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

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.

Graphical abstract

Keywords

Nano-TiO ₂ / 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

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