|
|
Photosynthesis and related metabolic mechanism of promoted rice (Oryza sativa L.) growth by TiO2 nanoparticles |
Yingdan Zhang1,2, Na Liu1,2, Wei Wang1,2, Jianteng Sun1,3, Lizhong Zhu1,2() |
1. College of Environmental and Resource Sciences, Zhejiang University, Hangzhou 310058, China 2. Zhejiang Provincial Key Laboratory of Organic Pollution Process and Control, Hangzhou 310058, China 3. School of Environmental Science and Engineering, Guangdong University of Petrochemical Technology, Maoming 525000, China |
|
|
Abstract • The rice growth was promoted by nano-TiO2 of 0.1–100 mg/L. • Nano-TiO2 enhanced the energy storage in photosynthesis. • Nano-TiO2 reduced energy consumption in carbohydrate metabolism and TCA cycle. Titanium dioxide nanoparticle (nano-TiO2), as an excellent UV absorbent and photo-catalyst, has been widely applied in modern industry, thus inevitably discharged into environment. We proposed that nano-TiO2 in soil can promote crop yield through photosynthetic and metabolic disturbance, therefore, we investigated the effects of nano-TiO2 exposure on related physiologic-biochemical properties of rice (Oryza sativa L.). Results showed that rice biomass was increased >30% at every applied dosage (0.1–100 mg/L) of nano-TiO2. The actual photosynthetic rate (Y(II)) significantly increased by 10.0% and 17.2% in the treatments of 10 and 100 mg/L respectively, indicating an increased energy production from photosynthesis. Besides, non-photochemical quenching (Y(NPQ)) significantly decreased by 19.8%–26.0% of the control in all treatments respectively, representing a decline in heat dissipation. Detailed metabolism fingerprinting further revealed that a fortified transformation of monosaccharides (D-fructose, D-galactose, and D-talose) to disaccharides (D-cellobiose, and D-lactose) was accompanied with a weakened citric acid cycle, confirming the decrease of energy consumption in metabolism. All these results elucidated that nano-TiO2 promoted rice growth through the upregulation of energy storage in photosynthesis and the downregulation of energy consumption in metabolism. This study provides a mechanistic understanding of the stress-response hormesis of rice after exposure to nano-TiO2, and provides worthy information on the potential application and risk of nanomaterials in agricultural production.
|
Keywords
Nano-TiO2
Rice
Photosynthesis
Metabolomics
Energy storage
|
Corresponding Author(s):
Lizhong Zhu
|
Issue Date: 11 June 2020
|
|
1 |
D H Atha, H H Wang, E J Petersen, D Cleveland, R D Holbrook, P Jaruga, M Dizdaroglu, B S Xing, B C Nelson (2012). Copper oxide nanoparticle mediated DNA damage in terrestrial plant models. Environmental Science & Technology, 46(3): 1819–1827
https://doi.org/10.1021/es202660k
|
2 |
Y Bo, C Y Jin, Y M Liu, W J Yu, H Z Kang (2014). Metabolomic analysis on the toxicological effects of TiO2 nanoparticles in mouse fibroblast cells: from the perspective of perturbations in amino acid metabolism. Toxicology Mechanisms and Methods, 24(7): 461–469
https://doi.org/10.3109/15376516.2014.939321
|
3 |
J, Dalsgaard M St John, G Kattner, D Muller-Navarra, W Hagen (2003). Fatty acid trophic markers in the pelagic marine environment. Advances in Marine Biology, 46: 225–340
https://doi.org/10.1016/S0065-2881(03)46005-7
|
4 |
P Das, I Manna, P Sil, M Bandyopadhyay, A K Biswas (2019). Exogenous silicon alters organic acid production and enzymatic activity of TCA cycle in two NaCl stressed indica rice cultivars. Plant Physiology and Biochemistry, 136: 76–91
https://doi.org/10.1016/j.plaphy.2018.12.026
|
5 |
F Demailly, I Elfeky, L Malbezin, M Le Guedard, M Eon, J J Bessoule, A Feurtet-Mazel, F Delmas, N Mazzella, P Gonzalez, S Morin (2019). Impact of diuron and S-metolachlor on the freshwater diatom Gomphonema gracile: Complementarity between fatty acid profiles and different kinds of ecotoxicological impact-endpoints. Science of the Total Environment, 688: 960–969
https://doi.org/10.1016/j.scitotenv.2019.06.347
|
6 |
F Q Gao, F H Hong, C Liu, L Zheng, M Y Su, X Wu, F Yang, C Wu, P Yang (2006). Mechanism of nano-anatase TiO2 on promoting photosynthetic carbon reaction of spinach: Inducing complex of Rubisco-Rubisco activase. Biological Trace Element Research, 111(1-3): 239–253
https://doi.org/10.1385/BTER:111:1:239
|
7 |
M Ghosh, M Bandyopadhyay, A Mukherjee (2010). Genotoxicity of titanium dioxide (TiO2) nanoparticles at two trophic levels: Plant and human lymphocytes. Chemosphere, 81(10): 1253–1262
https://doi.org/10.1016/j.chemosphere.2010.09.022
|
8 |
X Hao, G L Wang, S Chen, H T Yu, Q Xie (2019). Enhanced activation of peroxymonosulfate by CNT-TiO2 under UV-light assistance for efficient degradation of organic pollutants. Frontiers of Environmental Science & Engineering, 13(5): 77
https://doi.org/doi:org/10.1007/s11783-019-1161-0
|
9 |
J Harwood, J Moore Jr T S (1989). Lipid-metabolism in plants. Critical Reviews in Plant Sciences, 8(1): 1–43
https://doi.org/10.1080/07352688909382269
|
10 |
H Hernandez-Hernandez, T Quiterio-Gutierrez, G Cadenas-Pliego, H Ortega-Ortiz, A D Hernandez-Fuentes, M C Cabrera de la Fuente, J Valdes-Reyna, A Juarez-Maldonado (2019). Impact of selenium and copper nanoparticles on yield, antioxidant system, and fruit quality of tomato plants. Plants, 8(10): 355
https://doi.org/10.3390/plants8100355
|
11 |
S Hisajimai, T A Thorpe (1985). Lactose metabolism in lactose-adapted cells of Japanese morning-glory. Journal of Plant Physiology, 118(2): 145–151
https://doi.org/10.1016/S0176-1617(85)80143-7
|
12 |
F H Hong, F Yang, C Liu, Q Gao, Z G Wan, F G Gu, C Wu, Z N Ma, J Zhou, P Yang (2005a). Influences of nano-TiO2 on the chloroplast aging of spinach under light. Biological Trace Element Research, 104(3): 249–260
https://doi.org/10.1385/BTER:104:3:249
|
13 |
F H Hong, J Zhou, C Liu, F Yang, C Wu, L Zheng, P Yang (2005b). Effect of nano-TiO2 on photochemical reaction of chloroplasts of spinach. Biological Trace Element Research, 105(1-3): 269–279
https://doi.org/10.1385/BTER:105:1-3:269
|
14 |
F S Hong, P Yang, F Q Gao, C Liu, L Zheng, F Yang, J Zhou (2005c). Effect of nano-anatase TiO2 on spectral characterization of photosystem II particles from spinach. Chemical Research in Chinese Universities, 21: 196–200
|
15 |
A Iftikhar, S Ali, T Yasmeen, M S Arif, M Zubair, M Rizwan, H A S Alhaithloul, A A M Alayafi, M H Soliman (2019). Effect of gibberellic acid on growth, photosynthesis and antioxidant defense system of wheat under zinc oxide nanoparticle stress. Environmental Pollution, 254: 113109
https://doi.org/10.1016/j.envpol.2019.113109
|
16 |
N E Ioannidis, J A Cruz, K Kotzabasis, D M Kramer (2012). Evidence that putrescine modulates the higher plant photosynthetic proton circuit. PLoS One, 7(1): e29864
https://doi.org/10.1371/journal.pone.0029864
|
17 |
J A Ko, Y S Hwang (2019). Effects of nanoTiO2 on tomato plants under different irradiances. Environmental Pollution, 255: 113141
https://doi.org/10.1016/j.envpol.2019.113141
|
18 |
A A Lavell, C Benning (2019). Cellular organization and regulation of plant glycerolipid metabolism. Plant & Cell Physiology, 60(6): 1176–1183
https://doi.org/10.1093/pcp/pcz016
|
19 |
F A Loewus, P P N Murthy (2000). Myo-inositol metabolism in plants. Plant Science, 150(1): 1–19
https://doi.org/10.1016/S0168-9452(99)00150-8
|
20 |
A Nookaraju, S K Pandey, T Fujino, J Y Kim, M C Suh, C P Joshi(2014). Enhanced accumulation of fatty acids and triacylglycerols in transgenic tobacco stems for enhanced bioenergy production. Plant Cell Reports, 33(7): 1041–1052
https://doi.org/10.1007/s00299-014-1582-y
|
21 |
A Picado, S M Paixao, L Moita, L Silva, M Diniz, J Lourenco, I Peres, L Castro, J B Correia, J Pereira, I Ferreira, A P A Matos, P Barquinha, E Mendonca (2015). A multi-integrated approach on toxicity effects of engineered TiO2 nanoparticles. Frontiers of Environmental Science & Engineering, 9(5): 793–803
https://doi.org/10.1007/s11783-015-0775-0
|
22 |
F Piccinno, F Gottschalk, S Seeger, B Nowack (2012). Industrial production quantities and uses of ten engineered nanomaterials in Europe and the world. Journal of Nanoparticle Research, 14(9): 1109
https://doi.org/10.1007/s11051-012-1109-9
|
23 |
R Pratelli, G Pilot (2014). Regulation of amino acid metabolic enzymes and transporters in plants. Journal of Experimental Botany, 65(19): 5535–5556
https://doi.org/10.1093/jxb/eru320
|
24 |
Q Qu, Z Y Zhang, Y Li, Z G Zhou, Y Z Ye, T Lu, L W Sun, H F Qian (2019). Comparative molecular and metabolic responses of wheat seedlings (Triticum aestivum L.) to the imazethapyr enantiomers S-IM and R-IM. Science of the Total Environment, 692: 723–731
https://doi.org/10.1016/j.scitotenv.2019.07.333
|
25 |
C Ratnasekhar, M Sonane, A Satish, M K R Mudiam (2015). Metabolomics reveals the perturbations in the metabolome of Caenorhabditis elegans exposed to titanium dioxide nanoparticles. Nanotoxicology, 9(8): 994–1004
https://doi.org/10.3109/17435390.2014.993345
|
26 |
J W Riesmeier, L Willmitzer, W B Frommer (1994). Evidence for an essential role of the sucrose transporter in phloem loading and assimilate partitioning. EMBO Journal, 13(1): 1–7
https://doi.org/10.1002/j.1460-2075.1994.tb06229.x
|
27 |
J C Servaites, L E Schrader, D M Jung (1979). Energy-dependent loading of amino acids and sucrose into the phloem of soybean. Plant Physiology, 64(4): 546–550
https://doi.org/10.1104/pp.64.4.546
|
28 |
D Q Shi, D B Li, Y P Zhang, X J Li, Y Tao, Z N Yan, Y S Ao (2019). Effects of Pseudomonas alkylphenolica KL28 on immobilization of Hg in soil and accumulation of Hg in cultivated plant. Biotechnology Letters, 41: 1343–1354
https://doi.org/10.1007/s10529-019-02736-9
|
29 |
U Song, M Shin, G Lee, J Roh, Y Kim, E J Lee (2013). Functional analysis of TiO2 nanoparticle toxicity in three plant species. Biological Trace Element Research, 155(1): 93–103
https://doi.org/10.1007/s12011-013-9765-x
|
30 |
W Stock, L Blommaert, I Daveloose, W Vyverman, K Sabbe (2019). Assessing the suitability of imaging-PAM fluorometry for monitoring growth of benthic diatoms. Journal of Experimental Marine Biology and Ecology, 513: 35–41
https://doi.org/10.1016/j.jembe.2019.02.003
|
31 |
L L Sun, Y P Du, Q Y Duan, H Zhai (2018). Root temperature regulated frost damage in leaves of the grapevine Vitis vinifera L. Australian Journal of Grape and Wine Research, 24(2): 181–189
https://doi.org/10.1111/ajgw.12328
|
32 |
K Tokuhiro, N Ishida, A Kondo, H Takahashi (2008). Lactic fermentation of cellobiose by a yeast strain displaying beta-glucosidase on the cell surface. Applied Microbiology and Biotechnology, 79(3): 481–488
https://doi.org/10.1007/s00253-008-1454-x
|
33 |
J A Torres, A E Nogueira, G T S T da Silva, O F Lopes, Y J Wang, T He, C Ribeiro (2020). Enhancing TiO2 activity for CO2 photoreduction through MgO decoration. Journal of CO2 Utilization, 35: 106–114
https://doi.org/10.1016/j.jcou.2019.09.008
|
34 |
B Y Wu, L Z Zhu, X C Le (2017). Metabolomics analysis of TiO2 nanoparticles induced toxicological effects on rice (Oryza sativa L.). Environmental Pollution, 230: 302–310
https://doi.org/10.1016/j.envpol.2017.06.062
|
35 |
D Wu, S X Yang, W C Du, Y Yin, J X Zhang, H Y Guo (2019). Effects of titanium dioxide nanoparticles on Microcystis aeruginosa and microcystins production and release. Journal of Hazardous Materials, 377: 1–7
https://doi.org/10.1016/j.jhazmat.2019.05.013
|
36 |
M L Xu, Y G Zhu, K H Gu, J G Zhu, Y Yin, R Ji, W C Du, H Y Guo (2019). Transcriptome reveals the rice response to elevated free air CO2 concentration and TiO2 nanoparticles. Environmental Science & Technology, 53(20): 11714–11724
https://doi.org/10.1021/acs.est.9b02182
|
37 |
F Yang, C Liu, F Q Gao, M Y Su, X Wu, L Zheng, F S Hong, P Yang (2007). The improvement of spinach growth by nano-anatase TiO2 treatment is related to nitrogen photoreduction. Biological Trace Element Research, 119(1): 77–88
https://doi.org/10.1007/s12011-007-0046-4
|
38 |
L Zhang, X Y Wang, J Z Guo, Q L Xia, G Zhao, H N Zhou, F W Xie (2013). Metabolic profiling of Chinese tobacco leaf of different geographical origins by GC-MS. Journal of Agricultural and Food Chemistry, 61(11): 2597–2605
https://doi.org/10.1021/jf400428t
|
39 |
L Zheng, F Hong, S Lu, C Liu (2005). Effect of nano-TiO2 on strength of naturally aged seeds and growth of spinach. Biological Trace Element Research, 104(1): 83–92
https://doi.org/10.1385/BTER:104:1:083
|
40 |
R Zhou, B Quebedeaux (2003). Changes in photosynthesis and carbohydrate metabolism in mature apple leaves in response to whole plant source-sink manipulation. Journal of the American Society for Horticultural Science, 128(1): 113–119
https://doi.org/10.21273/JASHS.128.1.0113
|
|
Viewed |
|
|
|
Full text
|
|
|
|
|
Abstract
|
|
|
|
|
Cited |
|
|
|
|
|
Shared |
|
|
|
|
|
Discussed |
|
|
|
|