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Effects of elevated CO2 on phenolics in black locust seedlings inoculated with arbuscular mycorrhizal fungi under cadmium pollution by 13C isotopic tracer technique

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Abstract

Aims

Phenolics can help plants mitigate stress of adverse environments. Elevated CO2 (eCO2) and arbuscular mycorrhizal fungi (AMF) may improve phenolics synthesis, however, the contribution of eCO2 to phenolics in plants colonized by AMF under heavy metal exposure is still unclear.

Methods

We investigated the effect of eCO2 (285 ppm above ambient CO2) on phenolic acids and flavonoids in black locust (Robinia pseudoacacia L.) grown in cadmium (Cd)-contaminated soils under Funneliformis mosseae (FM) colonization using 13C isotope tracer technique.

Results

Elevated CO2 significantly enhanced leaf and root Cd by 25.7% and 38.7%, respectively, and reduced total Cd by 36.7% in rhizosphere soils under FM colonization. Total phenolic acids decreased by 48.5% under eCO2 + FM relative to FM colonization. Elevated CO2 significantly decreased gallic acid, chlorogenic acid, p-hydroxybenzoic acid, caffeic acid, p-coumaric acid, ferulic acid, robinin, quercetin, kaempferol, and acacetin by 52.2%, 45.1%, 9.7%, 89.1%, 45.2%, 24.8%, 26.2%, 13.5%, 32.6%, and 34.1% under FM colonization, respectively, and the contribution of + 285 ppm CO2 to these compounds was 0.15, 0.33, 0.74, 0.14, 0.62, 0.38, 0.14, 0.23, 0.10, and 0.17 µg g−1 DW, respectively. The contribution decreased under FM colonization except for to chlorogenic acid, and the contribution was the most to total phenolic acids. Phenylalanine ammonia-lyase and nitrogen significantly affected phenolic acids and flavonoids synthesis.

Conclusions

The results could provide some insights into the contribution of eCO2 to plant resistance to heavy metals and plant sequestering heavy metals under AMF colonization.

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Data Availability

The datasets are available upon reasonable request.

References

  • Agrawal M, Deepak SS (2003) Physiological and biochemical responses of two cultivars of wheat to elevated levels of CO2 and SO2, singly and in combination. Environ Pollut 121:189–197

    Article  CAS  PubMed  Google Scholar 

  • Ahmad A, Hadi F, Ali N (2015) Effective phytoextraction of cadmium (cd) with increasing concentration of total phenolics and free proline in Cannabis sativa (L.) plant under various treatments of fertilizers, plant growth regulators and sodium salt. Int J Phytoremediation 17(1–6):56–65

    Article  CAS  PubMed  Google Scholar 

  • Ainsworth EA, Long SP (2005) What have we learned from 15 years of free-air CO2 enrichment (FACE)? A meta‐analytic review of the responses of photosynthesis, canopy properties and plant production to rising CO2. New Phytol 165:351–372

    Article  PubMed  Google Scholar 

  • Ajiboye BO, Ojo OA, Akuboh OS, Abiola OM, Idowu O, Amuzat AO (2018) Anti-hyperglycemic and anti-inflammatory activities of polyphenolic-rich extract of Syzygium cumini Linn leaves in alloxan-induced diabetic rats. J evidence-based Integr Med 23:2515690X18770630

    Article  CAS  Google Scholar 

  • Akindoyeni IA, Ogunsuyi OB, Aletor VA, Oboh G (2022) Effect of selenium biofortification on phenolic content and antioxidant properties of jute leaf (Corchorus olitorius). Vegetos 35:94–103

    Article  Google Scholar 

  • Akula R, Ravishankar GA (2011) Influence of abiotic stress signals on secondary metabolites in plants. Plant Signal Behav 6:1720–1731

    Article  Google Scholar 

  • Alizadeh S, Fallahi Gharagoz S, Pourakbar L, Siavash Moghaddam S, Jamalomidi M (2021) Arbuscular mycorrhizal fungi alleviate salinity stress and alter phenolic compounds of moldavian balm. Rhizosphere 19:100417

    Article  Google Scholar 

  • Amanifar S, Toghranegar Z (2020) The efficiency of arbuscular mycorrhiza for improving tolerance of Valeriana officinalis L. and enhancing valerenic acid accumulation under salinity stress. Ind Crops Prod 147:112234

    Article  CAS  Google Scholar 

  • Andrade SAL, Mali S, Sawaya ACHF, Bottcher A, Mazzafera P (2013) Association with arbuscular mycorrhizal fungi influences alkaloid synthesis and accumulation in Catharanthus roseus and Nicotiana tabacum plants. Acta Physiol Plant 35:867–880

    Article  CAS  Google Scholar 

  • Ayuso-Álvarez A, Simón L, Nuñez O, Rodríguez-Blázquez C, Martín-Méndez I, Bel-lán A, López-Abente G, Merlo J, Fernandez-Navarro P, Galán I (2019) Association between heavy metals and metalloids in topsoil and mental health in the adult population of Spain. Environ Res 179:108784

    Article  PubMed  Google Scholar 

  • Baslam M, Garmendia I, Goicoechea N (2011) Arbuscular mycorrhizal fungi (AMF) improved growth and nutritional quality of greenhouse grown lettuce. J Agric Food Chem 59:5504–5515

    Article  CAS  PubMed  Google Scholar 

  • Baslam M, Garmendia I, Goicoechea N (2012) Elevated CO2 may impair the beneficial effect of arbuscular mycorrhizal fungi on the mineral and phytochemical quality of lettuce: elevated CO2 reduced nutritional quality of mycorrhizal lettuces. Ann Appl Biol 161:180–191

    Article  CAS  Google Scholar 

  • Bernardo L, Carletti P, Badeck FW, Rizza F, Morcia C, Ghizzoni R, Rouphael Y, Colla G, Terzi V, Lucini L (2019) Metabolomic responses triggered by arbuscular mycorrhiza enhance tolerance to water stress in wheat cultivars. Plant Physiol Biochem 137:203–212

    Article  CAS  PubMed  Google Scholar 

  • Cai R, Yuan Y, Cui L, Wang Z, Yue T (2018) Cyclodextrin-assisted extraction of phenolic compounds: current research and future prospects. Trends Food Sci Technol 79:19–27

    Article  CAS  Google Scholar 

  • Chen J, Zhang HQ, Zhang XL, Tang M (2017) Arbuscular mycorrhizal symbiosis alleviates salt stress in black locust through improved photosynthesis, water status, and K+/Na+ homeostasis. Front Plant Sci 8:1739

    Article  PubMed  PubMed Central  Google Scholar 

  • Cheynier V, Comte G, Davies KM, Lattanzio V, Martens S (2013) Plant phenolics: recent advances on their biosynthesis, genetics, and ecophysiology. Plant Physiol Biochem 72:1–20

    Article  CAS  PubMed  Google Scholar 

  • Deckers JA, Nachtergaele FO, Spaargaren OC (1998) ISSS working group RB, world reference base for soil resources: introduction. Soils Trop Forest Ecosyst Characteristics Ecol Managem 41:21–28

    Google Scholar 

  • Dos Santos EL, Da Silva FA, Da Silva FSB (2017) Arbuscular mycorrhical fungi increase the phenolic compounds concentration in the dark of the stem of Libidibia ferrea in field conditions. Open Microbiol J 11:283–291

    Article  PubMed  PubMed Central  Google Scholar 

  • Ferrer JL, Austin MB, Stewart C, Noel JP (2008) Structure and function of enzymes involved in the biosynthesis of phenylpropanoids. Plant Physiol Biochem 46:356–370

    Article  CAS  PubMed  Google Scholar 

  • Frew A, Powell JR, Glauser G, Bennett AE, Johanson SN (2018) Mycorrhizal fungi enhance nutrient uptake but disarm defences in plant roots, promoting plant-parasitic nematode populations. Soil Biol Biochem 126:123–132

    Article  CAS  Google Scholar 

  • Gavito ME (2000) Atmospheric CO2 and mycorrhiza effects on biomass allocation and nutrient uptake of nodulated pea (Pisum sativum L.) plants. J Exp Bot 51:1931–1938

    Article  CAS  PubMed  Google Scholar 

  • Giovannetti M, Mosse B (1980) An evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytol 84:489–500

    Article  Google Scholar 

  • Habeeb TH, Abdel-Mawgoud M, Yehia RS, Khalil AMA, Saleh AM, AbdElgawad H (2020) Interactive impact of arbuscular mycorrhizal fungi and elevated CO on growth and functional food value of Thymus vulgare. J Fungi 6:168

    Article  CAS  Google Scholar 

  • Ibrahim MH, Jaafar HZE (2012) Impact of elevated carbon dioxide on primary, secondary metabolites and antioxidant responses of Eleais guineensis Jacq. (oil palm) seedlings. Molecules 17:5195–5211

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • IPCC (2021) Global carbon and other biogeochemical cycles and feedbacks. In: Masson-Delmotte V, Zhai P, Pirani A, Connors SL, Péan C, Berger S, Caud N, Chen Y, Goldfarb L, Gomis MI, Huang M, Leitzell K, Lonnoy E, Matthews JBR, Maycock TK, Waterfield T, Yelekçi O, Yu R, Zhou B (eds) Climate Change 2021: the physical science basis. Contribution of working group I to the sixth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge, pp 673–1816

    Google Scholar 

  • Jansa J, Mozafar A, Frossard E (2003) Long-distance transport of P and zn through the hyphae of an arbuscular mycorrhizal fungus in symbiosis with maize. Agronomie 23:481–488

    Article  CAS  Google Scholar 

  • Jaouni SA, Saleh AM, Wadaan MAM, Hozzein WN, Selim S, AbdElgawad H (2018) Elevated CO2 induces a global metabolic change in basil (Ocimum basilicum L.) and peppermint (Mentha piperita L.) and improves their biological activity. J Plant Physiol 224–225:121–131

    Article  PubMed  Google Scholar 

  • Jia X, Wang W, Chen Z, He Y, Liu J (2014) Concentrations of secondary metabolites in tissues and root exudates of wheat seedlings changed under elevated atmospheric CO2 and cadmium-contaminated soils. Environ Exp Bot 107:134–143

    Article  CAS  Google Scholar 

  • Jia X, Zhang CY, Zhao YH, Liu T, He YH (2018) Three years of exposure to lead and elevated CO2 affects lead accumulation and leaf defenses in Robinia pseudoacacia L. seedlings. J Hazard Mater 349:215–223

    Article  CAS  PubMed  Google Scholar 

  • Jia X, Zhao YH, Liu T, He YH (2017) Leaf defense system of Robinia pseudoacacia L. seedlings exposed to 3 years pf elevated atmospheric CO2 and Cd-contaminated soils. Sci Total Environ 605–606:48–57

    Article  PubMed  Google Scholar 

  • Jia X, Zhao Y, Liu T, Huang S (2016) Elevated CO2 affects secondary metabolites in Robinia pseudoacacia L. seedlings in Cd- and Pb-contaminated soils. Chemosphere 160:199–207

    Article  CAS  PubMed  Google Scholar 

  • Jifon JL, Graham JH, Drouillard DL, Syvertsen JP (2002) Growth depression of mycorrhizal Citrus seedlings grown at high phosphorus supply is mitigated by elevated CO2. New Phytologist 153:133–142

    Article  Google Scholar 

  • Johny L, Cahill DM, Adholeya A (2021) AMF enhance secondary metabolite production in ashwagandha, licorice, and marigold in a fungi-host specific manner. Rhizosphere 17:100314

    Article  Google Scholar 

  • Jun SY, Sattler SA, Cortez GS, Vermerris W, Sattler SE, Kang C (2018) Biochemical and structural analysis of substrate specificity of a phenylalanine ammonia-lyase. Plant Physiol 176:1452–1468

    Article  CAS  PubMed  Google Scholar 

  • Kang S, Kim JE, Zhen S, Kim J (2022) Mild-intensity UV - a radiation applied over a long duration can improve the growth and phenolic contents of sweet basil. Front Plant Sci 13:858433

    Article  PubMed  PubMed Central  Google Scholar 

  • Kapoor R, Chaudhary V, Bhatnagar AK (2007) Effects of arbuscular mycorrhiza and phosphorus application on artemisinin concentration in Artemisia annua L. Mycorrhiza 17:581–587

    Article  CAS  PubMed  Google Scholar 

  • Kaur S, Suseela V (2020) Unraveling arbuscular mycorrhiza-induced changes in plant primary and secondary metabolome. Metabolites 10:335

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kennedy DO, Wightman EL (2011) Herbal extracts and phytochemicals: plant secondary metabolites and the enhancement of human brain function. Adv Nutrition 2:32–50

    Article  CAS  Google Scholar 

  • Khan Y, Shah S, Hui T (2022) The roles of arbuscular mycorrhizal fungi in influencing plant nutrients, photosynthesis, and metabolites of cereal crops - a review. Agronomy 12:2191

    Article  CAS  Google Scholar 

  • Khan Y, Yang X, Zhang X, Yaseen T, Shi L, Zhang T (2021) Arbuscular mycorrhizal fungi promote plant growth of Leymus chinensis (trin.) Tzvelev by increasing the metabolomics activity under nitrogen addition. Grassland Sci 67:128–138

    Article  CAS  Google Scholar 

  • Khanam D, Mridha MAU, Solaiman ARM, Hossain T (2006) Effect of edaphic factors on root colonization and spore population of arbuscular mycorrhizal fungi. Institute of Tropical Agriculture, Kyushu University, 29:97–104

  • Kováčik J, Klejdus B, Hedbavny J, Zoń J (2011) Significance of phenols in cadmium and nickel uptake. J Plant Physiol 168:576–584

    Article  PubMed  Google Scholar 

  • Li X, Jiang T, Chao Q, Xu H, Yuan J, Lin E (2015) The core conclusions and interpretation of working group II contribution to the fifth assessment report of the intergovernmental panel on climate change. Chin J Urban Environ Stud 3:1550004

    Article  Google Scholar 

  • Li G, Shi Y, Chen X (2008) Effects of elevated CO2 and O3 on phenolic compounds in spring wheat and maize leaves. Bull Environ Contam Toxicol 81:436–439

    Article  CAS  PubMed  Google Scholar 

  • Li Z, Tang S, Deng X, Wang R, Song Z (2010) Contrasting effects of elevated CO2 on Cu and Cd uptake by different rice varieties grown on contaminated soils with two levels of metals: implication for phytoextraction and food safety. J Hazard Mater 177:352–361

    Article  CAS  PubMed  Google Scholar 

  • Liu L, Li J, Yue F, Yan X, Wang F, Bloszies S, Wang Y (2018) Effects of arbuscular mycorrhizal inoculation and biochar amendment on maize growth, cadmium uptake and soil cadmium speciation in Cd-contaminated soil. Chemosphere 194:495–503

    Article  CAS  PubMed  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2–∆∆CT method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Luo Y, Su B, Currie WS, Dukes JS, Finzi A, Hartwig U, Hungate B, Mc Murtrie RE, Oren R, Parton WJ, Pataki DE, Shaw MR, Zak DR, Field CB (2004) Progressive nitrogen limitation of ecosystem responses to rising atmospheric carbon dioxide. Bio Science 54:731

    Google Scholar 

  • Lyu C, Zhang X, Huang L, Yuan X, Xue C, Chen X (2022) Widely targeted metabolomics analysis characterizes the phenolic compounds profiles in mung bean sprouts under sucrose treatment. Food Chem 395:133601

    Article  CAS  PubMed  Google Scholar 

  • Malekzadeh E, Alikhani HA, Savaghebi-Firoozabadi GR, Zarei M (2011) Influence of arbuscular mycorrhizal fungi and an improving growth bacterium on cd uptake and maize growth in Cd-polluted soils. Span J Agric Res 9(9):1213–1223

    Article  Google Scholar 

  • Manach C, Scalbert A, Morand C, Rémésy C, Jiménez L (2004) Polyphenols: food sources and bioavailability. Am J Clin Nutrition 79:727–747

    Article  CAS  Google Scholar 

  • McGrath SP, Zhao FJ (2003) Phytoextraction of metals and metalloids from contaminated soils. Curr Opinion Biotechnol 14:277–282

    Article  CAS  Google Scholar 

  • Qin J, Xi W, Rahmlow A, Kong H, Zhang Z, Shangguan Z (2016) Effects of forest plantation types on leaf traits of Ulmus pumila and Robinia pseudoacacia on the Loess Plateau, China. Ecol Eng 97:416–425

    Article  Google Scholar 

  • Räisänen T, Ryyppö A, Kellomäki S (2008) Effects of elevated CO2 and temperature on monoterpene emission of scots pine (Pinus sylvestris L). Atmos Environ 42:4160–4171

    Article  Google Scholar 

  • Rogers HH, Runion GB, Krupa SV (1994) Plant responses of atmospheric CO2 enrichment with emphasis on roots and the rhizosphere. Environ Pollut 83:155–189

    Article  CAS  PubMed  Google Scholar 

  • Saleh AM, Abdel-Mawgoud M, Hassan AR, Habeeb TH, Yehia RS, AbdElgawad H (2020) Global metabolic changes induced by arbuscular mycorrhizal fungi in oregano plants grown under ambient and elevated levels of atmospheric CO2. Plant Physiol Biochem 151:255–263

    Article  CAS  PubMed  Google Scholar 

  • Sancho AI, Bartolomé B, Gómez-Cordovés C, Williamson G, Faulds CB (2001) Release of ferulic acid from cereal residues by barley enzymatic extracts. J Cereal Sci 34:173–179

    Article  CAS  Google Scholar 

  • Schliemann W, Ammer C, Strack D (2008) Metabolite profiling of mycorrhizal roots of Medicago truncatula. Phytochemistry 69:112–146

    Article  CAS  PubMed  Google Scholar 

  • Sinclair TR, Horie T (1989) Leaf Nitrogen, Photosynthesis, and crop radiation use efficiency-a review. Crop Sci 29:90–98

    Article  Google Scholar 

  • Smith SE, Smith FA, Jakobsen I (2003) Mycorrhizal fungi can dominate phosphate supply to plants irrespective of growth responses. Plant Physiol 133:16–20

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tingey DT, Phillips DL, Johnson MG (2000) Elevated CO2 and conifer roots: effects on growth, life span, and turnover. New Phytologist 147:87–103

    Article  CAS  Google Scholar 

  • Toussaint JP, Smith FA, Smith SE (2007) Arbuscular mycorrhizal fungi can induce the production of phytochemicals in sweet basil irrespective of phosphorus nutrition. Mycorrhiza 17:291–297

    Article  CAS  PubMed  Google Scholar 

  • Vardhan KH, Kumar PS, Pand RC (2019) A review on heavy metal pollution, toxicity and remedial measures: current trends and future perspectives. J Mol Liq 290:111197

    Article  CAS  Google Scholar 

  • Vareda JP, Valente AJM, Durães L (2019) Assessment of heavy metal pollution from anthropogenic activities and remediation strategies: a review. J Environ Manag 246:101–118

    Article  CAS  Google Scholar 

  • Vierheilig H, Coughlan AP, Wyss U, Piché Y (1998) Ink and vinegar, a simple staining technique for arbuscular mycorrhizal fungi. Appl Environ Microbiol 64:5004–5007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang F, Guo W, Ma PK, Pan L, Zhang J (2016) Effects of arbuscular mycorrhizal fungi on the growth and ce uptake of maize grown in ce-contaminated soils. Huan Jing Ke Xue 37(1):309–316 (In Chinese)

  • Wang L, Jia X, Zhao YH, Zhang CY, Gao YF, Li XD, Cao KM, Zhang NJ (2021a) Effects of elevated CO2 on arbuscular mycorrhizal fungi associated with Robinia pseudoacacia L. grown in cadmium-contaminated soils. Sci Total Environ 768:144453

    Article  CAS  PubMed  Google Scholar 

  • Wang ZW, Jia X, Yan ZK, Cao KM, Zhang CY, Wang L, Zhang NJ, Gao YF (2021b) Responses of phenolic acids accumulation in the rhizosphere soil of Robinia pseudoacacia L. seedlings to the combination of elevated atmospheric CO2 and cd exposure. Chin J Ecol 40:2067–2075 (In Chinese))

    Google Scholar 

  • Wang L, Jia X, Zhao Y, Zhang C, Zhao J (2022) Effect of arbuscular mycorrhizal fungi in roots on antioxidant enzyme activity in leaves of Robinia pseudoacacia L. seedlings under elevated CO2 and cd exposure. Environ Pollut 294:118652

    Article  CAS  PubMed  Google Scholar 

  • Wang YJ, Zhang CY, Wang L, Zhao YH, Gao YF, Jia X (2023) Influence of arbuscular mycorrhizal fungi on low molecular weight soluble compounds in the rhizosphere soil of black locust seedlings grown in cadmium-contaminated soils under elevated CO2 scenarios. Plant Soil 486:469–486

    Article  CAS  Google Scholar 

  • Watanabe CK, Sato S, Yanagisawa S, Uesono Y, Terashima I, Noguchi K (2014) Effects of elevated CO2 on levels of primary metabolites and transcripts of genes encoding respiratory enzymes and their diurnal patterns in Arabidopsis thaliana: possible relationships with respiratory rates. Plant Cell Physiol 55:341–357

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu YH, Wang H, Liu M, Li B, Chen X, Ma YT, Yan ZY (2021) Effects of native arbuscular mycorrhizae isolated on root biomass and secondary metabolites of Salvia miltiorrhiza Bge. Front Plant Sci 12:617892

    Article  PubMed  PubMed Central  Google Scholar 

  • Xiao Y, Zhao Z, Chen L, Li Y (2020) Arbuscular mycorrhizal fungi and organic manure have synergistic effects on Trifolium repens in Cd-contaminated sterilized soil but not in natural soil. Appl Soil Ecol 149:103485

    Article  Google Scholar 

  • Xie W, Hao Z, Zhou X, Jiang X, Xu L, Wu S, Zhao A, Zhang X, Chen B (2018) Arbuscular mycorrhiza facilitates the accumulation of glycyrrhizin and liquiritin in Glycyrrhiza uralensis under drought stress. Mycorrhiza 28:285–300

    Article  CAS  PubMed  Google Scholar 

  • Xiong H, Duan C, A XX, Chen MH (2013) Response of scutellarin content to heavy metal in Erigeron breviscapus. International Journal of Environmental Science and Development 4:277–281

  • Xu M, Gao D, Fu S, Lu X, Wu S, Han X, Yang G, Feng Y (2020) Long-term effects of vegetation and soil on the microbial communities following afforestation of farmland with Robinia pseudoacacia plantations. Geoderma 367:114263

    Article  CAS  Google Scholar 

  • 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. J Hazard Mater 406:124325

    Article  CAS  PubMed  Google Scholar 

  • Zavalloni C, Vicca S, Büscher M, Providencia IEDL, Boulois HDD, Declerck S, Nijs I, Ceulemans R (2012) Exposure to warming and CO2 enrichment promotes greater above-ground biomass, nitrogen, phosphorus and arbuscular mycorrhizal colonization in newly established grasslands. Plant Soil 359:121–136

    Article  CAS  Google Scholar 

  • Zhang CY, Jia X, Zhao YH, Wang L, Cao KM, Zhang NJ, Gao YF, Wang ZW (2021) The combined effects of elevated atmospheric CO2 and cadmium exposure on flavonoids in the leaves of Robinia pseudoacacia L. seedlings. Ecotox Ecotoxicol Environ Saf 210:111878

    Article  CAS  Google Scholar 

  • Zhang Y, Li SF, Wu XW (2008) Pressurized liquid extraction of flavonoids from Houttuynia cordata Thunb. Sep Purif Technol 58:305–310

  • Zhao YH, Jia X, Wang WK, Liu T, Huang SP, Yang MY (2016) Growth under elevated air temperature alters secondary metabolites in Robinia pseudoacacia L. seedlings in Cd- and Pb-contaminated soils. Sci Total Environ 565:586–594

    Article  CAS  PubMed  Google Scholar 

  • Zhao FJ, Tang Z, Song JJ, Huang XY, Wang P (2022) Toxic metals and metalloids: Uptake, transport, detoxification, phytoremediation, and crop improvement for safer food. Mol Plant 15:27–44

    Article  PubMed  Google Scholar 

  • Zhu X, Song F, Liu S, Liu F (2016) Arbuscular mycorrhiza improve growth, nitrogen uptake, and nitrogen use efficiency in wheat grown under elevated CO2. Mycorrhiza 26:133–140

    Article  CAS  PubMed  Google Scholar 

  • Zubek S, Rola K, Szewczyk A, Majewska ML, Turnau K (2015) Enhanced concentrations of elements and secondary metabolites in Viola tricolor L. induced by arbuscular mycorrhizal fungi. Plant Soil 390:129–142

    Article  CAS  Google Scholar 

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Acknowledgements

This work was jointly supported by the National Natural Science Foundation of China (grant Nos. 31870582 and 31270665) and the Project Supported by Shaanxi Key Laboratory of Land Consolidation of China (Program No. 2019TD-01).

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Authors and Affiliations

  1. Key Laboratory of Subsurface Hydrology and Ecological Effects in Arid Region of Ministry of Education, Key Laboratory of Eco-hydrology and Water Security in Arid and Semi-arid Regions of Ministry of Water Resources, School of Water and Environment, Chang’an University, Xi’an, 710054, People’s Republic of China

    Liangyu Huang, Xiaojuan Feng, Xuelian Yang & Chunyan Zhang

  2. Key Laboratory of Subsurface Hydrology and Ecological Effects in Arid Region of Ministry of Education, Shaanxi Key Laboratory of Land Consolidation, Key Laboratory of Eco-hydrology and Water Security in Arid and Semi-arid Regions of Ministry of Water Resources, School of Water and Environment, Chang’an University, No. 126, Yanta Road, Xi’an, 710054, People’s Republic of China

    Xia Jia

  3. School of Land Engineering, Chang’an University, Xi’an, 710054, People’s Republic of China

    Yonghua Zhao & Yufeng Gao

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  1. Liangyu Huang
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Contributions

Liangyu Huang performed experiments, analyzed data, and wrote the manuscript. Xia Jia planned and designed the research and edited and reviewed the manuscript. Yonghua Zhao, Xiaojuan Feng, Xuelian Yang, Chunyan Zhang, and Yufeng Gao provided some help for the experiments.

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Huang, L., Jia, X., Zhao, Y. et al. Effects of elevated CO2 on phenolics in black locust seedlings inoculated with arbuscular mycorrhizal fungi under cadmium pollution by 13C isotopic tracer technique. Plant Soil 494, 547–566 (2024). https://doi.org/10.1007/s11104-023-06303-0

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