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Arbuscular mycorrhizal fungi: key players in avoiding cadmium accumulation in food crops

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Abstract

Background

Cadmium (Cd) levels of food crops can be elevated through management activities and geogenic factors. While emphasis is placed on reducing Cd in phosphorus (P) fertilizers, increasing evidence shows that Cd accumulation in plants is markedly influenced by arbuscular mycorrhizal fungi (AMF). Mycorrhizas are highly effective in reducing shoot Cd accumulation through various mechanisms including Cd immobilization in fungal structures and increasing root zinc (Zn) uptake.

Scope

The increase in plant Cd concentrations in response to short- or long-term P fertilization is not necessarily related to fertilizer Cd concentration. Novel results suggest that this counterintuitive result is related to suppressed mycorrhizal colonization by P fertilization. When applied P fertilizers reduce mycorrhizal colonization, there is risk for concurrent increased Cd accumulation in plants. Although the mechanism is not fully understood, grain Cd concentrations in crop rotations are highest in plants grown after non-mycorrhizal (e.g. rapeseed), rather than mycorrhizal species (e.g., wheat), probably due to diminished mycorrhizal activity by non-mycorrhizal plants. These findings indicate that rapeseed-wheat rotations may enhance Cd concentrations in human diets. Published data also show that AMF contribute up to 50% of total Zn uptake in plants.

Conclusions

Considering various soil and crop management factors that negatively affect mycorrhizal colonization, a priority should be to maintain functional AMF in soils to support healthy food systems. Considering also the fundamental role of AMF in root Zn uptake and the global prevalence of human Zn deficiency, improving functioning of AMF may provide a dual benefit to healthy and nutritious food production.

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References

  • Abbott LK, Robson AD, De Boer G (1984) The effect of phosphorus on the formation of hyphae in soil by the vesicular-arbuscular mycorrhizal fungus, Glomus fasciculatum. New Phytol 97:437–446

    Article  CAS  Google Scholar 

  • Adams ML, Zhao FJ, McGrath SP, Nicholson FA, Chambers BJ (2004) Predicting cadmium concentrations in wheat and barley grain using soil properties. J Environ Qual 33:532–541

    Article  CAS  PubMed  Google Scholar 

  • Adams SV, Newcomb PA, Shafer MM, Atkinson C, Bowles EJA, Newton KM, Lampe JW (2011) Sources of cadmium exposure among healthy premenopausal women. Sci Total Environ 409:1632–1637

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Agnello AC, Huguenot D, Van Hullebusch ED, Esposito G (2014) Enhanced phytoremediation: A review of low molecular weight organic acids and surfactants used as amendments. Crit Rev Environ Sci Technol 44:2531–2576

    Article  CAS  Google Scholar 

  • Åkesson A, Julin B, Wolk A (2008) Long-term dietary cadmium intake and postmenopausal endometrial cancer incidence: a population-based prospective cohort study. Cancer Res 68:6435–6441

    Article  PubMed  Google Scholar 

  • Albornoz FE, Hayes PE, Orchard S, Clode PL, Nazeri N, Standish RJ, Dickie IA, Bending GD, Hilton S, Ryan MH (2020) First cryo-scanning electron microscopy images and X-ray microanalyses of mucoromycotinian fine root endophytes in vascular plants. Front Microbiol 11:2018

    Article  PubMed  PubMed Central  Google Scholar 

  • Alloway BJ (2009) Soil factors associated with zinc deficiency in crops and humans. Environ Geochem Health 31:537–548

    Article  CAS  PubMed  Google Scholar 

  • Angus JF, Kirkegaard JA, Hunt JR, Ryan MH, Ohlander L, Peoples MB (2015) Break crops and rotations for wheat. Crop Pasture Sci 66:523–552

    Article  Google Scholar 

  • Aoshima K (2016) Itai-itai disease: renal tubular osteomalacia induced by environmental exposure to cadmium—historical review and perspectives. Soil Sci Plant Nut 62:319–326

    Article  CAS  Google Scholar 

  • Bailey RL, West KP Jr, Black RE (2015) The epidemiology of global micronutrient deficiencies. Ann Nutr Metab 66:22–33

    Article  CAS  PubMed  Google Scholar 

  • Bakhshandeh S, Corneo PE, Mariotte P, Kertesz MA, Dijkstra FA (2017) Effect of crop rotation on mycorrhizal colonization and wheat yield under different fertilizer treatments. Agric Ecosyst Environ 247:130–136

    Article  Google Scholar 

  • Baldantoni D, Morra L, Zaccardelli M, Alfani A (2016) Cadmium accumulation in leaves of leafy vegetables. Ecotoxicol Environ Saf 123:89–94

    Article  CAS  PubMed  Google Scholar 

  • Bergen B, Verbeeck M, Smolders E (2022) Trace metal accumulation in agricultural soils from mineral phosphate fertiliser applications in European long-term field trials. Eur J Soil Sci 73:e13167

  • Birke M, Reimann C, Rauch U, Ladenberger A, Demetriades A, Jaehne-Klingberg F, Oorts K, Gosar M, Dinelli E, Halamić J, Team TG (2017) GEMAS: Cadmium distribution and its sources in agricultural and grazing land soil of Europe—Original data versus clr-transformed data. J Geochem Explor 173:13–30

    Article  CAS  Google Scholar 

  • Bouis HE, Saltzman A (2017) Improving nutrition through biofortification: a review of evidence from HarvestPlus, 2003 through 2016. Glob Food Sec 12:49–58

    Article  PubMed  PubMed Central  Google Scholar 

  • Bowles TM, Jackson LE, Loeher M, Cavagnaro TR (2017) Ecological intensification and arbuscular mycorrhizas: a meta-analysis of tillage and cover crop effects. J Appl Ecol 54:1785–1793

    Article  Google Scholar 

  • Bracher C, Frossard E, Bigalke M, Imseng M, Mayer J, Wiggenhauser M (2021) Tracing the fate of phosphorus fertilizer derived cadmium in soil-fertilizer-wheat systems using enriched stable isotope labeling. Environ Pollut 287:117314

    Article  CAS  PubMed  Google Scholar 

  • Brennan RF, Bolland MDA (2003) Lupinus luteus cv. Wodjil takes up more phosphorus and cadmium than Lupinus angustifolius cv. Kalya. Plant Soil 248:167–185

    Article  CAS  Google Scholar 

  • Brennan RF, Bolland MDA (2005) Canola takes up more cadmium and phosphorus from soil than spring wheat. J Plant Nutr 28:931–948

    Article  CAS  Google Scholar 

  • Brennan RF, Bolland MDA, Shea G (2001) Comparing how Lupinus angustifolius and Lupinus luteus use zinc fertilizer for seed production. Nutr Cycl Agroecosyst 59:209–217

    Article  CAS  Google Scholar 

  • Brito I, Goss MJ, de Carvalho M, Chatagnier O, van Tuinen D (2012) Impact of tillage system on arbuscular mycorrhiza fungal communities in the soil under Mediterranean conditions. Soil till Res 121:63–67

    Article  Google Scholar 

  • Cakmak I (2008) Enrichment of cereal grains with zinc: agronomic or genetic biofortification? Plant Soil 302:1–17

    Article  CAS  Google Scholar 

  • Cakmak I, Kutman UB (2018) Agronomic biofortification of cereals with zinc: a review. Eur J Soil Sci 69:172–180

    Article  Google Scholar 

  • Cakmak I, Marschner H (1986) Mechanism of phosphorus-induced zinc deficiency in cotton. I. Zinc deficiency-enhanced uptake rate of phosphorus. Physiol Plant 68:483–490

    Article  CAS  Google Scholar 

  • Cakmak I, Welch RM, Erenoglu B, Römheld V, Norvell WA, Kochian LV (2000) Influence of varied zinc supply on re-translocation of cadmium (109Cd) and rubidium (86Rb) applied on mature leaf of durum wheat seedlings. Plant Soil 219:279–284

    Article  CAS  Google Scholar 

  • Cakmak I, Yazici A, Tutus Y, Ozturk L (2009) Glyphosate reduced seed and leaf concentrations of calcium, manganese, magnesium, and iron in non-glyphosate resistant soybean. Eur J Agron 31:114–119

    Article  CAS  Google Scholar 

  • Camprubí A, Estaún V, El Bakali MA, Garcia-Figueres F, Calvet C (2007) Alternative strawberry production using solarization, metham sodium and beneficial soil microbes as plant protection methods. Agron Sustain Dev 27:179–184

    Article  Google Scholar 

  • Cao XR, Wang XZ, Tong WB, Gurajala HK, He ZL, Yang XE (2020) Accumulation and distribution of cadmium and lead in 28 oilseed rape cultivars grown in a contaminated field. Environ Sci Pollut Res 27:2400–2411

    Article  CAS  Google Scholar 

  • Cao JL, Ren SX, Wang CL, She JY, Jiang YJ, Liu YY, Zhou YT, Wang L, Wang J, Wang YX, Liu J, Chen YH (2021) Cadmium and lead distribution in pyrite ores: environmental concerns over geochemically mobile fractions. Elem Sci Anth 9:00093

    Article  Google Scholar 

  • Carne G, Leconte S, Sirot V, Breysse N, Badot PM, Bispo A, Deportes IZ, Dumat C, Rivière G, Crepet A (2021) Mass balance approach to assess the impact of cadmium decrease in mineral phosphate fertilizers on health risk: The case-study of French agricultural soils. Sci Total Environ 760:143374

    Article  CAS  PubMed  Google Scholar 

  • Carretta L, Cardinali A, Onofri A, Masin R, Zanin G (2021) Dynamics of glyphosate and aminomethylphosphonic acid in soil under conventional and conservation tillage. Int J Environ Res 15:1037–1055

    Article  CAS  Google Scholar 

  • Cartea ME, de Haro A, Obregón S, Soengas P, Velasco P (2012) Glucosinolate variation in leaves of Brassica rapa crops. Plant Foods Human Nutr 67:283–288

    Article  CAS  Google Scholar 

  • Cavagnaro TR (2008) The role of arbuscular mycorrhizas in improving plant zinc nutrition under low soil zinc concentrations: a review. Plant Soil 304:315–325

    Article  CAS  Google Scholar 

  • Chaney RL (2015) How does contamination of rice soils with Cd and Zn cause high incidence of human Cd disease in subsistence rice farmers. Curr Pollut Rep 1:13–22

    Article  CAS  Google Scholar 

  • Chang JD, Huang S, Yamaji N, Zhang W, Zhao MJF, FJ, (2020) OsNRAMP1 transporter contributes to cadmium and manganese uptake in rice. Plant Cell Environ 43:2476–2491

    Article  CAS  PubMed  Google Scholar 

  • Chen HP, Yang XP, Wang P, Wang ZX, Li M, Zhao FJ (2018a) Dietary cadmium intake from rice and vegetables and potential health risk: A case study in Xiangtan, southern China. Sci Total Environ 639:271–277

    Article  CAS  PubMed  Google Scholar 

  • Chen B, Nayuki K, Kuga Y, Zhang X, Wu S, Ohtomo R (2018b) Uptake and intraradical immobilization of cadmium by arbuscular mycorrhizal fungi as revealed by a stable isotope tracer and synchrotron radiation μX-ray fluorescence analysis. Microbes Environ 33:253–263

    Article  Google Scholar 

  • Chen L, Wan H, Qian J, Guo J, Sun C, Wen J et al (2018c) Genome-wide association study of cadmium accumulation at the seedling stage in rapeseed (Brassica napus L). Front Plant Sci. 9:375

    Article  PubMed  PubMed Central  Google Scholar 

  • Christie P, Li XL, Chen BD (2004) Arbuscular mycorrhiza can depress translocation of zinc to shoots of host plants in soils moderately polluted with zinc. Plant Soil 261:209–217

    Article  CAS  Google Scholar 

  • Clemens S, Aarts MGM, Thomine S, Verbruggen N (2013) Plant science: the key to preventing slow cadmium poisoning. Trends Plant Sci 18:2

    Article  Google Scholar 

  • Coccina A, Cavagnaro TR, Pellegrino E, Ercoli L, McLaughlin MJ, Watts-Williams SJ (2019) The mycorrhizal pathway of zinc uptake contributes to zinc accumulation in barley and wheat grain. BMC Plant Biol 19:1–4

    Article  Google Scholar 

  • Dann PR, Derrick JW, Dumaresq DC, Ryan MH (1996) The response of organic and conventionally grown wheat to superphosphate and reactive phosphate rock. Aust J Exp Agric 36:71–78

    Article  Google Scholar 

  • Di Mola I, Ventorino V, Cozzolino E, Ottaiano L, Romano I, Duri LG, Pepe O, Mori M (2021) Biodegradable mulching vs traditional polyethylene film for sustainable solarization: Chemical properties and microbial community response to soil management. Appl Soil Ecol 163:103921

    Article  Google Scholar 

  • Dietrich P, Roscher C, Clark AT, Eisenhauer N, Schmid B, Wagg C (2020) Diverse plant mixtures sustain a greater arbuscular mycorrhizal fungi spore viability than monocultures after 12 years. J Plant Ecol 13:478–488

    Article  Google Scholar 

  • Druille M, Cabello MN, Omacini M, Golluscio RA (2013) Glyphosate reduces spore viability and root colonization of arbuscular mycorrhizal fungi. Appl Soil Ecol 64:99–103

    Article  Google Scholar 

  • Edge CB, Brown MI, Heartz S, Thompson D, Ritter L, Ramadoss M (2021) The persistence of glyphosate in vegetation one year after application. Forests 12:601

    Article  Google Scholar 

  • EFSA (2012) European Food Safety Authority; Cadmium dietary exposure in the European population. EFSA J 10:2551. https://doi.org/10.2903/j.efsa.2012.2551

  • EFSA (2009) Cadmium in food: Scientific opinion of the panel on contaminants in the food chain. EFSA J 980:1–139. https://efsa.onlinelibrary.wiley.com/doi/epdf/10.2903/j.efsa.2009.980. Accessed 24 August 2021

  • Ercoli L, Schüßler A, Arduini I, Pellegrino E (2017) Strong increase of durum wheat iron and zinc content by field-inoculation with arbuscular mycorrhizal fungi at different soil nitrogen availabilities. Plant Soil 419:153–167

    Article  CAS  Google Scholar 

  • Fang X, Wang J, Chen H, Christl I, Wang P, Kretzschmar R, Zhao FJ (2021) Two-year and multi-site field trials to evaluate soil amendments for controlling cadmium accumulation in rice grain. Environ Pollut 289:117918

    Article  CAS  PubMed  Google Scholar 

  • Ferrol N, Tamayo E, Vargas P (2016) The heavy metal paradox in arbuscular mycorrhizas: From mechanisms to biotechnological applications. J Exp Bot 67:6253–6265

    Article  CAS  PubMed  Google Scholar 

  • Gao X, Akhter F, Tenuta M, Flaten DN, Gawalko EJ, Grant CA (2010) Mycorrhizal colonization and grain Cd concentration of field-grown durum wheat in response to tillage, preceding crop and phosphorus fertilization. J Sci Food Agric 90:750–758

    Article  CAS  PubMed  Google Scholar 

  • Gao MY, Chen XW, Huang WX, Wu L, Yu ZS, Xiang L, Li H (2021) Cell wall modification induced by an arbuscular mycorrhizal fungus enhanced cadmium fixation in rice root. J Hazard Mater 416:125894

    Article  CAS  PubMed  Google Scholar 

  • Gavito ME, Miller MH (1998) Changes in mycorrhiza development in maize induced by crop management practices. Plant Soil 198:185–192

    Article  CAS  Google Scholar 

  • Genchi G, Sinicropi MS, Lauria G, Carocci A, Catalano A (2020) The effects of cadmium toxicity. Int J Env Res Pub HE 17:3782

    Article  CAS  Google Scholar 

  • Gosling P, Hodge A, Goodlass G, Bending GD (2006) Arbuscular mycorrhizal fungi and organic farming. Agric Ecosyst Environ 113:17–35

    Article  Google Scholar 

  • Gosling P, Mead A, Proctor M, Hammond JP, Bending GD (2013) Contrasting arbuscular mycorrhizal communities colonizing different host plants show a similar response to a soil phosphorus concentration gradient. New Phytol 198:546–556

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grant CA, Buckley WT, Bailey LD, Selles F (1998) Cadmium accumulation in crops. Can J Plant Sci 78:1–17

    Article  CAS  Google Scholar 

  • Grant CA, Bailey L, Flore N, Harapiak J (2002) Effect of phosphate source, rate and cadmium content and use of Penicillium bilaii on phosphorus, zinc and cadmium concentration in durum wheat grain. J Sci Food Agric 82:301–308

    Article  CAS  Google Scholar 

  • Grant C, Bittman S, Montreal M, Plenchette C, Morel C (2005) Soil and fertilizer phosphorus: Effects on plant P supply and mycorrhizal development. Can J Plant Sci 85:3–14

    Article  Google Scholar 

  • Grant CA, Monreal MA, Irvine RB, Mohr RM, McLaren DL, Khakbazan M (2010) Preceding crop and phosphorus fertilization affect cadmium and zinc concentration of flaxseed under conventional and reduced tillage. Plant Soil 333:337–350

    Article  CAS  Google Scholar 

  • Grant C, Flaten D, Tenuta M, Malhi S, Akinremi W (2013) The effect of rate and Cd concentration of repeated phosphate fertilizer applications on seed Cd concentration varies with crop type and environment. Plant Soil 372:221–233

    Article  CAS  Google Scholar 

  • Gray CW, Yi Z, Munir K, Lehto NJ, Robinson BH, Cavanagh JA (2019) Cadmium concentrations in New Zealand wheat: effect of cultivar type, soil properties, and crop management. J Environ Qual 48:701–708

    Article  CAS  PubMed  Google Scholar 

  • Grioni S, Agnoli C, Krogh V, Pala V, Rinaldi S, Vinceti M et al (2019) Dietary cadmium and risk of breast cancer subtypes defined by hormone receptor status: a prospective cohort study. Int J Cancer 144:2153–2160

    Article  CAS  PubMed  Google Scholar 

  • Grispen VM, Nelissen HJ, Verkleij JA (2006) Phytoextraction with Brassica napus L.: A tool for sustainable management of heavy metal contaminated soils. Environ Pollut 144:77–83

    Article  CAS  PubMed  Google Scholar 

  • Gullino ML, Garibaldi A, Gamliel A, Katan J (2022) Soil disinfestation: from soil treatment to soil and plant health. Plant Dis 106:1541–1554

    Article  CAS  PubMed  Google Scholar 

  • Guttieri MJ, Seabourn BW, Liu C, Baenziger PS, Waters BM (2015) Distribution of cadmium, iron, and zinc in millstreams of hard winter wheat (Triticum aestivum L.). J Agric Food Chem 63:10681–10688

    Article  CAS  PubMed  Google Scholar 

  • Guzman A, Montes M, Hutchins L, DeLaCerda G, Yang P, Kakouridis A, Dahlquist-Willard RM, Firestone MK, Bowles T, Kremen C (2021) Crop diversity enriches arbuscular mycorrhizal fungal communities in an intensive agricultural landscape. New Phytol 231:447–459

    Article  PubMed  PubMed Central  Google Scholar 

  • Hamon RE, McLaughlin MJ, Naidu R, Correll R (1998) Long-term changes in cadmium bioavailability in soil. Environ Sci Technol 32:3699–3703

    Article  CAS  Google Scholar 

  • Han F, Shan XQ, Zhang SZ, Wen B, Owens G (2006) Enhanced cadmium accumulation in maize roots—the impact of organic acids. Plant Soil 289:355–368

    Article  CAS  Google Scholar 

  • Hansen JC, Schillinger WF, Sullivan TS, Paulitz TC (2019) Soil microbial biomass and fungi reduced with canola introduced into long-term monoculture wheat rotations. Front Microbiol 10:1488

    Article  PubMed  PubMed Central  Google Scholar 

  • Hart JJ, Welch RM, Norvell WA, Clarke JM, Kochian LV (2005) Zinc effects on cadmium accumulation and partitioning in near-isogenic lines of durum wheat that differ in grain cadmium concentration. New Phytol 167:391–401

    Article  CAS  PubMed  Google Scholar 

  • He LL, Huang DY, Zhang Q, Zhu HH, Xu C, Li B, Zhu QH (2021) Meta-analysis of the effects of liming on soil pH and cadmium accumulation in crops. Ecotoxicol Environ Saf 223:112621

    Article  CAS  PubMed  Google Scholar 

  • Helander M, Saloniemi I, Omacini M, Druille M, Salminen JP, Saikkonen K (2018) Glyphosate decreases mycorrhizal colonization and affects plant-soil feedback. Sci Total Environ 642:285–291

    Article  CAS  PubMed  Google Scholar 

  • Heyes PE, Guilherme Pereira C, Clode PL, Lambers H (2019) Calcium-enhanced phosphorus toxicity in calcifuge and soil-indifferent Proteaceae along the Jurien Bay chronosequence. New Phytol 221:764–777

    Article  Google Scholar 

  • Hirzel J, Retamal-Salgado J, Walter I, Matus I (2019) Residual effect of cadmium applications in different crop rotations and environments on durum wheat cadmium accumulation. J Soil Water Conserv 74:41–50

    Article  Google Scholar 

  • Hirzel J, Undurraga P, León L, Carrasco J, González J, Matus I (2021) Medium-term crop rotations with different residue incorporation rates: effect on durum wheat production and plant nutrient concentration and extraction. J Soil Sci Plant Nut 21:2145–2152

    Article  CAS  Google Scholar 

  • Houben GJ, Sitnikova MA, Post VE (2017) Terrestrial sedimentary pyrites as a potential source of trace metal release to groundwater–A case study from the Emsland, Germany. Appl Geochem 76:99–111

    Article  CAS  Google Scholar 

  • Hu W, Huang B, Tian K, Holm PE, Zhang Y (2017) Heavy metals in intensive greenhouse vegetable production systems along Yellow Sea of China: Levels, transfer and health risk. Chemosphere 167:82–90

    Article  CAS  PubMed  Google Scholar 

  • IARC (2012) Cadmium and cadmium compounds. In Monographs, Vol 100C, A review of human carcinogens, pp 121–145. http://monographs.iarc.fr/ENG/Monographs/vol100C/mono100C-8.pdf. Accessed 1 Sept 2021

  • Imseng M, Wiggenhauser M, Keller A, Müller M, Rehkämper M, Murphy K, Kreissig K, Frossard E, Wilcke W, Bigalke M (2018) Fate of Cd in agricultural soils: a stable isotope approach to anthropogenic impact, soil formation, and soil-plant cycling. Environ Sci Tech 52:1919–1928

    Article  CAS  Google Scholar 

  • Ishikawa S (2020) Mechanisms of cadmium accumulation in rice grains and molecular breeding for its reduction. Soil Sci Plant Nutr 66:28–33

    Article  CAS  Google Scholar 

  • Jackson GD (2000) Effects of nitrogen and sulfur on canola yield and nutrient uptake. Agron J 92:644–649

    Article  CAS  Google Scholar 

  • Janoušková M, Pavlíková D, Vosátka M (2006) Potential contribution of arbuscular mycorrhiza to cadmium immobilisation in soil. Chemosphere 65:1959–1965

    Article  PubMed  Google Scholar 

  • Jansa J, Weimken A, Frossard E (2006) The effects of agricultural practices on arbuscular mycorrhizal fungi. In: Frossard E, Blum W, Warkentin B (eds) Function of Soils for Human Societies and the Environment. Geological Society, London, pp 89–115

    Google Scholar 

  • Jensen H, Mosbæk H (1990) Relative availability of 200 years old cadmium from soil to lettuce. Chemosphere 20:693–702

    Article  CAS  Google Scholar 

  • Jeske ES, Tian H, Hanford K, Walters DT, Drijber RA (2018) Long-term nitrogen fertilization reduces extraradical biomass of arbuscular mycorrhizae in a maize (Zea mays L.) cropping system. Agric Ecosyst Environ 255:111–118

    Article  Google Scholar 

  • Jiao Y, Grant CA, Bailey LD (2004) Effects of phosphorus and zinc fertilizer on cadmium uptake and distribution in flax and durum wheat. J Sci Food Agric 84:777–785

    Article  CAS  Google Scholar 

  • Joner EJ (2000) The effect of long-term fertilization with organic or inorganic fertilizers on mycorrhiza-mediated phosphorus uptake in subterranean clover. Biol Fertility Soils 32:435–440

    Article  Google Scholar 

  • Joner EJ, Briones R, Leyval C (2000) Metal-binding capacity of arbuscular mycorrhizal mycelium. Plant Soil 226:227–234

    Article  CAS  Google Scholar 

  • Kabir Z (2005) Tillage or no-tillage: Impact on mycorrhizae. Can J Plant Sci 85:23–29

    Article  Google Scholar 

  • Khan D, Qiu L, Liang C, Mirza K, Rehman SU, Han Y, Hannan A, Kashif M, Kra KL (2022) Genesis and distribution of pyrite in the Lacustrine Shale: evidence from the Es3x shale of the eocene shahejie formation, Zhanhua Sag, East China. ACS Omega 7:1244–1258

    Article  CAS  PubMed  Google Scholar 

  • Kim SJ, Fujii K, Mohamed ZI, Kim HW, Yamauchi H, Ishii G (2008) Identification and quantitative determination of glucosinolates in Brassica napus cv. Hanakkori Food Sci Biotechnol 17:1097–1101

    CAS  Google Scholar 

  • Kim K, Melough MM, Vance TM, Noh H, Koo SI, Chun OK (2019) Dietary cadmium intake and sources in the US. Nutrients 11:2

    Article  Google Scholar 

  • Kirkegaard J, Christen O, Krupinsky J, Layzell D (2008) Break crop benefits in temperate wheat production. Field Crop Res 107:185–195

    Article  Google Scholar 

  • Koeslin-Findeklee F, Horst WJ (2016) Contribution of nitrogen uptake and retranslocation during reproductive growth to the nitrogen efficiency of winter oilseed-rape cultivars (Brassica napus L.) differing in leaf senescence. Agronomy 6:1

    Article  Google Scholar 

  • Kubier A, Pichler T (2019) Cadmium in groundwater− A synopsis based on a large hydrogeochemical data set. Sci Tot Environ 689:831–842

    Article  CAS  Google Scholar 

  • Kubier A, Wilkin RT, Pichler T (2019) Cadmium in soils and groundwater: A review. Appl Geochem 108:104388

    Article  CAS  Google Scholar 

  • Laitinen P, Rämö S, Nikunen U, Jauhiainen L, Siimes K, Turtola E (2009) Glyphosate and phosphorus leaching and residues in boreal sandy soil. Plant Soil 323:267–283

    Article  CAS  Google Scholar 

  • Lambers H, Mougel C, Jaillard B, Hinsinger P (2009) Plant-microbe-soil interactions in the rhizosphere: an evolutionary perspective. Plant Soil 321:83–115

    Article  CAS  Google Scholar 

  • Lambers H, Clements JC, Nelson MN (2013) How a phosphorus-acquisition strategy based on carboxylate exudation powers the success and agronomic potential of lupines (Lupinus, Fabaceae). Am J Bot 100:263–288

    Article  CAS  PubMed  Google Scholar 

  • Lan W, Yao C, Luo F, Jin Z, Lu S, Li J, Wang X, Hu X (2022) Effects of application of pig manure on the accumulation of heavy metals in rice. Plants 11:207

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lang M, Zhang C, Su W, Chen X, Zou C, Chen X (2022) Long-term P fertilization significantly altered the diversity, composition and mycorrhizal traits of arbuscular mycorrhizal fungal communities in a wheat-maize rotation. Applied Soil Ecol 170:104261

    Article  Google Scholar 

  • Lehmann A, Veresoglou SD, Leifheit EF, Rillig MC (2014) Arbuscular mycorrhizal influence on zinc nutrition in crop plants – A meta-analysis. Soil Biol Biochem 69:123–131

    Article  CAS  Google Scholar 

  • Li X, Zhou D (2019) A meta-analysis on phenotypic variation in cadmium accumulation of rice and wheat: implications for food cadmium risk control. Pedosphere 29:545–553

    Article  CAS  Google Scholar 

  • Li YX, Xiong X, Lin CY, Zhang FS, Li W, Han W (2010) Cadmium in animal production and its potential hazard on Beijing and Fuxin farmlands. J Hazard Mater 177:475–480

    Article  CAS  PubMed  Google Scholar 

  • Li H, Luo N, Zhang LJ, Zhao HM, Li YW, Cai QY, Wong MH, Mo CH (2016) Do arbuscular mycorrhizal fungi affect cadmium uptake kinetics, subcellular distribution and chemical forms in rice? Sci Tot Environ 571:1183–1190

    Article  CAS  Google Scholar 

  • Liedschulte V, Laparra H, Battey JND, Schwaar JD, Broye H, Mark R, Klein M, Goepfert S, Bovet L (2017) Impairing both HMA4 homeologs is required for cadmium reduction in tobacco. Plant Cell Environ 40:364–377

    Article  CAS  PubMed  Google Scholar 

  • Liu Y, Xiao T, Perkins RB, Zhu J, Zhu Z, Xiong Y, Ning Z (2017) Geogenic cadmium pollution and potential health risks, with emphasis on black shale. J Geochem Explor 176:42–49

    Article  CAS  Google Scholar 

  • Loneragan JF, Grunes DL, Welch RM, Aduayi EA, Tengah A, Lazar VA, Cary EE (1982) Phosphorus accumulation and toxicity in leaves in relation to zinc supply. Soil Sci Soc Am J 46:345–352

    Article  CAS  Google Scholar 

  • Luo N, Li X, Chen AY, Zhang LJ, Zhao HM, Xiang L, Cai QY, Mo CH, Wong MH, Li H (2017) Does arbuscular mycorrhizal fungus affect cadmium uptake and chemical forms in rice at different growth stages? Sci Tot Environ 599:1564–1572

    Article  Google Scholar 

  • Ma X, Geng Q, Zhang H, Bian C, Chen HY, Jiang D, Xu X (2021) Global negative efects of nutrient enrichment on arbuscular mycorrhizal fungi, plant diversity and ecosystem multifunctionality. New Phytol 229:2957–2969

    Article  CAS  PubMed  Google Scholar 

  • Mäder P, Edenhofer S, Boller T, Wiemken A, Niggli U (2000) Arbuscular mycorrhizae in a long-term field trial comparing low-input (organic, biological) and high-input (conventional) farming systems in a crop rotation. Biol Fertil Soils 31:150–156

    Article  Google Scholar 

  • MAFF (Ministry of Agriculture, Forestry and Fisheries) (2018) Cadmium Intake from Foods in Japan.” Accessed 18 October 2022. http://www.maff.go.jp/j/syouan/nouan/kome/k_cd/jitai_sesyu/02_int.html

  • Marschner P (ed) (2012) Marschner’s mineral nutrition of higher plants. Academic, London

    Google Scholar 

  • McCully ME, Miller C, Sprague SJ, Huang CX, Kirkegaard JA (2008) Distribution of glucosinolates and sulphur-rich cells in roots of field-grown canola (Brassica napus). New Phytol 180:193–205

    Article  CAS  PubMed  Google Scholar 

  • McGonigle TP, Hutton M, Greenley A, Karamanos R (2011) Role of mycorrhiza in a wheat–flax versus canola–flax rotation: A case study. Commun Soil Sci Plant 42:2134–2142

    Article  CAS  Google Scholar 

  • McLaughlin MJ, Maier NA, Freeman K, Tiller KG, Williams CM, Smart MK (1995) Effect of potassic and phosphatic fertilizer type, fertilizer Cd concentration and zinc rate on cadmium uptake by potatoes. Fert Res 40:63–70

    Article  CAS  Google Scholar 

  • McLaughlin MJ, Maier NA, Rayment GE, Sparrow LA, Berg G, McKay A, Milham P, Merry RH, Smart MK (1997) Cadmium in Australian potato tubers and soils. J Environ Qual 26:1644–1649

    Article  CAS  Google Scholar 

  • McLaughlin MJ, Smolders E, Zhao FJ, Grant C, Montalvo D (2021) Chapter One - Managing cadmium in agricultural systems. Adv Agron 166:1–129

    Article  Google Scholar 

  • Mench MJ (1998) Cadmium availability to plants in relation to major long-term changes in agronomy systems. Agric Ecosyst Environ 67:175–187

    Article  CAS  Google Scholar 

  • Menéndez AB, Scervino JM, Godeas AM (2001) Arbuscular mycorrhizal populations associated with natural and cultivated vegetation on a site of Buenos Aires province, Argentina. Biol Fertil Soils 33:373–381

    Article  Google Scholar 

  • Mertens M, Höss S, Neumann G, Afzal J, Reichenbecher W (2018) Glyphosate, a chelating agent—Relevant for ecological risk assessment? Environ Sci Pollut Res 25:5298–5317

    Article  CAS  Google Scholar 

  • Miller SP (2000a) Arbuscular mycorrhizal colonization of semi-aquatic grasses along a wide hydrologic gradient. New Phytol 145:145–155

    Article  Google Scholar 

  • Miller MH (2000b) Arbuscular mycorrhizae and the phosphorus nutrition of maize: A review of Guelph studies. Canad J Plant Sci 80:47–52

    Article  CAS  Google Scholar 

  • Miller MH, McGonigle TP, Addy HD (1995) Functional ecology of vesicular arbuscular mycorrhizas as influ- enced by phosphate fertilization and tillage in an agricultural ecosystem. Crit Rev Biotechnol 15:241–255

    Article  Google Scholar 

  • Mortvedt JJ (1987) Cadmium levels in soils and plants from some long-term soil fertility experiments in the United States of America. J Environ Qual 16:37–142

    Article  Google Scholar 

  • Nawrot T, Plusquin M, Hogervorst J, Roels HA, Celis H, Thijs L, Vangronsveld J, Van Hecke E, Staessen JA (2006) Environmental exposure to cadmium and risk of cancer: a prospective population-based study. Lancet Onc 7:119–126

    Article  CAS  Google Scholar 

  • Oliver DP, Schultz JE, Tiller KG, Merry RH (1993) The effect of crop rotations and tillage practices on cadmium concentration in wheat grain. Aust J Agr Res 44:1221–1234

    Article  Google Scholar 

  • Ova EA, Kutman UB, Ozturk L, Cakmak I (2015) High phosphorus supply reduced zinc concentration of wheat in native soil but not in autoclaved soil or nutrient solution. Plant Soil 393:147–162

    Article  CAS  Google Scholar 

  • Owen KJ, Clewett TG, Thompson JP (2010) Pre-cropping with canola decreased Pratylenchus thornei populations, arbuscular mycorrhizal fungi, and yield of wheat. Crop past Sci 61:399–410

    Article  Google Scholar 

  • Pacyna JM, Pacyna EG, Aas W (2009) Changes of emissions and atmospheric deposition of mercury, lead, and cadmium. Atmospheric Environ 43:117–127

    Article  CAS  Google Scholar 

  • Panth M, Hassler SC, Baysal-Gurel F (2020) Methods for management of soilborne diseases in crop production. Agriculture 10:16

    Article  CAS  Google Scholar 

  • Plenchette C, Clermont-Dauphin C, Meynard JM, Fortin JA (2005) Managing arbuscular mycorrhizal fungi in cropping systems. Can J Plant Sci 85:31–40

    Article  Google Scholar 

  • Read SA, Obeid S, Ahlenstiel C, Ahlenstiel G (2019) The role of zinc in antiviral immunity. Adv Nutr 10:696–710

    Article  PubMed  PubMed Central  Google Scholar 

  • Rhee JH, Choi S, Lee JE, Hur OS, Ro NY, Hwang AJ, Ko HC, Chung YJ, Noh JJ, Assefa AD (2020) Glucosinolate content in Brassica genetic resources and their distribution pattern within and between inner, middle, and outer leaves. Plants 11:1421

    Article  Google Scholar 

  • Römer W, Kang DK, Egle K, Gerke J, Keller H (2000) The acquisition of cadmium by Lupinus albus L., Lupinus angustifolius L., and Lolium multiflorum L. J Plant Nutr Soil Sci 163:623–628

    Article  Google Scholar 

  • Romih N, Grabner B, Lakota M, Ribaric-Lasnik C (2012) Distribution of Cd, Pb, Zn, Mo, and S in juvenile and mature Brassica napus L. var. napus. Int J Phytorem 14:282–301

    Article  CAS  Google Scholar 

  • Ryan MH, Angus JF (2003) Arbuscular mycorrhizae in wheat and field pea crops on a low P soil: increased Zn-uptake but no increase in P-uptake or yield. Plant Soil 250:225–239

    Article  CAS  Google Scholar 

  • Ryan MH, Graham JH (2018) Little evidence that farmers should consider abundance or diversity of arbuscular mycorrhizal fungi when managing crops. New Phytol 220:1092–1107

    Article  PubMed  Google Scholar 

  • Ryan MH, McCully ME, Huang CX (2003) Location and quantification of phosphorus and other elements in fully hydrated, soil-grown arbuscular mycorrhizas: a cryo-analytical scanning electron microscopy study. New Phytol 160:429–441

    Article  CAS  PubMed  Google Scholar 

  • Ryan MH, McInerney JK, Record IR, Angus JF (2008) Zinc bioavailability in wheat grain in relation to phosphorus fertiliser, crop sequence and mycorrhizal fungi. J Sci Food and Agric 88:1208–1216

    Article  CAS  Google Scholar 

  • Säle V, Aguilera P, Laczko E, Mäder P, Berner A, Zihlmann U et al (2015) Impact of conservation tillage and organic farming on the diversity of arbuscular mycorrhizal fungi. Soil Biol Biochem 84:38–52

    Article  Google Scholar 

  • Sanderson DV, Voutchkov M, Benkeblia N (2019) Bioaccumulation of cadmium in potato tuber grown on naturally high levels cadmium soils in Jamaica. Sci Total Environ 649:909–915

    Article  CAS  PubMed  Google Scholar 

  • Sasaki A, Yamaji N, Yokosho K, Ma JF (2012) Nramp5 is a major transporter responsible for manganese and cadmium uptake in rice. Plant Cell 24:2155–2167

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Satarug S, Ruangyuttikarn W, Nishijo M, Ruiz P (2018) Urinary cadmium threshold to prevent kidney disease development. Toxics 6:26

    Article  PubMed  PubMed Central  Google Scholar 

  • Schaefer HR, Dennis S, Fitzpatrick S (2020) Cadmium: Mitigation strategies to reduce dietary exposure. J Food Sci 85:260–267

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schreiner PR, Ivors KL, Pinkerton JN (2001) Soil solarization reduces arbuscular mycorrhizal fungi as a consequence of weed suppression. Mycorrhiza 11:273–277

    Article  CAS  PubMed  Google Scholar 

  • Sheppard SC, Grant CA, Sheppard MI, de Jong R, Long J (2009) Risk indicator for agricultural inputs of trace elements to Canadian soils. J Environ Qual 38:919–932

    Article  CAS  PubMed  Google Scholar 

  • Siebers M, Rohr T, Ventura M, Schütz V, Thies S, Kovacic F, Jaeger KE, Berg M, Dörmann P, Schulz M (2018) Disruption of microbial community composition and identification of plant growth promoting microorganisms after exposure of soil to rapeseed-derived glucosinolates. PLoS ONE 13:e0200160

    Article  PubMed  PubMed Central  Google Scholar 

  • Singh BR, Dependra KC, Åsgeir RA (2017) Long-term effect of phosphate fertilization on cadmium uptake by oat and its accumulation in soil. J Environ Analytic Toxic 7:516

    Google Scholar 

  • Six L, Smolders E (2014) Future trends in soil cadmium concentration under current cadmium fluxes to European agricultural soils. Sci Total Environ 485:319–328

    Article  PubMed  Google Scholar 

  • Smolders E, Six L (2013) Revisiting and updating the effect of phosphate fertilizers to cadmium accumulation in European agricultural soils; Leuven, Division Soil and Water Management, Heverlee, Belgium, pp 14–20.

  • Smolders E, Mertens J (2013) Cadmium. In: Alloway JB (ed) Heavy Metals in Soils – Trace Metals and Metalloids in Soils and Their Bioavailability, 3rd edn. Springer, Dordrecht, pp 283–299

    Chapter  Google Scholar 

  • Song Y, Wang Y, Mao W, Sui H, Yong L, Yang D, Jiang D, Zhang L, Gong Y (2017) Dietary cadmium exposure assessment among the Chinese population. PLoS ONE 12:e0177978

    Article  PubMed  PubMed Central  Google Scholar 

  • Sterckeman T (2021) Arbuscular mycorrhizal fungi reduce cadmium accumulation in plants: evidence and uncertainty. Plant Soil 468:37–43

    Article  CAS  Google Scholar 

  • Sterckeman T, Thomine S (2020) Mechanisms of cadmium accumulation in plants. Crit Rev Plant Sci 39:322–359

    Article  Google Scholar 

  • Sterckeman T, Gossiaux L, Guimont S, Sirguey C, Lin Z (2018) Cadmium mass balance in French soils under annual crops: scenarios for the next century. Sci Total Environ 639:1440–1452

    Article  CAS  PubMed  Google Scholar 

  • Sun Y, Luo T, Zhong S, Zhou F, Zhang Y, Ma Y, Fu Q (2021) Long-term effects of low-molecular-weight organic acids on remobilization of Cd, Cr, Pb, and As in alkaline coastal wetland soil. Env Pollut Bioavail 33:266–277

    Article  CAS  Google Scholar 

  • Szczepaniak W (2014) A mineral profile of winter oilseed rape in critical stages of growth – Nitrogen. J Elem 19:759–778

    Google Scholar 

  • Takahashi R, Ishimaru Y, Shimo H, Ogo Y, Senoura T, Nishizawa NK, Nakanishi H (2012) The OsHMA2 transporter is involved in root-to-shoot translocation of Zn and Cd in rice. Plant Cell Environ 35:1948–1957

    Article  CAS  PubMed  Google Scholar 

  • Tan J, Wang J, Chai T, Zhang Y, Feng S, Li Y, Zhao H, Liu H, Chai X (2013) Functional analyses of TaHMA2, a P1B-type ATPase in wheat. Plant Biotechnol J 11:420–431

    Article  CAS  PubMed  Google Scholar 

  • Thielecke F, Nugent A (2018) Contaminants in grain—a major risk for whole grain safety? Nutrients 10:1213

    Article  PubMed  PubMed Central  Google Scholar 

  • Torma S, Vilček J, Lošák T, Kužel S, Martensson A (2018) Residual plant nutrients in crop residues–an important resource. Acta Agr Scand B—S P 68: 358–366

  • Vega A, Delgado N, Handford M (2022) Increasing heavy metal tolerance by the exogenous application of organic acids. Int J Mol Sci 23:5438

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Velasco P, Soengas P, Vilar M, Cartea ME, del Rio M (2008) Comparison of glucosinolate profiles in leaf and seed tissues of different Brassica napus crops. J Am Soc Hort Sci 133:551–558

    Article  Google Scholar 

  • Verbeeck M, Salaets P, Smolders E (2020) Trace element concentrations in mineral phosphate fertilizers used in Europe: A balanced survey. Sci Tot Environ 712:136419

    Article  CAS  Google Scholar 

  • Verbruggen E, van der Heijden MG, Rillig MC, Kiers ET (2013) Mycorrhizal fungal establishment in agricultural soils: factors determining inoculation success. New Phytol 197:1104–1109

    Article  PubMed  Google Scholar 

  • Vergine M, Aprile A, Sabella E, Genga A, Siciliano M, Rampino P, Lenucci MS, Luvisi A, Bellis LD (2017) Cadmium concentration in grains of durum wheat (Triticum turgidum L. subsp. durum). J Agr Food Chem 65:6240–6246

    Article  CAS  Google Scholar 

  • Vilela LAF, Barbosa MV (2019) Contribution of arbuscular mycorrhizal fungi in promoting cadmium tolerance in plants. In Cadmium Tolerance in Plants (pp. 553–586). Academic Press, London

  • Wang Z, Sun Y, Yao W, Ba Q, Wang H (2021) Effects of cadmium exposure on the immune system and immunoregulation. Front Immun 12:695484

    Article  CAS  Google Scholar 

  • Wang L, Liu S, Li J, Li S (2022) Effects of several organic fertilizers on heavy metal passivation in Cd contaminated gray-purple soil. Front Environ Sci 10:895646

    Article  Google Scholar 

  • Watts-Williams SJ, Cavagnaro TR (2018) Arbuscular mycorrhizal fungi increase grain zinc concentration and modify the expression of root ZIP transporter genes in a modern barley (Hordeum vulgare) cultivar. Plant Sci 274:163–170

    Article  CAS  PubMed  Google Scholar 

  • Watts-Williams SJ, Patti AF, Cavagnaro TR (2013) Arbuscular mycorrhizas are beneficial under both deficient and toxic soil zinc conditions. Plant Soil 371:299–312

    Article  CAS  Google Scholar 

  • Watts-Williams SJ, Smith FA, McLaughlin MJ, Patti AF, Cavagnaro TR (2015) How important is the mycorrhizal pathway for plant Zn uptake? Plant Soil 390:157–166

    Article  CAS  Google Scholar 

  • Weissenhorn I, Leyval C, Berthelin J (1993) Cd-tolerant arbuscular mycorrhizal (AM) fungi from heavy metal polluted soils. Plant Soil 157:247–256

    Article  CAS  Google Scholar 

  • Weissenhorn I, Leyval C, Belgy G, Berthelin J (1995) Arbuscular mycorrhizal contribution to heavy metal uptake by maize (Zea mays L.) in pot culture with contaminated soil. Mycorrhiza 5:245–251

    CAS  Google Scholar 

  • Welikala D, Robinson BH, Moltchanova E, Hartland A, Lehto NJ (2021) Soil cadmium mobilisation by dissolved organic matter from soil amendments. Chemosphere 271:129536

    Article  CAS  PubMed  Google Scholar 

  • Wetzel K, Silva G, Matczinski U, Oehl F, Fester T (2014) Superior differentiation of arbuscular mycorrhizal fungal communities from till and no-till plots by morphological spore identification when compared to T-RFLP. Soil Biol Biochem 72:88e96

    Article  Google Scholar 

  • Wiggenhauser M, Bigalke M, Imseng M, Keller A, Rehkämper M, Wilcke W, Frossard E (2019) Using isotopes to trace freshly applied cadmium through mineral phosphorus fertilization in soil-fertilizer-plant systems. Sci Total Environ 648:779–786

    Article  CAS  PubMed  Google Scholar 

  • Wilkes TI, Warner DJ, Davies KG, Edmonds-Brown V (2020) Tillage, glyphosate and beneficial arbuscular mycorrhizal fungi: Optimising crop management for plant–fungal symbiosis. Agriculture 10:520

    Article  CAS  Google Scholar 

  • Wong CKE, Cobbett CS (2009) HMA P-type ATPases are the major mechanism for root-to-shoot Cd translocation in Arabidopsis thaliana. New Phytol 181:71–78

    Article  CAS  PubMed  Google Scholar 

  • World Health Organization (2019) Preventing disease through healthy environments: exposure to cadmium: a major public health concern. World Health Organization. https://apps.who.int/iris/handle/10665/329480. License: CC BY-NC-SA 3.0 IGO. Accessed 24 Aug 2021

  • Woźniak E, Waszkowska E, Zimny T, Sowa S, Twardowski T (2019) The rapeseed potential in Poland and Germany in the context of production, legislation, and intellectual property rights. Front Plant Sci 10:1423

    Article  PubMed  PubMed Central  Google Scholar 

  • Xia X, Ji J, Yang Z, Han H, Huang C, Li Y, Zhang W (2020) Cadmium risk in the soil-plant system caused by weathering of carbonate bedrock. Chemosphere 254:126799

    Article  CAS  PubMed  Google Scholar 

  • Yang W, Gu S, Xin Y, Bello A, Sun W, Xu X (2018) Compost addition enhanced hyphal growth and sporulation of arbuscular mycorrhizal fungi without affecting their community composition in the soil. Front Microbiol 9:169

    Article  PubMed  PubMed Central  Google Scholar 

  • Yang X, Wan Y, Zheng Y, He F, Yu Z, Huang J, Wang H, Ok YS, Jiang Y, Gao B (2019) Surface functional groups of carbon-based adsorbents and their roles in the removal of heavy metals from aqueous solutions: A critical review. Chem Eng J 366:608–621

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yazici MA, Asif M, Tutus Y, Ortas I, Ozturk L, Lambers H, Cakmak I (2021) Reduced root mycorrhizal colonization as affected by phosphorus fertilization is responsible for high cadmium accumulation in wheat. Plant Soil 468:19–35

    Article  CAS  Google Scholar 

  • Yu H, Yang A, Wang K, Li Q, Ye D, Huang H, Zhang X, Wang Y, Zheng Z, Li T (2021) The role of polysaccharides functional groups in cadmium binding in root cell wall of a cadmium-safe rice line. Ecotoxicol Environ Saf 226:112818

    Article  CAS  PubMed  Google Scholar 

  • Zaller JG, Cantelmo C, Santos GD, Muther S, Gruber E, Pallua P, Mandl K, Friedrich B, Hofstetter I, Schmuckenschlager B, Faber F (2018) Herbicides in vineyards reduce grapevine root mycorrhization and alter soil microorganisms and the nutrient composition in grapevine roots, leaves, xylem sap and grape juice. Environ Sci Pollut Res 25:23215–23226

    Article  CAS  Google Scholar 

  • Zhang XF, Hu ZH, Yan TX, Lu RR, Peng CL, Li SS, Jing YX (2019) Arbuscular mycorrhizal fungi alleviate Cd phytotoxicity by altering Cd subcellular distribution and chemical forms in Zea mays. Ecotoxicol Environ Saf 171:352–360

    Article  CAS  PubMed  Google Scholar 

  • Zhang H, Tao R, Nie J, Zhou X, Wang W, Han FX, Ma Y (2022) Cadmium distribution, availability, and translocation in soil-oilseed rape (Brassica napus L.) system and its risk assessment. ACS Earth Space Chem 6(8):2053–2062

    Article  CAS  Google Scholar 

  • Zhao FJ, Wang P (2020) Arsenic and cadmium accumulation in rice and mitigation strategies. Plant Soil 446:1–21

    Article  CAS  Google Scholar 

  • Zhao FJ, Adams ML, Dumont C, McGrath SP, Chaudri AM, Nicholson FA, Chambers BJ, Sinclair AH (2004) Factors affecting the concentrations of lead in British wheat and barley grain. Environ Pollut 131:461–468

    Article  CAS  PubMed  Google Scholar 

  • Zhao FJ, Jiang RF, Dunham SJ, McGrath SP (2006) Cadmium uptake, translocation and tolerance in the hyperaccumulator Arabidopsis halleri. New Phytol 172:646–654

    Article  CAS  PubMed  Google Scholar 

  • Zhao FJ, Ma YB, Zhu YG, Tang Z, McGrath SP (2015) Soil contamination in China: Current status and mitigation strategies. Environ Sci Technol 49:750–759

    Article  CAS  PubMed  Google Scholar 

  • Zhou DM, Wang YJ, Cang L, Hao XZ, Luo XS (2004) Adsorption and cosorption of cadmium and glyphosate on two soils with different characteristics. Chemosphere 57:1237–1244

    Article  CAS  PubMed  Google Scholar 

  • Zhu HH, Chen C, Xu C, Zhu QH, Huang DY (2016a) Effects of soil acidification and liming on the phytoavailability of cadmium in paddy soils of central subtropical China. Environ Pollut 219:99–106

    Article  CAS  PubMed  Google Scholar 

  • Zhu C, Ling N, Guo J, Wang M, Guo S, Shen Q (2016b) Impacts of fertilization regimes on arbuscular mycorrhizal fungal (AMF) community composition were correlated with organic matter composition in maize rhizosphere soil. Front Microbiol 7:1840

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We thank Prof Dr Megan Ryan, The University of Western Australia for internal review of the paper and Dr M. Asif for his practical support in drawing the figures and checking the references

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Authors and Affiliations

  1. Faculty of Engineering and Natural Sciences, Sabanci University, 34956, Tuzla, Istanbul, Turkey

    Ismail Cakmak

  2. School of Biological Sciences and Institute of Agriculture, The University of Western Australia, 35 Stirling Highway, Crawley, Perth, WA, 6009, Australia

    Hans Lambers

  3. Box 744, Minnedosa, MB, R0J 1E0, Canada

    Cynthia A. Grant

  4. College of Resources and Environmental Sciences, Nanjing Agricultural University, Nanjing, 210095, China

    Fang-Jie Zhao

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Cakmak, I., Lambers, H., Grant, C.A. et al. Arbuscular mycorrhizal fungi: key players in avoiding cadmium accumulation in food crops. Plant Soil 484, 13–32 (2023). https://doi.org/10.1007/s11104-022-05802-w

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