Growth, metal partitioning and antioxidant enzyme activities of mung beans as influenced by zinc oxide nanoparticles under cadmium stress
Md Harunur Rashid
A B C , Mohammad Mahmudur Rahman A B * , Md Abdul Halim A B and Ravi Naidu A B *
+ Author Affiliations
- Author Affiliations
A Global Centre for Environmental Remediation (GCER), College of Engineering, Science and Environment, The University of Newcastle, Callaghan, Newcastle, NSW 2308, Australia.
B Cooperative Research Centre for Contamination Assessment and Remediation of the Environment (CRC CARE), ATC Building, The University of Newcastle, Callaghan, Newcastle, NSW 2308, Australia.
C Bangladesh Agricultural Research Institute (BARI), Gazipur 1701, Bangladesh.
* Correspondence to: mahmud.rahman@newcastle.edu.au, ravi.naidu@newcastle.edu.au
Handling Editor: Shahid Hussain
Crop & Pasture Science - https://doi.org/10.1071/CP21598
Submitted: 4 May 2021 Accepted: 8 December 2021 Published online: 11 May 2022
© 2021 The Author(s) (or their employer(s)). Published by CSIRO Publishing. This is an open access article distributed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (CC BY-NC-ND)
Abstract
Context: Cadmium (Cd) toxicity and zinc (Zn) deficiency are of major concerns for crop growth and quality. Moreover, their interactive effects exert some controversial reports.
Aims: The effects of zinc oxide nanoparticles (ZnO NPs) and Cd on growth, physiology, and metal distribution in mung beans (Vigna radiata L.) was investigated.
Methods: Seven-day-old seedlings were treated with Zn (0, 1, 2, 4, 8, 16 and 32 μM) and Cd (0, 0.5, 1 μM) for 14 days.
Key results: Photosynthetic pigments, antioxidant enzyme activities, dry matter yield and metal concentration in tissues were significantly influenced by ZnO NPs and Cd. Considered on its own as a main effect, Zn application (16 μM) enhanced its accumulation in roots, stem and leaf by about 33-fold (314 mg kg−1), 10-fold (60.6 mg kg−1) and 17-fold (110.8 mg kg−1), respectively, compared to control. However, accumulation was slower for interactions with Cd. While leaf Zn increased approximately 27 times (180 mg kg−1) at 32 μM Zn, its interactions with lower and higher Cd increased only 6-fold (41.2 mg kg−1) and 3-fold (21.4 mg kg−1), respectively. Added ZnO NPs up to 4 μM under Cd contamination elevated the leaf Cd, which was restricted by higher supply. However, Cd accumulation in stem and root consistently rose, indicating a synergistic effect. ZnO NPs induced an upregulation of antioxidant enzymes to avert oxidative stress and maintain growth performance.
Implications: These findings may be suitable for formulating nanomaterials of desired particle sizes and testing on other crop to remediate Cd.
Keywords: antioxidant enzymes, biofortification, cadmium, chlorophyll, metal partitioning, mung beans, photosynthetic pigments, reactive oxygen species (ROS), transfer/translocation factor, zinc oxide nanoparticles.
References
Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiology 24, 1| Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris.Crossref | GoogleScholarGoogle Scholar | 16654194PubMed |
Bayçu G, Gevrek-Kürüm N, Moustaka J, Csatári I, Rognes SE, Moustakas M (2017) Cadmium–zinc accumulation and photosystem II responses of Noccaea caerulescens to Cd and Zn exposure. Environmental Science and Pollution Research 24, 2840–2850.
| Cadmium–zinc accumulation and photosystem II responses of Noccaea caerulescens to Cd and Zn exposure.Crossref | GoogleScholarGoogle Scholar | 27838905PubMed |
Borker AR, David K, Singhal N (2020) Analysis of time varying response on uptake patterns of Cu and Zn ions under application of ethylene diamine disuccinic acid and gibberellic acid in Lolium perenne. Chemosphere 260, 127541
| Analysis of time varying response on uptake patterns of Cu and Zn ions under application of ethylene diamine disuccinic acid and gibberellic acid in Lolium perenne.Crossref | GoogleScholarGoogle Scholar | 32688311PubMed |
Cherif J, Mediouni C, Ammar WB, Jemal F (2011) Interactions of zinc and cadmium toxicity in their effects on growth and in antioxidative systems in tomato plants (Solarium lycopersicum). Journal of Environmental Sciences 23, 837–844.
| Interactions of zinc and cadmium toxicity in their effects on growth and in antioxidative systems in tomato plants (Solarium lycopersicum).Crossref | GoogleScholarGoogle Scholar |
Cohen CK, Fox TC, Garvin DF, Kochian LV (1998) The role of iron-deficiency stress responses in stimulating heavy-metal transport in plants. Plant Physiology 116, 1063–1072.
| The role of iron-deficiency stress responses in stimulating heavy-metal transport in plants.Crossref | GoogleScholarGoogle Scholar | 9501139PubMed |
Cojocaru P, Gusiatin ZM, Cretescu I (2016) Phytoextraction of Cd and Zn as single or mixed pollutants from soil by rape (Brassica napus). Environmental Science and Pollution Research 23, 10693–10701.
| Phytoextraction of Cd and Zn as single or mixed pollutants from soil by rape (Brassica napus).Crossref | GoogleScholarGoogle Scholar | 26884243PubMed |
Faizan M, Faraz A, Yusuf M, Khan ST, Hayat S (2018) Zinc oxide nanoparticle-mediated changes in photosynthetic efficiency and antioxidant system of tomato plants. Photosynthetica 56, 678–686.
| Zinc oxide nanoparticle-mediated changes in photosynthetic efficiency and antioxidant system of tomato plants.Crossref | GoogleScholarGoogle Scholar |
Faizan M, Faraz A, Mir AR, Hayat S (2021) Role of zinc oxide nanoparticles in countering negative effects generated by cadmium in Lycopersicon esculentum. Journal of Plant Growth Regulation 40, 101–115.
| Role of zinc oxide nanoparticles in countering negative effects generated by cadmium in Lycopersicon esculentum.Crossref | GoogleScholarGoogle Scholar |
Farahani AS, Taghavi M (2016) Changes of antioxidant enzymes of mung bean [Vigna radiata (L.) R. Wilczek] in response to host and non-host bacterial pathogens. Journal of Plant Protection Research 56, 95–99.
| Changes of antioxidant enzymes of mung bean [Vigna radiata (L.) R. Wilczek] in response to host and non-host bacterial pathogens.Crossref | GoogleScholarGoogle Scholar |
Forster SM, Rickertsen JR, Mehring GH, Ransom JK (2018) Type and placement of zinc fertilizer impacts cadmium content of harvested durum wheat grain. Journal of Plant Nutrition 41, 1471–1481.
| Type and placement of zinc fertilizer impacts cadmium content of harvested durum wheat grain.Crossref | GoogleScholarGoogle Scholar |
García-Gómez C, García S, Obrador AF, González D, Babín M, Fernández MD (2018) Effects of aged ZnO NPs and soil type on Zn availability, accumulation and toxicity to pea and beet in a greenhouse experiment. Ecotoxicology and Environmental Safety 160, 222–230.
| Effects of aged ZnO NPs and soil type on Zn availability, accumulation and toxicity to pea and beet in a greenhouse experiment.Crossref | GoogleScholarGoogle Scholar | 29807295PubMed |
Garg N, Kaur H (2013) Response of antioxidant enzymes, phytochelatins and glutathione production towards Cd and Zn stresses in Cajanus cajan (L.) Millsp. genotypes colonized by arbuscular mycorrhizal fungi. Journal of Agronomy and Crop Science 199, 118–133.
| Response of antioxidant enzymes, phytochelatins and glutathione production towards Cd and Zn stresses in Cajanus cajan (L.) Millsp. genotypes colonized by arbuscular mycorrhizal fungi.Crossref | GoogleScholarGoogle Scholar |
Ghasemi S, Khoshgoftarmanesh AH, Afyuni M, Hadadzadeh H (2013) The effectiveness of foliar applications of synthesized zinc-amino acid chelates in comparison with zinc sulfate to increase yield and grain nutritional quality of wheat. European Journal of Agronomy 45, 68–74.
| The effectiveness of foliar applications of synthesized zinc-amino acid chelates in comparison with zinc sulfate to increase yield and grain nutritional quality of wheat.Crossref | GoogleScholarGoogle Scholar |
Gong X, Huang D, Liu Y, Zeng G, Wang R, Wan J, Zhang C, Cheng M, Qin X, Xue W (2017) Stabilized nanoscale zerovalent iron mediated cadmium accumulation and oxidative damage of Boehmeria nivea (L.) Gaudich cultivated in cadmium contaminated sediments. Environmental Science & Technology 51, 11308–11316.
| Stabilized nanoscale zerovalent iron mediated cadmium accumulation and oxidative damage of Boehmeria nivea (L.) Gaudich cultivated in cadmium contaminated sediments.Crossref | GoogleScholarGoogle Scholar |
Green AC, Olsen CM (2017) Cutaneous squamous cell carcinoma: an epidemiological review. British Journal of Dermatology 177, 373–381.
| Cutaneous squamous cell carcinoma: an epidemiological review.Crossref | GoogleScholarGoogle Scholar |
Hassan M, Israr M, Mansoor S, Hussain SA, Basheer F, Azizullah A, Ur Rehman S (2021) Acclimation of cadmium-induced genotoxicity and oxidative stress in mung bean seedlings by priming effect of phytohormones and proline. PLoS ONE 16, e0257924
| Acclimation of cadmium-induced genotoxicity and oxidative stress in mung bean seedlings by priming effect of phytohormones and proline.Crossref | GoogleScholarGoogle Scholar | 34587203PubMed |
Hayat S, Hayat Q, Alyemeni MN, Wani AS, Pichtel J, Ahmad A (2012) Role of proline under changing environments: a review. Plant Signaling & Behavior 7, 1456–1466.
| Role of proline under changing environments: a review.Crossref | GoogleScholarGoogle Scholar |
Hossain MA, Bhattacharjee S, Armin S-M, Qian P, Xin W, Li H-Y, Burritt DJ, Fujita M, Tran L-SP (2015) Hydrogen peroxide priming modulates abiotic oxidative stress tolerance: insights from ROS detoxification and scavenging. Frontiers in Plant Science 6, 420
| Hydrogen peroxide priming modulates abiotic oxidative stress tolerance: insights from ROS detoxification and scavenging.Crossref | GoogleScholarGoogle Scholar | 26136756PubMed |
Huang G, Ding C, Zhou Z, Zhang T, Wang X (2019) A tillering application of zinc fertilizer based on basal stabilization reduces Cd accumulation in rice (Oryza sativa L.). Ecotoxicology and Environmental Safety 167, 338–344.
| A tillering application of zinc fertilizer based on basal stabilization reduces Cd accumulation in rice (Oryza sativa L.).Crossref | GoogleScholarGoogle Scholar | 30359900PubMed |
IARC (2018) List of classifications by cancer sites with sufficient or limited evidence in humans, volumes 1 to 121 [WWW document]. International Agency for Research on Cancer. Available at http://monographs.iarc.fr/ENG/Classification/Table4.pdf. [Accessed 27 June 2018]
Kamal AHM, Komatsu S (2015) Involvement of reactive oxygen species and mitochondrial proteins in biophoton emission in roots of soybean plants under flooding stress. Journal of Proteome Research 14, 2219–2236.
| Involvement of reactive oxygen species and mitochondrial proteins in biophoton emission in roots of soybean plants under flooding stress.Crossref | GoogleScholarGoogle Scholar |
Khaliq MA, James B, Chen YH, Saqib HSA, Li HH, Jayasuriya P, Guo W (2019) Uptake, translocation, and accumulation of Cd and its interaction with mineral nutrients (Fe, Zn, Ni, Ca, Mg) in upland rice. Chemosphere 215, 916–924.
| Uptake, translocation, and accumulation of Cd and its interaction with mineral nutrients (Fe, Zn, Ni, Ca, Mg) in upland rice.Crossref | GoogleScholarGoogle Scholar | 30408887PubMed |
Khan MN, Mobin M, Abbas ZK, AlMutairi KA, Siddiqui ZH (2017) Role of nanomaterials in plants under challenging environments. Plant Physiology and Biochemistry 110, 194–209.
| Role of nanomaterials in plants under challenging environments.Crossref | GoogleScholarGoogle Scholar | 27269705PubMed |
Köleli N, Eker S, Cakmak I (2004) Effect of zinc fertilization on cadmium toxicity in durum and bread wheat grown in zinc-deficient soil. Environmental Pollution 131, 453–459.
| Effect of zinc fertilization on cadmium toxicity in durum and bread wheat grown in zinc-deficient soil.Crossref | GoogleScholarGoogle Scholar | 15261409PubMed |
Lasat MM, Pence NS, Garvin DF, Ebbs SD, Kochian LV (2000) Molecular physiology of zinc transport in the Zn hyperaccumulator Thlaspi caerulescens. Journal of Experimental Botany 51, 71–79.
| Molecular physiology of zinc transport in the Zn hyperaccumulator Thlaspi caerulescens.Crossref | GoogleScholarGoogle Scholar | 10938797PubMed |
Leng Y, Li Y, Ma Y-H, He L-F, Li S-W (2021) Abscisic acid modulates differential physiological and biochemical responses of roots, stems, and leaves in mung bean seedlings to cadmium stress. Environmental Science and Pollution Research 28, 6030–6043.
| Abscisic acid modulates differential physiological and biochemical responses of roots, stems, and leaves in mung bean seedlings to cadmium stress.Crossref | GoogleScholarGoogle Scholar | 32986195PubMed |
Liu X, Wang F, Shi Z, Tong R, Shi X (2015) Bioavailability of Zn in ZnO nanoparticle-spiked soil and the implications to maize plants. Journal of Nanoparticle Research 17, 175
| Bioavailability of Zn in ZnO nanoparticle-spiked soil and the implications to maize plants.Crossref | GoogleScholarGoogle Scholar |
Malar S, Vikram SS, Favas PJC, Perumal V (2016) Lead heavy metal toxicity induced changes on growth and antioxidative enzymes level in water hyacinths [Eichhornia crassipes (Mart.)]. Botanical Studies 55, 54
| Lead heavy metal toxicity induced changes on growth and antioxidative enzymes level in water hyacinths [Eichhornia crassipes (Mart.)].Crossref | GoogleScholarGoogle Scholar | 28597420PubMed |
Martos S, Gallego B, Sáez L, López-Alvarado J, Cabot C, Poschenrieder C (2016) Characterization of zinc and cadmium hyperaccumulation in three Noccaea (Brassicaceae) populations from non-metalliferous sites in the eastern Pyrenees. Frontiers in Plant Science 7, 128
| Characterization of zinc and cadmium hyperaccumulation in three Noccaea (Brassicaceae) populations from non-metalliferous sites in the eastern Pyrenees.Crossref | GoogleScholarGoogle Scholar | 26904085PubMed |
Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends in Plant Science 7, 405–410.
| Oxidative stress, antioxidants and stress tolerance.Crossref | GoogleScholarGoogle Scholar | 12234732PubMed |
Mohammad A, Moheman A (2010) The effects of cadmium and zinc interactions on the accumulation and tissue distribution of cadmium and zinc in tomato (Lycopersicon esculentum Mill.). Archives of Agronomy and Soil Science 56, 551–561.
| The effects of cadmium and zinc interactions on the accumulation and tissue distribution of cadmium and zinc in tomato (Lycopersicon esculentum Mill.).Crossref | GoogleScholarGoogle Scholar |
Murtaza G, Javed W, Hussain A, Qadir M, Aslam M (2017) Soil-applied zinc and copper suppress cadmium uptake and improve the performance of cereals and legumes. International Journal of Phytoremediation 19, 199–206.
| Soil-applied zinc and copper suppress cadmium uptake and improve the performance of cereals and legumes.Crossref | GoogleScholarGoogle Scholar | 27419530PubMed |
Nair PMG, Chung IM (2014) Assessment of silver nanoparticle-induced physiological and molecular changes in Arabidopsisthaliana. Environmental Science and Pollution Research 21, 8858–8869.
| Assessment of silver nanoparticle-induced physiological and molecular changes in Arabidopsisthaliana.Crossref | GoogleScholarGoogle Scholar |
Pradhan S, Patra P, Das S, Chandra S, Mitra S, Dey KK, Akbar S, Palit P, Goswami A (2013) Photochemical modulation of biosafe manganese nanoparticles on Vigna radiata: a detailed molecular, biochemical, and biophysical study. Environmental Science & Technology 47, 13122–13131.
| Photochemical modulation of biosafe manganese nanoparticles on Vigna radiata: a detailed molecular, biochemical, and biophysical study.Crossref | GoogleScholarGoogle Scholar |
Qaswar M, Hussain S, Rengel Z (2017) Zinc fertilisation increases grain zinc and reduces grain lead and cadmium concentrations more in zinc-biofortified than standard wheat cultivar. Science of The Total Environment 605, 454–460.
| Zinc fertilisation increases grain zinc and reduces grain lead and cadmium concentrations more in zinc-biofortified than standard wheat cultivar.Crossref | GoogleScholarGoogle Scholar |
Ramzani PMA, Coyne MS, Anjum S, Khan W-U-D, Iqbal M (2017) In situ immobilization of Cd by organic amendments and their effect on antioxidant enzyme defense mechanism in mung bean (Vigna radiata L.) seedlings. Plant Physiology and Biochemistry 118, 561–570.
| In situ immobilization of Cd by organic amendments and their effect on antioxidant enzyme defense mechanism in mung bean (Vigna radiata L.) seedlings.Crossref | GoogleScholarGoogle Scholar | 28783510PubMed |
Rizwan M, Ali S, Abbas T, Zia-ur-Rehman M, Hannan F, Keller C, Al-Wabel MI, Ok YS (2016) Cadmium minimization in wheat: a critical review. Ecotoxicology and Environmental Safety 130, 43–53.
| Cadmium minimization in wheat: a critical review.Crossref | GoogleScholarGoogle Scholar | 27062345PubMed |
Rizwan M, Ali S, Zia-ur-Rehman MZ, Rinklebe J, Tsang DC, Bashir A, Maqbool A, Tack F, Ok YS (2018) Cadmium phytoremediation potential of Brassica crop species: a review. Science of The Total Environment 631, 1175–1191.
| Cadmium phytoremediation potential of Brassica crop species: a review.Crossref | GoogleScholarGoogle Scholar |
Rizwan M, Ali S, Zia-ur-Rehman MZ, Adrees M, Arshad M, Qayyum MF, Ali L, Hussain A, Chatha SAS, Imran M (2019a) Alleviation of cadmium accumulation in maize (Zea mays L.) by foliar spray of zinc oxide nanoparticles and biochar to contaminated soil. Environmental Pollution 248, 358–367.
| Alleviation of cadmium accumulation in maize (Zea mays L.) by foliar spray of zinc oxide nanoparticles and biochar to contaminated soil.Crossref | GoogleScholarGoogle Scholar | 30818115PubMed |
Rizwan M, Ali S, Zia-ur-Rehman MZ, Maqbool A (2019b) A critical review on the effects of zinc at toxic levels of cadmium in plants. Environmental Science and Pollution Research 26, 6279–6289.
| A critical review on the effects of zinc at toxic levels of cadmium in plants.Crossref | GoogleScholarGoogle Scholar | 30635881PubMed |
Saifullah Saifullah (2014) Effectiveness of zinc application to minimize cadmium toxicity and accumulation in wheat (Triticum aestivum L.). Environmental Earth Sciences 71, 1663–1672.
| Effectiveness of zinc application to minimize cadmium toxicity and accumulation in wheat (Triticum aestivum L.).Crossref | GoogleScholarGoogle Scholar |
Santhoshkumar J, Kumar SV, Rajeshkumar S (2017) Synthesis of zinc oxide nanoparticles using plant leaf extract against urinary tract infection pathogen. Resource-Efficient Technologies 3, 459–465.
| Synthesis of zinc oxide nanoparticles using plant leaf extract against urinary tract infection pathogen.Crossref | GoogleScholarGoogle Scholar |
Singh J, Lee B-K (2016) Influence of nano-TiO2 particles on the bioaccumulation of Cd in soybean plants (Glycine max): a possible mechanism for the removal of Cd from the contaminated soil. Journal of Environmental Management 170, 88–96.
| Influence of nano-TiO2 particles on the bioaccumulation of Cd in soybean plants (Glycine max): a possible mechanism for the removal of Cd from the contaminated soil.Crossref | GoogleScholarGoogle Scholar | 26803259PubMed |
Spomer LA, Berry WL, Tibbitts TW (1997) Plant culture in solid media. In ‘Plant growth chamber handbook’. (Eds RW Langhans, TW Tibbitts) pp. 105–118. (Iowa Agricultural and Home Economics Experiment Station: Iowa, IA, USA)
Tripathi DK, Singh S, Singh S, Pandey R, Singh VP, Sharma NC, Prasad SM, Dubey NK, Chauhan DK (2017) An overview on manufactured nanoparticles in plants: uptake, translocation, accumulation and phytotoxicity. Plant Physiology and Biochemistry 110, 2–12.
| An overview on manufactured nanoparticles in plants: uptake, translocation, accumulation and phytotoxicity.Crossref | GoogleScholarGoogle Scholar | 27601425PubMed |
Tripathy BC, Oelmüller R (2012) Reactive oxygen species generation and signaling in plants. Plant Signaling & Behavior 7, 1621–1633.
| Reactive oxygen species generation and signaling in plants.Crossref | GoogleScholarGoogle Scholar |
Venkatachalam P, Jayaraj M, Manikandan R, Geetha N, Rene ER, Sharma NC, Sahi SV (2017a) Zinc oxide nanoparticles (ZnONPs) alleviate heavy metal-induced toxicity in Leucaena leucocephala seedlings: a physiochemical analysis. Plant Physiology and Biochemistry 110, 59–69.
| Zinc oxide nanoparticles (ZnONPs) alleviate heavy metal-induced toxicity in Leucaena leucocephala seedlings: a physiochemical analysis.Crossref | GoogleScholarGoogle Scholar | 27622846PubMed |
Venkatachalam P, Priyanka N, Manikandan K, Ganeshbabu I, Indiraarulselvi P, Geetha N, Muralikrishna K, Bhattacharya RC, Tiwari M, Sharma N, Sahi SV (2017b) Enhanced plant growth promoting role of phycomolecules coated zinc oxide nanoparticles with P supplementation in cotton (Gossypium hirsutum L.). Plant Physiology and Biochemistry 110, 118–127.
| Enhanced plant growth promoting role of phycomolecules coated zinc oxide nanoparticles with P supplementation in cotton (Gossypium hirsutum L.).Crossref | GoogleScholarGoogle Scholar | 27622847PubMed |
Wang F, Jing X, Adams CA, Shi Z, Sun Y (2018) Decreased ZnO nanoparticle phytotoxicity to maize by arbuscular mycorrhizal fungus and organic phosphorus. Environmental Science and Pollution Research 25, 23736–23747.
| Decreased ZnO nanoparticle phytotoxicity to maize by arbuscular mycorrhizal fungus and organic phosphorus.Crossref | GoogleScholarGoogle Scholar | 29876848PubMed |
Zare AA, Khoshgoftarmanesh AH, Malakouti MJ, Bahrami HA, Chaney RL (2018) Root uptake and shoot accumulation of cadmium by lettuce at various Cd:Zn ratios in nutrient solution. Ecotoxicology and Environmental Safety 148, 441–446.
| Root uptake and shoot accumulation of cadmium by lettuce at various Cd:Zn ratios in nutrient solution.Crossref | GoogleScholarGoogle Scholar | 29102904PubMed |
