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Silicon Titanium Oxide Nanoparticles Can Stimulate Plant Growth and the Photosynthetic Pigments on Lettuce Crop

Silicon Titanium Oxide Nanoparticles Can Stimulate Plant Growth and the Photosynthetic Pigments... Agriculture (Poľnohospodárstvo), 66, 2020 (4): 148 − 160 DOI: 10.2478/agri-2020-0014 Original paper SILICON TITANIUM OXIDE NANOPARTICLES CAN STIMULATE PLANT GROWTH AND THE PHOTOSYNTHETIC PIGMENTS ON LETTUCE CROP 1 1 1 1 NUNO MARIZ-PONTE *, SARA SARIO , RAFAEL J. MENDES , CRISTIANA V. CORREIA , 2 2 1 JOSÉ MOUTINHO-PEREIRA , CARLOS M. CORREIA , CONCEIÇÃO SANTOS University of Porto, Porto, Portugal University of Trás-os-Montes e Alto Douro, Portugal MARIZ-PONTE, N. – SARIO, S. − MENDES, R.J − CORREIA, C.V. − MOUNTINHO-PEREIRA, J. − CORREIA, C.M. − SANTOS, C.: Silicon titanium oxide nanoparticles can stimulate plant growth and the photosynthetic pigments on lettuce crop. Agriculture (Poľnohospodárstvo), vol. 66, no. 4, pp. 148 – 160. Our knowledge of the bioactivity of silicon titanium oxide nanoparticles (TiSiO NPs) in crops is scarce, contrarily to TiO NPs and SiO NPs that are used in many industrial sectors, and have emerged in nanoagriculture (e.g., as pesticides or 2 2 nanofertilisers). To evaluate the potential of using TiSiO NPs in nanoagriculture, it is necessary to characterize their potential benefits on crops and the safety doses. Here, we report for the first time the bioactivity of TiSiO NPs (up to 100 mg/L) in the model crop lettuce (Lactuca sativa L.) exposed for three weeks (from seeds/seedlings to pre-harvesting phase). The doses applied did not compromise the germination rate, and highly stimulated plant fresh matter. TiSiO NPs had beneficial effects on photochemical processes by increasing chlorophyll levels. Effects on photosynthesis are less evident but TiSiO NPs (100 mg/L) stimulated the photosynthetic potential, increasing F /F and ETR when compared to the 50 mg/L conditions. v m TiSiO NPs did not influence the net photosynthetic rate and other Calvin-cycle variables. Soluble sugars and starch levels were overall maintained. In general, this first report on TiSiO NPs bioactivity suggests that they did not have a toxic effect, and may be used to potentiate crops’ growth. Principal component analysis (PCA) also shows that despite effects on photosynthetic performance is minimal regarding the control, the 50 and 100 mg/L doses strongly differ, with the lower dose promoting mostly pigment accumulation, while the higher dose slightly stimulates Photosystem II efficiency including the electron transport rate and other gas exchange parameters. Key words: gas exchange, nanoagriculture, nanofertilisers, photosynthesis, TiSiO Nanotechnologies are increasingly providing between titanium oxide (TiO ) and silicon oxide new and promising manufactured nanomaterials, (SiO ) mixture that forms an orthorhombic struc- including nanoparticles, to the agricultural sector ture, being increasingly used in multiple industries, (Parisi et al. 2015). The first data regarding the use particularly in the electronics sector (Garcia et al. of titanium in plant production was obtained at the 2009), ceramics (Varghese et al. 2011), optical in- beginning of the last century and has become an im- struments (Liu et al. 2017) and lubricant oils (Taheri portant field in plant nutrition (Kováčik et al. 2014). et al. 2018). Despite their industrial potential, and Silicon titanium oxide (TiSiO ) is a ternary system unlike other metal nanoparticles, TiSiO NPs remain 4 4 Nuno Mariz-Ponte (*Corresponding author), Sara Sario, Rafael J. Mendes, Cristiana V. Correia, Conceição Santos, LAQV-REQUIMTE, Department of Biology, Faculty of Sciences, University of Porto, Rua do Campo Alegre 4169-007, Porto, Portugal. E-mail: nuno.ponte@fc.up.pt José Moutinho-Pereira, Carlos M. Correia, Department of Biology and Environment, Centre for the Research and Technology of Agro-Environmental and Biological Sciences (CITAB), University of Trás-os-Montes e Alto Douro, 5001-801 Vila Real, Portugal © 2020 Authors. This is an open access article licensed under the Creative Commons Attribution-NonComercial-NoDerivs License (http://creativecommons.org/licenses/by-nc-nd/4.0/). 148 Agriculture (Poľnohospodárstvo), 66, 2020 (4): 148 − 160 unexplored in the nano-agroindustrial sector. Their the cell walls (Guerreiro et al. 2016), has a mitiga- antimicrobial activity was shown on Vibrio fischeri tion role under abiotic stress (Behboudi et al. 2018), and Salmonella typhimurium (Pereira et al. 2011; Ro- and is also increasingly being used on agricultural dríguez-González et al. 2019). Also, using different applications (Jampílek & Kráľová 2017; Luyckx et concentrations up to 1,000 mg/kg soil or 1,000 mg/L al. 2017). (of aqueous suspensions), other authors as Bou- As TiSiO NPs impacts on plants remain un- guerra et al. (2016) observed that E. andrei only known, we hypothesise that these NPs may combine avoided the soils spiked with 1,000 mg/kg TiSiO the positive effects of the TiO and SiO NPs. Under 4 2 2 NPs. Despite still unknown, TiSiO NPs may be safe moderate doses, TiO NPs were reported to stimulate 4 2 at low doses to plants as no negative effects were plant biomass and positively regulate N metabolism found on corn and oat seedlings growth, and only (Yang et al. 2006). Recent data also pinpointed that small decreases of dry mass and fresh mass were ob- TiO NPs were able to modulate plants’ response to served on lettuce and tomato seedlings (Bouguerra other stressors, lowering the Cu(II) and Cd phyto- et al. 2016). Some authors suggested that AgNPs toxicity in rice (Wang et al. 2015; Ji et al. 2017) and induce more severe effects on the behavior of the increasing wheat tolerance to water deficit (Jaberza- terrestrial organisms than TiSiO NPs, supporting deh et al. 2013). Germination may not be affected the safe nature of these NPs. The lettuce market is or even be stimulated by TiO NPs up to 750 mg/kg huge being one of the most important leafy vegeta- (Yang et al. 2015; Andersen et al. 2016; Maity et al. ble worldwide (Shatilov et al. 2019). Thus, is im- (2018). SiO NPs have been presented as a stimula- portant to find strategies to improve the production tor of yield and plant performance under unfavour- of this crop. able environment conditions, such as drought in the On other hand, TiSiO NPs are photocatalyst par- cotton plants (Behboudi et al. 2018). ticles, and some NPs also with this characteristic, Positive impacts in photosynthesis have been re- such as TiO , have been demonstrated at moderate ported to TiO NPs and SiO NPs such as promoting 2 2 2 doses to increase the photosynthetic performance, electron transfer (Lei et al. 2007), increased transpi- plant productivity, and quality (Shabbir et al. 2019; ration rate (E), an increase of the net photosynthetic Gohari et al. 2020; Tighe-Neira et al. 2020). Also, rate (Pn), stomatal conductance (gs) (Ashkavand their antimicrobial activity opens perspectives for et al. 2018). However, it should be noted that most crop protection as suggested by Rodríguez-González studies on TiO NPs and SiO NPs bioactivity/phyto- 2 2 et al. (2019). Between the titanium oxide NPs (TiO toxicity are performed during short periods. Studies and TiSiO ), TiO NPs are vastly more studied in using chronical exposure, whilst scarce, are much 4 2 terms of plant response, using physiological and closer to real scenarios (Karunakaran et al. 2017; biochemical approaches (El-Ramady et al. 2018; Silva et al. 2017a). Additionally, besides the species Ghosh et al. 2019; Silva et al. 2016; 2017a,b, 2019, model, factors such as NPs size, shape, the presence Dias et al. 2019). Among the NPs with agricultural and type of surface-coating, and NPs concentration potential, those of TiO are increasingly being used vary greatly among studies, it can result in conflict - (Siddiqui et al. 2015; Duhan et al. 2017). The poten- ing reports of their bioactivity (Cox et al. 2016; tial usefulness of TiO NPs in nanoagriculture may Silva et al. 2016; 2017b). Finally, phytotoxicity of rely on their multiple functionalities, which include: high doses, particularly of the TiO NPs, is being a) antimicrobial activity (critical during germination unveiled by our and other groups, with description and seedlings’ first days) with the potential to man- for example of the reduction of root growth, among age plant diseases (Soni & Prakash 2012; Sekhon other effects (Andersen et al. 2016; Cox et al. 2016; 2014; Duhan et al. 2017); b) stimulation of plant Karunakaran et al. 2017; Silva et al. 2016, 2017a,b, growth under certain doses (Jaberzadeh et al. 2013; 2019). Siddiqui et al. 2015). Likewise, SiO (another com- Considering the complex data of the other NPs, ponent of the ternary system of TiSiO NPs) has it is critical to increase the available information on been reported to promote biofortification in plants, TiSiO NPs bioactivity on plant growth and yield, to to be responsible for promoting the strengthening of elucidate their potential for nanoagriculture. This in- 149 Agriculture (Poľnohospodárstvo), 66, 2020 (4): 148 − 160 formation is crucial to evaluate if and how these NPs weeks, plant growth and biomass were determined by assessing shoot and root length, and fresh (FM) interact with crops’ performance, their entrance into and dry (DM) matters. Morphological data were the food chain, and if they can replace/complement registered (senescence, chlorosis, necrotic spots, TiO NPs, SiO NPs, or both in nanoagroindustry. 2 2 and abscission). Here, we hypothesise that TiSiO NPs may re- tain some beneficial properties and effects of the Photosynthetic analyses TiO NPs and SiO NPs on crops, and thus may 2 2 L. sativa leaves in the rosette stage (first rosette combine little or none toxicity with stimulation of leaves) grown at 0, 50, and 100 mg/L were used in growth and crop’s performance, namely at the pho- photosynthetic assays. For pigments determination, tosynthetic level. To test this hypothesis, lettuce leaves were homogenized in acetone: 50 mM Tris plants (a major dicotyledonous model crop) were buffer (80:20) (pH ≈7.8) (Sims & Gamon 2002). exposed to two different doses of TiSiO NPs for Chlorophyll a (Chl a), chlorophyll b (Chl b), carot- three weeks, after which several photosynthesis-re- enoids, and anthocyanins were quantified at 470, lated endpoints (leaf gas exchange, chlorophyll a 537, 647, and 663 nm. fluorescence, ribulose-1,5-bisphosphate carboxy- The basal fluorescence yield of dark-adapted lase/oxygenase ‒ RuBisCO amount, pigments and samples (F ), the maximal fluorescence yield (F ), 0 m carbohydrates contents) were quantified. and the variable fluorescence (F =F ‒ F ) were mea- v m 0 sured with the respective light conditions. The pa- rameters F ’, F ’, and F ’ were also assessed in 30 0 m v MATERIAL AND METHODS min illuminated leaves. F / F and F ’/ F ’, and the v m v m effective photochemical efficiency of PSII (Φ ), PSII Nanoparticles stocks, characterization, and prepa- photochemical quenching (q ), and electron trans- ration of solutions port rate (ETR) were determined (Maxwell & John- TiSiO NPs (>99.8% purity) were purchased son 2000). from Sigma-Aldrich (St. Louis, MO-USA) having, For leaf gas exchange analysis, the infra-red gas according to the supplier, a primary size <50nm. analyser (LCpro+, ADC, Hoddesdon, UK), operat- TiSiO NPs dynamic light scattering (DLS) and zeta ing in open mode, was used. Measurements took potential were characterized according to our cur- place under atmospheric CO concentration with rent techniques (Bastos et al. 2017). A stock suspen- a saturating photosynthetic photon flux density of sion of 1.0 g/L TiSiO NPs (in distilled water) was 600 µmol m /s. Transpiration rate (E, mmol (H O) used for the preparation of final nutrient solutions 2 2 m /s), stomatal conductance (g , mmol (H O) m /s), s 2 (Hoagland basal salt mixture, Sigma-Aldrich, USA) net photosynthetic rate (Pn, µmol (CO ) m /s) and with concentrations up to 100 mg/L. All suspensions the ratio of intercellular CO concentration to ambi- were sonicated for ≈20 min prior to use. ent CO ( C /C ) were determined (Rodriguez et al. 2 i a 2015). Seed germination and exposure to TiSiO NPs Seeds of L. sativa cv. ‘Maravilha de Verão Ca- Carbohydrates quantification nasta’ (Vilmorin Jadin, France) were germinated in Total soluble sugars (TSS) and starch contents Petri dishes (100 seeds/petri dish), each with 10 mL (mg/g FM) were quantified by the anthrone method of nutrient solution with different TiSiO NPs con- (Osaki et al. 1991; Irigoyen et al. 1992). centrations: 0, 50, and 100 mg/L. Germination took RuBisCO quantification place at 16 h light period (Photosynthetically active Soluble proteins extracted from the first rosette radiation − PAR ≈100 µmol/m / s), 20 ± 2ºC, ≈50% leaves were quantified by the Bradford method (Sig- relative humidity (%RH). One-week-old seedlings ma-Aldrich, USA). For RuBisCO analysis, 15 µg of were hydroponically grown on the corresponding protein were separated by SDS-PAGE, using pro- media at PAR ≈200 µmol/m /s, 16 h light periods, tein molecular weight marker (Fermentas SM0441, 22 ± 2ºC, ≈45% RH. All media were renewed every ThermoFisher, USA) as a reference, and bands were 3 days, and pH was kept constant at ≈5.6. After 3 150 Agriculture (Poľnohospodárstvo), 66, 2020 (4): 148 −160 stained with 0.25% Coomassie Brilliant Blue R250 aggregates confirming previous data, and according (Li et al. 2013). Relative RuBisCO quantification to the DLS data, their hydrodynamic diameter was of large and small subunits was done after over- 2 to 3 times larger than the primary particle size, night incubation in 2 mL formamide at 50ºC, read- reaching average sizes of 115 ± 29 nm. ing absorbance at 595 nm. Results are expressed as Seeds in all concentrations reached a germina- ABS /ABS tion rate of >99%, supporting no negative effects of Rubisco content Protein content. these NPs on this crop’s germination. Whilst root Statistical analysis length and fresh matter (FM) of exposed plants were Experiments used 6 ‒ 8 plant samples (treated in- not affected compared to unexposed roots, both dividually or as leaf pools), and 3 independent tech- shoot length and, mainly shoots’ FM, were in gen- nical replicates. Comparisons between the different eral stimulated by TiSiO NPs compared to control conditions were made using the One-Way ANOVA plants (Table 1). test, using GraphPad Prism 6 (GraphPad Software, San Diego, California, USA). For different condi- Photosynthetic pigments content and fluorescence tions, the Tukey Comparison Test (p < 0.05) was The average values of Chl a and b contents were used. Multivariate analyses for data correlation used stimulated by TiSiO NPs (Figure 1a, b) with max- Principal component analysis (PCA) and were per- imum values being achieved at 50 mg/L (p < 0.05). formed with CANOCO 5 (WUR, Netherland). The ratio Chl a / Chl b was increased (p < 0.05) by both TiSiO NPs doses (Figure 1c). Carotenoids’ levels were not changed by TiSiO NPs (Figure 1d). RESULTS Finally, the anthocyanin levels were significantly in- creased at 50 mg/L TiSiO NPs (Figure 1e). Nanoparticles characterization and effect on germi- Basal chlorophyll fluorescence of dark-adapt - nation and plant growth ed leaves (F ) was slightly decreased (p < 0.05) by Taking into account the size of TiSiO NPs (<50 100 mg/L TiSiO NPs (Figure 2a). Maximum fluores- nm in aqueous suspensions), these NPs tend to form cence (F ) and variable fluorescence (Figure 2b, c) TiSiO concentrations [mg/L] TiSiO concentrations [mg/L] TiSiO concentrations [mg/L] 4 4 4 TiSiO concentrations [mg/L] TiSiO concentrations [mg/L] 4 4 Figure 1. Pigment contents (mg/kg (FM)) in plants exposed to TiSiO NPs. a) chlorophyll a; b) chlorophyll b ; c) ratio Chl a / Chl b; d) Carotenoids; e) Anthocyanins; FM − Fresh Matter. All conditions were compared by Tukey multi comparison test using one-way ANOVA for p < 0.05. mg/kg (FM) mg/kg (FM) mg/kg (FM) Agriculture (Poľnohospodárstvo), 66, 2020 (4): 148 − 160 were not compromised (p > 0.05) in exposed plants, 100 mg/L compared to 50 mg/L (Figure 2f). For the but the increase of F / F ratio at 100 mg/L was sig- photosystem efficiency, Φ was affected by TiSiO v m PSII 4 nificant compared to 50 mg/L condition (p < 0.05; NPs doses also with increases at 100 mg/L com- Figure 2d). Regarding the light-adapted state, F’ / F’ pared to 50 mg/L (Figure 2e). The q parameter was v m P ratio was affected increasing substantially at not affected by any NPs dose (Figure 2g). Lastly, T a b l e 1 Growth parameters of lettuce roots and shoots exposed to TiSiO NPs Plant area evaluated Control 50 mg/L 100 mg/L Root Length [cm] 12.83 ± 2.15 11.170 ± 1.56 12.46 ± 1.95 Shoot Length [cm] 9.94 ± 2.18 12.826 ± 2.30 10.44 ± 2.42 Root Fresh Matter [g] 8.49 ± 2.43 10.680 ± 3.52 10.62 ± 2.10 Shoot Fresh Matter [g] 11.22 ± 1.57 14.030 ± 1.33* 19.53 ± 2.54* For the same condition and organ *means significantly different values (p < 0.05) in comparison with the control. TiSiO concentrations [mg/L] TiSiO concentrations [mg/L] TiSiO concentrations [mg/L] 4 4 4 TiSiO concentrations [mg/L] TiSiO concentrations [mg/L] TiSiO concentrations [mg/L] 4 4 4 TiSiO concentrations [mg/L] TiSiO concentrations [mg/L] 4 4 Figure 2. Fluorescence data (AU − arbitrary units) of plants exposed to TiSiO NPs. a) F − minimal fluorescence of dark- 4 0 adapted leaves; b) F − variable fluorescence of dark-adapted leaves; c) F − maximum fluorescence of dark-adapted leaves; v m d) F / F − maximum quantum yield; e) Φ − effective quantum yield; f) F ’/ F ’ − maximum quantum yield in light-adapted v m PSII v m condition; g) q − photochemical quenching; h) ETR − electron transport rate. All conditions were compared by Tukey multi comparison test using one-way ANOVA for p < 0.05. 152 Agriculture (Poľnohospodárstvo), 66, 2020 (4): 148 −160 ETR was stimulated (p < 0.05) by 100 mg/L dose of CO by L. sativa plants. Significant differences compared to 50 mg/L (Figure 2h). between each condition for all parameters (Figure 3a-e) were not found. Also, the parameters related Gas exchange, RuBisCO, and carbohydrate levels to carbon assimilation, such as RuBisCO, TSS, and Leaf gas exchange parameters showed that the starch contents were not significantly affected by the use of TiSiO NPs did not affect the potential use TiSiO NPs doses used (Figure 4a-c). TiSiO concentrations [mg/L] TiSiO concentrations [mg/L] TiSiO concentrations [mg/L] 4 4 4 TiSiO concentrations [mg/L] TiSiO concentrations [mg/L] 4 4 Figure 3. Leaf gas-exchange in plants exposed to TiSiO NPs. a) E (mmol (H O) m /s) − transpiration rate; b) gs − stomatal 4 2 conductance; c) Pn (µmol (CO ) m /s) − net photosynthetic rate; d) Pn/gs ratio – Pn /gs − CO assimilation efficiency; 2 2 e) C / C − intercellular CO ratio. i a 2 All conditions were compared by Tukey multi comparison test using one-way ANOVA for p < 0.05. TiSiO concentrations [mg/L] TiSiO concentrations [mg/L] TiSiO concentrations [mg/L] 4 4 4 Figure 4. Relative RuBisCO content, starch, and total soluble sugars in plants exposed to TiSiO NPs. a) RuBisCO (ABS / ABS ); b) TSS (mg/g (FM)); c) Starch (mg/g (FM)); FM − Fresh Matter. RC TPC All conditions were compared by Tukey multi comparison test using one-way ANOVA for p < 0.05. mmol (H O) m /s ABS /ABS RC TPC 2 mmol (H O) m /s mg/kg (FM) mg/kg (FM) µmol (CO ) m /s 2 Agriculture (Poľnohospodárstvo), 66, 2020 (4): 148 − 160 beneficial effects with minimal toxicity. However, the characterization of the TiSiO NPs bioactivity in plants remains scarcely addressed. Moreover, most of the studies performed up to the moment with NPs used short term exposures, while agricultural pur- poses demand long term-exposure studies. Ti is well known to be an element that when found in soils and waters used for plant growth, it en- hances not only the plants’ photosynthesis, but also their chlorophyll content, which promotes nutrient uptake, better stress tolerance, and improves crop yield and quality, making this a beneficial element (Lyu et al. 2017). On the other hand, the beneficial effects of silicon to plants are widely demonstrated (Murad et al. 2020) and its oxidised form (SiO NPs) promoted plant protection against biotic and abiotic Figure 5. Principal component analysis (PCA) of functional stress (Luyckx et al. 2017). Our work contains the responses of plants exposed to TiSiO NPs first results addressing TiSiO NPs photosynthetic bioactivity in plants, and we demonstrate that, after PCA (Figure 5) shows a distinct separation be- short-term exposure, moderate doses of TiSiO NPs tween all conditions used in physiological studies might stimulate lettuce growth, and may positively (0, 50, and 100 mg/L). PC1 (F1) explains 61.9% of influence, in yet to unveil mechanisms, photosyn- the variance, while PC2 (F2) explains 39.1%. The thetic parameters, such as the increase of photosyn- control population is located on the down-right thetic pigments at lower doses (50 mg/L) and gas quadrant, and this parameter is the only located in exchange and PSII efficiency at higher doses (100 the down-side of the Y-axis, associated with TSS mg/L). and some fluorescence parameters (F and F ). On Recently we have demonstrated for Triticum aes- v m the other hand, 50 mg/L is in the top-left quadrant tivum that chronical exposure to TiO NPs influences and has positive scores for all photosynthetic pig- photosynthesis, and for example, 150 mg/L TiO NPs ments and g parameter. Regarding yield parame- had phytotoxic effects (stimulating oxidative stress ters of photosynthesis, such as Φ , F / F , F’ / F’ , and water disorders), which impaired plant growth, PSII v m v m ETR, Pn / g , RuBisCO, and starch contents, these being toxicity more severe in shoots than in roots are clusters on the top-right quadrant, corresponding (Silva et al. 2017a; 2019). Using fresh and dry mat- to the 100 mg/L samples. ter as growth indicators, and soils contaminated with extremely high doses (1,000 mg/kg soil ), DM Bouguerra et al. (2016) reported TiSiO NPs phy- DISCUSSION totoxicity in lettuce and tomato plants. Comparing the available literature for TiO NPs with our current TiO and SiO NPs bioactivity in plants are cur- data for TiSiO NPs, there is evidence of lower tox- 2 2 rently under debate to support their potential use icity of TiSiO NPs, but further comparative studies in nanoagriculture (Srivastava et al. 2015). Whilst under similar conditions must be conducted. most studies are focused on TiO showing antibiotic We demonstrate here that the interference of activity and at some limited doses a stimulation of TiSiO NPs with photosynthesis is complex and growth (but also toxicity at higher doses), SiO is related to the dose, but overall a neutral or slight mostly pinpointed as a potential source of release of stimulation is found. Photophosphorylation is the Si with demonstrated benefits to plant growth, and source of ATP and NADPH + H for the Calvin cy- thus with potential as a nano fertiliser. The combi- cle to proceed, and its status here was evaluated ac- nation of Ti and Si may thus combine some of the cording to changes in the chlorophyll quantity/ratio 154 Agriculture (Poľnohospodárstvo), 66, 2020 (4): 148 −160 for 50 mg/L TiSiO NPs compared to control plants. 50 mg/L can promote a positive effect in photosyn- It was evident that 50 mg/L TiSiO NPs stimulated thesis performance and the 100 mg/L concentration chlorophylls and anthocyanins contents (by increas- may not be the maximum endpoint of high photo- ing synthesis or preventing damage) which, besides synthetic performance for L. sativa. photosynthesis, also have protective roles. The ob- Interestingly, the PCA analyses confirm a horme- served increase of Chl levels has been described in sis response in some parameters, shown by a negative response to TiO NPs, often paralleled with an in- correlation between 50 mg/L and the dark-adapted crease of N uptake, but the targets of these NPs in parameters of F , F , F / F , and F’ /F’ , while 100 m v v m v m the plant metabolism remain unknown (Lyu et al. mg/L had a similar negative correlation with F . A 2017). Kheyrkhah et al. (2018) showed that SiO higher F can be interpreted as indicating irrevers- 2 0 and TiO increased the chlorophylls and carotenoids ible damage to PSII (Bussotti et al. 2011), therefore content in oilseed rape cultivars. Also, Aliabadi et the decrease of F in exposed leaves may indicate al. (2015) showed that 100 mg/L TiO NPs increased a protective role exerted by these NPs on the PSII, the Chl a content and the ratio (Chl a / Chl b) in decreasing the uncontrolled dissipation of heat. This T. aestivum. However, the same study also showed hypothesis is also supported by the F / F ratio, v m that using 20 times more concentration (2,000 which gives information on the maximum quantum mg/L) reduced Chl content and its ratio. This study, efficiency of the PSII photochemistry. In TiSiO in parallel with our data, demonstrates that moder- NPs exposed plants, this ratio remains around the ate doses are capable to increase the photosynthetic 0.79 ‒ 0.84 values, which is an indicator of healthy potential, however, the species factor should be con- plants (Maxwell & Johnson 2000) and indicates sidered. These rises may increase the efficiency of a balance between reduction of plastoquinone Q CO assimilation (Yang et al. 2006; Sanshez-Zabala and its reoxidation by Q . This ratio is widely used 2 B et al. 2015; Lyu et al. 2017). Ti oxides NPs may as a sensitive endpoint for several stress-related pho- also exert a protective role of photostability of chlo- tosynthetic disorders. For example, its disturbance rophylls, similarly to what was reported for silver was reported in some species exposed to TiO NPs nanoparticles (AgNPs) that slowed down the photo- like T. aestivum (Dias et al. 2019). Also, in Chlorella degradation of Chl a (Barazzouk et al. 2012). Thus, pyrenoidosa, the inhibition of the photosynthetic ac- the increase of chlorophylls by TiSiO NPs suggests tivity was attributed to the damage of the reaction either increased synthesis or an improved photosta- center of PSII (Middepogu et al. 2018). bility of the pigments. This increase of pigments will Whilst the decrease of F / F may indicate some v m improve the capacity for harvesting photons to fos- slowly relaxing quenching processes and photodam- ter the photophosphorylation process. The protec- age to PSII reaction centres, reducing the maximum tive role of these pigments against photooxidation quantum efficiency of PSII photochemistry (Baker should also not be excluded. On the other hand, the & Rosenqvist 2004), its increase – as observed in absence of changes in fluorescence parameters and TiSiO NPs exposed plants – suggests increased gas exchange compared to control were a positive protection to chlorophyll photoinhibition. This pro- indicator that the doses tested are not a toxic con- tective role is also in accordance with the increase centration of this compound for L. sativa growing in of chlorophyll levels in TiSiO NPs exposed plants’ hydroponic systems, using the photosynthesis and leaves. Regarding light-adapted parameters, F ’/ F ’ v m carbon metabolism as control endpoints. Neverthe- was positively correlated with the 100 mg/L, mean- less, the use of TiO NPs in another crop, such as So- ing an increased capture efficiency of excitation lanum lycopersicum, was capable to promote an in- energy by open PSII reaction centres in this NP crease in photosynthetic parameters (Qi et al. 2013). concentration (Lima et al. 2002). Thus, we suggest Besides, our data showed a particularity on the that these NPs, directly or indirectly, stimulated the 100 mg/L conditions, as increases occurred in some chlorophyll protection against photodamage (Wang photosynthetic parameters (F / F , Φ , F’ / F’ , et al. 2016), and/or increased chlorophyll synthe- v m PSII v m and ETR) compared to 50 mg/L. These results sis to compensate for alleged increased damages as suggest that an increase of TiSiO NPs relative to suggested by Middepogu et al. (2018). It should be 155 Agriculture (Poľnohospodárstvo), 66, 2020 (4): 148 −160 stressed/highlighted that this protective role may However, TiO NPs had a different effect on gly- have slightly increased the efficiency of the photo- cometabolism, as it decreased the levels of starch in phosphorylation process, which may lead to an in- T. aestivum, putatively as a mechanism to maintain crease in the amount of ATP and NADPH available the soluble sugars levels (Dias et al. 2019). Also, to be used in Calvin Cycle. changes in carbohydrates after exposure to TiO NPs Data related to the gas exchange parameters did were reported in cucumber fruits (Servin et al. not show any responsive effect with the studied 2013). Contrarily, despite negative effects on chlo- TiSiO NPs doses to L. sativa. However, the multi- rophyll, TiO NPs increased total sugar and reduced 4 2 variance analysis showed that g had a positive cor- sugar in basil exposed to TiO NPs (Tan et al. 2018). s 2 relation with 50 mg/L and a Pn with opposite cor- Those authors suggested that TiO NPs led to the relation for control plants and associated positively transfer of an active electron which might disrupt for 50 and 100 mg/L (Figure 5). A potential increase enzyme activities related to glycometabolism, like of Pn can be associated with the increase of CO those as β-amylases (Thalmann & Santelia 2017), supply from outside to the intercellular airspaces of supporting the associated increase of sugar levels leaves (Dias et al. 2019). However, the non-signif- (Tan et al. 2018). Moreover, in TiSiO NPs exposed icant changes in Pn do not follow the increase of plants, while starch content showed some PCA-cor- Chl, nevertheless, the increase of Chl is not always relation with Pn and RuBisCO content, it showed an accompanied by Pn increase (Da-yong et al. 2012). opposite correlation to these parameters in control This is controlled by the stomatal function and the plants, supporting a trend to increase with these NPs CO diffusion from intercellular airspaces towards (Figure 5), however, this concentration did not show the carboxylation sites. These NPs do not interfere significant differences. Our results demonstrate that with the accumulation of CO inside the mesophyll TiSiO NPs doses up to 100 mg/L did not affect the 2 4 intercellular space, which suggests a proper function plant glycometabolism, while the positive correla- of RuBisCO and even a putative stimulation of its tion of some parameters such as Pn and RuBisCO transcription, despite its relative amount not being for 100 mg/L showed that maybe the endpoints changed. Different results with high concentrations were not detected, and other upper doses could have of TiO NPs were reported, namely the TiO NPs con- a positive effect for L. sativa. 2 2 centration of 1,000 mg/L, which decreased CO fix- Mainly, some differences between the reported ation, transpiration rate, and stomatal conductance effects of TiO and TiSiO NPs perhaps occurred by 2 4 (Da Costa & Sharma 2015). Also, we have recent- the presence of Si element. Once this mineral is re- ly demonstrated that TiO NPs (anatase: rutile) are lated with plant recovery for abiotic stress (Etesami chronically applied to T. aestivum, decreased max- & Jeong 2018) and is involved in photoprotection imal and effective efficiency of PSII, net photosyn- processes (Li et al. 2018), including the photosyn- thetic rate, transpiration rate, stomatal conductance, thetic stimulation by the increase of the chlorophyll intercellular CO concentration, and starch content levels (Sarma et al. 2018), such as in L. sativa ex- (Dias et al. 2019). On the other hand, the application posed to TiSiO NPs. of SiO NPs improves the gas exchange performance in Passiflora edulis with an increase of Pn, E, and gs (Costa et al. 2018). Overall, our data suggest that CONCLUSIONS low doses of TiSiO NPs play some protective role in photosystem II, not having the negative impacts In conclusion, this is one of the first approaches of TiO NPs. regarding the bioactivity of the understudied TiSiO 2 4 The protective role of TiSiO NPs on the pho- NPs, and it demonstrates that TiSiO NPs stimulate 4 4 tosynthetic apparatus and the stimulation of RuBis- plant growth, and different doses may promote pho- CO subunits show stimulation of photosynthesis, tosynthetic apparatus and performance in different supporting the observed plant growth increase. The ways, namely lower doses may stimulate chloro- TSS and starch levels are in line with all photosyn- phyll levels, while higher doses show a stimulato- thetic mechanisms under the effect of TiSiO NPs. ry trend to stimulate photosynthetic performance. 156 Agriculture (Poľnohospodárstvo), 66, 2020 (4): 148 −160 53, no. 2, pp. 207 ‒ 219. DOI: 10.31055/1851.2372.v53. The tested doses did not have a negative effect on n2.20578. the net photosynthetic rate, nor influenced RuBis- BAKER, N. ‒ ROSENQVIST, E. 2004. Applications of chloro- CO subunit amount. Being the first study on the phyll fluorescence can improve crop production strategies: an examination of future possibilities. In Journal of Ex- biochemical effects of TiSiO NPs this study also perimental Botany, vol. 55, no. 403, pp. 1607 – 1621. DOI: shows the need to better understand how manufac- 10.1093/jxb/erh196. BARAZZOUK, S. ‒ BEKALÉ, L. ‒ HOTCHANDANI, S. tures nanoparticles interfere in crop performance 2012. Enhanced photostability of chlorophyll-a using gold and identify safety and realistic doses. nanoparticlesas an efficient photoprotector. In Journal of Material Chemistry, no. 22, pp. 25316 ‒ 25324. DOI: 10.1039/C2JM33681B. Acknowledgements. Work supported by FED- BASTOS, V. ‒ DE OLIVEIRA, J.F. ‒ BROWN, D. ‒ ER/COMPETE [POCI/01/0145/FEDER/007265 JONHSTON, H. ‒ MALHEIRO, E. ‒ DANIEL-DA-SIL- VA, A.L. ‒ DUARTE, I.F. ‒ SANTOS, C. ‒ OLIVEIRA, and FCT/MEC PT2020 UID/QUI/50006/2013]; H. 2016. The influence of Citrate or PEG coating on silver FCT funded N. Mariz-Ponte, S. Sario, and R.J. nanoparticle toxicity to a human keratinocyte cell line. In Mendes, fellowships [SFRH/BD/138187/2018, Toxicology Letters, vol. 249, pp. 29 ‒ 41. DOI: 10.1016/j. toxlet.2016.03.005. SFRH/BD/138186/2018, SFRH/BD/133519/2017]; BEHBOUDI, F. ‒ SARVESTANI, Z.T. ‒ KASSAEE, M.Z. ‒ Also supported by National Funds by FCT - Portu- MODARES, S.A.M. 2018. Improving growth and yield of wheat under drought stress via application of SiO nanopar- guese Foundation for Science and Technology, un- ticles. In Journal of Agricultural Science and Technology, der the project UID/AGR/04033/2019. vol. 20, no. 7, pp. 1479 ‒ 1492. 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Silicon Titanium Oxide Nanoparticles Can Stimulate Plant Growth and the Photosynthetic Pigments on Lettuce Crop

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10.2478/agri-2020-0014
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Abstract

Agriculture (Poľnohospodárstvo), 66, 2020 (4): 148 − 160 DOI: 10.2478/agri-2020-0014 Original paper SILICON TITANIUM OXIDE NANOPARTICLES CAN STIMULATE PLANT GROWTH AND THE PHOTOSYNTHETIC PIGMENTS ON LETTUCE CROP 1 1 1 1 NUNO MARIZ-PONTE *, SARA SARIO , RAFAEL J. MENDES , CRISTIANA V. CORREIA , 2 2 1 JOSÉ MOUTINHO-PEREIRA , CARLOS M. CORREIA , CONCEIÇÃO SANTOS University of Porto, Porto, Portugal University of Trás-os-Montes e Alto Douro, Portugal MARIZ-PONTE, N. – SARIO, S. − MENDES, R.J − CORREIA, C.V. − MOUNTINHO-PEREIRA, J. − CORREIA, C.M. − SANTOS, C.: Silicon titanium oxide nanoparticles can stimulate plant growth and the photosynthetic pigments on lettuce crop. Agriculture (Poľnohospodárstvo), vol. 66, no. 4, pp. 148 – 160. Our knowledge of the bioactivity of silicon titanium oxide nanoparticles (TiSiO NPs) in crops is scarce, contrarily to TiO NPs and SiO NPs that are used in many industrial sectors, and have emerged in nanoagriculture (e.g., as pesticides or 2 2 nanofertilisers). To evaluate the potential of using TiSiO NPs in nanoagriculture, it is necessary to characterize their potential benefits on crops and the safety doses. Here, we report for the first time the bioactivity of TiSiO NPs (up to 100 mg/L) in the model crop lettuce (Lactuca sativa L.) exposed for three weeks (from seeds/seedlings to pre-harvesting phase). The doses applied did not compromise the germination rate, and highly stimulated plant fresh matter. TiSiO NPs had beneficial effects on photochemical processes by increasing chlorophyll levels. Effects on photosynthesis are less evident but TiSiO NPs (100 mg/L) stimulated the photosynthetic potential, increasing F /F and ETR when compared to the 50 mg/L conditions. v m TiSiO NPs did not influence the net photosynthetic rate and other Calvin-cycle variables. Soluble sugars and starch levels were overall maintained. In general, this first report on TiSiO NPs bioactivity suggests that they did not have a toxic effect, and may be used to potentiate crops’ growth. Principal component analysis (PCA) also shows that despite effects on photosynthetic performance is minimal regarding the control, the 50 and 100 mg/L doses strongly differ, with the lower dose promoting mostly pigment accumulation, while the higher dose slightly stimulates Photosystem II efficiency including the electron transport rate and other gas exchange parameters. Key words: gas exchange, nanoagriculture, nanofertilisers, photosynthesis, TiSiO Nanotechnologies are increasingly providing between titanium oxide (TiO ) and silicon oxide new and promising manufactured nanomaterials, (SiO ) mixture that forms an orthorhombic struc- including nanoparticles, to the agricultural sector ture, being increasingly used in multiple industries, (Parisi et al. 2015). The first data regarding the use particularly in the electronics sector (Garcia et al. of titanium in plant production was obtained at the 2009), ceramics (Varghese et al. 2011), optical in- beginning of the last century and has become an im- struments (Liu et al. 2017) and lubricant oils (Taheri portant field in plant nutrition (Kováčik et al. 2014). et al. 2018). Despite their industrial potential, and Silicon titanium oxide (TiSiO ) is a ternary system unlike other metal nanoparticles, TiSiO NPs remain 4 4 Nuno Mariz-Ponte (*Corresponding author), Sara Sario, Rafael J. Mendes, Cristiana V. Correia, Conceição Santos, LAQV-REQUIMTE, Department of Biology, Faculty of Sciences, University of Porto, Rua do Campo Alegre 4169-007, Porto, Portugal. E-mail: nuno.ponte@fc.up.pt José Moutinho-Pereira, Carlos M. Correia, Department of Biology and Environment, Centre for the Research and Technology of Agro-Environmental and Biological Sciences (CITAB), University of Trás-os-Montes e Alto Douro, 5001-801 Vila Real, Portugal © 2020 Authors. This is an open access article licensed under the Creative Commons Attribution-NonComercial-NoDerivs License (http://creativecommons.org/licenses/by-nc-nd/4.0/). 148 Agriculture (Poľnohospodárstvo), 66, 2020 (4): 148 − 160 unexplored in the nano-agroindustrial sector. Their the cell walls (Guerreiro et al. 2016), has a mitiga- antimicrobial activity was shown on Vibrio fischeri tion role under abiotic stress (Behboudi et al. 2018), and Salmonella typhimurium (Pereira et al. 2011; Ro- and is also increasingly being used on agricultural dríguez-González et al. 2019). Also, using different applications (Jampílek & Kráľová 2017; Luyckx et concentrations up to 1,000 mg/kg soil or 1,000 mg/L al. 2017). (of aqueous suspensions), other authors as Bou- As TiSiO NPs impacts on plants remain un- guerra et al. (2016) observed that E. andrei only known, we hypothesise that these NPs may combine avoided the soils spiked with 1,000 mg/kg TiSiO the positive effects of the TiO and SiO NPs. Under 4 2 2 NPs. Despite still unknown, TiSiO NPs may be safe moderate doses, TiO NPs were reported to stimulate 4 2 at low doses to plants as no negative effects were plant biomass and positively regulate N metabolism found on corn and oat seedlings growth, and only (Yang et al. 2006). Recent data also pinpointed that small decreases of dry mass and fresh mass were ob- TiO NPs were able to modulate plants’ response to served on lettuce and tomato seedlings (Bouguerra other stressors, lowering the Cu(II) and Cd phyto- et al. 2016). Some authors suggested that AgNPs toxicity in rice (Wang et al. 2015; Ji et al. 2017) and induce more severe effects on the behavior of the increasing wheat tolerance to water deficit (Jaberza- terrestrial organisms than TiSiO NPs, supporting deh et al. 2013). Germination may not be affected the safe nature of these NPs. The lettuce market is or even be stimulated by TiO NPs up to 750 mg/kg huge being one of the most important leafy vegeta- (Yang et al. 2015; Andersen et al. 2016; Maity et al. ble worldwide (Shatilov et al. 2019). Thus, is im- (2018). SiO NPs have been presented as a stimula- portant to find strategies to improve the production tor of yield and plant performance under unfavour- of this crop. able environment conditions, such as drought in the On other hand, TiSiO NPs are photocatalyst par- cotton plants (Behboudi et al. 2018). ticles, and some NPs also with this characteristic, Positive impacts in photosynthesis have been re- such as TiO , have been demonstrated at moderate ported to TiO NPs and SiO NPs such as promoting 2 2 2 doses to increase the photosynthetic performance, electron transfer (Lei et al. 2007), increased transpi- plant productivity, and quality (Shabbir et al. 2019; ration rate (E), an increase of the net photosynthetic Gohari et al. 2020; Tighe-Neira et al. 2020). Also, rate (Pn), stomatal conductance (gs) (Ashkavand their antimicrobial activity opens perspectives for et al. 2018). However, it should be noted that most crop protection as suggested by Rodríguez-González studies on TiO NPs and SiO NPs bioactivity/phyto- 2 2 et al. (2019). Between the titanium oxide NPs (TiO toxicity are performed during short periods. Studies and TiSiO ), TiO NPs are vastly more studied in using chronical exposure, whilst scarce, are much 4 2 terms of plant response, using physiological and closer to real scenarios (Karunakaran et al. 2017; biochemical approaches (El-Ramady et al. 2018; Silva et al. 2017a). Additionally, besides the species Ghosh et al. 2019; Silva et al. 2016; 2017a,b, 2019, model, factors such as NPs size, shape, the presence Dias et al. 2019). Among the NPs with agricultural and type of surface-coating, and NPs concentration potential, those of TiO are increasingly being used vary greatly among studies, it can result in conflict - (Siddiqui et al. 2015; Duhan et al. 2017). The poten- ing reports of their bioactivity (Cox et al. 2016; tial usefulness of TiO NPs in nanoagriculture may Silva et al. 2016; 2017b). Finally, phytotoxicity of rely on their multiple functionalities, which include: high doses, particularly of the TiO NPs, is being a) antimicrobial activity (critical during germination unveiled by our and other groups, with description and seedlings’ first days) with the potential to man- for example of the reduction of root growth, among age plant diseases (Soni & Prakash 2012; Sekhon other effects (Andersen et al. 2016; Cox et al. 2016; 2014; Duhan et al. 2017); b) stimulation of plant Karunakaran et al. 2017; Silva et al. 2016, 2017a,b, growth under certain doses (Jaberzadeh et al. 2013; 2019). Siddiqui et al. 2015). Likewise, SiO (another com- Considering the complex data of the other NPs, ponent of the ternary system of TiSiO NPs) has it is critical to increase the available information on been reported to promote biofortification in plants, TiSiO NPs bioactivity on plant growth and yield, to to be responsible for promoting the strengthening of elucidate their potential for nanoagriculture. This in- 149 Agriculture (Poľnohospodárstvo), 66, 2020 (4): 148 − 160 formation is crucial to evaluate if and how these NPs weeks, plant growth and biomass were determined by assessing shoot and root length, and fresh (FM) interact with crops’ performance, their entrance into and dry (DM) matters. Morphological data were the food chain, and if they can replace/complement registered (senescence, chlorosis, necrotic spots, TiO NPs, SiO NPs, or both in nanoagroindustry. 2 2 and abscission). Here, we hypothesise that TiSiO NPs may re- tain some beneficial properties and effects of the Photosynthetic analyses TiO NPs and SiO NPs on crops, and thus may 2 2 L. sativa leaves in the rosette stage (first rosette combine little or none toxicity with stimulation of leaves) grown at 0, 50, and 100 mg/L were used in growth and crop’s performance, namely at the pho- photosynthetic assays. For pigments determination, tosynthetic level. To test this hypothesis, lettuce leaves were homogenized in acetone: 50 mM Tris plants (a major dicotyledonous model crop) were buffer (80:20) (pH ≈7.8) (Sims & Gamon 2002). exposed to two different doses of TiSiO NPs for Chlorophyll a (Chl a), chlorophyll b (Chl b), carot- three weeks, after which several photosynthesis-re- enoids, and anthocyanins were quantified at 470, lated endpoints (leaf gas exchange, chlorophyll a 537, 647, and 663 nm. fluorescence, ribulose-1,5-bisphosphate carboxy- The basal fluorescence yield of dark-adapted lase/oxygenase ‒ RuBisCO amount, pigments and samples (F ), the maximal fluorescence yield (F ), 0 m carbohydrates contents) were quantified. and the variable fluorescence (F =F ‒ F ) were mea- v m 0 sured with the respective light conditions. The pa- rameters F ’, F ’, and F ’ were also assessed in 30 0 m v MATERIAL AND METHODS min illuminated leaves. F / F and F ’/ F ’, and the v m v m effective photochemical efficiency of PSII (Φ ), PSII Nanoparticles stocks, characterization, and prepa- photochemical quenching (q ), and electron trans- ration of solutions port rate (ETR) were determined (Maxwell & John- TiSiO NPs (>99.8% purity) were purchased son 2000). from Sigma-Aldrich (St. Louis, MO-USA) having, For leaf gas exchange analysis, the infra-red gas according to the supplier, a primary size <50nm. analyser (LCpro+, ADC, Hoddesdon, UK), operat- TiSiO NPs dynamic light scattering (DLS) and zeta ing in open mode, was used. Measurements took potential were characterized according to our cur- place under atmospheric CO concentration with rent techniques (Bastos et al. 2017). A stock suspen- a saturating photosynthetic photon flux density of sion of 1.0 g/L TiSiO NPs (in distilled water) was 600 µmol m /s. Transpiration rate (E, mmol (H O) used for the preparation of final nutrient solutions 2 2 m /s), stomatal conductance (g , mmol (H O) m /s), s 2 (Hoagland basal salt mixture, Sigma-Aldrich, USA) net photosynthetic rate (Pn, µmol (CO ) m /s) and with concentrations up to 100 mg/L. All suspensions the ratio of intercellular CO concentration to ambi- were sonicated for ≈20 min prior to use. ent CO ( C /C ) were determined (Rodriguez et al. 2 i a 2015). Seed germination and exposure to TiSiO NPs Seeds of L. sativa cv. ‘Maravilha de Verão Ca- Carbohydrates quantification nasta’ (Vilmorin Jadin, France) were germinated in Total soluble sugars (TSS) and starch contents Petri dishes (100 seeds/petri dish), each with 10 mL (mg/g FM) were quantified by the anthrone method of nutrient solution with different TiSiO NPs con- (Osaki et al. 1991; Irigoyen et al. 1992). centrations: 0, 50, and 100 mg/L. Germination took RuBisCO quantification place at 16 h light period (Photosynthetically active Soluble proteins extracted from the first rosette radiation − PAR ≈100 µmol/m / s), 20 ± 2ºC, ≈50% leaves were quantified by the Bradford method (Sig- relative humidity (%RH). One-week-old seedlings ma-Aldrich, USA). For RuBisCO analysis, 15 µg of were hydroponically grown on the corresponding protein were separated by SDS-PAGE, using pro- media at PAR ≈200 µmol/m /s, 16 h light periods, tein molecular weight marker (Fermentas SM0441, 22 ± 2ºC, ≈45% RH. All media were renewed every ThermoFisher, USA) as a reference, and bands were 3 days, and pH was kept constant at ≈5.6. After 3 150 Agriculture (Poľnohospodárstvo), 66, 2020 (4): 148 −160 stained with 0.25% Coomassie Brilliant Blue R250 aggregates confirming previous data, and according (Li et al. 2013). Relative RuBisCO quantification to the DLS data, their hydrodynamic diameter was of large and small subunits was done after over- 2 to 3 times larger than the primary particle size, night incubation in 2 mL formamide at 50ºC, read- reaching average sizes of 115 ± 29 nm. ing absorbance at 595 nm. Results are expressed as Seeds in all concentrations reached a germina- ABS /ABS tion rate of >99%, supporting no negative effects of Rubisco content Protein content. these NPs on this crop’s germination. Whilst root Statistical analysis length and fresh matter (FM) of exposed plants were Experiments used 6 ‒ 8 plant samples (treated in- not affected compared to unexposed roots, both dividually or as leaf pools), and 3 independent tech- shoot length and, mainly shoots’ FM, were in gen- nical replicates. Comparisons between the different eral stimulated by TiSiO NPs compared to control conditions were made using the One-Way ANOVA plants (Table 1). test, using GraphPad Prism 6 (GraphPad Software, San Diego, California, USA). For different condi- Photosynthetic pigments content and fluorescence tions, the Tukey Comparison Test (p < 0.05) was The average values of Chl a and b contents were used. Multivariate analyses for data correlation used stimulated by TiSiO NPs (Figure 1a, b) with max- Principal component analysis (PCA) and were per- imum values being achieved at 50 mg/L (p < 0.05). formed with CANOCO 5 (WUR, Netherland). The ratio Chl a / Chl b was increased (p < 0.05) by both TiSiO NPs doses (Figure 1c). Carotenoids’ levels were not changed by TiSiO NPs (Figure 1d). RESULTS Finally, the anthocyanin levels were significantly in- creased at 50 mg/L TiSiO NPs (Figure 1e). Nanoparticles characterization and effect on germi- Basal chlorophyll fluorescence of dark-adapt - nation and plant growth ed leaves (F ) was slightly decreased (p < 0.05) by Taking into account the size of TiSiO NPs (<50 100 mg/L TiSiO NPs (Figure 2a). Maximum fluores- nm in aqueous suspensions), these NPs tend to form cence (F ) and variable fluorescence (Figure 2b, c) TiSiO concentrations [mg/L] TiSiO concentrations [mg/L] TiSiO concentrations [mg/L] 4 4 4 TiSiO concentrations [mg/L] TiSiO concentrations [mg/L] 4 4 Figure 1. Pigment contents (mg/kg (FM)) in plants exposed to TiSiO NPs. a) chlorophyll a; b) chlorophyll b ; c) ratio Chl a / Chl b; d) Carotenoids; e) Anthocyanins; FM − Fresh Matter. All conditions were compared by Tukey multi comparison test using one-way ANOVA for p < 0.05. mg/kg (FM) mg/kg (FM) mg/kg (FM) Agriculture (Poľnohospodárstvo), 66, 2020 (4): 148 − 160 were not compromised (p > 0.05) in exposed plants, 100 mg/L compared to 50 mg/L (Figure 2f). For the but the increase of F / F ratio at 100 mg/L was sig- photosystem efficiency, Φ was affected by TiSiO v m PSII 4 nificant compared to 50 mg/L condition (p < 0.05; NPs doses also with increases at 100 mg/L com- Figure 2d). Regarding the light-adapted state, F’ / F’ pared to 50 mg/L (Figure 2e). The q parameter was v m P ratio was affected increasing substantially at not affected by any NPs dose (Figure 2g). Lastly, T a b l e 1 Growth parameters of lettuce roots and shoots exposed to TiSiO NPs Plant area evaluated Control 50 mg/L 100 mg/L Root Length [cm] 12.83 ± 2.15 11.170 ± 1.56 12.46 ± 1.95 Shoot Length [cm] 9.94 ± 2.18 12.826 ± 2.30 10.44 ± 2.42 Root Fresh Matter [g] 8.49 ± 2.43 10.680 ± 3.52 10.62 ± 2.10 Shoot Fresh Matter [g] 11.22 ± 1.57 14.030 ± 1.33* 19.53 ± 2.54* For the same condition and organ *means significantly different values (p < 0.05) in comparison with the control. TiSiO concentrations [mg/L] TiSiO concentrations [mg/L] TiSiO concentrations [mg/L] 4 4 4 TiSiO concentrations [mg/L] TiSiO concentrations [mg/L] TiSiO concentrations [mg/L] 4 4 4 TiSiO concentrations [mg/L] TiSiO concentrations [mg/L] 4 4 Figure 2. Fluorescence data (AU − arbitrary units) of plants exposed to TiSiO NPs. a) F − minimal fluorescence of dark- 4 0 adapted leaves; b) F − variable fluorescence of dark-adapted leaves; c) F − maximum fluorescence of dark-adapted leaves; v m d) F / F − maximum quantum yield; e) Φ − effective quantum yield; f) F ’/ F ’ − maximum quantum yield in light-adapted v m PSII v m condition; g) q − photochemical quenching; h) ETR − electron transport rate. All conditions were compared by Tukey multi comparison test using one-way ANOVA for p < 0.05. 152 Agriculture (Poľnohospodárstvo), 66, 2020 (4): 148 −160 ETR was stimulated (p < 0.05) by 100 mg/L dose of CO by L. sativa plants. Significant differences compared to 50 mg/L (Figure 2h). between each condition for all parameters (Figure 3a-e) were not found. Also, the parameters related Gas exchange, RuBisCO, and carbohydrate levels to carbon assimilation, such as RuBisCO, TSS, and Leaf gas exchange parameters showed that the starch contents were not significantly affected by the use of TiSiO NPs did not affect the potential use TiSiO NPs doses used (Figure 4a-c). TiSiO concentrations [mg/L] TiSiO concentrations [mg/L] TiSiO concentrations [mg/L] 4 4 4 TiSiO concentrations [mg/L] TiSiO concentrations [mg/L] 4 4 Figure 3. Leaf gas-exchange in plants exposed to TiSiO NPs. a) E (mmol (H O) m /s) − transpiration rate; b) gs − stomatal 4 2 conductance; c) Pn (µmol (CO ) m /s) − net photosynthetic rate; d) Pn/gs ratio – Pn /gs − CO assimilation efficiency; 2 2 e) C / C − intercellular CO ratio. i a 2 All conditions were compared by Tukey multi comparison test using one-way ANOVA for p < 0.05. TiSiO concentrations [mg/L] TiSiO concentrations [mg/L] TiSiO concentrations [mg/L] 4 4 4 Figure 4. Relative RuBisCO content, starch, and total soluble sugars in plants exposed to TiSiO NPs. a) RuBisCO (ABS / ABS ); b) TSS (mg/g (FM)); c) Starch (mg/g (FM)); FM − Fresh Matter. RC TPC All conditions were compared by Tukey multi comparison test using one-way ANOVA for p < 0.05. mmol (H O) m /s ABS /ABS RC TPC 2 mmol (H O) m /s mg/kg (FM) mg/kg (FM) µmol (CO ) m /s 2 Agriculture (Poľnohospodárstvo), 66, 2020 (4): 148 − 160 beneficial effects with minimal toxicity. However, the characterization of the TiSiO NPs bioactivity in plants remains scarcely addressed. Moreover, most of the studies performed up to the moment with NPs used short term exposures, while agricultural pur- poses demand long term-exposure studies. Ti is well known to be an element that when found in soils and waters used for plant growth, it en- hances not only the plants’ photosynthesis, but also their chlorophyll content, which promotes nutrient uptake, better stress tolerance, and improves crop yield and quality, making this a beneficial element (Lyu et al. 2017). On the other hand, the beneficial effects of silicon to plants are widely demonstrated (Murad et al. 2020) and its oxidised form (SiO NPs) promoted plant protection against biotic and abiotic Figure 5. Principal component analysis (PCA) of functional stress (Luyckx et al. 2017). Our work contains the responses of plants exposed to TiSiO NPs first results addressing TiSiO NPs photosynthetic bioactivity in plants, and we demonstrate that, after PCA (Figure 5) shows a distinct separation be- short-term exposure, moderate doses of TiSiO NPs tween all conditions used in physiological studies might stimulate lettuce growth, and may positively (0, 50, and 100 mg/L). PC1 (F1) explains 61.9% of influence, in yet to unveil mechanisms, photosyn- the variance, while PC2 (F2) explains 39.1%. The thetic parameters, such as the increase of photosyn- control population is located on the down-right thetic pigments at lower doses (50 mg/L) and gas quadrant, and this parameter is the only located in exchange and PSII efficiency at higher doses (100 the down-side of the Y-axis, associated with TSS mg/L). and some fluorescence parameters (F and F ). On Recently we have demonstrated for Triticum aes- v m the other hand, 50 mg/L is in the top-left quadrant tivum that chronical exposure to TiO NPs influences and has positive scores for all photosynthetic pig- photosynthesis, and for example, 150 mg/L TiO NPs ments and g parameter. Regarding yield parame- had phytotoxic effects (stimulating oxidative stress ters of photosynthesis, such as Φ , F / F , F’ / F’ , and water disorders), which impaired plant growth, PSII v m v m ETR, Pn / g , RuBisCO, and starch contents, these being toxicity more severe in shoots than in roots are clusters on the top-right quadrant, corresponding (Silva et al. 2017a; 2019). Using fresh and dry mat- to the 100 mg/L samples. ter as growth indicators, and soils contaminated with extremely high doses (1,000 mg/kg soil ), DM Bouguerra et al. (2016) reported TiSiO NPs phy- DISCUSSION totoxicity in lettuce and tomato plants. Comparing the available literature for TiO NPs with our current TiO and SiO NPs bioactivity in plants are cur- data for TiSiO NPs, there is evidence of lower tox- 2 2 rently under debate to support their potential use icity of TiSiO NPs, but further comparative studies in nanoagriculture (Srivastava et al. 2015). Whilst under similar conditions must be conducted. most studies are focused on TiO showing antibiotic We demonstrate here that the interference of activity and at some limited doses a stimulation of TiSiO NPs with photosynthesis is complex and growth (but also toxicity at higher doses), SiO is related to the dose, but overall a neutral or slight mostly pinpointed as a potential source of release of stimulation is found. Photophosphorylation is the Si with demonstrated benefits to plant growth, and source of ATP and NADPH + H for the Calvin cy- thus with potential as a nano fertiliser. The combi- cle to proceed, and its status here was evaluated ac- nation of Ti and Si may thus combine some of the cording to changes in the chlorophyll quantity/ratio 154 Agriculture (Poľnohospodárstvo), 66, 2020 (4): 148 −160 for 50 mg/L TiSiO NPs compared to control plants. 50 mg/L can promote a positive effect in photosyn- It was evident that 50 mg/L TiSiO NPs stimulated thesis performance and the 100 mg/L concentration chlorophylls and anthocyanins contents (by increas- may not be the maximum endpoint of high photo- ing synthesis or preventing damage) which, besides synthetic performance for L. sativa. photosynthesis, also have protective roles. The ob- Interestingly, the PCA analyses confirm a horme- served increase of Chl levels has been described in sis response in some parameters, shown by a negative response to TiO NPs, often paralleled with an in- correlation between 50 mg/L and the dark-adapted crease of N uptake, but the targets of these NPs in parameters of F , F , F / F , and F’ /F’ , while 100 m v v m v m the plant metabolism remain unknown (Lyu et al. mg/L had a similar negative correlation with F . A 2017). Kheyrkhah et al. (2018) showed that SiO higher F can be interpreted as indicating irrevers- 2 0 and TiO increased the chlorophylls and carotenoids ible damage to PSII (Bussotti et al. 2011), therefore content in oilseed rape cultivars. Also, Aliabadi et the decrease of F in exposed leaves may indicate al. (2015) showed that 100 mg/L TiO NPs increased a protective role exerted by these NPs on the PSII, the Chl a content and the ratio (Chl a / Chl b) in decreasing the uncontrolled dissipation of heat. This T. aestivum. However, the same study also showed hypothesis is also supported by the F / F ratio, v m that using 20 times more concentration (2,000 which gives information on the maximum quantum mg/L) reduced Chl content and its ratio. This study, efficiency of the PSII photochemistry. In TiSiO in parallel with our data, demonstrates that moder- NPs exposed plants, this ratio remains around the ate doses are capable to increase the photosynthetic 0.79 ‒ 0.84 values, which is an indicator of healthy potential, however, the species factor should be con- plants (Maxwell & Johnson 2000) and indicates sidered. These rises may increase the efficiency of a balance between reduction of plastoquinone Q CO assimilation (Yang et al. 2006; Sanshez-Zabala and its reoxidation by Q . This ratio is widely used 2 B et al. 2015; Lyu et al. 2017). Ti oxides NPs may as a sensitive endpoint for several stress-related pho- also exert a protective role of photostability of chlo- tosynthetic disorders. For example, its disturbance rophylls, similarly to what was reported for silver was reported in some species exposed to TiO NPs nanoparticles (AgNPs) that slowed down the photo- like T. aestivum (Dias et al. 2019). Also, in Chlorella degradation of Chl a (Barazzouk et al. 2012). Thus, pyrenoidosa, the inhibition of the photosynthetic ac- the increase of chlorophylls by TiSiO NPs suggests tivity was attributed to the damage of the reaction either increased synthesis or an improved photosta- center of PSII (Middepogu et al. 2018). bility of the pigments. This increase of pigments will Whilst the decrease of F / F may indicate some v m improve the capacity for harvesting photons to fos- slowly relaxing quenching processes and photodam- ter the photophosphorylation process. The protec- age to PSII reaction centres, reducing the maximum tive role of these pigments against photooxidation quantum efficiency of PSII photochemistry (Baker should also not be excluded. On the other hand, the & Rosenqvist 2004), its increase – as observed in absence of changes in fluorescence parameters and TiSiO NPs exposed plants – suggests increased gas exchange compared to control were a positive protection to chlorophyll photoinhibition. This pro- indicator that the doses tested are not a toxic con- tective role is also in accordance with the increase centration of this compound for L. sativa growing in of chlorophyll levels in TiSiO NPs exposed plants’ hydroponic systems, using the photosynthesis and leaves. Regarding light-adapted parameters, F ’/ F ’ v m carbon metabolism as control endpoints. Neverthe- was positively correlated with the 100 mg/L, mean- less, the use of TiO NPs in another crop, such as So- ing an increased capture efficiency of excitation lanum lycopersicum, was capable to promote an in- energy by open PSII reaction centres in this NP crease in photosynthetic parameters (Qi et al. 2013). concentration (Lima et al. 2002). Thus, we suggest Besides, our data showed a particularity on the that these NPs, directly or indirectly, stimulated the 100 mg/L conditions, as increases occurred in some chlorophyll protection against photodamage (Wang photosynthetic parameters (F / F , Φ , F’ / F’ , et al. 2016), and/or increased chlorophyll synthe- v m PSII v m and ETR) compared to 50 mg/L. These results sis to compensate for alleged increased damages as suggest that an increase of TiSiO NPs relative to suggested by Middepogu et al. (2018). It should be 155 Agriculture (Poľnohospodárstvo), 66, 2020 (4): 148 −160 stressed/highlighted that this protective role may However, TiO NPs had a different effect on gly- have slightly increased the efficiency of the photo- cometabolism, as it decreased the levels of starch in phosphorylation process, which may lead to an in- T. aestivum, putatively as a mechanism to maintain crease in the amount of ATP and NADPH available the soluble sugars levels (Dias et al. 2019). Also, to be used in Calvin Cycle. changes in carbohydrates after exposure to TiO NPs Data related to the gas exchange parameters did were reported in cucumber fruits (Servin et al. not show any responsive effect with the studied 2013). Contrarily, despite negative effects on chlo- TiSiO NPs doses to L. sativa. However, the multi- rophyll, TiO NPs increased total sugar and reduced 4 2 variance analysis showed that g had a positive cor- sugar in basil exposed to TiO NPs (Tan et al. 2018). s 2 relation with 50 mg/L and a Pn with opposite cor- Those authors suggested that TiO NPs led to the relation for control plants and associated positively transfer of an active electron which might disrupt for 50 and 100 mg/L (Figure 5). A potential increase enzyme activities related to glycometabolism, like of Pn can be associated with the increase of CO those as β-amylases (Thalmann & Santelia 2017), supply from outside to the intercellular airspaces of supporting the associated increase of sugar levels leaves (Dias et al. 2019). However, the non-signif- (Tan et al. 2018). Moreover, in TiSiO NPs exposed icant changes in Pn do not follow the increase of plants, while starch content showed some PCA-cor- Chl, nevertheless, the increase of Chl is not always relation with Pn and RuBisCO content, it showed an accompanied by Pn increase (Da-yong et al. 2012). opposite correlation to these parameters in control This is controlled by the stomatal function and the plants, supporting a trend to increase with these NPs CO diffusion from intercellular airspaces towards (Figure 5), however, this concentration did not show the carboxylation sites. These NPs do not interfere significant differences. Our results demonstrate that with the accumulation of CO inside the mesophyll TiSiO NPs doses up to 100 mg/L did not affect the 2 4 intercellular space, which suggests a proper function plant glycometabolism, while the positive correla- of RuBisCO and even a putative stimulation of its tion of some parameters such as Pn and RuBisCO transcription, despite its relative amount not being for 100 mg/L showed that maybe the endpoints changed. Different results with high concentrations were not detected, and other upper doses could have of TiO NPs were reported, namely the TiO NPs con- a positive effect for L. sativa. 2 2 centration of 1,000 mg/L, which decreased CO fix- Mainly, some differences between the reported ation, transpiration rate, and stomatal conductance effects of TiO and TiSiO NPs perhaps occurred by 2 4 (Da Costa & Sharma 2015). Also, we have recent- the presence of Si element. Once this mineral is re- ly demonstrated that TiO NPs (anatase: rutile) are lated with plant recovery for abiotic stress (Etesami chronically applied to T. aestivum, decreased max- & Jeong 2018) and is involved in photoprotection imal and effective efficiency of PSII, net photosyn- processes (Li et al. 2018), including the photosyn- thetic rate, transpiration rate, stomatal conductance, thetic stimulation by the increase of the chlorophyll intercellular CO concentration, and starch content levels (Sarma et al. 2018), such as in L. sativa ex- (Dias et al. 2019). On the other hand, the application posed to TiSiO NPs. of SiO NPs improves the gas exchange performance in Passiflora edulis with an increase of Pn, E, and gs (Costa et al. 2018). Overall, our data suggest that CONCLUSIONS low doses of TiSiO NPs play some protective role in photosystem II, not having the negative impacts In conclusion, this is one of the first approaches of TiO NPs. regarding the bioactivity of the understudied TiSiO 2 4 The protective role of TiSiO NPs on the pho- NPs, and it demonstrates that TiSiO NPs stimulate 4 4 tosynthetic apparatus and the stimulation of RuBis- plant growth, and different doses may promote pho- CO subunits show stimulation of photosynthesis, tosynthetic apparatus and performance in different supporting the observed plant growth increase. The ways, namely lower doses may stimulate chloro- TSS and starch levels are in line with all photosyn- phyll levels, while higher doses show a stimulato- thetic mechanisms under the effect of TiSiO NPs. ry trend to stimulate photosynthetic performance. 156 Agriculture (Poľnohospodárstvo), 66, 2020 (4): 148 −160 53, no. 2, pp. 207 ‒ 219. DOI: 10.31055/1851.2372.v53. The tested doses did not have a negative effect on n2.20578. the net photosynthetic rate, nor influenced RuBis- BAKER, N. ‒ ROSENQVIST, E. 2004. Applications of chloro- CO subunit amount. Being the first study on the phyll fluorescence can improve crop production strategies: an examination of future possibilities. In Journal of Ex- biochemical effects of TiSiO NPs this study also perimental Botany, vol. 55, no. 403, pp. 1607 – 1621. DOI: shows the need to better understand how manufac- 10.1093/jxb/erh196. BARAZZOUK, S. ‒ BEKALÉ, L. ‒ HOTCHANDANI, S. tures nanoparticles interfere in crop performance 2012. Enhanced photostability of chlorophyll-a using gold and identify safety and realistic doses. nanoparticlesas an efficient photoprotector. In Journal of Material Chemistry, no. 22, pp. 25316 ‒ 25324. DOI: 10.1039/C2JM33681B. Acknowledgements. Work supported by FED- BASTOS, V. ‒ DE OLIVEIRA, J.F. ‒ BROWN, D. ‒ ER/COMPETE [POCI/01/0145/FEDER/007265 JONHSTON, H. ‒ MALHEIRO, E. ‒ DANIEL-DA-SIL- VA, A.L. ‒ DUARTE, I.F. ‒ SANTOS, C. ‒ OLIVEIRA, and FCT/MEC PT2020 UID/QUI/50006/2013]; H. 2016. The influence of Citrate or PEG coating on silver FCT funded N. Mariz-Ponte, S. Sario, and R.J. nanoparticle toxicity to a human keratinocyte cell line. In Mendes, fellowships [SFRH/BD/138187/2018, Toxicology Letters, vol. 249, pp. 29 ‒ 41. DOI: 10.1016/j. toxlet.2016.03.005. SFRH/BD/138186/2018, SFRH/BD/133519/2017]; BEHBOUDI, F. ‒ SARVESTANI, Z.T. ‒ KASSAEE, M.Z. ‒ Also supported by National Funds by FCT - Portu- MODARES, S.A.M. 2018. Improving growth and yield of wheat under drought stress via application of SiO nanopar- guese Foundation for Science and Technology, un- ticles. In Journal of Agricultural Science and Technology, der the project UID/AGR/04033/2019. vol. 20, no. 7, pp. 1479 ‒ 1492. 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Journal

Agriculturede Gruyter

Published: Dec 1, 2020

Keywords: gas exchange; nanoagriculture; nanofertilisers; phot osynthesis; TiSiO 4

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