Abstract
Purpose
Cadmium (Cd) is amongst the most toxic heavy metals which severely affects the plant growth. Application of nanoparticles (NPs) could be helpful to negate the deleterious impacts of Cd stress in crop plants.
Methods
In this study, seed priming of two fragrant rice cultivars, i.e., Xiangyaxiangzhan and Yuxiangyouzhan, applied with four levels of Lanthanum oxide nanoparticles (La2O3 NPs) i.e., 0, 50, 100, and 300 mg L–1, grown under three Cd levels i.e., 0, 50, and 100 mg L−1.
Result
Results revealed that the nano-priming with La2O3 significantly improved the seed germination rate under the Cd stress. Nano-priming exhibited substantial improvements in the total fresh weight, shoot length, root length, leaf sheath length and prophyll leaf length under the Cd stress. Moreover, nano-priming with La2O3 NPs substantially modulate the antioxidant activities i.e., superoxide dismutase, peroxidase, and catalase, and enhanced the α-amylase activity. Nano-priming further reduced the malondialdehyde, metallothionein, glutathione, proline, and soluble protein contents whilst enhanced the chlorophyll and carotenoids contents.
Conclusions
Seed priming with La2O3 NPs substantially enhanced the early growth of rice seedlings by improving morphological attributes and modulating the physiological and biochemical responses under Cd toxicity. The insights gained from this study may be of assistance to understand the effects of La2O3 NPs on early growth of rice, and its potential applications in enhancing the Cd tolerance of crops.
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1 Introduction
Rice is an essential food for more than four billion people worldwide which is grown all over the world under different climatic conditions (Li et al. 2021b). Among heavy metals, cadmium (Cd) is considered to be the most toxic and cause severe inhabitation of plant growth at high concentration (Kanu et al. 2019). Industrialization, excessive use of agrochemicals and other anthropogenic activities are major factors for arable land pollution with heavy metals (Rascio et al. 2008; Roberts 2014). Rice has a high bioaccumulation of numerous toxic metals, such as cadmium (Cd), lead (Pb), and arsenic (As) (Ashraf et al. 2015; Khanam et al. 2020) whereas consumption of foods of plant origin with high levels of toxic metals, especially Cd, poses a severe health risk to consumers (Clemens and Ma 2016). Rice accounted about half of the total Cd intake for those who consume rice as staple food (Wang et al. 2019). Therefore, it is essential to minimize the transfer of Cd from the environment to the plants, especially rice.
Although Cd is a non-essential element, it is readily absorbed via plant roots by competing with other divalent ions and accumulates in edible plant parts (Clemens 2001, 2006; Palmgren et al. 2008). Cd toxicity often inhibits the development of plants (Huang et al. 2020a; Rao et al. 2019). Cd could decrease rice germination, biomass, root-shoot ratio, as well as leaf growth (Ahsan et al. 2007; Song et al. 2015). Rice growth and biomass reduction is linked to Cd-toxicity-related alterations at molecular level (Lee et al. 2013; Srivastava et al. 2014). Moreover, Cd uptake in rice plants causes oxidative stress owing to excessive production of reactive oxygen species (ROS) and lipid peroxidation (Srivastava et al. 2014; Yu et al. 2013). Plants activate its antioxidant defense system to counteract the oxidative stress (Ashraf et al. 2018; Yu et al. 2013). Furthermore, Cd toxicity significantly reduces the rice germination, seed vigor, the length of radicle, and amylase activities (He et al. 2008).
Currently, nanotechnology is becoming popular due to its wide scale application and potential benefits in agriculture and recognized as a convenient tool for increasing crop yields and ensuring food security (Hussain et al. 2019; Shang et al. 2019). Due to high surface area and reactive character, as well as potent adsorption ability, the nanoparticles (NPs) could negatively impact the transport of heavy metals, pesticides, and other toxic chemicals (Deng et al. 2017; Glomstad et al. 2016; Yang and Xing 2010; Zhang et al. 2019). The application of NPs has a substantial impact on the heavy metal uptake and accumulation in plants (Rizwan et al. 2019; Singh et al. 2018). No doubt, nano-materials are well popularized in the field of science, however nano-enabled agriculture is still in its infancy (Li et al. 2021b; Pulizzi 2019; Zahedi et al. 2020).
In addition, rare earth oxide nanoparticles (REO NPs) are quite efficient due to their excellent magnetic, optical, and electronic properties (Hwang et al. 2019). Lanthanum oxide nanoparticles (La2O3 NPs) are one of the REO NPs used in agro-film, vehicle emissions cleaning, electrode materials, as well as optical fibers (Ma et al. 2011; Yue et al. 2017). Currently scientists have different opinions on whether NPs have a beneficial or harmful effect on plants, e.g., 10 mg L−1 of La2O3 NPs increased the root biomass of radish (Xiao et al. 2021). On the contrary, several studies have reported the negative impact of La2O3 NPs in plants. The elongation of root was greatly inhibited by La2O3 NPs in a variety of higher plants, including wheat, tomato, rape, lettuce, cucumber, and cabbage (Ma et al. 2010). La2O3 NPs can significantly down-regulate photosynthesis-related genes in maize. (Liu et al. 2020). Thus, NPs could have beneficial or detrimental impacts on plants depending upon plant variety, growth stage, growing environment, treatment method, and application dose (Rastogi et al. 2017).
Nano-priming is thought to be a simple method to improve early plant growth under unfavorable conditions (Mahakham et al. 2017). Previous studies reported some biotransformation and potential adverse effects of La2O3 in plants (Hwang et al. 2019), however, nano-priming with La2O3 NPs in fragrant rice under Cd stress have not yet been investigated. The present study was therefore conducted to assess the effectiveness of nano-priming with La2O3 NPs on the early growth and the related physio-biochemical attributes of fragrant rice under Cd stress, with the hypothesis that the La2O3 NPs application would alleviate Cd toxicity and improve the early growth of fragrant rice. This research may find potential applications in improving the resistance of rice against Cd toxicity.
2 Materials and Methods
2.1 Experimental Materials
Seed of two fragrant rice cultivars i.e., Xiangyaxiangzhan and Yuxiangyouzhan were obtained from College of Agriculture, South China Agricultural University, Guangzhou, China. These two varieties are commercially planted in south China and are highly popular (Gui et al. 2022). Based on the evaluation of shoot dry weight under 100 mg L−1 of Cd, Xiangyaxiangzhan and Yuxiangyouzhan are tolerant and sensitive to Cd toxcity, respectively (Li et al. 2021b). Qing et al. (2022) also reported that the 100 mg L−1 of Cd significantly reduced the total dry weight of Xiangyaxiangzhan and Yuxiangyouzhan. The La2O3 NPs (purity: 99.99%, particle size: 50 nm) were purchased from Macklin Biochemical Co. Ltd., Shanghai, China. The structural properties of La2O3 NPs were visualized under the scanning electron microscope (SEM, Sigma-500, Carl Zeiss AG, Germany). The La2O3 NPs were ranging from 27.81 to 156.66 nm and an average SEM size of 72.14 nm (Fig. 1).
2.2 Experimental Details
The experiment was conducted in September 2021 at the College of Agriculture, South China Agricultural University, Guangzhou, China. Seeds were sterilized in 5% sodium hypochlorite solution for 15 min, and thoroughly washed with deionized water. La2O3 NPs were stirred in deionized water (pH = 6.5) for 5 min before being dispersed in deionized water using a water bath and ultrasonic treatment chamber (HZS-H, China) for 30 min (Huang et al. 2020b). Seeds were subsequently immersed in solutions of varying concentrations of La2O3 NPs, i.e., 0, 50, 100, and 300 mg L−1 over-night and denoted as the LNP0, LNP50, LNP100, and LNP300, respectively, and continuously aerated for 20 h at 25 °C, and then rinsed with deionized water.
Rice seeds of uniform size were placed on filter paper in transparent culture box 13.6 × 8.6 × 4.8 cm in length, width and height, respectively, and treated with Kimura B nutrient solution (pH 4.7–4.9) as described previously (Chen et al. 2015), containing 0, 50 and 100 mg L−1 of CdCl2 denoted as Cd0, Cd50 and Cd100. The filter paper was rinsed daily with Kimura B nutrient solution containing the same concentration of CdCl2 to keep it moist and to keep the concentration of the treatment constant. The culture boxes were placed in an incubator (G&G Measurement Plant, Suzhou, Jiangsu, China) with 14/10 h light/dark period at 28/25 °C, respectively for 7 days, and the relative humidity was set at 70%. Here, the concentration of Cd and La2O3 NPs are based on previous studies (He et al. 2008; He et al. 2014; Li et al. 2021b; Xiao et al. 2021) which reported that low concentrations of lanthanum (20–100 mg L−1) had a promotive effect on rice at the early growth stages, while Cd at 100 mg L−1 caused significant reduction in rice growth. The experiment was comprised of 24 treatments with seven replicates.
2.3 Sampling and Measurements
Germination was measured at every 2 days after sowing. Seedlings were harvested after 7 days of growth for morpho-physiological traits (Li et al. 2019). Four boxes of 60 rice seedlings were randomly selected from each treatment and the samples were immediately soaked in liquid nitrogen and stored in -80 °C for physio-biochemical assays.
2.4 Determination of Germination and Morphological traits
Rice seeds are considered to have germinated when the roots break through the seed coat and extend 2 mm. Germination rate is defined as the number of germinated seeds as a percentage of the number of seeds sown (Li et al. 2021b). The germination index (GI) of each treatment were measured as described previously (Fashui et al. 2000). The seed vigor index is defined as the germination index multiplied by the shoot length (Li et al. 2014). The shoot, root, coleoptile, leaf sheath, and prophyll leaf length of five seedlings from each of six randomly selected incubators were measured at 7 days after sowing. The fresh weight was determined by an electronic balance of five seedlings from each of six randomly selected incubators. After drying for three days at 60 °C, the dry weights of each plant part were measured by an electronic balance. The shoot-to-root ratio was defined as the ratio of the dry weight of the shoot to the dry weight of the root.
2.5 Determination of Antioxidant Enzyme Activities and MDA Contents
The activities of antioxidant enzymes were quantified according to previous method (Li et al. 2019). Fresh samples (0.3 g) were taken, homogenized in 3 ml of 100 mM phosphate buffered saline (PBS) solution (pH = 7.8) and centrifuged for 15 min at 14,000 rpm at 4 °C. PBS is a water-based salt solution generally used as a solvent and protective reagent whose main components are Na2HPO4, KH2PO4, NaCl, and KCl (Drummond and Austin 2013). The supernatant was the crude enzyme extract, which was used for subsequent determination of antioxidant activities.
For superoxide dismutase (SOD) activity, the reagents were mixed in proportion (150 μL of 50 mM PBS, 30 μL of 130 mmol Met, 30 μL of 750 μmol NBT, and 30 μL of 100 μmol EDTA-Na2). An aliquot of 5 μL of enzyme extract was added with 240 μL of the reaction mixture, mixed well and added with 30 μL of 20 μmol riboflavin. The reaction was carried out for 20 min under 4000 lx light and the absorbance was read at 560 nm, using 50% inhibition as a unit of enzyme activity. The enzyme solution was replaced by PBS as a control, one in the light as a blank control. The amount of enzyme required to inhibit 50% of the NBT photoreduction reaction was taken as one enzyme activity unit (U). To detect absorbance at 560 nm, SOD activity was calculated as U g-1 FW. For peroxidase (POD) activity, 100μL of mM PBS, 95 μL of 0.2% guaiacol, 100 μL of 0.3% hydrogen peroxide (H2O2), and 5 μL enzyme solution were mixed and read at 470 nm. The absorbance was recorded every 30 s for 2.5 min. The absorbance increase of one unit per minute (U g-1 FW) was the unit of POD activity. For catalase (CAT) activity, 1.95 ml of 50 mM PBS, 1 ml of 0.3% H2O2 solution and 0.05 ml of enzyme extract was added to the sample tube. The reaction was started immediately after the addition of the enzyme extract and the absorbance value was measured at 240 nm. A decrease in A240 of 0.01 per minute was used as a unit of enzyme activity (U). CAT activity was calculated as U g-1 FW.
The MDA was quantified according to previous method (Qing et al. 2022). Fresh samples (0.1 g) of the seedlings were homogenized with 2 ml of phosphate buffer (pH = 7.8) and centrifuged at 8000 rpm for 15 min at 4 °C. The supernatant was used as the sample extract. The reaction mixture was comprised of 0.4 ml of 0.5% thiobarbituric acid and 0.2 ml of sample extract. The absorbance was read at 532, 600 and 450 nm. The content of malondialdehyde was calculated as n(µmol) = 6.45(OD532—OD600)—0.56OD450 and expressed as µmol g−1 FW.
2.6 Determination of Proline and Soluble Protein Content
The proline was quantified according to previous method (Bates et al. 1973). Fresh leaves samples (0.1 g) were homogenized with 2 ml of 3% sulfosalicylic acid solution. Supernatant (0.4 ml) was added to 0.4 ml of glacial acetic acid and 0.4 ml of 6.25 g ninhydrin dissolved in 150 ml glacial acetic acid and 100 ml of 6 mol L−1 PBS were placed in boiling water bath for to 30 min. After cooling, 0.8 ml toluene was mixed into the reaction mixture and the absorbance of the red chromophore in the toluene fraction was measured at 520 nm and the proline contents were expressed as μg g−1 FW.
The soluble protein was measured according to the method described previously (Qing et al. 2022). Fresh leaves (0.1 g) were homogenized with 2 ml of PBS and centrifuged at 4000 rpm for 20 min at 4℃. The reaction mixture contained 0.1 ml sample extract and 1 ml coomassie brilliant blue. After mixing the reaction mixture, the color development was set at 2 min at room temperature and then absorbance was read at 595 nm. The soluble protein content was expressed as μg g−1 FW.
2.7 Determination of Glutathione (GSH), Metallothionein (MT) Contents, and α-Amylase Enzyme Activity
The glutathione (GSH) content was measured according to the method described previously (Zhang et al. 2013). Fresh samples (0.1 g) were homogenized with 2 ml of 5% trichloroacetic acid and centrifuged at 13,000 rpm for 20 min at 4℃. The reaction mixture was comprised of 0.2 ml supernatant, 4.4 ml PBS, and 0.4 ml 0.04% 2-nitrobenzoic acid solution. The absorbance of the reaction mixture was read at 412 nm and the GSH contents were expressed as μg g−1 FW.
The metallothionein (MT) contents were measured according to the method described previously (Erk et al. 2002). Fresh samples (0.1 g) were homogenized with 0.5 ml of solution containing 20 μmol Tris–HCl and 0.5 μmol phenylmethylsulfonyl fluoride (pH = 8.6), and 1.5 ml of 0.01% β-mercaptoethanol and centrifuged at 13,000 rpm at 4 °C. The supernatant was heated in a water bath at 70 °C for 10 min and centrifuged. The reaction mixture for the determination of MT was comprised of 4.4 ml of demetallic solution, 0.2 ml of extraction solution and 0.4 ml of 0.04% 2-nitrobenzoic acid solution containing 0.8 mmol NaCl. The reaction was carried out at 30 °C for 30 min and the absorbance was measured at 412 nm. The MT content was calculated by following the standard curve and expressed as μmol g−1 FW.
The α-amylase activity was estimated according to the method described previously (Li et al. 2021a). Fresh samples (0.3 g) were homogenized with 3.75 ml of citric acid buffer (pH = 5.6) and centrifuged at 4000 rpm for 10 min at 4 °C. The supernatant was mixed with distilled water to a final volume of 25 ml and the resultant solution was used as enzyme extract. 1 ml of enzyme extract was heated in a water bath at 70 °C for 15 min. 1 ml of citric acid buffer (pH = 5.6) was added to the reaction mixture water bath at 40 °C for 15 min and then 4 ml of 0.4 mol L−1 NaOH was quickly added to terminate the amylase reaction. 1 ml of the reaction mixture was added with 1 ml of 3,5-dinitrosalicylic acid reagent was read at 520 nm. The α-amylase activity was expressed as mg (g 5 min)−1.
2.8 Determination of Chlorophyll and Carotenoid Contents
Fresh leaves (0.1 g) were added to 6 ml of 95% ethanol and placed in the dark at 4 °C. After 24 h, centrifugation was carried out at 5000 rpm for 10 min at 4 °C. The absorbance was recorded at 665, 649, and 470 nm, respectively (Arnon 1949). The chlorophyll and carotenoid contents were expressed as mg kg-1.
2.9 Statistical Analyses
The data were recorded in Microsoft Excel 2019 and analyzed by Statistix version 8.0 for ANOVA and multiple comparisons. The means of each treatment were compared at the least significant difference LSD test at 5% probability. Pearson correlation analysis was performed on the data using the software IBM SPSS Statistics 21. Figures were created by Origin 2021. We kept one concentration of Cd for germination analysis and growth and physiological and biochemical parameters analysis in the main text. All the experimental data were presented in the supplementary file.
3 Results
3.1 The Germination, Germination Index, and Seed Vigor index
Seed germination was affected by V, Cd, La2O3 NPs, V × La2O3 NPs, and La2O3 NPs × Cd significantly (Table 1). Cd treatments significantly reduced the germination rate by 2.41%-14.57% compared with Cd0 for both varieties (Fig. 2a, b). Nano-priming with La2O3 NPs treatments significantly improved the germination rate at 1 DAS by 13.44%, 8.60%, and 5.04% at LNP50, LNP100, and LNP300, respectively under the Cd100 treatment for Xiangyaxiangzhan (Fig. 2c). However, for Yuxiangyouzhan, all of La2O3 NPs treatments significantly decreased the germination rate at 1 DAS under the Cd100 treatment (Fig. 2c). Similarly, seed germination index and seed vigor index were affected by V, Cd, La2O3 NPs, V × La2O3 NPs, and Cd × La2O3 NPs significantly. Overall, seed priming with La2O3 NPs (LPN50 and LPN100) significantly improved the germination index, however, germination index was significantly decreased at LNP300 for Yuxiangyouzhan (Fig. 2d). For Xiangyaxiangzhan, the LNP50 and LNP100 significantly increased the seed vigor index by 29.70% and 23.17%, respectively compared with the LNP0 under the Cd0. For Yuxiangyouzhan, the LNP100 significantly improved the seed vigor index by 22.19% under the Cd50 treatment (Fig. 2e, Additional file: Table S1).
3.2 Morphological Attributes
V, Cd, La2O3 NPs, V × Cd, V × La2O3 NPs, and La2O3 NPs × Cd were significantly affected the fresh weight of shoot, root, and the total fresh weight, shoot length, root length, leaf sheath, coleoptile length, and prophyll length of rice seedlings, root and shoot dry weight, and shoot / root ratio (Table 1).
The total fresh weight significantly increased for all La2O3 NPs treatments for Xiangyaxiangzhan, and at LNP300 for Yuxiangyouzhan compared with LNP0 under Cd0. For Xiangyaxiangzhan, nano-priming significantly improved the total fresh weight by 9.78%, 33.70%, and 27.17% at the LNP50, LNP100, and LNP300, respectively, compared with LNP0 under Cd50 (Fig. 3a). The shoot fresh weight of Xiangyaxiangzhan was significantly enhanced by 9.7%, 45.96%, and 27.17% at the LNP50, LNP100, and LNP300, respectively. For Yuxiangyouzhan, the shoot fresh weight was improved by 12.08% at the LNP100 compared with the LNP0 under Cd50 (Fig. 3b). Similarly, under the Cd0 treatment, the root fresh weight was significantly enhanced by 3.27% and 14.86% at LNP100 and LNP300 for Xiangyaxiangzhan. The Cd treatment significantly reduced the root fresh weight by 47.15% and 46.80% of Xiangyaxiangzhan and Yuxiangyouzhan in non-primed seeds. The root fresh weight substantially improved at LNP100 under Cd treatment for Xiangyaxiangzhan (Fig. 3c). The root fresh weight was enhanced in Yuxiangyouzhan at the LNP100 treatment compared with LNP0 under the Cd100 (Additional file: Table S2).
Moreover, the shoot length was significantly increased by 9.24% at LNP50 under Cd0 for Xiangyaxiangzhan. Under Cd50, the shoot length increased by 3.86% and 13.77% at LNP50 and LNP100, respectively, compared with LNP0. In Yuxiangyouzhan, the LNP100 significantly improved the shoot length under Cd stress (Fig. 4a). Under the Cd50, the LNP100 increased the root length by 33.41% compared with LNP0, whereas LNP300 decreased the root length 22.27%. In Yuxiangyouzhan, the treatment of LNP and Cd had a co-inhibitory effect on root length (Fig. 4b). The coleoptile length was increased by 4.58% under Cd50, compared with the Cd0 in non-primed seeds. Compared to LNP0, the LNP100 increased the coleoptile length of Xiangyaxiangzhan by 10.47% under Cd50 (Fig. 4c). In addition, Cd treatment reduced prophyll leaf length by 22.99% compared to the Cd0. For Xiangyaxiangzhan, under Cd treatment, the LNP100 significantly increased the length of prophyll leaf by 8.39% compared with the LNP0 (Fig. 4d). Furthermore, the leaf sheath length was reduced by 22.98–31.06% under both Cd stress, compared with Cd0. On the other hand, the leaf sheath length was increased by 16.02% and 9.17%, respectively, at LNP100 compared with the LNP0 under Cd50 for both varieties (Fig. 4e, Additional file: Table S3).
For Xiangyaxiangzhan, total dry weight of seedlings was increased by 34.03%, 43.35% and 109.54% at the LNP50, LNP100 and LNP300, respectively, compared with LNP0 under Cd0. For Yuxiangyouzhan, the total dry weight was decreased by 20.84% at LNP300 under Cd0, compared with LNP0. (Fig. 5a). For Xiangyaxiangzhan, the shoot dry weight was significantly improved by 13.19% and 13.56% at LNP50 and LNP100, respectively, compared with LNP0, under Cd0. However, for Yuxiangyouzhan, nano-priming with La2O3 NPs decreased the dry weight of shoot by 12.10%-19.01%, compared with non-priming (Fig. 5b). For Xiangyaxiangzhan, the root dry weight was significantly enhanced by 84.96% and 256.39% at the LNP100 and the LNP300, respectively, compared with the LNP0 under Cd0. For Yuxiangyouzhan, the root dry weight was significantly improved by 25.92% at LNP100 under Cd50. (Fig. 5c). Furthermore, for Xiangyaxiangzhan, the shoot / root ratio was significantly increased by 247.95% at LNP300 under Cd0 whereas LNP100 significantly improved the shoot / root ratio by 94.86% under Cd50, compared with LNP0 for Yuxiangyouzhan (Fig. 5d, Additional file: Table S4).
3.3 Physio-Biochemical Attributes
3.3.1 Antioxidant Enzymes Activity
V, Cd, Cd × V, La2O3 NPs × V, Cd × La2O3 NPs and V × Cd × La2O3 NPs significantly affected the activity of SOD, POD, and CAT in shoots of rice seedlings (Table 1). The Cd100 treatment significantly reduced the SOD activity by 41.07% in Xiangyaxiangzhan compared with Cd0, whilst the SOD activity in shoots was significantly increased by 247.32% in Yuxiangyouzhan, compared with Cd0 (Additional file: Table). The La2O3 NPs treatments significantly improved the SOD activity of the shoots for Xiangyaxiangzhan, but had no significant effect for Yuxiangyouzhan under Cd0. At Cd50, the SOD activity was significantly increased by 48.75% and 21.31% at LNP50 and LNP100, respectively, compared to LNP0 (Fig. 6a). The POD activity was significantly enhanced by 78.86% under Cd50, compared with Cd0. On the other hand, the La2O3 NPs significantly reduced the POD activity, and the effect was more pronounced in Xiangyaxiangzhan. On an average, the La2O3 NPs significantly reduced the POD activity in Xiangyaxiangzhan by 16.95% under Cd50 (Fig. 6b). Under Cd50, nano-priming with La2O3 NPs significantly reduced the CAT activity in Xiangyaxiangzhan and Yuxiangyouzhan in shoots by 33.28% and 13.03%, respectively, compared with non-primed seeds (Fig. 6c). However, under Cd100, nano-priming with La2O3 NPs significantly enhanced the CAT activity by 19.52% compared with non-primed seeds (Additional file: Table S5).
3.3.2 The MDA, Proline, and Soluble Protein Contents
Individual factors and their interaction i.e., Cd, Cd × V, La2O3 NPs, La2O3 NPs × V, Cd and V × La2O3 NPs × Cd significantly affected the MDA content in shoots (Table 1). The Cd50 significantly enhanced the shoot MDA content by 16.49% for Xiangyaxiangzhan, but the MDA content was significantly decreased by 16.72% under the across Cd treatments for Yuxiangyouzhan, compared with Cd0 in non-primed seeds. For Xiangyaxiangzhan, nano-priming with La2O3 NPs significantly enhanced the MDA content. For example, the MDA content was significantly increased by 18.90% and 19.98% in LNP50 and LNP100, respectively, as compared with LNP0 under Cd0. In contrast, the MDA content was substantially reduced in Yuxiangyouzhan under La2O3 NPs nano-priming. Overall, nano-priming with La2O3 NPs reduced the MDA content by 20.63% and 18.67%, for Xiangyaxiangzhan and Yuxiangyouzhan, respectively, compared with non-priming under Cd50 (Fig. 7a).
Cd, V, La2O3 NPs, and their interaction affected the proline and protein content in shoots (Table 1). For Xiangyaxiangzhan, the proline content was significantly reduced by 16.40%, 41.68% and 11.19% at the LNP50, LNP100, and LNP300 treatment respectively, under Cd50. Under Cd100, the proline content was significantly reduced by 17.52%, 34.21% and 30.80% at the LNP50, the LNP100 and LNP300 respectively, compared with LNP0. For Yuxiangyouzhan the LNP300 significantly increased the proline content by 51.74% compared with LNP0 (Fig. 7b). Moreover, under the Cd50, the soluble protein content was significantly increased by 28.34% and 19.94% for Xiangyaxiangzhan and Yuxiangyouzhan, respectively, compared with Cd0. On the other hand, seed priming with La2O3 NPs reduced the soluble protein content up to 28.85% and 19.74%, respectively under Cd50 (Fig. 7c) whilst the soluble protein content was enhanced by nano-priming under Cd100 for Yuxiangyouzhan (Additional file: Table S6).
3.3.3 The GSH and MT Content
Nano-priming with La2O3 NPs and its interaction with Cd and V substantially affected the GSH and MT content in shoots (Table 1). The GSH content was increased by 62.23% and 142.09% at Cd 50 and Cd100 treatment, respectively, for Xiangyaxiangzhan and increased by 44.44% and 103.01%, respectively, at the Cd50 and Cd100 treatment for Yuxiangyouzhan (Fig. 8a, Additional file: Table S7). Nano-priming with La2O3 NPs significantly improved the GSH content under normal conditions whereas significantly decreased under Cd stress. For example, seed priming with LNP50 significantly reduced the GSH content by 25.04% and 26.94% compared with LNP0, for Xiangyaxiangzhan and Yuxiangyouzhan respectively, under Cd100. Furthermore, the Cd100 increased the MT content by 85.45% for Xiangyaxiangzhan whereas Cd treatments had no significant effect on Yuxiangyouzhan (Additional file: Table S7). Under Cd50, nano-priming with LNP50 reduced the MT content by 35.28% and 42.85% compared to non-priming treatment for Xiangyaxiangzhan and Yuxiangyouzhan, respectively (Fig. 8b).
3.3.4 Activity of α-Amylase Enzymes
The activity of α-amylase of shoots was significantly affected by Cd, Cd × V, La2O3 NPs, La2O3 NPs × V, and V × La2O3 NPs × Cd (Table 1). Cd treatment significantly enhanced the activity of α-amylase. For instance, the Cd100 significantly increased the α-amylase activity by 5.52% for Xiangyaxiangzhan and 7.28% for Yuxiangyouzhan compared with Cd0. Moreover, the La2O3 NPs treatments enhanced α-amylase activity at low concentrations of Cd, but at high concentrations of Cd, the nano-priming with La2O3 NPs treatments showed an inhibitory effect on α-amylase activity (Fig. 8c, Additional file: Table S7).
3.3.5 The Chlorophyll and Carotenoids Contents
The contents of chlorophyll and carotenoids was significantly affected by Cd, La2O3 NPs, La2O3 NPs × V, and V × La2O3 NPs × Cd (Table 1). Under Cd stress, the chlorophyll a, chlorophyll b and total chlorophyll content was significantly decreased for both rice cultivars and the effects were more pronounced as the Cd concentration increased. However, nano-priming with La2O3 NPs significantly improved the chlorophyll a, chlorophyll b and total chlorophyll content. In contrast, for Yuxiangyouzhan under Cd stress, the nano-priming with La2O3 NPs showed a significant inhibitory effect on the total chlorophyll a, chlorophyll b and chlorophyll content (Fig. 9a-c). Furthermore, the carotenoids content was significantly decreased for all La2O3 NPs treatments with and without Cd stress for Yuxiangyouzhan. On contrary, for Xiangyaxiangzhan, the carotenoids content was increased for nano-priming with La2O3 NPs under Cd stress (Fig. 9e, Additional file: Table S8).
3.4 Correlation Analysis
The germination rate had a significant positive correlation with the chlorophyll and MDA content. Moreover, the germination rate showed a significant and negative correlation with the SOD activity, α-amylase activity, as well as the soluble protein content. Additionally, the morphological growth attributes, i.e., the shoot fresh weight, shoot dry weight, root fresh weight, root dry weight, total fresh weight, the total dry weight, length of shoot and root, prophyll leaf length, and leaf sheath length were significantly and positively associated with the chlorophyll content but negatively associated with POD activity, proline content, and GSH content (Fig. 9).
4 Discussion
Previously, several reports have shown that the Cd stress could decrease the seed germination in plants of various species (Arezoo et al. 2015; Nabaei and Amooaghaie 2019; Kanu et al. 2019). In this study, Cd treatment showed a severe inhibitory effect on the seed gemination rate and seed vigor index of two rice varieties (Fig. 2a-e). In accordance with the present results, previous studies have demonstrated that Cd toxicity significantly reduced the seed germination attributes in rice plants because the Cd stress severely impacts the seeds metabolic pathways such as alanine, aspartate, glutamate, phenylpropanoid, taurine and hypotaurine metabolism (Li et al. 2021b).
In the present study, the shoot fresh weight, shoot dry weight, root fresh weight, root dry weight, total fresh weight, the total dry weight, length of shoot and root, prophyll leaf length, and leaf sheath length of rice seedlings were inhibited by Cd stress, and the inhibitory effects were concentration-dependent (Fig. 3, 4 and 5). Our findings were consistent with the previous study. Cd toxicity can influence the morphological growth attributes, physiological responses and protein contents of rice (Ahsan et al. 2007). In this study, the roots were significantly more inhibited than shoots, probably due to the high accumulation of Cd ions in roots as a result of direct exposure to Cd (Fig. 4a, b). Results also revealed that the Cd50 treatment significantly increased the coleoptile length (Fig. 4c). This may be a self-regulatory mechanism in rice under Cd stress, as the growth of the coleoptile helps to protect the germination and growth of the embryo and improve the plant’s resistance to stress (Morgan 1988). At the same time, the plant roots secrete large amounts of cytokinin and transport to the above-ground parts of the plant, promoting the elongation of the coleoptile and inhibiting the growth of the roots, thus enhancing the plant’s ability to transport nutrients (Munzuroglu and Zengin 2006). This may also be one of the mechanisms by which the rice responds to Cd stress.
Previous research has reported the inhibition of shoot and root growth, and biomass of rice seedlings caused by Cd (Ahsan et al. 2007; He et al. 2008), whereas nano-priming with La2O3 NPs on rice growth remains controversial. La2O3 NPs can be adsorbed to the plant surface and enter the plant as lanthanum ions through natural nano-channels or micro-scale channels (Ma et al. 2011). Lanthanum can alleviate cadmium stress in plants such as wheat and cucumber (Yang et al. 2019). Here, nano-priming with La2O3 NPs (at lower concentrations) alleviated the Cd stress on rice early growth by enhancing the morphological growth attributes, i.e., shoot and root length, prophyll leaf length, leaf sheath length, notably in the fresh weight (Fig.3). Moreover, the LNP50 and LNP100 treatments significantly improved the growth of rice seedling. Our findings were consistent with previous study which reported that low concentration of La2O3 NPs could enhance the root biomass of radish (Xiao et al. 2021). This may be due to lanthanum can mitigate cadmium-induced oxidative damage by regulating the metabolism of ascorbic acid and glutathione, thereby improving cadmium tolerance in plants (Dai et al. 2016). The positive effect of lanthanum with low concentrations were noticed, however, treatment with high concentrations had a detrimental impact on the development of the early stages of rice (Si et al. 2018). Previous research has also demonstrated the phytotoxicity of La2O3 NPs (Yue et al. 2017; Ma et al. 2011). In this study, the LNP300 treatment showed a negative impact on the root growth (Fig. 4b). La2O3 NPs can regulate genes related to cell wall and lignin synthesis, affecting the development of the cell wall and causing embolization and lignification of plant root cells and forming apoplastic barriers of root (Yue et al. 2019). This may explain the inhibition of root length under LNP300 treatment in this study. However, the formation of root apoplastic barriers may also improve the resistance to stress and reduce the uptake of harmful ions through the roots in plants. Therefore, application of La2O3 NPs at appropriate concentrations would be capable of improving the early growth of rice, while higher concentrations could result in inhibition. In summary, LNP100 treatment has a better growth promotion effect on Xiangyaxiangzhan under Cd stress.
Machinery for ROS scavenging in plants is important and necessary (Noman and Aqeel 2017). Cd impedes plant antioxidative systems as a result of enhanced ROS and MDA accumulation (Mostofa et al. 2019; Hayat et al. 2021). Typically, SOD consumes O2− through reduction reactions to produce H2O2 and O2, while the H2O2 produced by the photorespiration and the β-oxidation of fatty acids are consumed by CAT (Shah et al. 2001; Lin and Kao 2000). POD is found in the extracellular space, cell walls, cell membranes and vesicles and utilizes guaiacol as an electron donor, while using H2O2 to oxidize a variety of inorganic and organic substrates in ROS scavenging system (Li et al. 2019). In this study, Cd toxicity enhanced the SOD, POD and CAT activity in rice seedlings, indicating that Cd can cause oxidative stress and induce membrane lipid peroxidation which is in agreement with previous studies (Qing et al. 2022). Here, nano-priming with La2O3 NPs reduced the SOD, POD, and CAT activity under Cd stress (Fig. 6a-c). Correlation analysis also revealed that activity of POD showed a negative correlation significantly with the morphological growth attributes e.g., fresh weight, length, dry weight, confirming that La2O3 NPs alleviated oxidative stress and improved the seedling growth under Cd toxicity. These results revealed that the promotion effect of La2O3 NPs on the development of rice seedlings under Cd toxicity was related to the alleviation of Cd-induced oxidative stress, which can reduce the ROS production and thus reduce the activities of antioxidant enzymes. A possible explanation for this might be La and Cd probably share the same binding sites in calmodulin. By interacting with calmodulin, La can down-regulating the expression of TaNramp5 and affect Cd uptake in plant (Yang et al. 2021). It is also reported that La3+ has a higher charge than Cd2+, the greater electro-positivity allows it to compete with Cd easily for adsorption in plant tissues (Yang et al. 2019). Therefore, it seems possible that the alleviation of Cd-induced oxidative stress in this study are due to the La2O3 NPs application negatively affected the Cd accumulation in rice seedlings.
In addition to antioxidants, the content of MDA is a fundamental indicator of oxidative stress, which confers properties on inter- and intracellular membranes and therefore leads to increased ionic permeability of the cell membrane (Kong et al. 2017). GSH relieves heavy metals in plants and it can function as antioxidants in plant cells (Zhang et al. 2013). The MT is the most effective bioactive substances to scavenge ROS (Cai et al. 2019) whereas the proline and soluble proteins are osmoregulatory substances in plants that prevent disrupting the cell structure and function under heavy metal stress conditions (Ashraf et al. 2017; Ashraf and Tang 2017). In present study, Cd toxicity significantly enhanced the content of MDA, GSH, MT, proline, as well as soluble proteins in the rice seedlings (Fig. 7, 8), indicating that Cd can cause oxidative stress, quite in line with the previous studies of Cd stress in rice (Ahsan et al. 2007; Li et al. 2021b; Qing et al. 2022). Meanwhile, substantial reductions in MDA, GSH, MT, proline, and soluble proteins content were noticed in La2O3 NPs treatments under Cd stress, indicating that nano-priming with La2O3 NPs could alleviate the heavy metal stress in rice. A significant negative correlation was found between rice morphological indices and proline contents (Fig. 9) which confirms that La2O3 NPs can alleviate oxidative and osmotic stress caused by Cd stress and promote rice morphological growth. This also accords with earlier study, which showed that lanthanum decreased the MDA and proline so as to maintain normal plasmolemma permeability (Yan et al. 200720072007). On the contrary, high concentrations of La2O3 NPs significantly increased the content of MDA, proline, GSH, and MT, which indicating that the La2O3 NPs may also cause phytotoxicity, especially at higher concentrations (Fig. 7a, b, Fig. 8a, b). Therefore, optimization of the La2O3 NPs is prerequisite before its practice on large scale.
Starch is an essential energy-storing carbohydrate that participates in the growth of rice seedlings. Previous research has established that by mobilizing resources in the endosperm, α-amylases stimulates seed germination and seedling growth, while starch is immobilized under Cd stress, leading to growth suppression. (Seneviratne et al. 2019). In this study, nano-priming with La2O3 NPs substantially improved the α-amylase activity (Fig. 8c) with and without Cd stress, which could be beneficial to the metabolism of stored substances hence improving the early growth of rice.
Chlorophyll is the main pigment for photosynthesis in plants, converting light energy into chemical energy and regulating a variety of biochemical processes in plants (Sardar et al. 2022). Cd toxicity could inactive the chlorophyll-generation-related enzymes. It has previously been observed that Cd toxicity resulted in substantial reduction in chlorophyll content and stomatal conductance in plants (Chaudhary and Sharma 2009; Kilic et al. 2017). In this study, it was found that Cd could lead to an inhibitory effect of chlorophyll and carotenoids contents (Fig. 10). Previously, application of NPs such as ZnO NPs was found to affect the chlorophyll content and carotenoids content of rice (Li et al. 2021a). Here, it was noticed that application of La2O3 NPs could significantly increase the chlorophyll content for Xiangyaxiangzhan (Fig. 10a). These results corroborate the findings that La can lead to the chlorophyll protein complexes increasing which results in the improvement of chlorophyll content and the absorption of photoelectron as well as energy transport in the process of photosynthesis (Zeng et al. 2000). It is also reported that La2O3 NPs can significantly regulate the light utilization and electron transport in photosynthesis (Liu et al. 2020). In summary, we deduced that the application of La2O3 NPs can enhance the photosynthesis of rice seedling with and without Cd toxicity.
5 Conclusion
In summary, early growth of rice seedlings was inhibited under Cd toxicity. Seed priming with La2O3 NPs substantially enhanced the early growth of rice seedlings by improving morphological attributes and modulating the physiological and biochemical responses under Cd toxicity. Comparatively, the LNP100 treatment is the most effective in mitigating Cd toxicity in rice. No doubt, nano-priming of rice seeds with La2O3 NPs improved the early growth of rice under Cd toxic conditions, nevertheless, the precise mechanisms of La2O3 NPs in regulating and improving early growth of rice under Cd stress remain to be elucidated. The insights gained from this study may be of assistance to understand the effects of La2O3 NPs on early growth of rice, and its potential applications in enhancing the Cd tolerance of crops.
Data Availability
The data sets supporting the results of this article are included within the article.
Code Availability
No code.
Abbreviations
- NPs:
-
Nanoparticles
- La:
-
Lanthanum
- Cd:
-
Cadmium
- La2O3 NPs:
-
Lanthanum oxide nanoparticles
- LNP 0, LNP 50, LNP 100, and LNP 300:
-
0, 50, 100, and 300 mg L −1 La2O3 NPs
- DAS:
-
Days after sowing
- Cd 0, Cd 50, and Cd100:
-
0, 50, and 100 mg L −1 CdCl2
- SOD:
-
Superoxide dismutase
- POD:
-
Peroxidase
- CAT:
-
Catalase
- MDA:
-
Malondialdehyde
- MT:
-
Metallothionein
- GSH:
-
Glutathione
- ANOVA:
-
Analysis of variance
- Ns:
-
Nonsignificant
- SEM:
-
Scanning electron microscopy
- V:
-
Variety
References
Ahsan N, Lee SH, Lee DG, Lee H, Lee SW, Bahk JD, Lee BH (2007) Physiological and protein profiles alternation of germinating rice seedlings exposed to acute cadmium toxicity. CR Biol 330(10):735–746. https://doi.org/10.1016/j.crvi.2007.08.001
Arezoo E, Seyfollah F, Ali T (2015) The Effect of Halopriming and Salicylic Acid on the Germination of Fenugreek (Trigonella foenum-graecum) under Different Cadmium Concentrations. Notulae Scientia Biologicae 7(3). https://doi.org/10.15835/nsb739563
Arnon DI (1949) Copper Enzymes in Isolated Chloroplasts. Polyphenoloxidase in Beta Vulgaris Plant Physiology 24(1):1–15. https://doi.org/10.1104/pp.24.1.1
Ashraf U, Tang X (2017) Yield and quality responses, plant metabolism and metal distribution pattern in aromatic rice under lead (Pb) toxicity. Chemosphere 176:141–155. https://doi.org/10.1016/j.chemosphere.2017.02.103
Ashraf U, Kanu AS, Mo Z, Hussain S, Anjum SA, Khan I, Tang X (2015) Lead toxicity in rice: effects, mechanisms, and mitigation strategies a mini review. Environ Sci Pollut Res 22(23):18318–18332. https://doi.org/10.1007/s11356-015-5463-x
Ashraf U, Kanu AS, Deng Q, Mo Z, Pan S, Tian H, Tang X (2017) Lead (Pb) toxicity; physio-biochemical mechanisms, grain yield, quality, and Pb distribution proportions in scented rice. Front Plant Sci 8:259. https://doi.org/10.1016/j.ibiod.2020.104992
Ashraf U, Hussain S, Akbar N, Anjum SA, Hassan W, Tang X (2018) Water management regimes alter Pb uptake and translocation in fragrant rice. Ecotoxicol Environ Saf 149:128–134. https://doi.org/10.1016/j.ecoenv.2017.11.033
Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207. https://doi.org/10.1007/BF00018060
Cai Y, Xu W, Wang M, Chen W, Li X, Li Y, Cai Y (2019) Mechanisms and uncertainties of Zn supply on regulating rice Cd uptake. Environ Pollut 253:959–965. https://doi.org/10.1016/j.envpol.2019.07.077
Chaudhary S, Sharma YK (2009) Interactive studies of potassium and copper with cadmium on seed germination and early seedling growth in maize (Zea mays L.). J Environ Biol 30(3):427–432
Chen J, Liu X, Wang C, Yin SS, Li XL, Hu WJ, Zheng HL (2015) Nitric oxide ameliorates zinc oxide nanoparticles-induced phytotoxicity in rice seedlings. J Hazard Mater 297:173–182. https://doi.org/10.1016/j.jhazmat.2015.04.077
Clemens S (2001) Molecular mechanisms of plant metal tolerance and homeostasis. Planta 212(4):475–486. https://doi.org/10.1007/s004250000458
Clemens S (2006) Toxic metal accumulation, responses to exposure and mechanisms of tolerance in plants. Biochimie 88(11):1707–1719. https://doi.org/10.1016/j.biochi.2006.07.003
Clemens S, Ma JF (2016) Toxic Heavy Metal and Metalloid Accumulation in Crop Plants and Foods. Annu Rev Plant Biol 67(1):489–512. https://doi.org/10.1146/annurev-arplant-043015-112301
Dai H, Shan C, Zhao H, Jia G, Chen D (2016) Lanthanum improves the cadmium tolerance of Zea mays seedlings by the regulation of ascorbate and glutathione metabolism. Biologia Plantarum 61. https://doi.org/10.1007/s10535-016-0669-4
Deng Y, Eitzer B, White JC, Xing B (2017) Impact of multiwall carbon nanotubes on the accumulation and distribution of carbamazepine in collard greens (Brassica oleracea). Environ Sci Nano 4(1):149–159. https://doi.org/10.1039/C6EN00419A
Drummond I, Austin C (2013) Methods in Enzymology. In: Marshall WF (ed) Chapter Eleven - Zebrafish Cilia, vol 525. Academic Press, USA, pp 219–244
Erk M, Ivanković D, Raspor B, Pavičić J (2002) Evaluation of different purification procedures for the electrochemical quantification of mussel metallothioneins. Talanta 57(6):1211–1218. https://doi.org/10.1016/S0039-9140(02)00239-4
Fashui H, Zhenggui W, Guiwen Z (2000) Effect of lanthanum on aged seed germination of rice. Biol Trace Elem Res 75(1–3):205–213. https://doi.org/10.1385/BTER:75:1-3:205
Glomstad B, Altin D, Sørensen L, Liu J, Jenssen BM, Booth AM (2016) Carbon Nanotube Properties Influence Adsorption of Phenanthrene and Subsequent Bioavailability and Toxicity to Pseudokirchneriella subcapitata. Environmental Science Technology 50(5):2660–2668. https://doi.org/10.1021/acs.est.5b05177
Gui RF, Chen YJ, Jiang Y, Li L, Wang ZM, Pan SG, Zhang MH, Tang XR, Mo ZW (2022) Deep placement of liquid fertilizer at tillering stage influences grain quality, 2-acetyl-1-pyrroline synthesis, and antioxidant response of fragrant rice. Field Crops Res 289. https://doi.org/10.1016/j.fcr.2022.108716
Hayat K, Khan J, Khan A, Ullah S, Ali S, Salahuddin, Fu Y (2021) Ameliorative Effects of Exogenous Proline on Photosynthetic Attributes, Nutrients Uptake, and Oxidative Stresses under Cadmium in Pigeon Pea (Cajanus cajan L.). Plants 10(4). https://doi.org/10.3390/plants10040796
He JY, Ren YF, Zhu C, Jiang DA (2008) Effects of Cadmium Stress on Seed Germination, Seedling Growth and Seed Amylase Activities in Rice (Oryza sativa). Rice Sci 15(4):319–325. https://doi.org/10.1016/S1672-6308(09)60010-X
He J, Ren Y, Chen X, Chen H (2014) Protective roles of nitric oxide on seed germination and seedling growth of rice (Oryza sativa L.) under cadmium stress. Ecotoxicol Environ Saf 108:114–119. https://doi.org/10.1016/j.ecoenv.2014.05.021
Huang S, Rao G, Ashraf U, He L, Zhang Z, Zhang H, Tang X (2020a) Application of inorganic passivators reduced Cd contents in brown rice in oilseed rape-rice rotation under Cd contaminated soil. Chemosphere 259:127404. https://doi.org/10.1016/j.chemosphere.2020.127404
Huang Z, Xie W, Wang M, Liu X, Ashraf U, Qin D, Mo Z (2020b) Response of rice genotypes with differential nitrate reductase-dependent NO synthesis to melatonin under ZnO nanoparticles’ (NPs) stress. Chemosphere 250:126337. https://doi.org/10.1016/j.chemosphere.2020.126337
Hussain A, Ali S, Rizwan M, Rehman MZU, Qayyum MF, Wang H, Rinklebe J (2019) Responses of wheat (Triticum aestivum) plants grown in a Cd contaminated soil to the application of iron oxide nanoparticles. Ecotoxicol Environ Saf 173:156–164. https://doi.org/10.1016/j.ecoenv.2019.01.118
Hwang R, Chang CH, Zhu Y, Xia T (2019) Biotransformation and Potential Adverse Effects of Rare Earth Oxide Nanoparticles. In: Kumar CSSR (ed) Nanotechnology Characterization Tools for Environment, Health, and Safety. Springer, Berlin Heidelberg, pp 47–63
Kanu AS, Ashraf U, Mo Z, Sabir SUR, Baggie I, Charley CS, Tang X (2019) Calcium amendment improved the performance of fragrant rice and reduced metal uptake under cadmium toxicity. Environ Sci Pollut Res 26(24):24748–24757. https://doi.org/10.1007/s11356-019-05779-7
Khanam R, Kumar A, Nayak AK, Shahid M, Tripathi R, Vijayakumar S, Pathak H (2020) Metal(loid)s (As, Hg, Se, Pb and Cd) in paddy soil: Bioavailability and potential risk to human health. Sci Total Environ 699:134330. https://www.sciencedirect.com/science/article/pii/S0048969719343219
Kilic S, Karaboyacı M, Sencan A, Kiliç M (2017) Ecotoxicological responses of morphological and physiological parameters of cadmium-stressed maize seeds. Bangladesh J Bot 46:211–216
Kong L, Ashraf U, Cheng S, Rao G, Mo Z, Tian H, Tang X (2017) Short-term water management at early filling stage improves early-season rice performance under high temperature stress in South China. Eur J Agron 90:117–126. https://doi.org/10.1016/j.eja.2017.07.006
Lee HJ, Abdula SE, Jang DW, Park SH, Yoon UH, Jung YJ, Cho YG (2013) Overexpression of the glutamine synthetase gene modulates oxidative stress response in rice after exposure to cadmium stress. Plant Cell Rep 32(10):1521–1529. https://doi.org/10.1007/s00299-013-1464-8
Li L, Jiang JF, Li JG, Shen MC, He X, Shao HL, Dong YH (2014) Effects of cold plasma treatment on seed germination and seedling growth of soybean. Sci Rep 4(1):5859. https://doi.org/10.1038/srep05859
Li S, Jiang H, Wang J, Wang Y, Pan S, Tian H, Mo Z (2019) Responses of plant growth, physiological, gas exchange parameters of super and non-super rice to rhizosphere temperature at the tillering stage. Sci Rep 9(1):10618. https://doi.org/10.1038/s41598-019-47031-9
Li S, Liu J, Wang Y, Gao Y, Zhang Z, Xu J, Xing G (2021a) Comparative physiological and metabolomic analyses revealed that foliar spraying with zinc oxide and silica nanoparticles modulates metabolite profiles in cucumber (Cucumis sativus L.). Food Energy Secur 10(1):e269. https://doi.org/10.1002/fes3.269
Li Y, Liang L, Li W, Ashraf U, Ma L, Tang X, Mo Z (2021b) ZnO nanoparticle-based seed priming modulates early growth and enhances physio-biochemical and metabolic profiles of fragrant rice against cadmium toxicity. J Nanobiotechnol 19(1):75. https://doi.org/10.1186/s12951-021-00820-9
Lin CC, Kao CH (2000) Effect of NaCl stress on H2O2 metabolism in rice leaves. Plant Growth Regul 30(2):151–155. https://doi.org/10.1023/A:1006345126589
Liu Y, Yue L, Wang C, Zhu X, Wang Z, Xing B (2020) Photosynthetic response mechanisms in typical C3 and C4 plants upon La2O3 nanoparticle exposure. Environ Sci Nano 7(1):81–92. https://doi.org/10.1039/C9EN00992B
Ma Y, Kuang L, He X, Bai W, Ding Y, Zhang Z, Chai Z (2010) Effects of rare earth oxide nanoparticles on root elongation of plants. Chemosphere 78(3):273–279. https://doi.org/10.1016/j.chemosphere.2009.10.050
Ma Y, He X, Zhang P, Zhang Z, Guo Z, Tai R, Chai Z (2011) Phytotoxicity and biotransformation of La2O3 nanoparticles in a terrestrial plant cucumber (Cucumis sativus). Nanotoxicology 5(4):743–753. https://doi.org/10.3109/17435390.2010.545487
Mahakham W, Sarmah AK, Maensiri S, Theerakulpisut P (2017) Nanopriming technology for enhancing germination and starch metabolism of aged rice seeds using phytosynthesized silver nanoparticles. Sci Rep 7(1):8263. https://doi.org/10.1038/s41598-017-08669-5
Morgan JM (1988) The use of coleoptile responses to water stress to differentiate wheat genotypes for osmo-regulation, growth and yield. Ann Bot 62:193–198
Mostofa MG, Rahman MM, Ansary MM, Fujita M, Tran LSP (2019) Interactive Effects of Salicylic Acid and Nitric Oxide in Enhancing Rice Tolerance to Cadmium Stress. Int J Mol Sci 20(22). https://doi.org/10.3390/ijms20225798
Munzuroglu O, Zengin FK (2006) Effect of cadmium on germination, coleoptile and root growth of barley seeds in the presence of gibberellic acid and kinetin. J Environ Biol 27(4):671–677
Nabaei M, Amooaghaie R (2019) Interactive Effect of Melatonin and Sodium Nitroprusside on Seed Germination and Seedling Growth of Catharanthus roseus under Cadmium Stress. Russ J Plant Physiol 66(1):128–139. https://doi.org/10.1134/S1021443719010126
Noman A, Aqeel M (2017) miRNA-based heavy metal homeostasis and plant growth. Environ Sci Pollut Res 24(11):10068–10082. https://doi.org/10.1007/s11356-017-8593-5
Palmgren MG, Clemens S, Williams LE, Krämer U, Borg S, Schjørring JK, Sanders D (2008) Zinc biofortification of cereals: problems and solutions. Trends Plant Sci 13(9):464–473. https://doi.org/10.1016/j.tplants.2008.06.005
Pulizzi F (2019) Nano in the future of crops. Nat Nanotechnol 14(6):507–507. https://doi.org/10.1038/s41565-019-0475-1
Qing B, Jiang Y, Chen Y, Chen J, Xie H, Mo Z (2022) Nitrogen modulates early growth and physio-biochemical attributes in fragrant rice grown under cadmium and multiwall carbon nanotubes stresses. Environ Sci Pollut Res 29(45):67837–67855. https://doi.org/10.1007/s11356-022-20432-6
Rao G, Huang S, Ashraf U, Mo Z, Duan M, Pan S, Tang X (2019) Ultrasonic seed treatment improved cadmium (Cd) tolerance in Brassica napus L.. Ecotoxicol Environ Saf 185:109659. https://doi.org/10.1016/j.ecoenv.2019.109659
Rascio N, Dalla VF, La RN, Barbato R, Pagliano C, Raviolo M, Gabbrielli R (2008) Metal accumulation and damage in rice (cv. Vialone nano) seedlings exposed to cadmium. Environ Exp Bot 62(3):267–278. https://doi.org/10.1016/j.envexpbot.2007.09.002
Rastogi A, Zivcak M, Sytar O, Kalaji HM, He X, Mbarki S, Brestic M (2017) Impact of metal and metal oxide nanoparticles on plant: A Critical Review. Front Chem 5. https://www.frontiersin.org/articles/10.3389/fchem.2017.00078. Accessed 4 Jan 2023
Rizwan M, Ali S, Ali B, Adrees M, Arshad M, Hussain A, Waris AA (2019) Zinc and iron oxide nanoparticles improved the plant growth and reduced the oxidative stress and cadmium concentration in wheat. Chemosphere 214:269–277. https://doi.org/10.1016/j.chemosphere.2018.09.120
Roberts TL (2014) Cadmium and Phosphorous Fertilizers: The Issues and the Science. Procedia Engineering 83:52–59. https://doi.org/10.1016/j.proeng.2014.09.012
Sardar R, Ahmed S, Yasin NA (2022) Titanium dioxide nanoparticles mitigate cadmium toxicity in Coriandrum sativum L. through modulating antioxidant system, stress markers and reducing cadmium uptake. Environ Pollut 292(Pt A):118373. https://doi.org/10.1016/j.envpol.2021.118373
Seneviratne M, Rajakaruna N, Rizwan M, Madawala HMSP, Ok YS, Vithanage M (2019) Correction to: Heavy metal-induced oxidative stress on seed germination and seedling development: a critical review. Environ Geochem Health 41(3):1635–1635. https://doi.org/10.1007/s10653-017-0040-5
Shah K, Kumar RG, Verma S, Dubey RS (2001) Effect of cadmium on lipid peroxidation, superoxide anion generation and activities of antioxidant enzymes in growing rice seedlings. Plant Sci 161(6):1135–1144. https://doi.org/10.1016/S0168-9452(01)00517-9
Shang Y, Hasan MK, Ahammed GJ, Li M, Yin H, Zhou J (2019) Applications of Nanotechnology in Plant Growth and Crop Protection: A Review. Molecules 24(14). https://doi.org/10.3390/molecules24142558
Si Y, Wang LH, Zhou Q, Huang XH (2018) Effects of lanthanum and silicon stress on bio-sequestration of lanthanum in phytoliths in rice seedlings. Environ Sci Pollut Res 25(11):10752–10770. https://doi.org/10.1007/s11356-018-1360-4
Singh A, Prasad SM, Singh S (2018) Impact of nano ZnO on metabolic attributes and fluorescence kinetics of rice seedlings. Environ Nanotechnol Monit Manag 9:42–49. https://doi.org/10.1016/j.enmm.2017.11.006
Song WE, Chen SB, Liu JF, Chen L, Song NN, Li N, Liu B (2015) Variation of Cd concentration in various rice cultivars and derivation of cadmium toxicity thresholds for paddy soil by species-sensitivity distribution. J Integr Agric 14(9):1845–1854. https://doi.org/10.1016/S2095-3119(14)60926-6
Srivastava RK, Pandey P, Rajpoot R, Rani A, Dubey RS (2014) Cadmium and lead interactive effects on oxidative stress and antioxidative responses in rice seedlings. Protoplasma 251(5):1047–1065. https://doi.org/10.1007/s00709-014-0614-3
Wang W, Yamaji N, Ma JF (2019) Molecular Mechanism of Cadmium Accumulation in Rice. In: Himeno S, Aoshima K (eds) Cadmium Toxicity: New Aspects in Human Disease, Rice Contamination, and Cytotoxicity. Springer, Singapore, pp 115–124
Xiao Z, Yue L, Wang C, Chen F, Ding Y, Liu Y, Wang Z (2021) Downregulation of the photosynthetic machinery and carbon storage signaling pathways mediate La2O3 nanoparticle toxicity on radish taproot formation. J Hazard Mater 411:124971. https://doi.org/10.1016/j.jhazmat.2020.124971
Yan SR, Huang XH, Zhou Q (2007) Effect of Lanthanum (III) on Reactive Oxigen Metabolism of Soybean Seedlings under Supplemental UV-B Irradiation. J Rare Earths 25(3):352–358. https://doi.org/10.1016/S1002-0721(07)60435-9
Yang K, Xing B (2010) Adsorption of Organic Compounds by Carbon Nanomaterials in Aqueous Phase: Polanyi Theory and Its Application. Chem Rev 110(10):5989–6008. https://doi.org/10.1021/cr100059s
Yang H, Xu Z, Liu R et al (2019) Lanthanum reduces the cadmium accumulation by suppressing expression of transporter genes involved in cadmium uptake and translocation in wheat. Plant Soil 441(1):235–252. https://doi.org/10.1007/s11104-019-04112-y
Yang H, Xiong Z, Xu Z, Liu R (2021) Interactive Effects of Lanthanum and Calcium on Cadmium Accumulation in Wheat with Special Reference to TaNramp5 Expression Regulated by Calmodulin. J Agric Food Chem 69(24):6870–6878. https://doi.org/10.1021/acs.jafc.1c00365
Yu F, Liu K, Li M, Zhou Z, Deng H, Chen B (2013) Effects of Cadmium on Enzymatic and Non-Enzymatic Antioxidative Defenses of Rice (Oryza Sativa L.). Int J Phytoremediation 15(6):513–521. https://doi.org/10.1080/15226514.2012.702807
Yue L, Ma C, Zhan X, White JC, Xing B (2017) Molecular mechanisms of maize seedling response to La2O3 NP exposure: water uptake, aquaporin gene expression and signal transduction. Environ Sci Nano 4(4):843–855. https://doi.org/10.1039/C6EN00487C
Yue L, Chen F, Yu K, Xiao Z, Yu X, Wang Z, Xing B (2019) Early development of apoplastic barriers and molecular mechanisms in juvenile maize roots in response to La2O3 nanoparticles. Sci Total Environ 653:675–683. https://doi.org/10.1016/j.scitotenv.2018.10.320
Zahedi SM, Karimi M, Silva JAT (2020) The use of nanotechnology to increase quality and yield of fruit crops. J Sci Food Agric 100(1):25–31. https://doi.org/10.1002/jsfa.10004
Zeng F, An Y, Ren L et al (2000) Effects of lanthanum and calcium on photoelectron transport activity and the related protein complexes in chloroplast of cucumber leaves. Biol Trace Elem Res 77:83–91. https://doi.org/10.1385/BTER:77:1:83
Zhang C, Yin X, Gao K, Ge Y, Cheng W (2013) Non-protein thiols and glutathione S-transferase alleviate Cd stress and reduce root-to-shoot translocation of Cd in rice. J Plant Nutr Soil Sci 176(4):626–633. https://doi.org/10.1002/jpln.201100276
Zhang W, Long J, Li J, Zhang M, Xiao G, Ye X, Zeng H (2019) Impact of ZnO nanoparticles on Cd toxicity and bioaccumulation in rice (Oryza sativa L.). Environ Sci Pollut Res 26(22):23119–23128. https://doi.org/10.1007/s11356-019-05551-x
Acknowledgements
We gratefully acknowledge the Guangdong Provincial Key Field Research and Development Plan Project (2019B020221003), the National Natural Science Foundation of China (31971843), the Technology System of Modern Agricultural Industry in Guangdong (2020KJ105) and the Guangzhou Science and Technology Project (202103000075) for the financial support.
Funding
This study was funded by the Guangdong Provincial Key Field Research and Development Plan Project (2019B020221003), the National Natural Science Foundation of China (31971843), the Technology System of Modern Agricultural Industry in Guangdong (2020KJ105) and Guangzhou Science and Technology Project (202103000075).
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Feiyang Sun, Weifen Chen, and Yong Ren: Investigation, Data Curation, Formal analysis, Visualization, and Writing Original Draft;
Siren Cheng and Umair Ashraf: Investigation, Data Curation, Writing-Review, and Editing; Jiewen Zheng, Li Lin, and Yixian Ma: Investigation and Data Curation; Xiangru Tang and Zhaowen Mo: Project administration and Funding acquisition.
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Sun, F., Chen, W., Ren, Y. et al. Nano-Priming with La2O3 Improves Early Growth and Regulates Physio-Biochemical Mechanisms in Fragrant Rice Against Cadmium Toxicity. J Soil Sci Plant Nutr 23, 4004–4020 (2023). https://doi.org/10.1007/s42729-023-01318-z
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DOI: https://doi.org/10.1007/s42729-023-01318-z