Barto, E.K., Weidenhamer, J.D., Cipollini, D., Rillig, M.C., 2012. Fungal superhighways: do common mycorrhizal networks enhance below ground communication? Trends in Plant Science 17, 633–637

[10] Bini, D., dos Santos, C.A., da Silva, M.C.P., Bonfim, J.A., Cardoso, E., 2018. Intercropping Acacia mangium stimulates AMF colonization and soil phosphatase activity in Eucalyptus grandis. Scientia Agricola 75, 102–110

[11] Birhane, E., Gebremeskel, K., Taddesse, T., Hailemariam, M., Hadgu, K.M., Norgrove, L., Negussie, A., 2018. Integrating Faidherbia albida trees into a sorghum field reduces striga infestation and improves mycorrhiza spore density and colonization. Agroforestry Systems 92, 643–653

[12] Boudreau, M.A., 2013. Diseases in intercropping systems. Annual Review of Phytopathology 51, 499–519

[13] Brooker, R.W., Bennett, A.E., Cong, W.F., Daniell, T.J., George, T.S., Hallett, P.D., Hawes, C., Iannetta, P.P.M., Jones, H.G., Karley, A.J., Li, L., McKenzie, B.M., Pakeman, R.J., Paterson, E., Schob, C., Shen, J., Squire, G., Watson, C.A., Zhang, C., Zhang, F., Zhang, J., White, P.J., 2015. Improving intercropping: a synthesis of research in agronomy, plant physiology and ecology. New Phytologist 206, 107–117

[14] Bruinsma, J., 2003. World Agriculture: Towards 2015/2030: An FAO Perspective. Landon: Earthscan.

[15] Brundrett, M.C., Tedersoo, L., 2018. Evolutionary history of mycorrhizal symbioses and global host plant diversity. New Phytologist 220, 1108–1115

[16] Caruso, C., Maucieri, C., Cavallaro, V., Borin, M., Barbera, A.C., 2018. Olive mill wastewater spreading and AMF inoculation effects in a low-input semi-arid Mediterranean crop succession. Archives of Agronomy and Soil Science 64, 2060–2074

[17] Chen, X., Tang, M., Zhang, X., Hamel, C., Liu, S., Huo, Y., Sheng, M., 2018. Effects of plant neighborhood on arbuscular mycorrhizal fungal attributes in afforested zones. Forest Ecology and Management 422, 253–262

[18] Chifflot, V., Rivest, D., Olivier, A., Cogliastro, A., Khasa, D., 2009. Molecular analysis of arbuscular mycorrhizal community structure and spores distribution in tree-based intercropping and forest systems. Agriculture, Ecosystems & Environment 131, 32–39

[19] de Freitas, M.A.M., Silva, D.V., Guimaraes, F.R., Leal, P.L., Moreira, F.M.D., da Silva, A.A., Souza, M.D., 2018. Biological attributes of soil cultivated with corn intercropped with Urochloa brizantha in different plant arrangements with and without herbicide application. Agriculture, Ecosystems & Environment 254, 35–40

[20] Dieng, A., Duponnois, R., Ndoye, I., Baudoin, E., 2017. Positive feedback with mycorrhizal fungi alleviates negative effects of intercropping the energy crop Jatropha curcas with Crotalaria retusa. Symbiosis 73, 107–116

[21] Dobo, B., Asefa, F., Asfaw, Z., 2018. Diversity and abundance of arbuscular mycorrhizal fungi under different plant and soil properties in Sidama, southern Ethiopia. Agroforestry Systems 92, 91–101

[22] Dong, Y., Zhu, Y., Smith, F.A., Wang, Y., Chen, B., 2008. Arbuscular mycorrhiza enhanced arsenic resistance of both white clover (Trifolium repens Linn.) and ryegrass (Lolium perenne L.) plants in an arsenic- contaminated soil. Environmental Pollution 155, 174–181

[23] Duchene, O., Vian, J.F., Celette, F., 2017. Intercropping with legume for agroecological cropping systems: Complementarity and facilitation processes and the importance of soil microorganisms. A review. Agriculture, Ecosystems & Environment 240, 148–161

[24] Egerton-Warburton, L.M., Querejeta, J.I., Allen, M.F., 2007. Common mycorrhizal networks provide a potential pathway for the transfer of hydraulically lifted water between plants. Journal of Experimental Botany 58, 1473–1483

[25] Ehrmann, J., Ritz, K., 2014. Plant: soil interactions in temperate multi-cropping production systems. Plant and Soil 376, 1–29

[26] Furze, J.R., Martin, A.R., Nasielski, J., Thevathasan, N.V., Gordon, A.M., Isaac, M.E., 2017. Resistance and resilience of root fungal communities to water limitation in a temperate agroecosystem. Ecology and Evolution 7, 3443–3454

[27] Gao, D., Pan, X., Zhou, X., Wei, Z., Li, N., Wu, F., 2020. Phosphorus fertilization and intercropping interactively affect tomato and potato onion growth and rhizosphere arbuscular mycorrhizal fungal community. Archives of Agronomy and Soil Science, 1–15

[28] Gianinazzi, S., Gollotte, A., Binet, M.N., van Tuinen, D., Redecker, D., Wipf, D., 2010. Agroecology: the key role of arbuscular mycorrhizas in ecosystem services. Mycorrhiza 20, 519–530

[29] Gong, X., Liu, C., Li, J., Luo, Y., Yang, Q., Zhang, W., Yang, P., Feng, B., 2019. Responses of rhizosphere soil properties, enzyme activities and microbial diversity to intercropping patterns on the Loess Plateau of China. Soil & Tillage Research 195, 104355

[30] Gorzelak, M.A., Asay, A.K., Pickles, B.J., Simard, S.W., 2015. Inter-plant communication through mycorrhizal networks mediates complex adaptive behaviour in plant communities. AoB Plants 7, plv050

[31] Gunes, A., Bagci, E.G., Inal, A., 2007. Interspecific facilitative root interactions and rhizosphere effects on phosphorus and iron nutrition between mixed grown chickpea and barley. Journal of Plant Nutrition 30, 1455–1469

[32] Gurr, G.M., Wratten, S.D., Luna, J.M., 2003. Multi-function agricultural biodiversity: pest management and other benefits. Basic and Applied Ecology 4, 107–116

[33] Hage-Ahmed, K., Krammer, J., Steinkellner, S., 2013. The intercropping partner affects arbuscular mycorrhizal fungi and Fusarium oxysporum f. sp. lycopersici interactions in tomato. Mycorrhiza 23, 543–550

[34] Hailemariam, M., Birhane, E., Asfaw, Z., Zewdie, S., 2013. Arbuscular mycorrhizal association of indigenous agroforestry tree species and their infective potential with maize in the rift valley, Ethiopia. Agroforestry Systems 87, 1261–1272

[35] Hajiboland, R., Sadeghzadeh, N., Moradtalab, N., Aliasgharzad, N., Schweikert, K., Poschenrieder, C., 2020. The arbuscular mycorrhizal mycelium from barley differentially influences various defense parameters in the non-host sugar beet under co-cultivation. Mycorrhiza 30, 647–661.

[36] Hamel, C., Smith, D.L., 1991. Interspecific N-transfer and plant development in a mycorrhizal field-grown mixture. Soil Biology & Biochemistry 23, 661–665

[37] Hauggaard-Nielsen, H., Jensen, E.S., 2005. Facilitative root interactions in intercrops. Plant and Soil 274, 237–250

[38] He, Y., Ding, N., Shi, J., Wu, M., Liao, H., Xu, J., 2013. Profiling of microbial PLFAs: Implications for interspecific interactions due to intercropping which increase phosphorus uptake in phosphorus limited acidic soils. Soil Biology & Biochemistry 57, 625–634

[39] Hu, J., Chan, P.T., Wu, F., Wu, S., Zhang, J., Lin, X., Wong, M.H., 2013a. Arbuscular mycorrhizal fungi induce differential Cd and P acquisition by Alfred stonecrop (Sedum alfredii Hance) and upland kangkong (Ipomoea aquatica Forsk.) in an intercropping system. Applied Soil Ecology 63, 29–35

[40] Hu, J., Li, J., Wu, F., Wu, S., Ye, Z., Lin, X., Wong, M.H., 2013b. Arbuscular mycorrhizal fungi induced differential Cd and P phytoavailability via intercropping of upland kangkong (Ipomoea aquatica Forsk.) with Alfred stonecrop (Sedum alfredii Hance): post-harvest study. Environmental Science and Pollution Research 20, 8457–8463

[41] Hu, J., Li, M., Liu, H., Zhao, Q., Lin, X., 2019. Intercropping with sweet corn (Zea mays L. var. rugosa Bonaf.) expands P acquisition channels of chili pepper (Capsicum annuum L.) via arbuscular mycorrhizal hyphal networks. Journal of Soils and Sediments 16, 1632–1639

[42] Hu, J., Wu, F., Wu, S., Lam, C.L., Lin, X., Wong, M.H., 2014. Biochar and Glomus caledonium influence Cd accumulation of upland kangkong (Ipomoea aquatica Forsk.) intercropped with Alfred stonecrop (Sedum alfredii Hance). Scientific Reports 4, 4671

[43] 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, e0213672

[44] Kumar, A., Choudhary, A.K., Suri, V.K., Rana, K.S., 2016. AM fungi lead to fertilizer phosphorus economy and enhanced system productivity and profitability in okra (Abelmoschus esculentus L.)-pea (Pisum sativum L.) cropping system in Himalayan acid Alfisol. Journal of Plant Nutrition 39, 1380–1390

[45] Leifheit, E.F., Veresoglou, S.D., Lehmann, A., Morris, E.K., Rillig, M.C., 2014. Multiple factors influence the role of arbuscular mycorrhizal fungi in soil aggregation-a meta-analysis. Plant and Soil 374, 523–537

[46] Li, L., Sun, S., Sun, J., Zhou, L., Bao, X., Zhang, H., Zhang, F., 2007. Diversity enhances agricultural productivity via rhizosphere phosphorus facilitation on phosphorus-deficient soils. Proceedings of the National Academy of Sciences of the United States of America 104, 11192–11196

[47] Li, L., Tilman, D., Lambers, H., Zhang, F., 2014. Plant diversity and overyielding: insights from belowground facilitation of intercropping in agriculture. New Phytologist 203, 63–69

[48] Li, Y., Ran, W., Zhang, R., Sun, S., Xu, G., 2009. Facilitated legume nodulation, phosphate uptake and nitrogen transfer by arbuscular inoculation in an upland rice and mung bean intercropping system. Plant and Soil 315, 285–296

[49] Lin, G., McCormack, M.L., Guo, D., 2015. Arbuscular mycorrhizal fungal effects on plant competition and community structure. Journal of Ecology 103, 1224–1232

[50] Liu, Y., Hou, S., Hu, J., Cai, P., Li, M., Wu, F., Lin, X., 2021. Intercropping with maize influences arbuscular mycorrhizal network formation and pepper Phytophthora blight suppression in facility sheds. Acta Pedologica Sinica DOI: 10.11766/trxb202102280112.

[51] Liu, Y., Zhao, Q., Deng, X., Wang, B., Zhang, N., Zong, Q., Xia, Y., 2020. Effects of indigenous arbuscular mycorrhizal fungi and nitrogen forms on plant nitrogen utilization and the influencing factors in a pepper-common bean intercropping system. Chinese Journal of Eco-Agriculture 28, 245–254.

[52] Malezieux, E., Crozat, Y., Dupraz, C., Laurans, M., Makowski, D., Ozier-Lafontaine, H., Rapidel, B., de Tourdonnet, S., Valantin-Morison, M., 2009. Mixing plant species in cropping systems: concepts, tools and models. A review. Agronomy for Sustainable Development 29, 43–62

[53] Martins, M.A., Cruz, A.F., 1998. The role of the external mycelial network of arbuscular mycorrhizal fungi: III. A study of nitrogen transfer between plants interconnected by a common mycelium. Revista de Microbiologia 29, 289–294

[54] Martins, M.A., Read, D.J., 1996. The role of the external mycelial network of arbuscular mycorrhizal (AM) fungi. 2. A study of phosphorous transfer between plants interconnected by a common mycelium. Revista de Microbiologia 27, 100–105.

[55] Meding, S.M., Zasoski, R.J., 2008. Hyphal-mediated transfer of nitrate, arsenic, cesium, rubidium, and strontium between arbuscular mycorrhizal forbs and grasses from a California oak woodland. Soil Biology & Biochemistry 40, 126–134

[56] Menezes, K.M.S., Silva, D.K.A., Queiroz, M.A.A., Felix, W.P., Yano-Melon, A.M., 2016. Arbuscular mycorrhizal fungal communities in buffelgrass pasture under intercropping and shading systems in Brazilian semiarid conditions. Agriculture, Ecosystems & Environment 230, 55–67

[57] Meng, L., Zhang, A., Wang, F., Han, X., Wang, D., Li, S., 2015. Arbuscular mycorrhizal fungi and rhizobium facilitate nitrogen uptake and transfer in soybean/maize intercropping system. Frontiers in Plant Science 6, 339

[58] Montesinos-Navarro, A., Segarra-Moragues, J.G., Valiente-Banuet, A., Verdu, M., 2012. Plant facilitation occurs between species differing in their associated arbuscular mycorrhizal fungi. New Phytologist 196, 835–844

[59] Montesinos-Navarro, A., Valiente-Banuet, A., Verdu, M., 2019. Processes underlying the effect of mycorrhizal symbiosis on plant-plant interactions. Fungal Ecology 40, 98–106

[60] Montesinos-Navarro, A., Verdu, M., Querejetac, J.I., Sortibran, L., Valiente-Banuet, A., 2016. Soil fungi promote nitrogen transfer among plants involved in long-lasting facilitative interactions. Perspectives in Plant Ecology, Evolution and Systematics 18, 45–51

[61] Moora, M., 2014. Mycorrhizal traits and plant communities: perspectives for integration. Journal of Vegetation Science 25, 1126–1132

[62] Njira, K.O.W., Semu, E., Mrema, J.P., Nalivata, P.C., 2017. Pigeon pea and cowpea-based cropping systems improve vesicular arbuscular mycorrhizal fungal colonisation of subsequent maize on the alfisols in central Malawi. International Journal of Microbiology 2017, 2096314

[63] Pereira, A.P.D., Santana, M.C., Bonfim, J.A., Mescolotti, D.D., Cardoso, E., 2018. Digging deeper to study the distribution of mycorrhizal arbuscular fungi along the soil profile in pure and mixed Eucalyptus grandis and Acacia mangium plantations. Applied Soil Ecology 128, 1–11

[64] Qiao, X., Bei, S., Li, C., Dong, Y., Li, H., Christie, P., Zhang, F., Zhang, J., 2015. Enhancement of faba bean competitive ability by arbuscular mycorrhizal fungi is highly correlated with dynamic nutrient acquisition by competing wheat. Scientific Reports 5, 8122

[65] 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

[66] Rajeshkumar, P.P., Thomas, G.V., Gupta, A., Gopal, M., 2015. Diversity, richness and degree of colonization of arbuscular mycorrhizal fungi in coconut cultivated along with intercrops in high productive zone of Kerala, India. Symbiosis 65, 125–141

[67] Ren, H., Gao, T., Hu, J., Yang, G., 2017. The effects of arbuscular mycorrhizal fungi and root interaction on the competition between Trifolium repens and Lolium perenne. PeerJ 5, e4183

[68] Ren, L., Lou, Y., Zhang, N., Zhu, X., Hao, W., Sun, S., Shen, Q., Xu, G., 2013. Role of arbuscular mycorrhizal network in carbon and phosphorus transfer between plants. Biology and Fertility of Soils 49, 3–11

[69] Robinson, D., Fitter, A., 1999. The magnitude and control of carbon transfer between plants linked by a common mycorrhizal network. Journal of Experimental Botany 50, 9–13

[70] Schuman, M.C., Baldwin, I.T., 2018. Field studies reveal functions of chemical mediators in plant interactions. Chemical Society Reviews 47, 5338–5353

[71] Shan, M., Qin, H., Chen, J., Xu, Q., 2018. Effects of two different intercropping systems on arbuscular mycorrhizal fungal colonization and polychlorinated biphenyl (PCB) dissipation. Chinese Journal of Applied and Environmental Biology 24, 470–477.

[72] Shukla, A., Kumar, A., Chaturvedi, O.P., Nagori, T., Kumar, N., Gupta, A., 2018. Efficacy of rhizobial and phosphate-solubilizing bacteria and arbuscular mycorrhizal fungi to ameliorate shade response on six pulse crops. Agroforestry Systems 92, 499–509.

[73] Simard, S.W., Durall, D.M., 2004. Mycorrhizal networks: a review of their extent, function, and importance. Canadian Journal of Botany 82, 1140–1165

[74] Singh, D., Mathimaran, N., Boller, T., Kahmen, A., 2019. Bioirrigation: a common mycorrhizal network facilitates the water transfer from deep-rooted pigeon pea to shallow-rooted finger millet under drought. Plant and Soil 440, 277–292

[75] Singh, D., Mathimaran, N., Boller, T., Kahmen, A., 2020. Deep-rooted pigeon pea promotes the water relations and survival of shallow-rooted finger millet during drought—Despite strong competitive interactions at ambient water availability. PLoS One 15, e0228993

[76] Smith, S.E., Facelli, E., Pope, S., Smith, F.A., 2010. Plant performance in stressful environments: interpreting new and established knowledge of the roles of arbuscular mycorrhizas. Plant and Soil 326, 3–20

[77] Smith, S.E., Read, D., 2008. Mycorrhizal Symbiosis, 3rd edition. Landon: Academic Press.

[78] Song, Y., Chen, D., Lu, K., Sun, Z., Zeng, R., 2015. Enhanced tomato disease resistance primed by arbuscular mycorrhizal fungus. Frontiers in Plant Science 6, 786

[79] Song, Y.Y., Zeng, R.S., Xu, J.F., Li, J., Shen, X., Yihdego, W.G., 2010. Interplant communication of tomato plants through underground common mycorrhizal networks. PLoS One 5, e13324

[80] Tang, X., Bernard, L., Brauman, A., Daufresne, T., Deleporte, P., Desclaux, D., Souche, G., Placella, S.A., Hinsinger, P., 2014. Increase in microbial biomass and phosphorus availability in the rhizosphere of intercropped cereal and legumes under field conditions. Soil Biology & Biochemistry 75, 86–93

[81] Thevathasan, N.V., Gordon, A.M., 2004. Ecology of tree intercropping systems in the north temperate region: experiences from southern Ontario, Canada. Agroforestry Systems 61, 257–268

[82] Thilakarathna, M.S., McElroy, M.S., Chapagain, T., Papadopoulos, Y.A., Raizada, M.N., 2016. Belowground nitrogen transfer from legumes to non-legumes under managed herbaceous cropping systems. A review. Agronomy for Sustainable Development 36, 58

[83] Tong, Y., Gabriel-Neumann, E., Krumbein, A., Ngwene, B., George, E., Schreiner, M., 2015. Interactive effects of arbuscular mycorrhizal fungi and intercropping with sesame (Sesamum indicum) on the glucosinolate profile in broccoli (Brassica oleracea var. Italica). Environmental and Experimental Botany 109, 288–295

[84] van der Heijden, M.G.A., Klironomos, J.N., Ursic, M., Moutoglis, P., Streitwolf-Engel, R., Boller, T., Wiemken, A., Sanders, I.R., 1998. Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396, 69–72

[85] van Tuinen, D., Tranchand, E., Hirissou, F., Wipf, D., Courty, P.E., 2020. Carbon partitioning in a walnut-maize agroforestry system through arbuscular mycorrhizal fungi. Rhizosphere 15, 100230

[86] Vandermeer, J.H., 1989. The Ecology of Intercropping. UK: Cambridge University Press.

[87] Wagg, C., Jansa, J., Stadler, M., Schmid, B., van der Heijden, M.G.A., 2011. Mycorrhizal fungal identity and diversity relaxes plant-plant competition. Ecology 92, 1303–1313

[88] Wahbi, S., Maghraoui, T., Hafidi, M., Sanguin, H., Oufdou, K., Prin, Y., Duponnois, R., Galiana, A., 2016. Enhanced transfer of biologically fixed N from faba bean to intercropped wheat through mycorrhizal symbiosis. Applied Soil Ecology 107, 91–98

[89] Wang, G., Sheng, L., Zhao, D., Sheng, J., Wang, X., Liao, H., 2016. Allocation of nitrogen and carbon is regulated by nodulation and mycorrhizal networks in soybean/maize intercropping system. Frontiers in Plant Science 7, 1901

[90] Wang, G., Ye, C., Zhang, J., Koziol, L., Bever, J.D., Li, X., 2019. Asymmetric facilitation induced by inoculation with arbuscular mycorrhizal fungi leads to overyielding in maize/faba bean intercropping. Journal of Plant Interactions 14, 10–20

[91] Wheeler, T., von Braun, J., 2013. Climate change impacts on global food security. Science 341, 508–513

[92] Wilson, G.W.T., Hartnett, D.C., Rice, C.W., 2006. Mycorrhizal-mediated phosphorus transfer between tallgrass prairie plants Sorghastrum nutans and Artemisia ludoviciana. Functional Ecology 20, 427–435

[93] Xiao, T., Yang, Q., Ran, W., Xu, G., Shen, Q., 2010. Effect of inoculation with arbuscular mycorrhizal fungus on nitrogen and phosphorus utilization in upland rice-mungbean intercropping system. Agricultural Sciences in China 9, 528–535

[94] 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

[95] Yao, Q., Li, X., Ai, W., Christie, P., 2003. Bi-directional transfer of phosphorus between red clover and perennial ryegrass via arbuscular mycorrhizal hyphal links. European Journal of Soil Biology 39, 47–54

[96] Zeng, P., Guo, Z., Xiao, X., Peng, C., 2019. Dynamic response of enzymatic activity and microbial community structure in metal(loid)-contaminated soil with tree-herb intercropping. Geoderma 345, 5–16

[97] 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 and Soil 466, 23–41

[98] 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 intercropping systems with different nitrogen application rates. Science of the Total Environment 740, 139810

[99] Zhang, X., Ren, B., Wu, S., Sun, Y., Chen, B., Li, R., 2018a. Rhizophagus irregularis influences As and P uptake by alfafa and the neighboring non-host pepperweed growing in an As-contaminated soil. Journal of Environmental Sciences 67, 36–44

[100] Zhang, Y., Hu, J., Bai, J., Qin, H., Wang, J., Wang, J., Lin, X., 2019. Intercropping with sunflower and inoculation with arbuscular mycorrhizal fungi promotes growth of garlic chive in metal-contaminated soil at a WEEE-recycling site. Ecotoxicology and Environmental Safety 167, 376–384

[101] Zhang, Y.C., Zou, Y.N., Liu, L.P., Wu, Q.S., 2018b. Common mycorrhizal networks activate salicylic acid defense responses of trifoliate orange (Poncirus trifoliata). Journal of Integrative Plant Biology 61, 1099–1111

Acknowledgments

This work was funded by the National Natural Science Foundation of China (No.41671265) and the National Key R&D Programs (2017YFD0200603 and 2016YFD0200306) of China. J.H. is supported by the Youth Innovation Promotion Association (No. 2016285) of Chinese Academy of Sciences.

Conflict of interest

All authors declare that they have no conflict of interest.

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