Effects of iron oxide nanoparticles on phenotype and metabolite changes in hemp clones (Cannabis sativa L.)
Received date: 04 Nov 2021
Revised date: 18 Jan 2022
Accepted date: 09 Feb 2022
Published date: 15 Oct 2022
Copyright
● Fe3O4 NPs increased the biomass and chlorophyll content of hemp clones. ● Fe3O4 NPs penetrated and were internalized by root cells. ● Fe3O4 NPs induced the alteration of metabolite profiles in hemp leaves. ● The psychoactive compound THC in hemp leaves was significantly down-regulated.
We investigated the effect of iron oxide nanoparticles (Fe3O4 NPs, ~17 nm in size) on the phenotype and metabolite changes in hemp (Cannabis sativa L.), an annual crop distributed worldwide. Hemp clones were grown in hydroponic cultures with Fe3O4 NPs (50, 100, 200, or 500 mg/L) for four weeks. TEM and ICP-MS were used to determine Fe3O4 NPs uptake and translocation. LC-MS-based metabolomics was employed to explore the deep insight into the effect of Fe3O4 NPs on hemp plants. The results revealed that plant growth enhanced gradually with increasing concentrations of given NPs up to 200 mg/L, which improved the fresh weight and dry weight by 36.13% and 74.68%, respectively, compared to the control. Even at a high dose (500 mg/L), Fe3O4 NPs promoted plant growth, including increased biomass and tissue length. NPs significantly increased the iron and chlorophyll content in plant tissues Increased catalase activity and reduced hydrogen peroxide content in hemp leaves suggested that the Fe3O4 NPs activated the defense system. TEM showed that NPs were abundantly attached to the cell wall and dispersed throughout the root cells. Metabolomics revealed that Fe3O4 NPs induced metabolic reprogramming in hemp leaves, including the up-regulation of carbohydrates and organic acids, and down-regulation of antioxidants, especially tetrahydrocannabinol (THC). The significantly up-regulated metabolites, including peonidin and 2-hydroxycinnamic acid, could be involved in photosynthesis in hemp plants. These results demonstrate the potential of Fe3O4 NPs for promoting hemp growth and decreasing the THC content at low doses.
Key words: Fe3O4 nanoparticle; Hemp; Growth enhancement; THC; Metabolite
Canhui Deng , Qing Tang , Zemao Yang , Zhigang Dai , Chaohua Cheng , Ying Xu , Xiaojun Chen , Xiaoyu Zhang , Jianguang Su . Effects of iron oxide nanoparticles on phenotype and metabolite changes in hemp clones (Cannabis sativa L.)[J]. Frontiers of Environmental Science & Engineering, 2022 , 16(10) : 134 . DOI: 10.1007/s11783-022-1569-9
1 |
Agrawal B , Lakshmanan V , Kaushik S , Bais H P . (2012). Natural variation among Arabidopsis accessions reveals malic acid as a key mediator of Nickel (Ni) tolerance. Planta, 236( 2): 477– 489
|
2 |
Al-Amri N , Tombuloglu H , Slimani Y , Akhtar S , Barghouthi M , Almessiere M , Alshammari T , Baykal A , Sabit H , Ercan I , Ozcelik S . (2020). Size effect of iron (III) oxide nanomaterials on the growth, and their uptake and translocation in common wheat (Triticum aestivum L.). Ecotoxicology and Environmental Safety, 194 : 110377
|
3 |
Atak Q, Celik O, Olgun A, Alikamanoglu S, Rzakoulieva A ( 2007). Effect of magnetic field on peroxidase activities of soybean tissue culture.Biotechnology, Biotechnological Equipment, 21( 2): 166− 171
|
4 |
Bar-Sela G , Vorobeichik M , Drawsheh S , Omer A , Goldberg V , Muller E . (2013). The medical necessity for medicinal cannabis: prospective, observational study evaluating the treatment in cancer patients on supportive or palliative care. Evidence-based complementary and alternative medicine: eCAM, 2013 : 1– 8
|
5 |
Barhoumi L , Oukarroum A , TaherL B , SmiriL S , Abdelmelek H , Dewez D . (2015). Effects of superparamagnetic iron oxide nanoparticles on photosynthesis and growth of the aquatic plant Lemna gibba. Archives of Environmental Contamination and Toxicology, 68( 3): 510– 520
|
6 |
Borges R S, Batista J Jr, Viana R B, Baetas A C, Orestes E, Andrade M A, Honório K M, da Silva A B F ( 2013). Understanding the molecular aspects of tetrahydrocannabinol and cannabidiol as antioxidants. Molecules (Basel, Switzerland), 18( 10): 12663− 12674
|
7 |
Cai L , Cai L , Jia H , Liu C , Wang D , Sun X . (2020). Foliar exposure of Fe3O4 nanoparticles on Nicotiana benthamiana: Evidence for nanoparticles uptake, plant growth promoter and defense response elicitor against plant virus. Journal of Hazardous Materials, 393 : 122415
|
8 |
Carvalho I S , Cavaco T , Carvalho L M , Duque P . (2010). Effect of photoperiod on flavonoid pathway activity in sweet potato (Ipomoea batatas (L.) Lam.). leaves. Food Chemistry, 118( 2): 384– 390
|
9 |
Chichiriccò G, Poma A ( 2015). Penetration and toxicity of nanomaterials in higher plants. Nanomaterials (Basel, Switzerland), 5( 2): 851− 873
|
10 |
Deng J H , Zhang X R , Zeng G M , Gong J L , Niu Q Y , Liang J . (2013). Simultaneous removal of Cd(II) and ionic dyes from aqueous solution using magnetic graphene oxide nanocomposite as an adsorbent. Chemical Engineering Journal, 226 : 189– 200
|
11 |
Feyissa B A , Arshad M , Gruber M Y , Kohalmi S E , Hannoufa A . (2019). The interplay between miR156/SPL13 and DFR/WD40-1 regulate drought tolerance in alfalfa. BMC Plant Biology, 19( 1): 434– 453
|
12 |
Ghafariyan M H , Malakouti M J , Dadpour M R , Stroeve P , Mahmoudi M . (2013). Effects of magnetite nanoparticles on soybean chlorophy Ⅱ. Environmental Science & Technology, 47( 18): 10645– 10652
|
13 |
Hu J , Wu X Y , Wu F , Chen W X , Zhang X Y , White J C , Li J L , Wan Y , Liu J F , Wang X L . (2020). TiO2 nanoparticle exposure on lettuce (Lactuca sativa L.):. Dose-dependent deterioration of nutritional quality. Environmental Science-Nano, 7( 2): 501– 513
|
14 |
Júnior A L G , Islam M T , Nicolau L A D , de Souza L K M , Araújo T D S , Lopes de Oliveira G A , de Melo Nogueira K , da Silva Lopes L , Medeiros J R , Mubarak M S , Melo-Cavalcante A A C . (2020). Anti-Inflammatory, antinociceptive, and antioxidant properties of anacardic acid in experimental models. ACS Omega, 5( 31): 19506– 19515
|
15 |
Kim J H , Lee Y , Kim E J , Gu S , Sohn E J , Seo Y S , An H J , ChangY S . (2014). Exposure of iron nanoparticles to Arabidopsis thaliana enhances root elongation by triggering cell wall loosening. Environmental Science & Technology, 48( 6): 3477– 3485
|
16 |
Labille J , Catalano R , Slomberg D , Motellier S , Pinsino A , Hennebert P , Santaella C , Bartolomei V . (2020). Assessing sunscreen lifecycle to minimize environmental risk posed by nanoparticulate uv-filters: A review for safer-by design products. Frontiers in Environmental Science, 8 : 1– 25
|
17 |
Li J , Hu J , Ma C , Wang Y , Wu C , Huang J , Xing B . (2016a). Uptake, translocation and physiological effects of magnetic iron oxide (gamma-Fe2O3) nanoparticles in corn (Zea mays L.). Chemosphere, 159 : 326– 334
|
18 |
Li J , Hu J , Xiao L , Wang Y , Wang X . (2018). Interaction mechanisms between α-Fe2O3, γ-Fe2O3 and Fe3O4 nanoparticles and Citrus maxima seedlings. Science of the Total Environment, 625 : 677– 685
|
19 |
Li P Y , Wang A D , Du W C , Mao L , Wei Z B , Wang S F , Yuan H Y , Ji R , Zhao L J . (2020). Insight into the interaction between Fe-based nanomaterials and maize (Zea mays) plants at metabolic level. Science of the Total Environment, 738 : 139795– 139804
|
20 |
Liu Y H , Offler C E , Ruan Y L . (2014). A simple, rapid, and reliable protocol to localize hydrogen peroxide in large plant organs by DAB-mediated tissue printing. Frontiers in Plant Science, 5 : 1– 6
|
21 |
Li Y , Niu J , Shang E , Crittenden J C . (2016b). Influence of dissolved organic matter on photogenerated reactive oxygen species and metal-oxide nanoparticle toxicity. Water Research, 98 : 9– 18
|
22 |
Lo Piccolo E , Landi M , Massai R , Remorini D , Guidi L . (2020). Girled-induced anthocyanin accumulation in red-leafed Prunus cerasifera: Effect on photosynthesis, photoprotection and sugar metabolism. Plant Science:An International Journal of Experimental Plant Biology, 294 : 110456
|
23 |
Lu A , Li Y , Ding H , Xu X , Li Y , Ren G , Liang J , Liu Y , Hong H , Chen N , Chu S , Liu F , Li Y , Wang H , Ding C , Wang C , Lai Y , Liu J , Dick J , Liu K , Hochella M F Jr . (2019). Photoelectric conversion on Earth’s surface via widespread Fe- and Mn-mineral coatings. Proceedings of the National Academy of Sciences of the United States of America, 116( 20): 9741– 9746
|
24 |
Morales M I , Rico C M , Hernandez-Viezcas J A , Nunez J E , Barrios A C , Tafoya A , Flores-Marges J P , Peralta-Videa J R , Gardea-Torresdey J L . (2013). Toxicity assessment of cerium oxide nanoparticles in cilantro (Coriandrum sativum L). plants grown in organic soil. Journal of Agricultural and Food Chemistry, 61( 26): 6224– 6230
|
25 |
Pariona N , Martínez A I , Hernandez-Flores H , Clark-Tapia R . (2017). Effect of magnetite nanoparticles on the germination and early growth of Quercus macdougallii. Science of the Total Environment, 575 : 869– 875
|
26 |
Parisi C, Vigani M, Rodriguez-Cerezo E ( 2015). Agricultural nanotechnologies: What are the current possibilities? Nano Today, 10( 2): 124− 127
|
27 |
Rico C M , Majumdar S , Duarte-Gardea M , Peralta-Videa J R , Gardea-Torresdey J L . (2011). Interaction of nanoparticles with edible plants and their possible implications in the food chain. Journal of Agricultural and Food Chemistry, 59( 8): 3485– 3498
|
28 |
Schluttenhofer C , Yuan L . (2017). Challenges towards revitalizing hemp: A multifaceted crop. Trends in Plant Science, 22( 11): 917– 929
|
29 |
Senge M O , Ryan A A , Letchford K A , MacGowan S A , Mielke T . (2014). Chlorophylls, symmetry, chirality, and photosynthesis. Symmetry, 6( 3): 781– 843
|
30 |
Tombuloglu H , Anıl I , Akhtar S , Turumtay H , Sabit H , Slimani Y , Almessiere M , Baykal A . (2020). Iron oxide nanoparticles translocate in pumpkin and alter the phloem sap metabolites related to oil metabolism. Scientia Horticulturae, 265 : 109223
|
31 |
Tombuloglu H , Slimani Y , Tombuloglu G , Almessiere M , Baykal A . (2019a). Uptake and translocation of magnetite (Fe3O4) nanoparticles and its impact on photosynthetic genes in barley (Hordeum vulgare L). Chemosphere, 226 : 110– 122
|
32 |
Tombuloglu H, Slimani Y, Tombuloglu G, Almessiere M, Baykal A, Ercan I, Sozeri H( 2019b). Tracking of NiFe2O4 nanoparticles in barley ( Hordeum vulgare L.) and their impact on plant growth, biomass, pigmentation, catalase activity, and mineral uptake . Environmental Nanotechnology, Monitoring & Management, 11: 100223
|
33 |
Wang H , Kou X , Pei Z , Xiao J Q , Shan X , Xing B . (2011). Physiological effects of magnetite (Fe3O4) nanoparticles on perennial ryegrass (Lolium perenne L. ) and pumpkin (Cucurbita mixta) plants. Nanotoxicology, 5( 1): 30– 42
|
34 |
Xu J , Sun J , Du L , Liu X . (2012). Comparative transcriptome analysis of cadmium responses in Solanum nigrum and Solanum torvum. New Phytologist, 196( 1): 110– 124
|
35 |
Xu Y , Qin Y , Palchoudhury S , Bao Y . (2011). Water-soluble iron oxide nanoparticles with high stability and selective surface functionality. Langmuir, 27( 14): 8990– 8997
|
/
〈 |
|
〉 |