Abstract
There is increasing evidence for graphene associated plant growth promotion, however, the chronic effects of soil-applied graphene remain largely unexplored. The present study investigated the morphological, physiological and biochemical responses of graphene oxide (GO) on Aloe vera L. over the concentration range of 0–100 mg/L for four months. Our results demonstrated that GO, with the best efficiency at 50 mg/L, could enhance the photosynthetic capacity of leaves, increase the yield and morphological characters of root and leaf, improve the nutrient (protein and amino acid) contents of leaf, without reducing the content of the main bioactive compound aloin. Compared with leaves, the effect of GO on root growth was more obvious. Although the electrolyte leakage and MDA content were raised at high concentrations, GO treatment did not increase the root antioxidant enzymes activity or decrease the root vigor, which excluding typical stress response. Furthermore, injection experiments showed that the GO in vivo did not change the plant growth state obviously. Taken together, our study revealed the role of GO in promoting Aloe vera growth by stimulating root growth and photosynthesis, which would provide theory basis for GO application in agriculture and forestry.
This is a preview of subscription content, access via your institution.






Data availability
The data sets generated and analyzed during the current study are available from the corresponding author on reasonable request.
References
Andelkovic IB, Kabiri S, Tavakkoli E, Kirby JK, McLaughlin MJ, Losic D (2018) Graphene oxide-Fe(III) composite containing phosphate—a novel slow release fertilizer for improved agriculture management. J Clean Prod 185:97–104. https://doi.org/10.1016/j.jclepro.2018.03.050
Anjum NA, Singh N, Singh MK, Sayeed I, Duarte AC, Pereira E, Ahmad I (2014) Single-bilayer graphene oxide sheet impacts and underlying potential mechanism assessment in germinating faba bean (Vicia faba L.). Sci Total Environ 472:834–841. https://doi.org/10.1016/j.scitotenv.2013.11.018
Avouris P (2010) Graphene: electronic and photonic properties and devices. Nano Lett 10:4285–4294. https://doi.org/10.1021/nl102824h
Begum P, Fugetsu B (2013) Induction of cell death by graphene in Arabidopsis thaliana (Columbia ecotype) T87 cell suspensions. J Hazard Mater 260:1032–1041. https://doi.org/10.1016/j.jhazmat.2013.06.063
Begum P, Ikhtiari R, Fugetsu B (2011) Graphene phytotoxicity in the seedling stage of cabbage, tomato, red spinach, and lettuce. Carbon 49:3907–3919. https://doi.org/10.1016/j.carbon.2011.05.029
Chakravarty D, Erande MB, Late DJ (2015) Graphene quantum dots as enhanced plant growth regulators: effects on coriander and garlic plants. J Agric Food Chem 95:2772–2778. https://doi.org/10.1002/jsfa.7106
Chatterjee N, Yang JS, Park K, Oh SM, Park J, Choi J (2015) Screening of toxic potential of graphene family nanomaterials using in vitro and alternative in vivo toxicity testing systems. Environ Anal Health Toxicol 30:e2015007–e2015000. https://doi.org/10.5620/eht.e2015007
Chen J, Yang L, Li S, Ding W (2018) Various physiological response to graphene oxide and amine-functionalized graphene oxide in wheat (Triticum aestivum). Molecules 23:1104. https://doi.org/10.3390/molecules23051104
De Jesus LR, Dennis RV, Depner SW, Jaye C, Fischer DA, Banerjee S (2010) Inside and outside: X-ray absorption spectroscopy mapping of chemical domains in graphene oxide. J Phys Chem Lett 4:3144–3151. https://doi.org/10.1021/jz401717j
Di Salvatore M, Carafa A, Mingo A, Carratù G (2012) Evaluation of heavy metal toxicity on radish: comparison between soil and floating hydroponics systems. Am J Exp Agr 2:174–185. https://doi.org/10.9734/AJEA/2012/862
Dong Z, Men Y, Liu Z, Li J, Ji J (2020) Application of chlorophyll fluorescence imaging technique in analysis and detection of chilling injury of tomato seedlings. Comput Electron Agr 168:105109. https://doi.org/10.1016/j.compag.2019.105109
Gao M, Yang Y, Song Z (2019) Effects of graphene oxide on cadmium uptake and photosynthesis performance in wheat seedlings. Ecotox Environ Safe 173:165–173. https://doi.org/10.1016/j.ecoenv.2019.01.093
Guo Z, Luo W, Xie C, Valsami-Jones E, Lynch I, Abdolahpur Monikh F (2020) Graphene oxide induced pH alteration, iron overload and subsequent oxidative damage in rice (Oryza. sativa L.): A new mechanism of nanomaterial phytotoxicity. Environ Sci Technol 54:3181–3190. https://doi.org/10.1021/acs.est.9b05794
Hazrati S, Sarvestani T, Modarres-Sanavy S, Mokhtassi-Bidgoli A, Nicola S (2016) Effects of water stress and light intensity on chlorophyll fluorescence parameters and pigments of Aloe vera L Plant. Physiol Bioch 106:141–148. https://doi.org/10.1016/j.plaphy.2016.04.046
Hazrati S, Sarvestani T, Mokhtassi-Bidgoli A, Modarres-Sanavy SAM, Mohammadi H, Nicola S (2017) Effects of zeolite and water stress on growth, yield and chemical compositions of Aloe vera L. Agr Water Manage 181:66–72. https://doi.org/10.1016/j.agwat.2016.11.026
He Y, Hu R, Zhong Y, Zhao X, Chen Q, Zhu H (2018) Graphene oxide as a water transporter promoting germination of plants in soil. Nano Res 11:1928–1937. https://doi.org/10.1007/s12274-017-1810-1
Heeb A, Lundegårdh B, Savage G, Ericsson T (2006) Impact of organic and inorganic fertilizers on yield, taste, and nutritional quality of tomatoes. J Plant Nutr Soil Sci 169:535–541. https://doi.org/10.1002/jpln.200520553
Hu X, Zhou Q (2014) Novel hydrated graphene ribbon unexpectedly promotes aged seed germination and root differentiation. Sci Rep 4:3782. https://doi.org/10.1038/srep03782
Huang C et al (2018) Transformation of (14) C-labeled graphene to (14) CO2 in the shoots of a rice plant. Angew Chem Int Edit 57:9759–9763. https://doi.org/10.1002/anie.201805099
Jiao J et al (2016) The role of graphene oxide on tobacco root growth and its preliminary mechanism. J Nanosci Nanotechno 16:12449–12454. https://doi.org/10.1166/jnn.2016.12987
Jin Z, Wang C, Liu Z, Gong W (2007) Physiological and ecological characters studies on Aloe vera under soil salinity and seawater irrigation. Process Biochem 42:710–714. https://doi.org/10.1016/j.procbio.2006.11.002
Kabiri S, Degryse F, Tran DNH, da Silva RC, McLaughlin MJ, Losic D (2017) Graphene oxide: a new carrier for slow release of plant micronutrients ACS. Appl Mater Inter 9:43325–43335. https://doi.org/10.1021/acsami.7b07890
Krause GH, Weis E (2003) Chlorophyll fluorescence and photosynthesis: the basics. Annu Rev Plant Biol 42:313–349. https://doi.org/10.1146/annurev.pp.42.060191.001525
Kumar S (2014) Ethnobotanical and pharmacological properties of Aloe vera: a review. J Med Plants Res 8(48):1387–1398
Lichtenthaler H (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Meth Enzymol 148C:350–382. https://doi.org/10.1016/0076-6879(87)48036-1
Li F, Xue J, Zhao J, Zhang S (2015) Graphene oxide: a promising nanomaterial for energy and environmental applications. Nano Energy 16:488–515. https://doi.org/10.1016/j.nanoen.2015.07.014
Liu L et al (2009) An efficient system to detect protein ubiquitination by agroinfiltration in Nicotiana benthamiana. Plant J 61:893–903. https://doi.org/10.1111/j.1365-313X.2009.04109.x
Lu M et al (2020) Nutritional quality and health risk of pepper fruit as affected by magnesium fertilization. J sci food agric. https://doi.org/10.1002/jsfa.10670
Ma Q et al (2013) A rapid and easy approach for the reduction of graphene oxide by formamidinesulfinic acid. Carbon 54:36–41. https://doi.org/10.1016/j.carbon.2012.10.067
Manzocco L et al (2011) Influence of hydroponic and soil cultivation on quality and shelf life of ready-to-eat lamb’s lettuce (Valerianella locusta L. Laterr). J Sci Food Agr 91:1373–1380. https://doi.org/10.1002/jsfa.4313
Mendonça M, Rodrigues N, De Jesus M, Amorim M (2019) Graphene-based nanomaterials in soil: ecotoxicity assessment using Enchytraeus crypticus reduced full life cycle. Nanomaterials. https://doi.org/10.3390/nano9060858
Mukherjee A, Majumdar S, Servin AD, Pagano L, Dhankher OP, White JC (2016) Carbon nanomaterials in agriculture: a critical review. Front Plant Sci. https://doi.org/10.3389/fpls.2016.00172
Pandey K, Anas M, Hicks V, Green M, Khodakovskaya M (2019) Improvement of commercially valuable traits of industrial crops by application of carbon-based nanomaterials. Sci Rep 9:19358. https://doi.org/10.1038/s41598-019-55903-3
Pei S, Wei Q, Huang K, Cheng H-M, Ren W (2018) Green synthesis of graphene oxide by seconds timescale water electrolytic oxidation. Nat Commun. https://doi.org/10.1038/s41467-017-02479-z
Raghavan N, Sakthivel T, Venugopal G (2017) A short review on preparation of graphene from waste and bioprecursors. Appl Mater Today 7:246–254. https://doi.org/10.1016/j.apmt.2017.04.005
Ren W, Chang H, Teng Y (2016) Sulfonated graphene-induced hormesis is mediated through oxidative stress in the roots of maize seedlings. Sci Total Environ 572:926–934. https://doi.org/10.1016/j.scitotenv.2016.07.214
Rutherford DW, Chiou CT (1992) Effect of water saturation in soil organic matter on the partition of organic compounds. Environ Sci Technol 26:965–970. https://doi.org/10.1021/es00029a015
Salehi B et al (2018) Aloe genus plants: from farm to food applications and phytopharmacotherapy. Int J mol Sci 19:2843. https://doi.org/10.3390/ijms19092843
Spielman-Sun E, Lombi E, Donner E, Howard D, Unrine JM, Lowry GV (2017) Impact of surface charge on cerium oxide nanoparticle uptake and translocation by wheat (Triticum aestivum). Environ Sci Technol 51:7361–7368. https://doi.org/10.1021/acs.est.7b00813
Sun YN, Jo AR, Kim JH, Kang JS, Kim YH (2016) Soluble epoxide hydrolase inhibitory activity of anthraquinone components from Aloe. Planta Med 81:S1–S381. https://doi.org/10.1055/s-0036-1596599
Tonelli FM et al (2015) Graphene-based nanomaterials: biological and medical applications and toxicity. Nanomedicine 10:2423–2450. https://doi.org/10.2217/nnm.15.65
Wang Q, Li C, Wang Y, Que X (2019) Phytotoxicity of graphene family nanomaterials and its mechanisms: a review. Front Chem 7:00292. https://doi.org/10.3389/fchem.2019.00292
Xu C-X, Liu Y-L, Zheng Q-S, Liu Z-P (2006) Silicate improves growth and ion absorption and distribution in Aloe vera under salt stress. J Plant Physiol Mol Biol 32:73–78
Yao J, Wang H, Chen M, Yang M (2019) Recent advances in graphene-based nanomaterials: properties, toxicity and applications in chemistry, biology and medicine. Microchim Acta. https://doi.org/10.1007/s00604-019-3458-x
Yu S, Sheng L, Mao H, Huang X, Luo L, Li Y (2020) Physiological response of Conyza Canadensis to cadmium stress monitored by Fourier transform infrared spectroscopy and cadmium accumulation. Spectrochim Acta A 229:118007. https://doi.org/10.1016/j.saa.2019.118007
Zhang M, Gao B, Chen J, Li Y, Creamer AE, Chen H (2014) Slow-release fertilizer encapsulated by graphene oxide films. Chem Eng J 255:107–113. https://doi.org/10.1016/j.cej.2014.06.023
Zhang P, Zhang R, Fang X, Song T, Cai X, Liu H, Du S (2016) Toxic effects of graphene on the growth and nutritional levels of wheat (Triticum aestivum L.): short- and long-term exposure studies. J Hazard Mater 317:543–551. https://doi.org/10.1016/j.jhazmat.2016.06.019
Zhao J, Guo Y, Li Z, Guo Q, Shi J, Wang L, Fan J (2012) An approach for synthesizing graphene with calcium carbonate and magnesium. Carbon 50:4939–4944. https://doi.org/10.1016/j.carbon.2012.06.024
Zhao S, Wang Q, Zhao Y, Rui Q, Wang D (2015) Toxicity and translocation of graphene oxide in Arabidopsis thaliana. Environ Toxicol Pharmacol 39:145–156. https://doi.org/10.1016/j.etap.2014.11.014
Zhao L et al (2020) Nano-biotechnology in agriculture: use of nanomaterials to promote plant growth and stress tolerance. J Agric Food Chem 68:1935–1947. https://doi.org/10.1021/acs.jafc.9b06615
Zuverza-Mena N et al (2017) Exposure of engineered nanomaterials to plants: insights into the physiological and biochemical responses-a review. Plant Physiol Biochem 110:236–264. https://doi.org/10.1016/j.plaphy.2016.05.037
Funding
This research was funded by Doctoral Scientific Research Foundation of Shanxi Datong University (2018-B-20), The Program for Scientific and Technological Innovation of Higher Education Institutions in Shanxi (2019L0767), Shanxi Datong University Students Innovation and Entrepreneurship Project (XDC2019232), Science and Technology Achievements Transformation Guide project of Shanxi province (201804D131041), The Program for Scientific and Technological Innovation of Higher Education Institutions in Shanxi (2020L0467), Natural Science Foundation of Shanxi Province (201901D211437) and The National Natural Science Foundation of China (52071192).
Author information
Authors and Affiliations
Contributions
Jianguo Zhao and Haiyan Wang conceived the project; Xiao Zhang and Huifen Cao designed the experiments, performed the experiment and wrote the manuscript; Zhiwen Chen supervised the project; Jin Zhang provided the GO material and performed the FT-IR analysis; Baoyan Xing performed the SEM analysis; Xinyu Li performed Raman spectra analysis. All authors have read and agreed to the published version of the manuscript.
Corresponding authors
Ethics declarations
Conflicts of Interest
The authors declare no conflict of interest.
Consent to participate
All authors participate to finish the work.
Consent for publication
All authors agreed for publication.
Ethics approval
Compliance with ethical standards.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Zhang, X., Cao, H., Zhao, J. et al. Graphene oxide exhibited positive effects on the growth of Aloe vera L. Physiol Mol Biol Plants 27, 815–824 (2021). https://doi.org/10.1007/s12298-021-00979-3
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12298-021-00979-3