Photosynthesis and related metabolic mechanism of promoted rice (Oryza sativa L.) growth by TiO₂ nanoparticles

Highlights

• 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.

Abstract

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.

Graphical abstract

Keywords

Nano-TiO₂ / Rice / Photosynthesis / Metabolomics / Energy storage

References

[1] Atha D H, Wang H H, Petersen E J, Cleveland D, Holbrook R D, Jaruga P, Dizdaroglu M, Xing B S, Nelson B C (2012). Copper oxide nanoparticle mediated DNA damage in terrestrial plant models. Environmental Science & Technology, 46(3): 1819–1827

[2] Bo Y, Jin C Y, Liu Y M, Yu W J, Kang H Z (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

[3] Dalsgaard J,St John M, Kattner G, Muller-Navarra D, Hagen W (2003). Fatty acid trophic markers in the pelagic marine environment. Advances in Marine Biology, 46: 225–340

[4] Das P, Manna I, Sil P, Bandyopadhyay M, Biswas A K (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

[5] Demailly F, Elfeky I, Malbezin L, Le Guedard M, Eon M, Bessoule J J, Feurtet-Mazel A, Delmas F, Mazzella N, Gonzalez P, Morin S (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

[6] Gao F Q, Hong F H, Liu C, Zheng L, Su M Y, Wu X, Yang F, Wu C, Yang P (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

[7] Ghosh M, Bandyopadhyay M, Mukherjee A (2010). Genotoxicity of titanium dioxide (TiO₂) nanoparticles at two trophic levels: Plant and human lymphocytes. Chemosphere, 81(10): 1253–1262

[8] Hao X, Wang G L, Chen S, Yu H T, Xie Q (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

[9] Harwood J, Moore J T S Jr (1989). Lipid-metabolism in plants. Critical Reviews in Plant Sciences, 8(1): 1–43

[10] Hernandez-Hernandez H, Quiterio-Gutierrez T, Cadenas-Pliego G, Ortega-Ortiz H, Hernandez-Fuentes A D, Cabrera de la Fuente M C, Valdes-Reyna J, Juarez-Maldonado A (2019). Impact of selenium and copper nanoparticles on yield, antioxidant system, and fruit quality of tomato plants. Plants, 8(10): 355

[11] Hisajimai S, Thorpe T A (1985). Lactose metabolism in lactose-adapted cells of Japanese morning-glory. Journal of Plant Physiology, 118(2): 145–151

[12] Hong F H, Yang F, Liu C, Gao Q, Wan Z G, Gu F G, Wu C, Ma Z N, Zhou J, Yang P (2005a). Influences of nano-TiO₂ on the chloroplast aging of spinach under light. Biological Trace Element Research, 104(3): 249–260

[13] Hong F H, Zhou J, Liu C, Yang F, Wu C, Zheng L, Yang P (2005b). Effect of nano-TiO₂ on photochemical reaction of chloroplasts of spinach. Biological Trace Element Research, 105(1-3): 269–279

[14] Hong F S, Yang P, Gao F Q, Liu C, Zheng L, Yang F, Zhou J (2005c). Effect of nano-anatase TiO₂ on spectral characterization of photosystem II particles from spinach. Chemical Research in Chinese Universities, 21: 196–200

[15] Iftikhar A, Ali S, Yasmeen T, Arif M S, Zubair M, Rizwan M, Alhaithloul H A S, Alayafi A A M, Soliman M H (2019). Effect of gibberellic acid on growth, photosynthesis and antioxidant defense system of wheat under zinc oxide nanoparticle stress. Environmental Pollution, 254: 113109

[16] Ioannidis N E, Cruz J A, Kotzabasis K, Kramer D M (2012). Evidence that putrescine modulates the higher plant photosynthetic proton circuit. PLoS One, 7(1): e29864

[17] Ko J A, Hwang Y S (2019). Effects of nanoTiO₂ on tomato plants under different irradiances. Environmental Pollution, 255: 113141

[18] Lavell A A, Benning C (2019). Cellular organization and regulation of plant glycerolipid metabolism. Plant & Cell Physiology, 60(6): 1176–1183

[19] Loewus F A, Murthy P P N (2000). Myo-inositol metabolism in plants. Plant Science, 150(1): 1–19

[20] Nookaraju A, Pandey S K, Fujino T, Kim J Y, Suh M C, Joshi C P(2014). Enhanced accumulation of fatty acids and triacylglycerols in transgenic tobacco stems for enhanced bioenergy production. Plant Cell Reports, 33(7): 1041–1052

[21] Picado A, Paixao S M, Moita L, Silva L, Diniz M, Lourenco J, Peres I, Castro L, Correia J B, Pereira J, Ferreira I, Matos A P A, Barquinha P, Mendonca E (2015). A multi-integrated approach on toxicity effects of engineered TiO₂ nanoparticles. Frontiers of Environmental Science & Engineering, 9(5): 793–803

[22] Piccinno F, Gottschalk F, Seeger S, Nowack B (2012). Industrial production quantities and uses of ten engineered nanomaterials in Europe and the world. Journal of Nanoparticle Research, 14(9): 1109

[23] Pratelli R, Pilot G (2014). Regulation of amino acid metabolic enzymes and transporters in plants. Journal of Experimental Botany, 65(19): 5535–5556

[24] Qu Q, Zhang Z Y, Li Y, Zhou Z G, Ye Y Z, Lu T, Sun L W, Qian H F (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

[25] Ratnasekhar C, Sonane M, Satish A, Mudiam M K R (2015). Metabolomics reveals the perturbations in the metabolome of Caenorhabditis elegans exposed to titanium dioxide nanoparticles. Nanotoxicology, 9(8): 994–1004

[26] Riesmeier J W, Willmitzer L, Frommer W B (1994). Evidence for an essential role of the sucrose transporter in phloem loading and assimilate partitioning. EMBO Journal, 13(1): 1–7

[27] Servaites J C, Schrader L E, Jung D M (1979). Energy-dependent loading of amino acids and sucrose into the phloem of soybean. Plant Physiology, 64(4): 546–550

[28] Shi D Q, Li D B, Zhang Y P, Li X J, Tao Y, Yan Z N, Ao Y S (2019). Effects of Pseudomonas alkylphenolica KL28 on immobilization of Hg in soil and accumulation of Hg in cultivated plant. Biotechnology Letters, 41: 1343–1354

[29] Song U, Shin M, Lee G, Roh J, Kim Y, Lee E J (2013). Functional analysis of TiO₂ nanoparticle toxicity in three plant species. Biological Trace Element Research, 155(1): 93–103

[30] Stock W, Blommaert L, Daveloose I, Vyverman W, Sabbe K (2019). Assessing the suitability of imaging-PAM fluorometry for monitoring growth of benthic diatoms. Journal of Experimental Marine Biology and Ecology, 513: 35–41

[31] Sun L L, Du Y P, Duan Q Y, Zhai H (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

[32] Tokuhiro K, Ishida N, Kondo A, Takahashi H (2008). Lactic fermentation of cellobiose by a yeast strain displaying beta-glucosidase on the cell surface. Applied Microbiology and Biotechnology, 79(3): 481–488

[33] Torres J A, Nogueira A E, da Silva G T S T, Lopes O F, Wang Y J, He T, Ribeiro C (2020). Enhancing TiO₂ activity for CO₂ photoreduction through MgO decoration. Journal of CO₂ Utilization, 35: 106–114

[34] Wu B Y, Zhu L Z, Le X C (2017). Metabolomics analysis of TiO₂ nanoparticles induced toxicological effects on rice (Oryza sativa L.). Environmental Pollution, 230: 302–310

[35] Wu D, Yang S X, Du W C, Yin Y, Zhang J X, Guo H Y (2019). Effects of titanium dioxide nanoparticles on Microcystis aeruginosa and microcystins production and release. Journal of Hazardous Materials, 377: 1–7

[36] Xu M L, Zhu Y G, Gu K H, Zhu J G, Yin Y, Ji R, Du W C, Guo H Y (2019). Transcriptome reveals the rice response to elevated free air CO₂ concentration and TiO₂ nanoparticles. Environmental Science & Technology, 53(20): 11714–11724

[37] Yang F, Liu C, Gao F Q, Su M Y, Wu X, Zheng L, Hong F S, Yang P (2007). The improvement of spinach growth by nano-anatase TiO₂ treatment is related to nitrogen photoreduction. Biological Trace Element Research, 119(1): 77–88

[38] Zhang L, Wang X Y, Guo J Z, Xia Q L, Zhao G, Zhou H N, Xie F W (2013). Metabolic profiling of Chinese tobacco leaf of different geographical origins by GC-MS. Journal of Agricultural and Food Chemistry, 61(11): 2597–2605

[39] Zheng L, Hong F, Lu S, Liu C (2005). Effect of nano-TiO₂ on strength of naturally aged seeds and growth of spinach. Biological Trace Element Research, 104(1): 83–92

[40] Zhou R, Quebedeaux B (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

Acknowledgements

This work was supported by the National Natural Science Foundation of China (Nos. 21836003 and 21520102009).

Electronic Supplementary Material

Supplementary material is available in the online version of this article at https://doi.org/10.1007/s11783-020-1282-5 and is accessible for authorized users.

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