Abstract
Different physiological and biochemical responses in mung bean (Vigna radiata L.) and tomato (Solanum lycopersicum L.) seedlings induced by graphene quantum dots (GQDs) (250–1500 mg L−1) were studied. Results showed that both seeds exposed to GQDs can still germinate normally. However, the growth of the seedlings after germination was adversely affected by the GQDs, and mung bean was more sensitive than tomato. In hydroponic experiments, the appropriate concentration of GQDs enhanced the accumulation of chlorophyll in mung bean (250–1250 mg L−1) and tomato (250–500 mg L−1) seedlings after exposure for 2 weeks. High concentrations of GQDs (1000–1500 mg L−1) led to an increase in the H2O2, malondialdehyde (MDA), proline, glutathione (GSH) levels, as well as increased catalase (CAT) and glutathione reductase (GR) activities in seedlings of both species. In addition, the migration of GQDs into plants was observed. Results showed that high concentrations of GQDs had an adverse effect on the growth of both plants, and mung bean seedlings were more sensitive than tomato seedlings. In addition, the problem of nanocontamination was suggested and the resulting food safety problems warrant further investigation.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Alimohammadi M, Xu Y, Wang D, Biris AS, Khodakovskaya MV (2011) Physiological responses induced in tomato plants by a two-component nanostructural system composed of carbon nanotubes conjugated with quantum dots and its in vivo multimodal detection. Nanotechnology 22:1–8. https://doi.org/10.1088/0957-4484/22/29/295101
Al-Salim N, Barraclough E, Burgess E, Clothier B, Deurer M, Green S, Malone L, Weir G (2011) Quantum dot transport in soil, plants, and insects. Sci Total Environ 409:3237–3248. https://doi.org/10.1016/j.scitotenv.2011.05.017
Andón FT, Fadeel B (2013) Programmed cell death: molecular mechanisms and implications for safety assessment of nanomaterials. Acc Chem Res 46:733–742. https://doi.org/10.1021/ar300020b
Antonoglou O, Moustaka J, Adamakis IDS, Sperdouli I, Pantazaki AA, Moustakas M, Dendrinou-Samara C (2018) Nanobrass CuZn nanoparticles as foliar spray non phytotoxic fungicides. ACS Appl Mater Interfaces 10:4450–4461. https://doi.org/10.1021/acsami.7b17017
Arnon DI (1949) Copper enzymes in isolated chloroplasts: polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1–15. https://doi.org/10.1104/pp.24.1.1
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
Baxter A, Mittler R, Suzuki N (2014) ROS as key players in plant stress signalling. J Exp Bot 65:1229–1240. https://doi.org/10.1093/jxb/ert375
Begum P, Fugetsu B (2012) Phytotoxicity of multi-walled carbon nanotubes on red spinach (Amaranthus tricolor L) and the role of ascorbic acid as an antioxidant. J Hazard Mater 243:212–222. https://doi.org/10.1016/j.jhazmat.2012.10.025
Carpita NC, Gibeaut DM (1993) Structural models of primary cell walls in flowering plants: consistency of molecular structure with the physical properties of the walls during growth. Plant J 3:1–30. https://doi.org/10.1111/j.1365-313X.1993.tb00007.x
Chen R, Ratnikova TA, Stone MB, Lin S, Lard M, Huang G, Hudson JS, Ke PC (2010) Differential uptake of carbon nanoparticles by plant and mammalian cells. Small 6:612–617. https://doi.org/10.1002/smll.200901911
Chichiriccò G, Poma A (2015) Penetration and toxicity of nanomaterials in higher plants. Nanomaterials 5:851–873. https://doi.org/10.3390/nano5020851
Choi HG, Moon BY, Bekhzod K, Park KS, Kwon JK, Lee JH, Cho MW, Kang NJ (2015) Effects of foliar fertilization containing titanium dioxide on growth, yield and quality of strawberries during cultivation. Hortic Environ Biotechnol 56:575–581. https://doi.org/10.1007/s13580-015-0023-3
Da Costa MVJ, Sharma PK (2016) Effect of copper oxide nanoparticles on growth, morphology, photosynthesis, and antioxidant response in Oryza sativa. Photosynthetica 54:110–119. https://doi.org/10.1007/s11099-015-0167-5
Drezek RA, Tour JM (2010) Is nanotechnology too broad to practise? Nat Nanotechnol 5:168–169. https://doi.org/10.1038/nnano.2010.37
Ghorbanpour M, Hadian J (2015) Multi-walled carbon nanotubes stimulate callus induction, secondary metabolites biosynthesis and antioxidant capacity in medicinal plant Satureja khuzestanica grown in vitro. Carbon 94:749–759. https://doi.org/10.1016/j.carbon.2015.07.056
Giraldo JP, Landry MP, Faltermeier SM, McNicholas TP, Iverson NM, Boghossian AA, Reuel NF, Hilmer AJ, Sen F, Brew JA, Strano MS (2014) Plant nanobionics approach to augment photosynthesis and biochemical sensing. Nat Mater 13:400–408. https://doi.org/10.1038/nmat3890
Gogos A, Knauer K, Bucheli TD (2012) Nanomaterials in plant protection and fertilization: current state, foreseen applications, and research priorities. J Agric Food Chem 60:9781–9792. https://doi.org/10.1021/jf302154y
Hatami M, Hadian J, Ghorbanpour M (2017) Mechanisms underlying toxicity and stimulatory role of single-walled carbon nanotubes in Hyoscyamus niger during drought stress simulated by polyethylene glycol. J Hazard Mater 324:306–320. https://doi.org/10.1016/j.jhazmat.2016.10.064
Hu C, Liu Y, Li X, Li M (2013) Biochemical responses of duckweed (Spirodela polyrhiza) to zinc oxide nanoparticles. Environ Contam Toxicol 64:643–651. https://doi.org/10.1007/s00244-012-9859-z
Keller AA, Wang H, Zhou D, Lenihan HS, Cherr G, Cardinale BJ, Miller R, Ji Z (2010) Stability and aggregation of metal oxide nanoparticles in natural aqueous matrices. Environ Sci Technol 44:1962–1967. https://doi.org/10.1021/es902987d
Keller AA, McFerran S, Lazareva A, Suh S (2013) Global life cycle releases of engineered nanomaterials. J Nanopart Res 15:1–17. https://doi.org/10.1007/s11051-013-1692-4
Klaine SJ, Alvarez PJJ, Batley GE, Fernandes TF, Handy RD, Lyon DY, Mahendra S, McLaughlin MJ, Lead JR (2008) Nanomaterials in the environment: behavior, fate, bioavailability, and effects. Environ Toxicol Chem 27:1825–1851. https://doi.org/10.1897/08-090.1
Lahiani MH, Chen J, Irin F, Puretzky AA, Green MJ, Khodakovskaya MV (2015) Interaction of carbon nanohorns with plants: uptake and biological effects. Carbon 81:607–619. https://doi.org/10.1016/j.carbon.2014.09.095
Li Y, Liu Y, Fu Y, Wei T, Guyader LL, Gao G, Liu RS, Chang YZ, Chen C (2012) The triggering of apoptosis in macrophages by pristine graphene through the MAPK and TGF-beta signaling pathways. Biomaterials 33:402–411. https://doi.org/10.1016/j.biomaterials.2011.09.091
Li J, Naeem MS, Wang X, Liu L, Chen C, Ma N, Zhang C (2015) Nano-TiO2 is not phytotoxic as revealed by the oilseed rape growth and photosynthetic apparatus ultra-structural response. PLoS ONE 10:e0143885. https://doi.org/10.1371/journal.pone.0143885
Lin S, Reppert J, Hu Q, Hudson JS, Reid ML, Ratnikova TA, Rao AM, Luo H, Ke PC (2009) Uptake, translocation, and transmission of carbon nanomaterials in rice plants. Small 5:1128–1132. https://doi.org/10.1002/smll.200801556
Liu Q, Chen B, Wang Q, Shi X, Xiao Z, Lin J, Fang X (2009) Carbon nanotubes as molecular transporters for walled plant cells. Nano Lett 9:1007–1010. https://doi.org/10.1021/nl803083u
Liu S, Wei H, Li Z, Li S, Yan H, He Y, Tian Z (2015) Effects of graphene on germination and seedling morphology in rice. J Nanosci Nanotechnol 15:2695–2701. https://doi.org/10.1166/jnn.2015.9254
Lushchak VI (2011) Environmentally induced oxidative stress in aquatic animals. Aquat Toxicol 101:13–30. https://doi.org/10.1016/j.aquatox.2010.10.006
Ma X, Geiser-Lee J, Deng Y, Kolmakov A (2010) Interactions between engineered nanoparticles (ENPs) and plants: phytotoxicity, uptake and accumulation. Sci Total Environ 408:3053–3061. https://doi.org/10.1016/j.scitotenv.2010.03.031
Ma C, White JC, Dhankher OP, Xing B (2015) Metal-Based nanotoxicity and detoxification pathways in higher plants. Environ Sci Technol 49:7109–7122. https://doi.org/10.1021/acs.est.5b00685
Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R (2010) Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ 33:453–467. https://doi.org/10.1111/j.1365-3040.2009.02041.x
Møller IM, Jensen PE, Hansson A (2007) Oxidative modifications to cellular components in plants. Annu Rev Plant Phys 58:459–481. https://doi.org/10.1146/annurev.arplant.58.032806.103946
Mondal A, Basu R, Das S, Nandy P (2011) Beneficial role of carbon nanotubes on mustard plant growth: an agricultural prospect. J Nanopart Res 13:4519–4528. https://doi.org/10.1007/s11051-011-0406-z
Moustaka J, Tanou G, Adamakis ID, Eleftheriou EP, Moustakas M (2015) Leaf age-dependent photoprotective and antioxidative response mechanisms to paraquat-induced oxidative stress in Arabidopsis thaliana. Int J Mol Sci 16:13989–14006. https://doi.org/10.3390/ijms160613989
Nel A, Xia T, Madler L, Li N (2006) Toxic potential of materials at the nanolevel. Science 311:622–627. https://doi.org/10.1126/science.1114397
Pérez-de-Luque A, Rubiales D (2009) Nanotechnology for parasitic plant control. Pest Manag Sci 65:540–545. https://doi.org/10.1002/ps.1732
Schwabe F, Schulin R, Limbach LK, Stark W, Buerge D, Nowack B (2013) Influence of two types of organic matter on interaction of CeO2 nanoparticles with plants in hydroponic culture. Chemosphere 91:512–520. https://doi.org/10.1016/j.chemosphere.2012.12.025
Shaymurat T, Gu J, Xu C, Yang Z, Zhao Q, Liu Y, Liu Y (2012) Phytotoxic and genotoxic effects of ZnO nanoparticles on garlic (Allium sativum L.): a morphological study. Nanotoxicology 6:241–248. https://doi.org/10.3109/17435390.2011.570462
Shen CX, Zhang QF, Li J, Bi FC, Yao N (2010) Induction of programmed cell death in Arabidopsis and rice by single-wall carbon nanotubes. Am J Bot 97:1602–1609. https://doi.org/10.3732/ajb.1000073
Slinkard K, Singleton VL (1977) Total phenol analysis: automation and comparison with manual methods. Am J Enol Vitic 28:49–55. https://doi.org/10.1002/star.19780301107
Somasundaran P, Fang X, Ponnurangam S, Li B (2010) Nanoparticles: characteristics, mechanisms and modulation of biotoxicity. KONA Powder Part J 28:38–49. https://doi.org/10.14356/kona.2010007
Stewart RR, Bewley JD (1980) Lipid peroxidation associated with accelerated aging of soybean axes. Plant Physiol 65:245–248. https://doi.org/10.1104/pp.65.2.245
Tripathi S, Sonkar SK, Sarkar S (2011) Growth stimulation of gram (Cicer arietinum) plant by water soluble carbon nanotubes. Nanoscale 3:1176–1181. https://doi.org/10.1039/c0nr00722f
Villagarcia H, Dervishi E, de Silva K, Biris AS, Khodakovskaya MV (2012) Surface chemistry of carbon nanotubes impacts the growth and expression of water channel protein in tomato plants. Small 8:2328–2334. https://doi.org/10.1002/smll.201102661
Wang Z, Xie X, Zhao J, Liu X, Feng W, White JC, Xing B (2012) Xylem-and phloem-based transport of CuO nanoparticles in maize (Zea mays L.). Environ Sci Technol 46:4434–4441. https://doi.org/10.1021/es204212z
Wang S, Liu H, Zhang Y, Xin H (2015) The effect of CuO NPs on reactive oxygen species and cell cycle gene expression in roots of rice. Environ Toxicol Chem 34:554–561. https://doi.org/10.1002/etc.2826
Wang L, Wu B, Li W, Li Z, Zhan J, Geng B, Wang S, Pan D, Wu M (2017) Industrial production of ultra-stable sulfonated graphene quantum dots for Golgi apparatus imaging. J Mater Chem B 5:5355–5361. https://doi.org/10.1039/c7tb01348e
Yang F, Liu C, Gao F, Su M, Wu X, Zheng L, Hong F, Yang P (2007) The improvement of spinach growth by nano-anatase TiO2 treatment is related to nitrogen photoreduction. Biol Trace Elem Res 119:77–88. https://doi.org/10.1007/s12011-007-0046-4
Zhao L, Sun Y, Hernandez-Viezcas JA, Servin AD, Hong J, Niu G, Peralta-Videa JR, Duarte-Gardea M, Gardea-Torresdey JL (2013) Influence of CeO2 and ZnO nanoparticles on cucumber physiological markers and bioaccumulation of Ce and Zn: a life cycle study. J Agric Food Chem 61:11945–11951. https://doi.org/10.1021/jf404328e
Author information
Authors and Affiliations
Contributions
PF performed the experiments, analyzed data and wrote the manuscript; BJG synthesized the GQDs and its characterization; ZC conducted partly the experiments and partly analyzed the data; XYL supplied the technique and methods to carry out the experiments; DYP provided GQDs and revised the manuscript; and JYH designed the research and corrected the manuscript. All authors read and approved the final manuscript.
Corresponding authors
Ethics declarations
Conflict of interest
The authors would like to express that they have no competing interests regarding this research.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Feng, P., Geng, B., Cheng, Z. et al. Graphene quantum dots-induced physiological and biochemical responses in mung bean and tomato seedlings. Braz. J. Bot 42, 29–41 (2019). https://doi.org/10.1007/s40415-019-00519-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s40415-019-00519-0