Abstract
The concentrations of cadmium (Cd) and zinc (Zn) in arable lands exceed the maximum permissible levels due to the excessive use of phosphorus fertilizers and fungicides by farmers. The increasing issues related to the application of agrochemicals have lead to the demand for the implementation of sustainable agricultural approaches. Association of arbuscular mycorrhizae with crop plants is an appropriate strategy due to the potential of these microorganisms to augment the metals tolerance of plants through the immobilization of Cd and Zn in an eco-friendly manner. In the present study, 45 d old Zea mays (var. CoHM6) plants inoculated with AM fungi (Claroideoglomus claroideum) were exposed to 1.95 g Zn Kg−1 soil and 0.45 g Cd Kg−1 soil. The major objective of this study was to determine the metabolic alterations in the leaves and roots of mycorrhizal and non-mycorrhizal plants exposed to CdCl2 and ZnSO4. Both non AM and AM plants exhibited alterations in the quantity of primary and secondary metabolites on exposure to Zn and Cd toxicity. Moreover, Zn and Cd-induced accumulation of γ-sitosterol reduced the quantity of neophytadiene (a well-known terpenoid) and aided the production of 3-β-acetoxystigmasta-4,6,22-triene in maize leaves. Mycorrhization and heavy metal toxicity induced significant metabolic changes in the roots by producing 4,22-stigmastadiene-3-one, eicosane, 9,19-cyclolanost-24-en-3-ol, pentacosane, oxalic acid, heptadecyl hexyl ester, l-norvaline, and n-(2-methoxyethoxycarbonyl). In addition, the metal-induced variations in leaf and root lignin composition were characterized with the aid of the FTIR technique. Mycorrhization improved the tolerance of maize plants to Cd and Zn toxicity by stabilizing these metal ions in the soil and/or limiting their uptake into the plants, thus ensuring normal metabolic functions of their roots and shoots.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Availability of data and materials
Data sharing is not applicable to this article as all new created data is already contained within this article.
References
Aboobucker SI, Suza WP (2019) Why do plants convert sitosterol to stigmasterol? Front Plant Sci 10:354. https://doi.org/10.3389/fpls.2019.00354
Adeyemi NO, Atayese MO, Sakariyawo OS, Azeez JO, Sobowale SPA, Olubode A, Adeoye S (2021) Alleviation of heavy metal stress by arbuscular mycorrhizal symbiosis in Glycine max (L.) grown in copper, lead and zinc contaminated soils. Rhizosphere 18:100325. https://doi.org/10.1016/j.rhisph.2021.100325
Ahmad I, Zaib S, Alves PCMS, Luthe DS, Bano A, Shakeel SN (2019) Molecular and physiological analysis of drought stress responses in Zea mays treated with plant growth promoting rhizobacteria. Biol Plant 63:536–547. https://doi.org/10.32615/bp.2019.092
Ai TN, Naing AH, Yun BW, Lim SH, Kim CK (2018) Overexpression of RsMYB1 enhances anthocyanin accumulation and heavy metal stress tolerance in transgenic petunia. Front Plant Sci 9:1388. https://doi.org/10.3389/fpls.2018.01388
Allan JE (1969) The preparation of agricultural samples for analysis by Atomic Absorption Spectrometry. Varian Techtron Bulletin SIS Edn 12:69
Andrade SA, Gratão PL, Azevedo RA, Silveira AP, Schiavinato MA, Mazzafera P (2010) Biochemical and physiological changes in jack bean under mycorrhizal symbiosis growing in soil with increasing Cu concentrations. Environ Exp Bot 68:198–207. https://doi.org/10.1016/j.envexpbot.2009.11.009
Andrejić G, Gajić G, Prica M, Dželetović Ž, Rakić T (2018) Zinc accumulation, photosynthetic gas exchange, and chlorophyll a fluorescence in Zn-stressed Miscanthus× giganteus plants. Photosynthetica 56:1249–1258. https://doi.org/10.1007/s11099-018-0827-3
Bartram S, Jux A, Gleixner G, Boland W (2006) Dynamic pathway allocation in early terpenoid biosynthesis of stress-induced lima bean leaves. Phytochemistry 67:1661–1672. https://doi.org/10.1016/j.phytochem.2006.02.004
Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207. https://doi.org/10.1007/BF00018060
Begum N, Qin C, Ahanger MA, Raza S, Khan MI, Ashraf M et al. (2019) Role of arbuscular mycorrhizal fungi in plant growth regulation: implications in abiotic stress tolerance. Front Plant Sci 10:1068
Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of proteins utilizing the principle of protein dye binding. Anal Biochem 72:248–54
Burleigh SH, Kristensen BK, Bechmann IE (2003) A plasma membrane zinc transporter from Medicago truncatula is up-regulated in roots by Zn fertilization, yet down-regulated by arbuscular mycorrhizal colonization. Plant Mol Biol 52:1077–1088. https://doi.org/10.1023/A:1025479701246
Chen JX, Wang XF (2006) Guidance for Plant Physiological Experiment. South China University of Technology Press, Guangzhou, China
Copetta A, Lingua G, Berta G (2006) Effects of three AM fungi on growth, distribution of glandular hairs, and essential oil production in Ocimum basilicum L. var. Genovese. Mycorrhiza 16:485–494. https://doi.org/10.1007/s00572-006-0065
Danneberg G, Latus C, Zimmer W, Hundeshagen B, Bothe H (1993) Influence of vesicular-arbuscular mycorrhiza on phytohormone balances in maize (Zea mays L.). J Plant Physiol 141:33–39
Davies KM, Albert NW, Zhou Y, Schwinn KE (2018) Functions of flavonoid and βlain pigments in abiotic stress tolerance in plants. Annu Rev Plant Biol 41:21–62. https://doi.org/10.1002/9781119312994.apr0604
Dell’Amico E, Cavalca L, Andreoni V (2008) Improvement of Brassica napus growth under cadmium stress by cadmium-resistant rhizobacteria. Soil Biol Biochem 40:74–84. https://doi.org/10.1016/j.soilbio.2007.06.024
Domínguez-Robles J, Sánchez R, Espinosa E, Savy D, Mazzei P, Piccolo A, Rodríguez A (2017) Isolation and characterization of gramineae and fabaceae soda lignins. Int J Mol Sci 18:327. https://doi.org/10.3390/ijms18020327
Dubois M, Gilles KA, Hamilton JK, Rebers PT, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356. https://doi.org/10.1021/ac60111a017
Ef A, Abeer H, Alqarawi AA, Hend AA (2015) Alleviation of adverse impact of cadmium stress in sunflower (Helianthus annuus L.) by arbuscular mycorrhizal fungi. Pak J Bot 47:785–795
El Dakak RA, Hassan IA (2020) The alleviative effects of salicylic acid on physiological indices and defense mechanisms of maize (Zea Mays L. Giza 2) stressed with cadmium. Environ Processes 7:873–884
Folin O, Denis W (1915) A colorimetric method for the determination of phenol (and derivatives) in urine. J Biol Chem 22:305–308. https://doi.org/10.1016/S0021-9258(18)87648-7
Garg N, Chandel S (2012) Role of arbuscular mycorrhizal (AM) fungi on growth, cadmium uptake, osmolyte, and phytochelatin synthesis in Cajanus cajan (L.) Millsp. under NaCl and Cd stresses. J Plant Growth Regul 31:292–308. https://doi.org/10.1007/s00344-011-9239-3
Garg N, Singh S (2018) Arbuscular mycorrhiza Rhizophagus irregularis and silicon modulate growth, proline biosynthesis and yield in Cajanus cajan L. Millsp. (pigeon pea) genotypes under cadmium and zinc stress. J Plant Growth Regul 37:46–63. https://doi.org/10.1007/s00344-017-9708-4
Garg N, Singla P, Bhandari P (2015) Metal uptake, oxidative metabolism, and mycorrhization in pigeon pea and pea under arsenic and cadmium stress. Turk J Agric For 39:234–250
Gao J, Chen B, Lin H, Liu Y, Wei Y, Chen F, Li W (2020) Identification and characterization of the glutathione S-transferase (GST) family in radish reveals a likely role in anthocyanin biosynthesis and heavy metal stress tolerance. Gene 743:144484. https://doi.org/10.3389/fpls.2018.01388
Ghaffari H, Tadayon MR, Bahador M, Razmjoo J (2021) Investigation of the proline role in controlling traits related to sugar and root yield of sugar beet under water deficit conditions. Agric Water Manag 243:106448. https://doi.org/10.1016/j.agwat.2020.106448
Gonzalez-Chavez MC, Carrillo-Gonzalez R, Wright SF, Nichols KA (2004) The role of glomalin, a protein produced by arbuscular mycorrhizal fungi, in sequestering potentially toxic elements. Environ Pollut 130:317–323. https://doi.org/10.1016/j.envpol.2004.01.004
Grover N, Patni V (2013) Phytochemical characterization using various solvent extracts and GC-MS analysis of methanolic extract of Woodfordia fruticosa (L) Kurz. Leaves. Int J Pharm Sci 5:91–5
Gurrieri L, Merico M, Trost P, Forlani G, Sparla F (2020) Impact of drought on soluble sugars and free proline content in selected Arabidopsis mutants. Biology 9:367. https://doi.org/10.3390/biology9110367
Hashem A, Abd-Allah EF, Alqarawi AA, Al Huqail AA, Egamberdieva D, Wirth S (2016b) Alleviation of cadmium stress in Solanum lycopersicum L. by arbuscular mycorrhizal fungi via induction of acquired systemic tolerance. Saudi J Biol Sci 23:272–281. https://doi.org/10.1016/j.sjbs.2015.11.002
Hashem A, Abd-Allah EF, Alqarawi AA, Egamberdieva D (2016a) Bioremediation of adverse impact of cadmium toxicity on Cassia italica Mill by arbuscular mycorrhizal fungi. Saudi J Biol Sci 23:39–47. https://doi.org/10.1016/j.sjbs.2015.11.007
Heidarabadi MD, Ghanati F, Fujiwara T (2011) Interaction between boron and aluminum and their effects on phenolic metabolism of Linum usitatissimum L. roots. Plant Physiol Biochem 49:1377–1383. https://doi.org/10.1016/j.plaphy.2011.09.008
Idrees M, Naeem M, Aftab T, Khan MMA (2013) Salicylic acid restrains nickel toxicity, improves antioxidant defence system and enhances the production of anticancer alkaloids in Catharanthus roseus (L.). J. Hazard Mater 252:367–374. https://doi.org/10.1016/j.jhazmat.2013.03.005.
Janeeshma E, Puthur JT (2020) Direct and indirect influence of arbuscular mycorrhizae on enhancing metal tolerance of plants. Arch Microbiol 202:1–16. https://doi.org/10.1007/s00203-019-01730-z
Janeeshma E, Rajan VK, Puthur (2020) Spectral variations associated with anthocyanin accumulation; an apt tool to evaluate zinc stress in Zea mays L. Chem Ecol 31:1–18
Jimoh MO, Afolayan AJ (2020) Heavy metal uptake and growth characteristics of Amaranthus caudatus L. under five different soils in a controlled environment. Notulae Botanicae Horti Agrobotanici Cluj-Napoca 48:417–425
Kandziora-Ciupa M, Nadgórska-Socha A, Barczyk G, Ciepał R (2017) Bioaccumulation of heavy metals and ecophysiological responses to heavy metal stress in selected populations of Vaccinium myrtillus L. and Vaccinium vitis-idaea L. Ecotoxicology 26:966–980. https://doi.org/10.1007/s10646-017-1825-0
Katahira R, Elder TJ, Beckham GT (2018) A brief introduction to lignin structure. 1–20. https://doi.org/10.1039/9781788010351-00001
Kaya C, Ashraf M, Akram NA (2018) Hydrogen sulfide regulates the levels of key metabolites and antioxidant defense system to counteract oxidative stress in pepper (Capsicum annuum L.) plants exposed to high zinc regime. Environ Sci Pollut Res 25:12612–12618. https://doi.org/10.1007/s11356-018-1510-8
Kısa D, Elmastaş M, Öztürk L, Kayır Ö (2016) Responses of the phenolic compounds of Zea mays under heavy metal stress. Appl Biol Chem 59:813–820. https://doi.org/10.1007/s13765-016-0229-9
Kothari SK, Marschner H, Römheld V (1991) Contribution of the VA mycorrhizal hyphae in acquisition of phosphorus and zinc by maize grown in a calcareous soil. Plant Soil 131:177–185
Kumar P, Dwivedi P (2018) Putrescine and Glomus mycorrhiza moderate cadmium actuated stress reactions in Zea mays L. by means of extraordinary reference to sugar and protein. Vegetos 31:74–77. https://doi.org/10.5958/2229-4473.2018.00076.9
Labidi O, Vives-Peris V, Gómez-Cadenas A, Pérez-Clemente RM, Sleimi N (2021) Assessing of growth, antioxidant enzymes, and phytohormone regulation in Cucurbita pepo under cadmium stress. Food Sci Nutr 9:2021–2031. https://doi.org/10.1002/fsn3.2169
Landi M, Guidi L, Pardossi A, Tattini M, Gould KS (2014) Photoprotection by foliar anthocyanins mitigates effects of boron toxicity in sweet basil (Ocimum basilicum). Planta 240:941–953. https://doi.org/10.1007/s00425-014-2087-1
Leyval C, Joner EJ (2001) Bioavailability of heavy metals in the mycorrhizosphere. In: Gobran GR, Wenze WW, Lombi E (Eds.) Trace elements in the rhizosphere. CRC Press, New York, NY, p 173–193
Lippold F, vom Dorp K, Abraham M, Hölzl G, Wewer V, Yilmaz JL et al. (2012) Fatty acid phytyl ester synthesis in chloroplasts of Arabidopsis. Plant Cell 24:2001–2014. https://doi.org/10.1105/tpc.112.095588
Liu L, Gong Z, Zhang Y, Li P (2014) Growth, cadmium uptake and accumulation of maize (Zea mays L.) under the effects of arbuscular mycorrhizal fungi. Ecotoxicology 23:1979–1986. https://doi.org/10.1007/s10646-014-1331-6
Liu Z, Bai Y, Luo L, Wan J, Wang W, Zhao G (2021) Effects of high dose copper on plant growth and mineral nutrient (Zn, Fe, Mg, K, Ca) uptake in spinach. Environ Sci Pollut Res 1:11. https://doi.org/10.1007/s11356-021-13395-7
Lokhande RS, Singare PU, Pimple DS (2011) Toxicity study of heavy metals pollutants in waste water effluent samples collected from Taloja industrial estate of Mumbai, India. Resources Environ 1:13–19. https://doi.org/10.5923/j.re.20110101.02
Mancinelli AL, Yang CPH, Lindquist P, Anderson OR, Rabino I (1975) Photocontrol of anthocyanin synthesis: III. The action of streptomycin on the synthesis of chlorophyll and anthocyanin. Plant Physiol 55:251–257. https://doi.org/10.1104/pp.55.2.251
Manquián-Cerda K, Escudey M, Zúñiga G, Arancibia-Miranda N, Molina M, Cruces E (2016) Effect of cadmium on phenolic compounds, antioxidant enzyme activity and oxidative stress in blueberry (Vaccinium corymbosum L.) plantlets grown in vitro. Ecotoxicol Environ Saf 133:316–326. https://doi.org/10.1016/j.ecoenv.2016.07.029
Mendoza-Soto AB, Naya L, Leija A, Hernández G (2015) Responses of symbiotic nitrogen-fixing common bean to aluminum toxicity and delineation of nodule responsive microRNAs. Front Plant Sci 6:587
Miransari M (2010) Contribution of arbuscular mycorrhizal symbiosis to plant growth under different types of soil stress. Plant Biol 12:563–569
Mirecki RM, Teramura AH (1984) Effects of ultraviolet-B irradiance on soybean: V. The dependence of plant sensitivity on the photosynthetic photon flux density during and after leaf expansion. Plant Physiol 74:475–480. https://doi.org/10.1104/pp.74.3.475
Mirshad PP, Puthur JT (2016) Arbuscular mycorrhizal association enhances drought tolerance potential of promising bioenergy grass (Saccharum arundinaceum retz.). Environ Monit Assess 188:1–20. https://doi.org/10.1007/s10661-016-5428-7
Mishra B, Sangwan NS (2019) Amelioration of cadmium stress in Withania somnifera by ROS management: active participation of primary and secondary metabolism. Plant Growth Regul 87:403–412. https://doi.org/10.1007/s10725-019-00480-8
Mishra B, Sangwan RS, Mishra S, Jadaun JS, Sabir F, Sangwan NS (2014) Effect of cadmium stress on inductive enzymatic and nonenzymatic responses of ROS and sugar metabolism in multiple shoot cultures of Ashwagandha (Withania somnifera Dunal). Protoplasma 251:1031–1045. https://doi.org/10.1007/s00709-014-0613-4
Mitra S, Pramanik K, Sarkar A, Ghosh PK, Soren T, Maiti TK (2018) Bioaccumulation of cadmium by Enterobacter sp. and enhancement of rice seedling growth under cadmium stress. Ecotoxicol Environ Saf 156:183–196. https://doi.org/10.1016/j.ecoenv.2018.03.001
Moore S, Stein WH (1948) Photometric ninhydrin method for use in the chromatography of amino acids. J Biol Chem 176:367–388
Naz R, Sarfraz A, Anwar Z, Yasmin H, Nosheen A, Keyani R, Roberts TH (2021) Combined ability of salicylic acid and spermidine to mitigate the individual and interactive effects of drought and chromium stress in maize (Zea mays L.). Plant Physiol Biochem 159:285–300. https://doi.org/10.1016/j.plaphy.2020.12.022
Phillips JM, Hayman DS (1970) Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans. Br Mycol Soc 55:158–161. https://doi.org/10.1016/S0007-1536(70)80110-3
Raj H, Sharma SD (2009) Integration of soil solarization and chemical sterilization with beneficial microorganisms for the control of white root rot and growth of nursery apple. Sci Hortic 119:126–131
Rivero J, Gamir J, Aroca R, Pozo MJ, Flors V (2015) Metabolic transition in mycorrhizal tomato roots. Front Microbiol 6:598. https://doi.org/10.3389/fmicb.2015.00598
Rizwan M, Ali S, Abbas T, Adrees M, Zia-ur-Rehman M, Ibrahim M et al. (2018) Residual effects of biochar on growth, photosynthesis and cadmium uptake in rice (Oryza sativa L.) under Cd stress with different water conditions. J Environ Manage 206:676–683. https://doi.org/10.1016/j.jenvman.2017.10.035
Rosa M, Prado C, Podazza G, Interdonato R, Juan A, Hilal M, Prado FE (2009) Soluble sugars: metabolism, sensing and abiotic stress. Plant Signal Behav 4:388–393
Rostami M, Mohammadi H, Müller T, Mirzaeitalarposhti R (2020) Silicon application affects cadmium translocation and physiological traits of Lallemantia royleana under cadmium stress. J Plant Nutr 43:753–761. https://doi.org/10.1080/01904167.2019.1701022
Sager SMA, Wijaya L, Alyemeni MN, Hatamleh AA, Ahmad P (2020) Impact of different cadmium concentrations on two Pisum sativum l. genotypes. Pak J Bot 52:821–829
Sameena PP, Puthur JT (2020) Cotyledonary leaves effectively shield the true leaves in Ricinus communis L. from copper toxicity. Int J Phytoremediation 10:1–13. https://doi.org/10.1080/15226514.2020.1825331
Santos JI, Martín-Sampedro R, Fillat Ú, Oliva JM, Negro MJ, Ballesteros M, Ibarra D (2015) Evaluating lignin-rich residues from biochemical ethanol production of wheat straw and olive tree pruning by FTIR and 2D-NMR. Int J Polym Sci 2015. https://doi.org/10.1155/2015/314891
Sarath NG, Puthur JT (2020) Heavy metal pollution assessment in a mangrove ecosystem scheduled as a community reserve. Wetlands Ecol Manage 11:1–12. https://doi.org/10.1007/s11273-020-09764-7
Schat H, Sharma SS, Vooijs R (1997) Heavy metal‐induced accumulation of free proline in a metal‐tolerant and a nontolerant ecotype of Silene vulgaris. Physiol Plant 101:477–482. https://doi.org/10.1111/j.1399-3054.1997.tb01026.x
Shackira AM, Puthur JT (2017) Enhanced phytostabilization of cadmium by a halophyte—Acanthus ilicifolius L. Int J Phytoremediation 19:319–326
Shah AA, Ahmed S, Ali A, Yasin NA (2020) 2-Hydroxymelatonin mitigates cadmium stress in Cucumis sativus seedlings: modulation of antioxidant enzymes and polyamines. Chemosphere 243:125308. https://doi.org/10.1016/j.chemosphere.2019.125308
Shahabivand S, Maivan HZ, Goltapeh EM, Sharifi M, Aliloo AA (2012) The effects of root endophyte and arbuscular mycorrhizal fungi on growth and cadmium accumulation in wheat under cadmium toxicity. Plant Physiol Biochem 60:53–58. https://doi.org/10.1016/j.plaphy.2012.07.018
Shahzad A, Qin M, Elahie M, Naeem M, Bashir T, Yasmin H et al. (2021) Bacillus pumilus induced tolerance of Maize (Zea mays L.) against Cadmium (Cd) stress. Sci Rep 11:1–11. https://doi.org/10.1038/s41598-021-96786-7
Sharma SS, Dietz KJ (2006) The significance of amino acids and amino acid-derived molecules in plant responses and adaptation to heavy metal stress. J Exp Bot 57:711–726. https://doi.org/10.1093/jxb/erj073
Sharma SS, Schat H, Vooijs R (1998) In vitro alleviation of heavy metal-induced enzyme inhibition by proline. Phytochemistry 49:1531–1535. https://doi.org/10.1016/S0031-9422(98)00282-9
Sharma V, Parmar P, Kumari N (2016) Differential cadmium stress tolerance in wheat genotypes under mycorrhizal association. J Plant Nutr 39:2025–2036. https://doi.org/10.1080/01904167.2016.1170851
Sruthi P, Puthur JT (2019) Characterization of physiochemical and anatomical features associated with enhanced phytostabilization of copper in Bruguiera cylindrica (L.) Blume. Int J phytoremediation 21:1423–1441
Steudle E (2000) Water uptake by roots: effects of water deficit. J Exp Bot 51:1531–1542. https://doi.org/10.1093/jexbot/51.350.1531
Talluri MR, Ketha A, Battu GR, Tadi RS, Tatipamula VB (2018) Protective effect of Aurelia aurita against free radicals and streptozotocin-induced diabetes. Bangladesh J Pharmacol 13:287–295
Thielemans W, Wool RP (2005) Lignin esters for use in unsaturated thermosets: lignin modification and solubility modeling. Biomacromolecules 6:1895–1905. https://doi.org/10.1021/bm0500345
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. https://doi.org/10.1007/s00572-006-0104-3
Tovar-Sánchez E, Cervantes-Ramírez T, Castañeda-Bautista J, Gómez-Arroyo S, Ortiz-Hernández L, Sánchez-Salinas E, Mussali-Galante P (2018) Response of Zea mays to multimetal contaminated soils: a multibiomarker approach. Ecotoxicology 27:1161–1177. https://doi.org/10.1007/s10646-018-1974-9
Vijayarengan P, Mahalakshmi G (2013) Zinc toxicity in tomato plants. World Appl Sci J 24:649–653
Weisany W, Raei Y, Salmasi SZ, Sohrabi Y, Ghassemi‐Golezani K (2016) Arbuscular mycorrhizal fungi induced changes in rhizosphere, essential oil and mineral nutrients uptake in dill/common bean intercropping system. Ann Appl Biol 169:384–397. https://doi.org/10.1111/aab.12309
Wu JT, Wang L, Zhao L, Huang XC, Ma F (2020) Arbuscular mycorrhizal fungi effect growth and photosynthesis of Phragmites australis (Cav.) Trin ex. Steudel under copper stress. Plant Biol 22:62–69
Yang L, Zou YN, Tian ZH, Wu QS, Kuča K (2021) Effects of beneficial endophytic fungal inoculants on plant growth and nutrient absorption of trifoliate orange seedlings. Sci Hortic 277:109815
Zhao R, Guo W, Bi N, Guo J, Wang L, Zhao J, Zhang J (2015) Arbuscular mycorrhizal fungi affect the growth, nutrient uptake and water status of maize (Zea mays L.) grown in two types of coal mine spoils under drought stress. Appl Soil Ecol 88:41–49
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. https://doi.org/10.1016/j.scitotenv.2016.05.058
Zhou C, Jiang W, Via BK, Fasina O, Han G (2015) Prediction of mixed hardwood lignin and carbohydrate content using ATR-FTIR and FT-NIR. Carbohydr Polym 121:336–341. https://doi.org/10.1016/j.carbpol.2014.11.062
Zoghlami LB, Djebali W, Abbes Z, Hediji H, Maucourt M, Moing A et al. (2011) Metabolite modifications in Solanum lycopersicum roots and leaves under cadmium stress. Afr J Biotechnol 10:567–579
Acknowledgements
The authors greatly acknowledge the Centre for Plant Breeding and 24 Genetics, Department of Millets, Tamil Nadu Agriculture University (TNAU), Coimbatore, 25 India, for providing seeds essential to conduct the experiments and Centre for Mycorrhizal 26 Culture Collection (CMCC), The Energy and Resources Institute (TERI), New Delhi for 27 providing the inoculum of mycorrhiza. The authors extend their sincere thanks to the Department 28 of Science & Technology (DST), Government of India for granting funds under the Fund for 29 Improvement of S&T Infrastructure (FIST) programme (SR/FST/LSI-532/2012).
Funding
This work was supported by the University Grant Commission (UGC), India in the form of JRF under grant 319492.
Author information
Authors and Affiliations
Contributions
EJ performed the analysis, processed the experimental data, interpreted the results, drafted the paper and designed the Figures. JTP provided critical feedback and helped shape the research and analysis aided in interpreting the results, and worked on the paper. HMK gave critical input and helped develop the study and interpretation that helped to understand the findings and work on the paper. JW offered valuable insight and helped to establish the research and analysis that helped to explain the paper observations and function.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no competing interests.
Additional information
Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary information
Rights and permissions
About this article
Cite this article
Janeeshma, E., Puthur, J.T., Wróbel, J. et al. Metabolic alterations elicited by Cd and Zn toxicity in Zea mays with the association of Claroideoglomus claroideum. Ecotoxicology 31, 92–113 (2022). https://doi.org/10.1007/s10646-021-02492-5
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10646-021-02492-5