Next Article in Journal
Genetic Response of Solanum lycopersicum L. (Tomato) to Phytophthora infestans and Aspergillus niger
Previous Article in Journal
The Optimization of In Vitro Culture Establishment and Shoot Proliferation of “GiSelA 17” (Prunus canescens × Prunus avium): A Novel Cherry Rootstock
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
IJPB
Volume 16
Issue 1
10.3390/ijpb16010034
ijpb-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Mitigating Salinity Stress in Pea Plants with Titanium Oxide Nanoparticles

by
Ekaterina Yotsova
,
Martin Stefanov
,
Georgi Rashkov
,
Anelia Dobrikova
and
Emilia Apostolova
*
Institute of Biophysics and Biomedical Engineering, Bulgarian Academy of Sciences, Acad. G. Bonchev Str., Bl. 21, 1113 Sofia, Bulgaria
*
Author to whom correspondence should be addressed.
Int. J. Plant Biol. 2025, 16(1), 34; https://doi.org/10.3390/ijpb16010034
Submission received: 15 January 2025 / Revised: 21 February 2025 / Accepted: 5 March 2025 / Published: 8 March 2025
(This article belongs to the Topic Tolerance to Drought and Salt Stress in Plants, 2nd volume)
Browse Figures
Versions Notes

Abstract

:
Changes in the environment have a significant impact on photosynthetic efficiency, which in turn influences plant growth and yield. Consequently, there is a greater focus on methods to enhance photosynthetic efficiency with the goal of raising plant productivity. In this study, the effects of titanium oxide nanoparticles (TiO2 NPs) on pea plants (Pisum sativum L.) subjected to moderate salt stress by the addition of 100 mM NaCl to the nutrient solution were investigated. Two concentrations of NPs (50 mg/L and 100 mg/L) were applied through foliar spray on pea leaves. Data showed that NPs prevent salt-induced membrane damage, growth inhibition, and the increase in hydrogen peroxide and lipid peroxidation. An analysis of the chlorophyll fluorescence curves revealed that TiO2 NPs decreased the effects of NaCl on the reduction in the open photosystem II centers (corresponding with qp) and their efficiency (Φexc), as well as the activity of the oxygen-evolving complex (Fv/Fo). The co-treatment with TiO2 NPs and NaCl also improved the photochemical energy conversion of photosystem II (ΦPSII), alleviated the interaction of QA− with plastoquinone, and enhanced electron transport activity and the rate of photosynthesis, compared to the plants treated with NaCl only. Additionally, NPs application under salt stress stimulated cyclic electron transport around photosystem I, thus protecting its photochemical activity. These protective effects of NPs were more pronounced at a concentration of 100 mg/L.

1. Introduction

The climate changes in recent years have led to an increase in numerous adverse environmental conditions. Salinity is one of the major abiotic stress factors that negatively affect plant growth and development by impacting multiple biochemical and physiological processes [1,2,3]. Previous investigations on different plant species have shown that salt stress causes significant changes in chloroplasts by altering the ultrastructure and composition of thylakoid membranes, inhibiting the functions of the photosynthetic apparatus [4,5,6,7,8], and thereby severely impairs the photosynthesis [9,10]. Additionally, salinity leads to an increase in the number of plastoglobules and reduces the number of thylakoids in the granum of the chloroplasts [11]. Furthermore, salinity strongly affects photosynthetic processes by influencing the activity of different enzymes, the content of leaf pigments, and the structural organization of the pigment–protein complexes of the photosynthetic apparatus [12]. Salt stress also impacts some other important chloroplast components such as the oxygen-evolving complex (OEC) [13,14,15], the light-harvesting complex of photosystem II (LHCII) [16,17,18], and the D1 core protein of photosystem II (PSII) [19,20,21]. Recent studies have revealed that salt-induced changes in the OEC correspond to the modification of Mn clusters and an increase in the number of blocked PSII centers [22,23].
Nanotechnology could be a useful tool for alleviating the effects of environmental stress factors and improving crop productivity [24,25,26]. Studies on the effects of metal and metal oxide nanoparticles on plants have recently increased in number [27,28]. The effect of the nanoparticles (NPs) correlates with their properties such as chemical composition, size, surface coverage area, reactive abilities, and effective doses [29]. Due to their specific characteristics, NPs could be a promising approach for improving the resistance of plants to abiotic stress factors [26] including salt stress [30,31]. The treatment of plant leaves has been proposed to be more effective than the soil application of nano-fertilizers [32,33,34,35]. It has been demonstrated that the application of suitable NPs, such as silver, iron, titanium oxide, zinc oxide, copper oxide, silicon oxide, and others, etc., could be a promising tool for mitigating the negative influence of abiotic stress factors on plants in a dose-dependent manner [32,36,37,38,39]. Moreover, the impact of nanoparticles depends on the plant species. It has been shown that the foliar application of CuO NPs induces salt tolerance by increasing photosynthetic efficiency and antioxidant activity in Brassica juncea [40]) and Solanum lycopersicum [41]. A recent study by Mahawar et al. [39] comparing the effects of the foliar application of CuO and ZnO NPs on radish plants under salinity has demonstrated that ZnO NPs are more efficient in alleviating salt stress than CuO NPs. Our previous study [42] has compared the impact of foliar-applied ZnO and ZnO-Si NPs (ZnO coated with SiO2 shell) on pea plants and showed that ZnO-Si NPs have better defense mechanisms against salt stress than bare ZnO NPs due to the altered surface characteristics of NPs. A study by Siddiqui et al. [43] has shown that SiO2 NPs improve the defense mechanisms of Cucurbita pepo plants against salt stress, as all these effects were dose-dependent. Additionally, the foliar application of both ZnO NPs and TiO2 NPs in low concentrations on tomato plants had a beneficial impact on early development and flowering compared to the controls, as TiO2 NPs increased the light absorption and chlorophyll content in plants, while ZnO NPs had a twin role of being an essential nutrient and a co-factor for nutrient mobilizing enzymes [44]. However, the application of high concentrations of NPs might inhibit plant growth and development due to the generation of reactive oxygen species (ROS), damage to cellular membranes, proteins, and nucleic acids, as well as a disturbance in mineral nutrition and photosynthesis [45,46,47,48,49,50].
Titanium (Ti) is the transition element that has been proposed to have a positive effect on photosynthesis [51]. This suggestion has led to increased attention in the recent years on the effects of TiO2 NPs on plants [52,53]. TiO2 also acts as a photocatalyst and induces oxidation-reduction reactions in pigment biosynthesis [54,55]. It has also been shown that TiO2 increases the contents of chlorophyll [56], carotenoids, and anthocyanin, which promote the crops’ growth and yield [57]. Foliar treatment with low concentrations of TiO2 NPs of mung bean plants resulted in increased leaf pigment content (chlorophylls, carotenoids) and stimulated plant growth and development [58]. Previous studies have shown that in different plant species the TiO2 NP treatment results in improved seed germination, stimulation of plants growth and development [53,59,60,61,62,63,64,65,66,67]. In different plants, the application of TiO2 NPs enhanced stomatal conductance [53,68,69], as well as transpiration rate and water use efficiency [53]. It has also been shown that the treatment of soybean plants with TiO2 NPs improved the photochemical efficiency of photosystem II (Fv/Fm) and the electron transfer rate (ETR) [70], thereby stimulating photosynthesis [67,68,69,71,72,73].
Moreover, previous studies have found that TiO2 NPs regulate the activity of several enzymes involved in the nitrogen metabolism of maize and spinach, including glutamate dehydrogenase, nitrate reductase, and glutamine synthase, as well as various antioxidant enzymes such as peroxidase, superoxide dismutase, catalase, and phenylalanine ammonia lyase [74,75]. All of the above could explain the positive effects of TiO2 NPs on plants under physiological conditions and abiotic stress [75,76]. The treatment of chickpea plants with TiO2 NPs resulted in better metabolic potential of photosynthesis, facilitating the adaptation of the plants to cold stress [77]. In broad bean plants grown under salt stress conditions, TiO2 NPs caused a positive effect on antioxidant enzyme activity and reduced H2O2 and MDA contents [78]. Tomato plants treated with TiO2 NPs showed reduced effects of salt stress in leaf chlorophyll and phenolic contents. Data also revealed an improvement in antioxidant enzyme activity and yield [79]. In Moldavian balm (Dracocephalum moldavica L.) the root application of TiO2 NPs increased the activity of antioxidant enzymes, which could induce secondary metabolite production and improve plant performance during salt stress [80]. In wheat plants grown under water deficit conditions, foliar treatment with TiO2 NPs increased gluten and starch contents, and reduced the negative effects of this stress on the wheat yield [81].
Recently, much attention has been paid to the protection of plant photosynthetic function under abiotic stress [82,83]. Several studies have suggested that improving photosynthetic performance under stress conditions can improve the production of plants under adverse environmental conditions, including salt stress [82]. Since salinity stress has a strong impact on plant photosynthetic membranes, causing damage at many levels, this determined the importance of studying the plant stress response and adaptation mechanisms of the photosynthetic apparatus, which can help develop crops that are better adapted to saline soils. The aim of this study was to investigate the protective effects of TiO2 NPs on the photosynthetic apparatus of pea plants in more detail, which will allow for a better understanding of the protective mechanisms of TiO2 NPs on photosynthesis under salt stress. For this purpose, pea plants were foliar treated with 50 and 100 mg/L TiO2 NPs under moderate salt stress (100 mM NaCl). The leaf pigment content, membrane stability, oxidative stress markers, and complexes of the photosynthetic apparatus were evaluated under moderate salt stress conditions. The data in this study give new information for the influence of the TiO2 NPs on the acceptor side of PSII, as well as its influence on the two subpopulations of PSI (in grana and stroma lamellae). The present study provides important insights into the practical ways of alleviating the deleterious effects of salt stress by applying the cheap and readily available TiO2 NPs.

2. Materials and Methods

2.1. Plant Material and Growth Conditions

The experiments were carried out with 14-day-old pea plants (Pisum sativum L. Ran 1), which have a moderate salt tolerance [84]. The plants grown in hydroponic cultures on a 1/2 strength Hoagland solution changed every 5 days, as described in [42]. The plants were grown under an illumination period of 12 h, with a light intensity of 150 µmol/m2s1, at a temperature of 25 °C, and a relative humidity of about 60%.
The plants were simultaneously treated with 100 mM NaCl and TiO2 NPs. The leaves of the plants were sprayed with two concentrations of TiO2 NPs (50 and 100 mg/L). The treatment was repeated after 4 days. The salt stress was induced by applying 100 mM NaCl in the nutrient solution, containing: 2.5 mM KNO3, 2.5 mM Ca (NO3)2, 1 mM MgSO4, 0.5 mM NH4NO3, 0.5 mM K2HPO4, 23 µM H3BO3, 4.5 µM MnCl2, 0.4 µM ZnSO4, 0.2 µM CuSO4, 0.25 µM Na2MoO4 and 20 µM Fe-EDTA (pH 6.0). Ten plants were grown in one pot with a volume of 1.2 L. The measurements were carried out on the 8th day of the salt treatment to assess the influence of the TiO2 NPs under salt stress. The concentrations of TiO2 NPs and NaCl were selected after preliminary experiments. The effects of different concentrations of the TiO2 NPs under physiological conditions were studied (Table S1). From the studied concentrations, those that had a beneficial effect on the chlorophyll content and function of the photosynthetic apparatus were selected. The influence of the different concentrations of NaCl were studied in our previous study [85]. The selected concentration leads to a 30% reduction in the Fv/Fo parameter (Table S1).

2.2. Characterization of TiO2 NPs

The nanoparticles of TiO2 were of analytical grade and commercially sold without further purification as a cheap and convenient source for potential further use (in agronomy). The stock solution of the TiO2 NPs was prepared directly by suspension in deionized water and dispersed by ultrasonic vibration for 30 min. The NP solution was diluted to 50 and 100 mg/L before the foliar spraying of plants. Dynamic light scattering measurements using a Zetasizer nano (ZS Pro, Malvern Instruments Ltd., Malvern, UK) were applied to evaluate the size distribution and zeta potential (surface charge) of the NPs. The mean hydrodynamic size of TiO2 NPs was 99 ± 6 nm, and the zeta potential was −16.9 ± 0.7 mV showing a good dispersion and stabilization of the nanoparticles (Figure S1a,b).

2.3. Growth Parameters

The determination of plant root and shoot lengths in centimeters (cm) was performed on the 8th day of the treatment.

2.4. Pigment Analysis

For the extraction of the leaf pigments, the frozen leaves were homogenized with ice-cold 80% acetone and the obtained leaf extracts were centrifuged at 5000× g for 5 min. To determine the amounts of total chlorophylls (Chl b) and carotenoids (Car) the supernatant was measured spectrophotometrically (Specord 210 Plus, Edition 2010, Analytik Jena AG, Jena, Germany) and the amounts of total Chl and Car were calculated according to the equations by Lichtenthaler [86]:
Chl (a + b) = 7.15 × A663.2 + 18.71 × A646.8
Car = (1000 × A470 − 1.82 × (Chl a) − 85.02 × (Chl b))/198

2.5. Determination of Markers of Oxidative Stress

The content of hydrogen peroxide (H2O2) in the leaves was determined according to the method described previously in [87]. The leaves of the plants were grinded with trichloroacetic acid at 4 °C. The suspension was centrifuged at 14,000× g for 20 min. A reaction mixture containing the supernatant (0.5 mL), 100 mM Na–K-phosphate buffer with pH 7.6 (0.5 mL) and 1 mL of 1 M KI was prepared. The samples were kept for 1 h in the dark at room temperature and the absorbance was measured at 390 nm (Specord 210 Plus, Edition 2010, Analytik Jena AG, Germany). The molar extinction coefficient was used to determine the amount of H2O2 was 0.28 µM−1 cm−1. The amount of H2O2 was expressed as nmol per gram of fresh weight (FW).
To determine the levels of lipid peroxidation, the content of malondialdehyde (MDA) was measured using a reaction with thiobarbituric acid (TBA), as described previously by Yotsova et al. [79]. The leaves were grinded with 1% TCA at 4 °C. Then, the suspension was centrifuged at 14,000× g for 20 min. The reaction mixture contained supernatant, 0.5 mL 100 mM Na–K-phosphate buffer (pH 7.6), and 1 mL reagent (20% TCA with 0.5% TBA). The samples were heated at 95 °C for 30 min. After that, they were cooled in ice to stop the reaction. The absorbance was measured at 532 nm (Specord 210 Plus, Edition 2010, Analytik Jena AG, Germany). A molar extinction coefficient of 0.155 µM−1 cm−1 was used to determine the MDA amount. The amount of MDA was expressed as nmol per gram fresh weight (FW) [88].

2.6. Measurements of Electrolyte Leakage

Pea leaves from different plants were cut into pieces without the midvein and washed with distilled water. Then, the leaf pieces were incubated in 30 mL of distilled water for 24 h at room temperature. Each treatment was evaluated with at least three replications. The electrical conductivity of the solutions was then measured once (EC1) and again after boiling the samples for 30 min, followed by cooling to room temperature (EC2). The electrolyte leakage (EL) was calculated using the equation: EL (%) = (EC1/EC2)*100 as in [42].

2.7. Chlorophyll a Fluorescence at Room Temperature

The measurements of the pulse-amplitude-modulated (PAM) chlorophyll fluorescence were made on the fluorometer (model 101/103, Walz GmbH, Effeltrich, Germany) as described in [85]. Leaves were dark-adapted for 20 min prior to measurement. The light intensity for determining the maximum fluorescence (Fm and Fm′) was 3000 μmol photons/m2s generated from a Schott KL 1500 lamp (Schott Glaswerke, Mainz, Germany). The active light intensity was 150 μmol/m2s. From the curves of the chlorophyll fluorescence, the following parameters were calculated: Fv/Fm (maximum quantum efficiency of PSII; Fv/Fo (the quantum yield ratio of photochemical to nonphotochemical processes); qp (photochemical quenching); ΦPSII (effective quantum yield of PSII); ΦNO (non-regulated energy loss in PSII); ΦNPQ (regulated energy loss in PSII); Φexc (the excitation efficiency of open PSII centers); and ETR (electron transport rate) [85]. Additionally, the kinetic of variable fluorescence relaxation after excitation by 3000 μmol photons/m2s of the dark-adapted leaves was measured. The details for the determination and calculation of the decay rate constants (k1 for fast and k2 for slow), as well as the ratio of these two components (fast A1 and slow A2) were previously described in [85]. The chlorophyll fluorescence decay ratio (RFd) was also determined as in [89]. This ratio (RFd) correlates with net CO2 assimilation [89].

2.8. P700 Photooxidation

The redox state of P700 was examined in leaf disks using a dual-wavelength (820 nm) detector (ED 700DW-E, Walz, Effeltrich, Germany) connected to the main control unit PAM101E (Walz, Germany) in reflectance mode. The method for determination was described in Dankov et al. [90]. The measurements were made on PAM101E (Walz, Germany) connected with a dual-wavelength (820 nm) detector (ED 700DW-E, Walz, Germany). Leaf disks were exposed to a far-red light emitted by a photodiode (102-FR, Walz GmbH, Effeltrich, Germany). The far-red light induced variations in the absorbance at 820 nm (∆A) were determined, which correspond with changes in P700 oxidation (P700+). The ∆A/A ratio and the times of dark reduction in P700+ (t1 and t2) were calculated [85].

2.9. Statistical Analysis

Mean values with standard errors (±SE) were calculated from the data, based on at least two independent treatments, each comprising four biological replicates. The statistical differences between the groups for the measured parameters were evaluated using analysis of variance (ANOVA) followed by Tukey’s post hoc test. A homogeneity of variance test was conducted to verify the assumptions for the parametric ANOVA. Values of p < 0.05 were considered as statistically significant differences.

3. Results

3.1. Growth Parameters and Pigment Analysis

The root (from 14% to 26%) and shoot (from 24% to 32%) length of pea plants treated with TiO2 NPs alone increased in comparison to the control plants (Figure 1a). The stimulation on plant growth was stronger in the plants treated with the higher studied concentration of 100 mg/L TiO2 NPs by 26% for roots and by 32% for shoots. The salt stress alone caused significant inhibition of the plant growth parameters (35% for shoots and 27% for roots). The foliar treatment with NPs alleviated the negative influence of NaCl on these growth parameters. The protective effect was bigger at 100 mg/L TiO2 NPs. In this case, the increase was 44% for roots and 63% for shoots in comparison with the plants treated with NaCl alone (Figure 1a).
The treatment of pea plants with 100 mM NaCl alone resulted in decreased total chlorophyll (by 40%) and carotenoid (by 34%) contents compared to the control plants. The negative influence of salt stress on pigments was less pronounced in the plants subjected to foliar treatment with TiO2 NPs, as the protective effect on the pigments’ content was greater after the treatment with 100 mg/L TiO2 NPs. The data also showed that the application of TiO2 NPs alone caused a slight increase in the total chlorophyll content (by 10%), but did not affect the carotenoid content compared to the untreated plants (Figure 1b).

3.2. Oxidative Stress Markers and Electrolyte Leakage

Malondialdehyde (MDA) is a secondary product of the peroxidation of polyunsaturated fatty acids of membrane lipids. The experimental results revealed that the root treatment with 100 mM NaCl significantly increases the content of MDA (by 120%) and H2O2 (by 80%) in leaves. Foliar treatment with the TiO2 NPs significantly reduced the content of these stress markers (MDA, from 17% to 39% and H2O2, from 19% to 32%) in salt stressed plants. The protective effect was again stronger for the higher studied concentration of 100 mg/L of TiO2 NPs (Figure 2a). Furthermore, the treatment of plants with TiO2 NPs alone led to an insignificant increase of H2O2 at both studied concentrations of NPs, while MDA slightly increased only at 100 mg/L TiO2 NPs (Figure 2a).
Electrolyte leakage (EL) was used as an indicator of the integrity of cell membranes [91]. The results revealed that there is no statistical difference in the EL values between the plants treated with the TiO2 NPs alone at both studied concentrations (50 and 100 mg/L) and those of the control plants (Figure 2b). The treatment of plants with NaCl alone resulted in a significant increase in the EL values (about six times), which was much less pronounced in the plants subjected to co-treatment with NaCl and both studied concentrations of TiO2 (50 and 100 mg/L). The protective effect of the NPs was higher in plants treated with the 100 mg/L NPs but remained higher than the control values (Figure 2b).

3.3. Chlorophyll Fluorescence Parameters

The experimental results revealed that 100 mM NaCl influences the studied parameters of the chlorophyll a fluorescence in the following aspects: the maximal quantum yield in dark-adapted state (Fv/Fm), the ration of photochemical to non-photochemical processes (Fv/Fo), the photochemical quenching (qp), the excitation efficiency of open PSII centers (Φexc), the electron transport rate (ETR), and the chlorophyll fluorescence decay ratio (RFd), corresponding to the rate of photosynthesis (Figure 3). The treatment with the TiO2 NPs only led to an increase in the qp and RFd parameters. Under salt stress a strong decrease was observed in the values of the parameters Φexc (by 53%), ETR (by 39%), and RFd (by 48%). In the plants subjected to salt stress, the foliar treatment with both of the studied concentrations of TiO2 NPs resulted in a smaller decrease in the values of all studied PAM parameters, i.e., TiO2 NPs alleviated the negative effects of NaCl (Figure 3).
Furthermore, the salinity increased the quantum yield of the non-regulated (ΦNO) and regulated (ΦNPQ) losses, as well as decreased the effective quantum yield of the photochemical conversions of PSII (ΦPSII) (Figure 4). The values of these parameters were not changed after the treatment with TiO2 NPs only, but the foliar spraying with these NPs under salt stress improved the quantum yield of PSII (ΦPSII) and decreased the energy losses in PSII (ΦNPQ and ΦNO), with more pronunciation at the concentration of 100 mg/L (Figure 4). The treatment of the plants with 100 mg/L NPs under salt stress led to a decrease in the ΦNO by 28% and ΦNPQ by 19%. At the same time, ΦPSII increased by 56% (Figure 4).
The dark relaxation of chlorophyll fluorescence after saturating light pulse provides information on electron flow between QA and plastoquinone (PQ) [85]. The fluorescence signals were fitted by the following two components, characterizing the two pathways of QA− reoxidation: through PQ (fast component A1 with rate constant k1) and that through oxygen-evolving complex (slow component A2 with rate constant k2). In the plants treated with NaCl alone, both constants (k1 and k2) decreased. At the same time, the A1/A2 ratio also decreased, i.e., the ratio of two pathways for QA− reoxidation was changed. The decrease of k1 (by 15%) was smaller than k2 (by 50%) (Table 1). After simultaneous treatment with NPs and NaCl, the values of k1, k2, and the A1/A2 ratio increased in comparison to the values of these parameters in plants treated with NaCl alone (Table 1).

3.4. Oxidation-Reduction Properties of P700

The impact of TiO2 NPs on the photochemical activity at physiological conditions and under salt stress was investigated by far-red-light-induced steady state oxidation of P700+ (ΔA/A) and decay times (t1 and t2) of the two components of dark reduction in P700+. The treatment of the plants with the studied concentrations of NPs (50 and 100 mg/L) led to an increase in the parameter ΔA/A, but the times t1 and t2 were not influenced (Table 2). Data about the NaCl treated plants revealed an increase in both times t1 (by 97%) and t2 (by 61%) as well as a decrease in the parameter ΔA/A (by 50%). The foliar treatment of plants with TiO2 NPs decreased the salt-induced changes caused in the parameter ΔA/A, as well as in both times t1 and t2. This protective effect was more pronounced at 100 mg/L TiO2 NPs than at 50 mg/L TiO2 NPs (Table 2).

4. Discussion

Previously, it was observed that the TiO2 NPs improved plant growth and crop productivity under unfavorable environmental conditions, including salt stress [74,79,92]. It has also been shown that TiO2 NPs increase light absorption, accelerate the transport and conversion of light energy, which further assists the protection of chloroplasts from the senescence [93]. It has been shown that the root treatment of pea plants with TiO2 lead to changes in the nutrient elements directly involved in photosynthesis (Cu, Zn, Mn, and Fe), as the Cu and Zn contents in leaves decreased, while the Mn and Fe levels increased. Furthermore, the same study also demonstrated that the defense mechanisms of pea plants to salt stress, which limits water uptake, were overcome by the photocatalytic activity of TiO2 NPs and, thus, stimulated photosynthesis. The water use efficiency was found to rise with increasing TiO2 supplementations, and the largest one was observed at 100 mg/L [72]. The same study has also proved that the catalytic properties of TiO2 NPs accelerated the photochemical phase responsible for the formation of ATP and NADPH [72]. Despite the many studies on the effects of TiO2 NPs on plants under abiotic stresses, the exact mechanisms of the photosynthetic protection are not fully known. This study reveals new data concerning the influence of TiO2 NPs on the functions of the photosynthetic apparatus under physiological conditions and salt stress.
The experimental results from the current study revealed that TiO2 NPs increase the length of roots and shoots under physiological conditions and alleviate the salt-induced inhibition of these parameters (Figure 1a). Similar effects of the TiO2 NPs on the growth parameters have been shown in moderate salinity tolerant plant species (Dracocephalum moldavica, Vicia faba, Linum usitatissimum) [78,80,94]. One reason for the beneficial influence of NPs on plant growth parameters is the improvement of the mineral nutrition and the activity of the nitrate reductase [75]. The protection of growth parameters in pea plants was better at a concentration of 100 mg/L TiO2 NPs. The stimulation of shoot length corresponds with an increased content of total chlorophylls after applying the TiO2 NPs under both physiological and stress conditions (Figure 1b). On the other hand, the NPs prevented the decrease in carotenoid content under salt stress at the higher studied concentration of NPs (100 mg/L). Our findings on the impact of TiO2 NPs on the prevention of salt-induced reduction in photosynthetic pigments are in agreement with the previous reports on Dracocephalum moldavica [80], Vicia faba [78] and Linum usitatissimum [94]. It has also been shown that the carotenoids protect thylakoid membranes from oxidative stress under high salt conditions [95,96]. Considering this role of carotenoids, it can be assumed that the prevention of carotenoid reduction after spraying with TiO2 NPs could be another reason for the alleviation of salt stress destruction.
Other important observed effects of the TiO2 NPs are the decrease in the levels of the oxidative stress markers (MDA and H2O2) and the damage of membrane integrity (EL) under salt stress (Figure 2). These effects can be explained by the modulation of ROS signaling mediated by TiO2 NPs and the activation of the biosynthesis of lipophilic antioxidants [78].
The observed negative impact of salinity on growth, leaf pigment composition, and integrity of membranes in turn causes an inhibition of functions of the photosynthetic apparatus in pea plants (Figure 3 and Figure 4 and Table 1 and Table 2). Data revealed that the NaCl treatment alone decreased the open PSII centers (qp) and their efficiency (Φexc) (Figure 3c,d). This effect may result from a decrease in the density of the photosynthetic structures and the relative size of the PQ pool [85]. Moreover, the present study, in agreement with previous investigations [85], demonstrated that salinity restricted the QA− reoxidation by PQ (Table 1). The two pathways of QA− reoxidation, by PQ and by recombination of the electrons with OEC, were influenced (i.e., constants k1 and k2, characterizing Fm decay, were reduced) (Table 1). In addition, the ratio of these two processes (A1/A2) strongly decreased due to an increase in the recombination of the electrons in QAQB− with the oxidized S2 (S3) state of the OEC. The modification of the OEC under salt stress led to a decrease in the ratio Fv/Fo (Figure 3b), corresponding to the OEC activity [97], which could result from the modification of the Mn clusters of the OEC under salt stress [22,98]. Simultaneous treatment with NaCl and TiO2 NPs prevented the decrease in parameters qp, Φexc and Fv/Fo (Figure 3b–d). At the same time, at an applied concentration of 100 mg/L TiO2 NPs under salt stress, the protection of photosynthetic function was better, which could result from better stimulation by the NPs of the QA− reoxidation by PQ as k1 increased strongly (Table 1), thus determining an improved electron transport rate (ETR) and rate of the photosynthesis (RFd) (Figure 3e,f). One of the explanations for the beneficial effects of TiO2 NPs on PSII and the photosynthetic apparatus is the observation of changes in the acceptor side of PSII. This observation may also help explain why TiO2 NPs improve photosynthesis efficiency under salt stress conditions. Improving the PSII functions under salt stress could also result from a direct effect of TiO2 NPs on protein conformation of OEC, as well as facilitating the access of Ca2− and Cl− to the complex as a result of increasing the permeability of the thylakoid membranes [99,100].
The presented data also revealed that a co-treatment with NaCl and TiO2 NPs decreased the salt-induced changes in the photochemical energy conversion of PSII (ΦPSII). The increase in the parameter ΦPSII was 32% and 46% after the application of 50 mg/L and 100 mg/L TiO2 NPs, respectively (Figure 4). The increased ΦPSII values may result from the increase in amounts of the open PSII centers (qp increased) and their efficiency (Φexc) (Figure 3c,d). The increase in the parameter ΦPSII corresponds with a decrease in energy losses (ΦNO and ΦNPQ), with the effect being more pronounced for non-regulated energy losses (ΦNO). The value of the parameter ΦNO was similar to the control plants after foliar spraying with 100 mg/L TiO2 NPs under salt stress. The decrease in the energy losses in the presence of the TiO2 NPs could be explained by the previous studies on the prevention of salt-induced changes in chlorophyll biosynthesis and the enhancement of light absorbance [99,101].
The observed oxidation-reduction changes in P700 revealed that NaCl alone inhibited PSI photochemistry (Table 2). It is assumed that the two components of P700+ decay, characterized by times t1 and t2, are related to the PSI complexes located in the stroma lamellae and grana margin, respectively [102,103]. Our data showed that a foliar spray with TiO2 NPs under salt stress alleviated the salt-induced inhibition of PSI, as ΔA/A was similar to the control plants. In addition, the experimental results revealed that a simultaneous treatment with NaCl and NPs decreased the salt-induced increase in t1 and t2. This fact suggests an impact of TiO2 NPs on both populations of PSI. The time t1 decreased relatively to the control values, indicating accelerated cyclic electron transport around PSI as a protective mechanism against photooxidation [104]. Moreover, the value of t2 was similar to the control plants, showing full protection of the PSI in the grana margin (Table 2).

5. Conclusions

In summary, the experimental results have clearly shown the protective effect of the studied concentrations of TiO2 NPs (50 and 100 mg/L) on the functions of the photosynthetic apparatus under salt stress conditions, with better protection at 100 mg/L (Figure 5). This study presents new data for the mechanisms of salt stress alleviation by TiO2 NPs, as well as establishes the optimal protective concentration of NPs. Foliar treatment with TiO2 NPs reduces the salt-induced effects on: (1) growth parameters; (2) photosynthetic pigments content; (3) MDA and H2O2 levels; (4) membrane integrity; (5) functions of the photosynthetic apparatus. The protection of the photosynthetic performance under salt stress by TiO2 NPs results from the alleviation of the interaction between QA− and PQ, the increase in the number and efficiency of open PSII centers, as well as the enhanced activity of the OEC and the cyclic electron transport around PSI. The results of the present study could contribute to providing a low-cost approach to improve the resistance of plants grown in moderate salinity soils.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/ijpb16010034/s1, Table S1: Influence of different concentrations of TiO2 NPs on the pea at physiological conditions. Figure S1: Size distribution (a) and zeta potential (b) of sonicated TiO2 NPs prepared for foliar treatment.

Author Contributions

Conceptualization, E.A.; software, E.Y., M.S. and G.R.; validation, E.A.; formal analysis, E.A.; investigation, E.Y., M.S., G.R., A.D. and E.A.; writing—original draft preparation, E.A.; writing—review and editing, E.Y., M.S., G.R. and E.A.; visualization, E.Y. and M.S.; supervision and project administration, E.A. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

Not applicable.

Data Availability Statement

Data are contained within the article and supplementary materials.

Acknowledgments

The authors thank the National Center for Biomedical Photonics D01-352/2023 (for measurements with Zetasizer Nano-Pro), which is part of the Bulgarian National Roadmap for Scientific Infrastructures 2020–2027. This study was supported by the Bulgarian Ministry of Education and Science under the National Research Programme “Young scientists and postdoctoral students” approved by PMC № 353/10.12.2020.

Conflicts of Interest

The authors declare no conflicts of interest.

Abbreviations

Chlchlorophyll
Carcarotenoids
MDAmalondialdehyde
ELelectrolyte leakage
NPsnanoparticles
PAMpulse-amplitude-modulated chlorophyll fluorescence
PSIphotosystem I
PSIIphotosystem II
OECoxygen evolving complex
Fv/Fmmaximum quantum efficiency of PSII
Fv/Foquantum yield ratio of photochemical and non-photochemical processes
qpphotochemical quenching
ΦPSIIeffective quantum yield of PSII
ΦNOnon-regulated energy loss in PSII
ΦNPQregulated energy loss in PSII
Φexcexcitation efficiency of open PSII centers
ETRelectron transport rate
k1decay rate constant for the fast component A1 of dark relaxation of chlorophyll fluorescence
k2decay rate constant for the slow component A2 of dark relaxation of chlorophyll fluorescence
t1time for the fast component A1 of dark relaxation of chlorophyll fluorescence
t2time for the slow component A2 of dark relaxation of chlorophyll fluorescence
RFdchlorophyll fluorescence decay ratio
A1/A2the ratio of two pathways for QA− re-oxidation
∆A/Aphoto-oxidation of P700+

References

  1. Isayenkov, S.V.; Maathuis, F.J.M. Plant salinity stress: Many unanswered questions remain. Front. Plant Sci. 2019, 10, 80. [Google Scholar] [CrossRef] [PubMed]
  2. Kumar, S.; Li, G.; Yang, J.; Huang, X.; Ji, Q.; Liu, Z.; Ke, W.; Hou, H. Effect of salt stress on growth, physiological parameters, and ionic concentration of water dropwort (Oenanthe javanica) cultivars. Front. Plant Sci. 2021, 12, 660409. [Google Scholar] [CrossRef] [PubMed]
  3. Munawar, W.; Hameed, A.; Khan, M.K.R. Differential morphophysiological and biochemical responses of cotton genotypes under various salinity stress levels during early growth stage. Front. Plant Sci. 2021, 12, 622309. [Google Scholar] [CrossRef] [PubMed]
  4. Stefanov, M.A.; Rashkov, G.D.; Yotsova, E.K.; Borisova, P.B.; Dobrikova, A.G.; Apostolova, E.L. Different sensitivity levels of the photosynthetic apparatus in Zea mays L. and Sorghum bicolor L. under salt Stress. Plants 2021, 10, 1469. [Google Scholar] [CrossRef]
  5. Zeeshan, M.; Lu, M.; Sehar, S.; Holford, P.; Wu, F. Comparison of biochemical, anatomical, morphological, and physiological responses to salinity stress in wheat and barley genotypes deferring in salinity tolerance. Agronomy 2020, 10, 127. [Google Scholar] [CrossRef]
  6. Hameed, A.; Ahmed, M.Z.; Hussain, T.; Aziz, I.; Ahmad, N.; Gul, B.; Nielsen, B.L. Effects of salinity stress on chloroplast structure and function. Cells 2021, 10, 2023. [Google Scholar] [CrossRef]
  7. Mitsuya, S.; Takeoka, Y.; Miyake, H. Effects of sodium chloride on foliar ultrastructure of sweet potato (Ipomoea batatas Lam.) plantlets grown under light and dark conditions in vitro. J. Plant Physiol. 2000, 157, 661–667. [Google Scholar] [CrossRef]
  8. Li, W.; Li, Q. Effect of environmental salt stress on plants and the molecular mechanism of salt stress tolerance. Int. J. Environ. Sci. Nat. Resour. 2017, 7, 555714. [Google Scholar] [CrossRef]
  9. Papadakis, I.E.; Sotiras, M.I.; Landi, M.; Ladikou, E.; Oikonomou, A.; Psychoyou, M.; Fasseas, C. Salinity alters plant’s allometry and sugar metabolism, and impairs the photosynthetic process and photosystem II efficiency in Eriobotrya japonica plants. Agrochimica 2019, 63, 27–42. [Google Scholar] [CrossRef]
  10. Stefanov, M.; Biswal, A.K.; Misra, M.; Misra, A.N.; Apostolova, E.L. Responses of Photosynthetic Apparatus to Salt Stress: Structure, Function, and Protection. In Handbook of Plant and Crop Stress, 4th ed.; Pessarakli, M., Ed.; Taylor & Francis CRC Press: New York, NY, USA, 2019; pp. 233–250. ISBN 9781351104609. [Google Scholar]
  11. Barhoumi, Z.; Djebali, W.; Chaïbi, W.; Abdelly, C.; Smaoui, A. Salt impact on photosynthesis and leaf ultrastructure of Aeluropus littoralis. J. Plant Res. 2007, 120, 529–537. [Google Scholar] [CrossRef]
  12. Muhammad, I.; Shalmani, A.; Ali, M.; Yang, Q.-H.; Ahmad, H.; Li, F.B. Mechanisms regulating the dynamics of photosynthesis under abiotic stresses. Front. Plant Sci. 2021, 11, 615942. [Google Scholar] [CrossRef] [PubMed]
  13. Ji, X.; Cheng, J.; Gong, D.; Zhao, X.; Qi, Y.; Su, Y.; Ma, W. The effect of NaCl stress on photosynthetic efficiency and lipid production in freshwater microalga—Scenedesmus obliquus XJ002. Sci. Total Environ. 2018, 633, 593–599. [Google Scholar] [CrossRef] [PubMed]
  14. Dąbrowski, P.; Baczewska, A.H.; Pawluśkiewicz, B.; Paunov, M.; Alexantrov, V.; Goltsev, V.; Kalaji, M.H. Prompt chlorophyll a fluorescence as a rapid tool for diagnostic changes in PSII structure inhibited by salt stress in Perennial ryegrass. J. Photochem. Photobiol. B. 2016, 157, 22–31. [Google Scholar] [CrossRef] [PubMed]
  15. Caruso, G.; Cavaliere, C.; Guarino, C.; Gubbiotti, R.; Foglia, P.; Laganà, A. Identification of changes in Triticum durum L. leaf proteome in response to salt stress by two-dimensional electrophoresis and MALDI-TOF mass Spectrom. Anal. Bioanal. Chem. 2008, 391, 381–390. [Google Scholar] [CrossRef]
  16. Huang, L.; Li, Z.; Liu, Q.; Pu, G.; Zhang, Y.; Li, J. Research on the adaptive mechanism of photosynthetic apparatus under salt stress: New directions to increase crop yield in saline soils. Ann. Appl. Biol. 2019, 175, 1–17. [Google Scholar] [CrossRef]
  17. Pang, Q.; Chen, S.; Dai, S.; Chen, Y.; Wang, Y.; Yan, X. Comparative proteomics of salt tolerance in Arabidopsis thaliana and Thellungiella halophila. J. Proteome Res. 2010, 9, 2584–2599. [Google Scholar] [CrossRef]
  18. Liu, Z.; Zou, L.; Chen, C.; Zhao, H.; Yan, Y.; Wang, C.; Liu, X. ITRAQ-based quantitative proteomic analysis of salt stress in Spica Prunellae. Sci. Rep. 2019, 9, 9590. [Google Scholar] [CrossRef]
  19. Ashraf, M.; Harris, P.J.C. Photosynthesis under stressful environments: An overview. Photosynthetica 2013, 51, 163–190. [Google Scholar] [CrossRef]
  20. Pandey, D.M.; Choi, I.; Yeo, U.-D. Photosystem 2-activity and thylakoid membrane polypeptides of in vitro cultured Chrysanthemum as affected by NaCl. Biol. Plant. 2009, 53, 329–333. [Google Scholar] [CrossRef]
  21. Mishra, S.K.; Subrahmanyam, D.; Singhal, G.S. Interrelationship between salt and light stress on primary processes of photosynthesis. J. Plant Physiol. 1991, 138, 92–96. [Google Scholar] [CrossRef]
  22. Rashkov, G.D.; Stefanov, M.A.; Yotsova, E.K.; Borisova, P.B.; Dobrikova, A.G.; Apostolova, E.L. Exploring nitric oxide as a regulator in salt tolerance: Insights into photosynthetic efficiency in maize. Plants 2024, 13, 1312. [Google Scholar] [CrossRef] [PubMed]
  23. Stefanov, M.A.; Rashkov, G.D.; Borisova, P.B.; Apostolova, E.L. Changes in photosystem II complex and physiological activities in pea and maize plants in response to salt stress. Plants 2024, 13, 1025. [Google Scholar] [CrossRef] [PubMed]
  24. Bora, K.A.; Hashmi, S.; Zulfiqar, F.; Abideen, Z.; Ali, H.; Siddiqui, Z.S.; Siddique, K.H.M. Recent progress in bio-mediated synthesis and applications of engineered nanomaterials for sustainable agriculture. Front. Plant Sci. 2022, 13, 999505. [Google Scholar] [CrossRef]
  25. Singh, S.P.; Keswani, C.; Minkina, T.; Ortiz, A.; Sansinenea, E. Nano-inputs: A next-generation solution for sustainable crop production. J. Plant Growth Regul. 2023, 42, 5311–5324. [Google Scholar] [CrossRef]
  26. Dilnawaz, F.; Kalaji, M.H.; Misra, A.N. Nanotechnology in improving photosynthesis under adverse climatic conditions: Cell to Canopy action. Plant Nano Biol. 2023, 4, 100035. [Google Scholar] [CrossRef]
  27. Rastogi, A.; Zivcak, M.; Sytar, O.; Kalaji, H.M.; He, X.; Mbarki, S.; Brestic, M. Impact of metal and metal oxide nanoparticles on plant: A critical review. Front. Chem. 2017, 5, 78. [Google Scholar] [CrossRef]
  28. Masarovičová, E.; Kráľová, K. Metal nanoparticles and plants / nanocząstki metaliczne I rośliny. Ecol. Chem. Eng. S 2013, 20, 9–22. [Google Scholar] [CrossRef]
  29. Khodakovskaya, M.V.; De Silva, K.; Biris, A.S.; Dervishi, E.; Villagarcia, H. Carbon nanotubes induce growth enhancement of tobacco cells. ACS Nano 2012, 6, 2128–2135. [Google Scholar] [CrossRef]
  30. Sheikhalipour, M.; Esmaielpour, B.; Behnamian, M.; Gohari, G.; Giglou, M.T.; Vachova, P.; Rastogi, A.; Brestic, M.; Skalicky, M. Chitosan–selenium nanoparticle (Cs–Se NP) foliar spray alleviates salt stress in bitter melon. Nanomaterials 2021, 11, 684. [Google Scholar] [CrossRef]
  31. Duhan, J.S.; Kumar, R.; Kumar, N.; Kaur, P.; Nehra, K.; Duhan, S. Nanotechnology: The new perspective in precision agriculture. Biotechnol. Rep. 2017, 15, 11–23. [Google Scholar] [CrossRef]
  32. Ding, Y.; Zhao, W.; Zhu, G.; Wang, Q.; Zhang, P.; Rui, Y. Recent trends in foliar nanofertilizers: A review. Nanomaterials 2023, 13, 2906. [Google Scholar] [CrossRef] [PubMed]
  33. Nemček, L.; Šebesta, M.; Urík, M.; Bujdoš, M.; Dobročka, E.; Vávra, I. Impact of bulk ZnO, ZnO nanoparticles and dissolved Zn on early growth stages of barley—A pot experiment. Plants 2020, 9, 1365. [Google Scholar] [CrossRef] [PubMed]
  34. Singh, A.; Singh, N.B.; Afzal, S.; Singh, T.; Hussain, I. Zinc oxide nanoparticles: A review of their biological synthesis, antimicrobial activity, uptake, translocation and biotransformation in plants. J. Mater. Sci. 2018, 53, 185–201. [Google Scholar] [CrossRef]
  35. Rossi, L.; Fedenia, L.N.; Sharifan, H.; Ma, X.; Lombardini, L. Effects of foliar application of zinc sulfate and zinc nanoparticles in coffee (Coffea arabica L.) plants. Plant Physiol. Biochem. 2019, 135, 160–166. [Google Scholar] [CrossRef]
  36. Jampílek, J.; Král’Ová, K. Application of nanotechnology in agriculture and food industry, its prospects and risks. Ecol. Chem. Eng. S 2015, 22, 321–361. [Google Scholar] [CrossRef]
  37. Hussain, A.; Ali, S.; Rizwan, M.; Zia ur Rehman, M.; Javed, M.R.; Imran, M.; Chatha, S.A.S.; Nazir, R. Zinc oxide nanoparticles alter the wheat physiological response and reduce the cadmium uptake by plants. Environ. Pollut. 2018, 242, 1518–1526. [Google Scholar] [CrossRef]
  38. Shafiq, T.; Yasmin, H.; Shah, Z.A.; Nosheen, A.; Ahmad, P.; Kaushik, P.; Ahmad, A. Titanium oxide and zinc oxide nanoparticles in combination with cadmium tolerant Bacillus pumilus ameliorates the cadmium toxicity in maize. Antioxidants 2022, 11, 2156. [Google Scholar] [CrossRef]
  39. Mahawar, L.; Živčák, M.; Barboricova, M.; Kovár, M.; Filaček, A.; Ferencova, J.; Vysoká, D.M.; Brestič, M. Effect of copper oxide and zinc oxide nanoparticles on photosynthesis and physiology of Raphanus sativus L. under salinity stress. Plant Physiol. Biochem. 2024, 206, 108281. [Google Scholar] [CrossRef]
  40. Faraz, A.; Faizan, M.; Hayat, S.; Alam, P. Foliar application of copper oxide nanoparticles increases the photosynthetic efficiency and antioxidant activity in Brassica juncea. J. Food Qual. 2022, 2022, 5535100. [Google Scholar] [CrossRef]
  41. Pérez-Labrada, F.; López-Vargas, E.R.; Ortega-Ortiz, H.; Cadenas-Pliego, G.; Benavides-Mendoza, A.; Juárez-Maldonado, A. Responses of tomato plants under saline stress to foliar application of copper nanoparticles. Plants 2019, 8, 151. [Google Scholar] [CrossRef]
  42. Elshoky, H.A.; Yotsova, E.; Farghali, M.A.; Farroh, K.Y.; El-Sayed, K.; Elzorkany, H.E.; Rashkov, G.; Dobrikova, A.; Borisova, P.; Stefanov, M.; et al. Impact of foliar spray of zinc oxide nanoparticles on the photosynthesis of Pisum sativum L. under salt stress. Plant Physiol. Biochem. 2021, 167, 607–618. [Google Scholar] [CrossRef] [PubMed]
  43. Siddiqui, M.H.; Al-Whaibi, M.H.; Faisal, M.; Al Sahli, A.A. Nano-silicon dioxide mitigates the adverse effects of salt stress on Cucurbita pepo L. Environ. Toxicol. Chem. 2014, 33, 2429–2437. [Google Scholar] [CrossRef]
  44. Raliya, R.; Nair, R.; Chavalmane, S.; Wang, W.-N.; Biswas, P. Mechanistic evaluation of translocation and physiological impact of titanium dioxide and zinc oxide nanoparticles on the tomato (Solanum lycopersicum L.) plant. Metallomics 2015, 7, 1584–1594. [Google Scholar] [CrossRef]
  45. Du, W.; Tan, W.; Peralta-Videa, J.R.; Gardea-Torresdey, J.L.; Ji, R.; Yin, Y.; Guo, H. Interaction of metal oxide nanoparticles with higher terrestrial plants: Physiological and biochemical aspects. Plant Physiol. Biochem. 2017, 110, 210–225. [Google Scholar] [CrossRef]
  46. Jampílek, J.; Kráľová, K. Impact of Nanoparticles on Photosynthesizing Organisms and Their Use in Hybrid Structures with Some Components of Photosynthetic Apparatus. In Nanotechnology in the Life Sciences; Prasad, R., Ed.; Springer Nature Switzerland AG: Cham, Switzerland, 2019; ISBN 978-3-030-12495-3. [Google Scholar]
  47. Jampílek, J.; Král’ová, K. Nanomaterials for Delivery of Nutrients and Growth-Promoting Compounds to Plants. In Nanotechnology: An Agricultural Paradigm; Prasad, R., Kumar, M., Kumar, V., Eds.; Springer Nature Singapore Pte Ltd.: Singapore, 2017. [Google Scholar]
  48. Rizwan, M.; Ali, S.; Qayyum, M.F.; Ok, Y.S.; Adrees, M.; Ibrahim, M.; Zia-ur-Rehman, M.; Farid, M.; Abbas, F. Effect of metal and metal oxide nanoparticles on growth and physiology of globally important food crops: A critical review. J. Hazard. Mater. 2017, 322, 2–16. [Google Scholar] [CrossRef]
  49. Zuverza-Mena, N.; Martínez-Fernández, D.; Du, W.; Hernandez-Viezcas, J.A.; Bonilla-Bird, N.; López-Moreno, M.L.; Komárek, M.; Peralta-Videa, J.R.; Gardea-Torresdey, J.L. Exposure of engineered nanomaterials to plants: Insights into the physiological and biochemical responses-A review. Plant Physiol. Biochem. 2017, 110, 236–264. [Google Scholar] [CrossRef] [PubMed]
  50. Malea, P.; Charitonidou, K.; Sperdouli, I.; Mylona, Z.; Moustakas, M. Zinc uptake, photosynthetic efficiency and oxidative stress in the seagrass Cymodocea nodosa exposed to ZnO nanoparticles. Materials 2019, 12, 2101. [Google Scholar] [CrossRef]
  51. Bacilieri, F.S.; de Vasconcelos, A.C.P.; Lana, R.M.Q.; Mageste, J.G.; Torres, J.L.R. Titanium (Ti) in plant nutrition—A review. Aust. J. Crop Sci. 2017, 11, 382–386. [Google Scholar] [CrossRef]
  52. Chaudhary, I.; Singh, V. Titanium dioxide nanoparticles and its impact on growth, biomass and yield of agricultural crops under environmental stress: A review. Res. J. Nanosci. Nanotechnol. 2020, 10, 1–8. [Google Scholar] [CrossRef]
  53. Li, X.; Ghanizadeh, H.; Han, Z.; Wang, Q.; Li, F.; Qiu, Y.; Zhang, Y.; Chen, X.; Liu, J.; Wang, A. Metabolic profile and physiological mechanisms underlying the promoting effects of TiO2NPs on the photosynthesis and growth of tomato. Sci. Hortic. 2023, 322, 112394. [Google Scholar] [CrossRef]
  54. Higashimoto, S. Titanium-dioxide-based visible-light-sensitive photocatalysis: Mechanistic insight and applications. Catalysts 2019, 9, 201. [Google Scholar] [CrossRef]
  55. Sang, L.; Zhao, Y.; Burda, C. TiO2 Nanoparticles as functional building blocks. Chem. Rev. 2014, 114, 9283–9318. [Google Scholar] [CrossRef] [PubMed]
  56. Scott, N.R.; Chen, H.; Cui, H. Nanotechnology Applications and Implications of Agrochemicals Toward Sustainable Agriculture and Food Systems. Proc. J. Agric. Food Chem. 2018, 66, 6451–6456. [Google Scholar] [CrossRef] [PubMed]
  57. Morteza, E.; Moaveni, P.; Farahani, H.A.; Kiyani, M. Study of photosynthetic pigments changes of maize (Zea mays L.) under nano TiO2 spraying at various growth stages. Springerplus 2013, 2, 247. [Google Scholar] [CrossRef]
  58. Raliya, R.; Biswas, P.; Tarafdar, J.C. TiO2 nanoparticle biosynthesis and its physiological effect on mung bean (Vigna radiata L.). Biotechnol. Rep. 2015, 5, 22–26. [Google Scholar] [CrossRef]
  59. Kamal, R.; Mogazy, A.M. Effect of doping on TiO2 nanoparticles characteristics: Studying of fertilizing effect on cowpea plant growth and yield. J. Soil Sci. Plant Nutr. 2023, 23, 338. [Google Scholar] [CrossRef]
  60. Lyu, S.; Wei, X.; Chen, J.; Wang, C.; Wang, X.; Pan, D. Titanium as a beneficial element for crop production. Front. Plant Sci. 2017, 8, 597. [Google Scholar] [CrossRef]
  61. Mohajjel Shoja, H.; Ahmadi, L.; Kolahi, M.; Mohajel Kazemi, E. Effect of TiO2 NPs on the growth, anatomic features and biochemistry parameters of Baby sun rose (Aptenia cordifolia). Physiol. Mol. Biol. Plants 2021, 27, 2071–2081. [Google Scholar] [CrossRef]
  62. Fraceto, L.F.; Grillo, R.; de Medeiros, G.A.; Scognamiglio, V.; Rea, G.; Bartolucci, C. Nanotechnology in agriculture: Which innovation potential does it have? Front. Environ. Sci. 2016, 4, 20. [Google Scholar] [CrossRef]
  63. Khot, L.R.; Sankaran, S.; Maja, J.M.; Ehsani, R.; Schuster, E.W. Applications of nanomaterials in agricultural production and crop protection: A review. Crop Prot. 2012, 35, 64–70. [Google Scholar] [CrossRef]
  64. Farooqui, A.; Tabassum, H.; Ahmad, A.; Mabood, A.; Ahmad, A.; Zareeen Ahmad, I. Role of nanoparticles in growth and development ofplants: A review. Int. J. Pharma Bio Sci. 2016, 7, P22–P37. [Google Scholar] [CrossRef]
  65. Khodakovskaya, M.V.; Lahiani, M.H. Nanoparticles and Plants: From Toxicity to Activation of Growth. In Handbook of Nanotoxicology, Nanomedicine and Stem Cell Use in Toxicology; Sahu, S.C., Casciano, D.A., Eds.; Wiley: Hoboken, NJ, USA, 2014; pp. 121–130. [Google Scholar]
  66. Chen, H.; Seiber, J.N.; Hotze, M. ACS select on nanotechnology in food and agriculture: A perspective on implications and applications. J. Agric. Food Chem. 2014, 62, 1209–1212. [Google Scholar] [CrossRef]
  67. Owolade, O.; Ogunleti, D. Effects of titanium dioxide on the diseases, development and yield of edible cowpea. J. Plant Prot. Res. 2008, 48, 329–336. [Google Scholar] [CrossRef]
  68. Tighe-Neira, R.; Reyes-Díaz, M.; Nunes-Nesi, A.; Recio, G.; Carmona, E.; Corgne, A.; Rengel, Z.; Inostroza-Blancheteau, C. Titanium dioxide nanoparticles provoke transient increase in photosynthetic performance and differential response in antioxidant system in Raphanus sativus L. Sci. Hortic. 2020, 269, 109418. [Google Scholar] [CrossRef]
  69. Ahmad, B.; Shabbir, A.; Jaleel, H.; Khan, M.M.A.; Sadiq, Y. Efficacy of titanium dioxide nanoparticles in modulating photosynthesis, peltate glandular trichomes and essential oil production and quality in Mentha piperita L. Curr. Plant Biol. 2018, 13, 6–15. [Google Scholar] [CrossRef]
  70. Hussain, S.; Iqbal, N.; Brestic, M.; Raza, M.A.; Pang, T.; Langham, D.R.; Safdar, M.E.; Ahmed, S.; Wen, B.; Gao, Y.; et al. Changes in morphology, chlorophyll fluorescence performance and Rubisco activity of soybean in response to foliar application of ionic titanium under normal light and shade environment. Sci. Total Environ. 2019, 658, 626–637. [Google Scholar] [CrossRef]
  71. Qi, M.; Liu, Y.; Li, T. Nano-TiO2 Improve the photosynthesis of tomato leaves under mild heat stress. Biol. Trace Elem. Res. 2013, 156, 323–328. [Google Scholar] [CrossRef]
  72. Skiba, E.; Pietrzak, M.; Michlewska, S.; Gruszka, J.; Malejko, J.; Godlewska-Żyłkiewicz, B.; Wolf, W.M. Photosynthesis governed by nanoparticulate titanium dioxide. The Pisum sativum L. case study. Environ. Pollut. 2024, 340, 122735. [Google Scholar] [CrossRef]
  73. Waghmode, M.S.; Gunjal, A.B.; Mulla, J.A.; Patil, N.N.; Nawani, N.N. Studies on the titanium dioxide nanoparticles: Biosynthesis, applications and remediation. SN Appl. Sci. 2019, 1, 310. [Google Scholar] [CrossRef]
  74. Shah, T.; Latif, S.; Saeed, F.; Ali, I.; Ullah, S.; Abdullah Alsahli, A.; Jan, S.; Ahmad, P. Seed priming with titanium dioxide nanoparticles enhances seed vigor, leaf water status, and antioxidant enzyme activities in maize (Zea mays L.) under salinity stress. J. King Saud. Univ.—Sci. 2021, 33, 101207. [Google Scholar] [CrossRef]
  75. Yang, F.; Hong, F.; You, W.; Liu, C.; Gao, F.; Wu, C.; Yang, P. Influences of nano-anatase TiO2 on the nitrogen metabolism of growing spinach. Biol. Trace Elem. Res. 2006, 110, 179–190. [Google Scholar] [CrossRef] [PubMed]
  76. Mishra, V.; Mishra, R.K.; Dikshit, A.; Pandey, A.C. Interactions of nanoparticles with plants. Emerg. Technol. Manag. Crop Stress Toler. 2014, 1, 159–180. [Google Scholar] [CrossRef]
  77. Hasanpour, H.; Maali-Amir, R.; Zeinali, H. Effect of TiO2 nanoparticles on metabolic limitations to photosynthesis under cold in chickpea. Russ. J. Plant Physiol. 2015, 62, 779–787. [Google Scholar] [CrossRef]
  78. Abdel Latef, A.A.H.; Srivastava, A.K.; El-sadek, M.S.A.; Kordrostami, M.; Tran, L.S.P. Titanium dioxide nanoparticles improve growth and enhance tolerance of broad bean plants under saline soil conditions. Land Degrad. Dev. 2018, 29, 1065–1073. [Google Scholar] [CrossRef]
  79. Khan, M.N. Nano-titanium dioxide (Nano-TiO2) mitigates NaCl stress by enhancing antioxidative enzymes and accumulation of compatible solutes in tomato (Lycopersicon Esculentum Mill.). J. Plant Sci. 2016, 11, 1–11. [Google Scholar] [CrossRef]
  80. Gohari, G.; Mohammadi, A.; Akbari, A.; Panahirad, S.; Dadpour, M.R.; Fotopoulos, V.; Kimura, S. Titanium dioxide nanoparticles (TiO2 NPs) promote growth and ameliorate salinity stress effects on essential oil profile and biochemical attributes of Dracocephalum moldavica. Sci. Rep. 2020, 10, 912. [Google Scholar] [CrossRef]
  81. Jaberzadeh, A.; Moaveni, P.; Tohidi Moghadam, H.R.; Zahedi, H. Influence of bulk and nanoparticles titanium foliar application on some agronomic traits, seed gluten and starch contents of wheat subjected to water deficit stress. Not. Bot. Horti Agrobot. Cluj-Napoca 2013, 41, 201–207. [Google Scholar] [CrossRef]
  82. Morales, F.; Ancín, M.; Fakhet, D.; González-Torralba, J.; Gámez, A.L.; Seminario, A.; Soba, D.; Ben Mariem, S.; Garriga, M.; Aranjuelo, I. Photosynthetic metabolism under stressful growth conditions as a bases for crop Breeding and yield improvement. Plants 2020, 9, 88. [Google Scholar] [CrossRef]
  83. Baslam, M.; Mitsui, T.; Hodges, M.; Priesack, E.; Herritt, M.T.; Aranjuelo, I.; Sanz-Sáez, Á. Photosynthesis in a changing global climate: Scaling up and scaling down in crops. Front. Plant Sci. 2020, 11, 882. [Google Scholar] [CrossRef]
  84. Grieve, C.M.; Grattan, S.R.; Maas, E.V. Plant Salt Tolerance. In Agricultural Salinity Assessment and Management; Wallender, W.W., Tanji, K.K., Eds.; American Society of Civil Engineers: Reston, VA, USA, 2011; pp. 405–459. [Google Scholar]
  85. Stefanov, M.A.; Rashkov, G.D.; Apostolova, E.L. Assessment of the photosynthetic apparatus functions by chlorophyll fluorescence and P700 absorbance in C3 and C4 plants under physiological conditions and under salt stress. Int. J. Mol. Sci. 2022, 23, 3768. [Google Scholar] [CrossRef]
  86. Lichtenthaler, H.K. Chlorophylls and carotenoids: Pigments of photosynthetic biomembranes. Methods Enzymol. 1987, 148, 350–382. [Google Scholar] [CrossRef]
  87. Yotsova, E.K.; Dobrikova, A.G.; Stefanov, M.A.; Kouzmanova, M.; Apostolova, E.L. Improvement of the rice photosynthetic apparatus defence under cadmium stress modulated by salicylic acid supply to roots. Theor. Exp. Plant Physiol. 2018, 30, 57–70. [Google Scholar] [CrossRef]
  88. Heath, R.L.; Packer, L. Photoperoxidation in isolated chloroplasts. Arch. Biochem. Biophys. 1968, 125, 189–198. [Google Scholar] [CrossRef]
  89. Lichtenthaler, H.K.; Buschmann, C.; Knapp, M. How to correctly determine the different chlorophyll fluorescence parameters and the chlorophyll fluorescence decrease ratio RFd of leaves with the PAM fluorometer. Photosynthetica 2005, 43, 379–393. [Google Scholar] [CrossRef]
  90. Dankov, K.; Busheva, M.; Stefanov, D.; Apostolova, E.L. Relationship between the degree of carotenoid depletion and function of the photosynthetic apparatus. J. Photochem. Photobiol. B Biol. 2009, 96, 49–56. [Google Scholar] [CrossRef]
  91. Mansour, M.M.F.; Salama, K.H.A. Cellular basis of salinity tolerance in plants. Environ. Exp. Bot. 2004, 52, 113–122. [Google Scholar] [CrossRef]
  92. Lei, Z.; Mingyu, S.; Xiao, W.; Chao, L.; Chunxiang, Q.; Liang, C.; Hao, H.; Xiaoqing, L.; Fashui, H. Antioxidant stress is promoted by nano-anatase in spinach chloroplasts under UV-B radiation. Biol. Trace Elem. Res. 2008, 121, 69–79. [Google Scholar] [CrossRef]
  93. Yang, X.; Cao, C.; Erickson, L.; Hohn, K.; Maghirang, R.; Klabunde, K. Synthesis of visible-light-active TiO2-based photocatalysts by carbon and nitrogen doping. J. Catal. 2008, 260, 128–133. [Google Scholar] [CrossRef]
  94. Singh, P.; Arif, Y.; Siddiqui, H.; Sami, F.; Zaidi, R.; Azam, A.; Alam, P.; Hayat, S. Nanoparticles enhances the salinity toxicity tolerance in Linum usitatissimum L. by modulating the antioxidative enzymes, photosynthetic efficiency, redox status and cellular damage. Ecotoxicol. Environ. Saf. 2021, 213, 112020. [Google Scholar] [CrossRef]
  95. Edge, R.; McGarvey, D.J.; Truscott, T.G. The carotenoids as anti-oxidants—A review. J. Photochem. Photobiol. B Biol. 1997, 41, 189–200. [Google Scholar] [CrossRef]
  96. Stefanov, M.; Yotsova, E.; Gesheva, E.; Dimitrova, V.; Markovska, Y.; Doncheva, S.; Apostolova, E.L. Role of flavonoids and proline in the protection of photosynthetic apparatus in Paulownia under salt stress. South Afr. J. Bot. 2021, 139, 246–253. [Google Scholar] [CrossRef]
  97. Moustakas, M.; Bayçu, G.; Sperdouli, I.; Eroğlu, H.; Eleftheriou, E.P. Arbuscular mycorrhizal symbiosis enhances photosynthesis in the medicinal herb Salvia fruticosa by improving photosystem II photochemistry. Plants 2020, 9, 962. [Google Scholar] [CrossRef] [PubMed]
  98. Stefanov, M.A.; Rashkov, G.D.; Yotsova, E.K.; Dobrikova, A.G.; Apostolova, E.L. Impact of salinity on the energy transfer between pigment–protein complexes in photosynthetic apparatus, functions of the oxygen-evolving complex and photochemical activities of photosystem II and photosystem I in two Paulownia lines. Int. J. Mol. Sci. 2023, 24, 3108. [Google Scholar] [CrossRef]
  99. Trela-Makowej, A.; Orzechowska, A.; Szymańska, R. Less is more: The hormetic effect of titanium dioxide nanoparticles on plants. Sci. Total Environ. 2024, 910, 168669. [Google Scholar] [CrossRef] [PubMed]
  100. Hong, F.; Zhou, J.; Liu, C.; Yang, F.; Wu, C.; Zheng, L.; Yang, P. Effect of nano-TiO2 on photochemical reaction of chloroplasts of spinach. Biol. Trace Elem. Res. 2005, 105, 269–280. [Google Scholar] [CrossRef]
  101. Agathokleous, E.; Feng, Z.; Iavicoli, I.; Calabrese, E.J. The two faces of nanomaterials: A quantification of hormesis in algae and plants. Environ. Int. 2019, 131, 105044. [Google Scholar] [CrossRef]
  102. Albertsson, P.Å. The structure and function of the chloroplast photosynthetic membrane—A model for the domain organization. Photosynth. Res. 1995, 46, 141–149. [Google Scholar] [CrossRef]
  103. Bukhov, N.; Egorova, E.; Carpentier, R. Electron flow to photosystem I from stromal reductants in vivo: The size of the pool of stromal reductants controls the rate of electron donation to both rapidly and slowly reducing photosystem I units. Planta 2002, 215, 812–820. [Google Scholar] [CrossRef]
  104. Takahashi, S.; Milward, S.E.; Milward, D.Y.F.; Chow, W.S.; Badger, M.R. How does cyclic electron flow alleviate photoinhibition in arabidopsis? Plant Physiol. 2009, 149, 1560–1567. [Google Scholar] [CrossRef]
Ijpb 16 00034 g001
Figure 1. Influence of TiO2 NPs (50 and 100 mg/L) on the growth parameters (root and shoot lengths) in pea seedlings (Pisum sativum L. Ran 1) at physiological conditions and salt stress (100 mM). (a) The growth parameters: root (light and dark green) and shoot (yellow and orange) lengths and (b) the pigment content: Chl (light and dark green) and Car (yellow and orange). Different letters indicate significant differences between the values in the variants of the respective parameter (p < 0.05).
Figure 1. Influence of TiO2 NPs (50 and 100 mg/L) on the growth parameters (root and shoot lengths) in pea seedlings (Pisum sativum L. Ran 1) at physiological conditions and salt stress (100 mM). (a) The growth parameters: root (light and dark green) and shoot (yellow and orange) lengths and (b) the pigment content: Chl (light and dark green) and Car (yellow and orange). Different letters indicate significant differences between the values in the variants of the respective parameter (p < 0.05).
Ijpb 16 00034 g001
Ijpb 16 00034 g002
Figure 2. Influence of TiO2 NPs (50 and 100 mg/L) on pea seedlings (Pisum sativum L.) at physiological conditions and salt stress (100 mM NaCl) (a) on some stress oxidative markers: MDA (light and dark green) and H2O2 (yellow and orange) and (b) the electrolyte leakage (%). Different letters indicate significant differences between the values in the variance of the respective parameters (p < 0.05).
Figure 2. Influence of TiO2 NPs (50 and 100 mg/L) on pea seedlings (Pisum sativum L.) at physiological conditions and salt stress (100 mM NaCl) (a) on some stress oxidative markers: MDA (light and dark green) and H2O2 (yellow and orange) and (b) the electrolyte leakage (%). Different letters indicate significant differences between the values in the variance of the respective parameters (p < 0.05).
Ijpb 16 00034 g002
Ijpb 16 00034 g003
Figure 3. Influence of the TiO2 NPs (50 and 100 mg/L) on the selected chlorophyll fluorescence parameters. The maximal quantum yield in dark-adapted state—Fv/Fm (a), the ratio of photochemical to nonphotochemical processes—Fv/Fo (b), the photochemical quenching—qp (c), the excitation efficiency of open PSII centers—Φexc (d), PSII-based electron transport rate—ETR (e), and the fluorescence decay ratio after single saturated illumination—RFd (f) in pea seedlings (Pisum sativum L.) at physiological conditions and salt stress (100 mM NaCl). Different letters indicate significant differences between the values for the respective parameter (p < 0.05).
Figure 3. Influence of the TiO2 NPs (50 and 100 mg/L) on the selected chlorophyll fluorescence parameters. The maximal quantum yield in dark-adapted state—Fv/Fm (a), the ratio of photochemical to nonphotochemical processes—Fv/Fo (b), the photochemical quenching—qp (c), the excitation efficiency of open PSII centers—Φexc (d), PSII-based electron transport rate—ETR (e), and the fluorescence decay ratio after single saturated illumination—RFd (f) in pea seedlings (Pisum sativum L.) at physiological conditions and salt stress (100 mM NaCl). Different letters indicate significant differences between the values for the respective parameter (p < 0.05).
Ijpb 16 00034 g003
Ijpb 16 00034 g004
Figure 4. Effects of TiO2 NPs (50 and 100 mg/L) on the chlorophyll fluorescence parameters of pea seedlings (Pisum sativum L. Ran 1) on the effective quantum yield of the photochemical energy conversion of PSII (ΦPSII), the regulated (ΦNPQ) and non-regulated (ΦNO) energy losses in PSII, at physiological conditions and salt stress (100 mM NaCl). Different letters indicate significant differences for the respective parameter (p < 0.05).
Figure 4. Effects of TiO2 NPs (50 and 100 mg/L) on the chlorophyll fluorescence parameters of pea seedlings (Pisum sativum L. Ran 1) on the effective quantum yield of the photochemical energy conversion of PSII (ΦPSII), the regulated (ΦNPQ) and non-regulated (ΦNO) energy losses in PSII, at physiological conditions and salt stress (100 mM NaCl). Different letters indicate significant differences for the respective parameter (p < 0.05).
Ijpb 16 00034 g004
Ijpb 16 00034 g005
Figure 5. Diagram of the main effects of TiO2 NPs on pea plants.
Figure 5. Diagram of the main effects of TiO2 NPs on pea plants.
Ijpb 16 00034 g005
Table 1. The effect of TiO2 NPs (50 and 100 mg/L) on the dark relaxation of chlorophyll fluorescence induced by a single saturating light pulse in the leaves of pea plants (Pisum sativum L.) at physiological conditions and salt stress (100 mM NaCl). Different letters indicate significant differences between the values in the same column (p < 0.05).
Table 1. The effect of TiO2 NPs (50 and 100 mg/L) on the dark relaxation of chlorophyll fluorescence induced by a single saturating light pulse in the leaves of pea plants (Pisum sativum L.) at physiological conditions and salt stress (100 mM NaCl). Different letters indicate significant differences between the values in the same column (p < 0.05).
Variantsk1 (s−1)k2 (s−1)A1/A2
Control2.212 ± 0.015 b0.061 ± 0.006 a7.194 ± 0.719 a
50 mg/L TiO2 NPs2.202 ± 0.066 b0.066 ± 0.006 a7.486 ± 0.746 a
100 mg/L TiO2 NPs2.293 ± 0.028 b0.073 ± 0.007 a6.992 ± 0.540 a
100 mM NaCl1.890 ± 0.021 d0.031 ± 0.009 c3.261 ± 0.288 c
50 mg/L TiO2 NPs + NaCl2.136 ± 0.056 c0.044 ± 0.004 b4.304 ± 0.250 b
100 mg/L TiO2 NPs + NaCl2.386 ± 0.029 a0.064 ± 0.023 a4.241 ± 0.131 b
Table 2. Influence of the TiO2 nanoparticles (50 and 100 mg/L) on the photooxidation of P700+ (ΔA/A x 10−3) and on the times t1 (for the fast component) and t2 (for the slow component) in pea seedlings (Pisum sativum L.) at physiological conditions and salt stress (100 mM NaCl). Different letters indicate significant differences between the values in the same column (p < 0.05).
Table 2. Influence of the TiO2 nanoparticles (50 and 100 mg/L) on the photooxidation of P700+ (ΔA/A x 10−3) and on the times t1 (for the fast component) and t2 (for the slow component) in pea seedlings (Pisum sativum L.) at physiological conditions and salt stress (100 mM NaCl). Different letters indicate significant differences between the values in the same column (p < 0.05).
Variantst1 (s)t2 (s)ΔA/A
Control1.38 ± 0.11 c10.13 ± 0.40 c11.81 ± 0.12 c
50 mg/L TiO2 NPs1.47 ± 0.06 c9.98 ± 0.28 c16.91 ± 0.19 b
100 mg/L TiO2 NPs1.52 ± 0.08 c9.856± 0.39 c15.35 ± 0.26 b
100 mM NaCl2.74 ± 0.03 a16.28 ± 0.12 a5.89 ± 0.12 e
50 mg/L TiO2 NPs + NaCl1.99 ± 0.04 b14.80 ± 0.21 b7.01 ± 0.14 d
100 mg/L TiO2 NPs + NaCl1.05 ± 0.05 d10.67 ± 0.36 c11.78 ± 0.23 c
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Yotsova, E.; Stefanov, M.; Rashkov, G.; Dobrikova, A.; Apostolova, E. Mitigating Salinity Stress in Pea Plants with Titanium Oxide Nanoparticles. Int. J. Plant Biol. 2025, 16, 34. https://doi.org/10.3390/ijpb16010034

AMA Style

Yotsova E, Stefanov M, Rashkov G, Dobrikova A, Apostolova E. Mitigating Salinity Stress in Pea Plants with Titanium Oxide Nanoparticles. International Journal of Plant Biology. 2025; 16(1):34. https://doi.org/10.3390/ijpb16010034

Chicago/Turabian Style

Yotsova, Ekaterina, Martin Stefanov, Georgi Rashkov, Anelia Dobrikova, and Emilia Apostolova. 2025. "Mitigating Salinity Stress in Pea Plants with Titanium Oxide Nanoparticles" International Journal of Plant Biology 16, no. 1: 34. https://doi.org/10.3390/ijpb16010034

APA Style

Yotsova, E., Stefanov, M., Rashkov, G., Dobrikova, A., & Apostolova, E. (2025). Mitigating Salinity Stress in Pea Plants with Titanium Oxide Nanoparticles. International Journal of Plant Biology, 16(1), 34. https://doi.org/10.3390/ijpb16010034

Article Metrics

Back to TopTop