Nano-Molybdenum is a valuable alternative to non-nano-Molybdenum fertilizers for winter wheat grown in acidic soil

doi:10.21203/rs.3.rs-3222767/v1

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Nano-Molybdenum is a valuable alternative to non-nano-Molybdenum fertilizers for winter wheat grown in acidic soil

https://doi.org/10.21203/rs.3.rs-3222767/v1

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Due to the essential role of nano-fertilizers in crop production, studies have yet to be conducted to evaluate nano-molybdenum (Mo) application on winter wheat (Triticum aestivum L.). The present study assessed the efficacy of nano-Mo on the Mo-uptake, plant growth, and winter wheat yield. Wheat was grown in the pot experiment using four experimental groups (deionized water: C, nano potassium molybdate: NMoK, potassium molybdate: MoK, and ammonium molybdate: MoA), each with six replicate samples applied-foliar three times in a 30-day interval. The results from the present findings advocated that NMoK improved Mo accumulation in seed, stomatal conductance, root dry weight, yield, and the number of spikes per pot of wheat compared with MoK. The principal component analysis (PCA) explains that 28 of 32 variables are in the positively correlated variable area, including yield parameters, photosynthetic machinery, and Mo uptake by the plant organs. The three application groups were separated, showing that NMoK had a more substantial effect on the 28 variables than MoK. Our results suggested that the nano-Mo is an adequate substitute for non-nano-Mo fertilizers when applied to winter wheat grown in acidic soil.

Agronomy

Plant Physiology and Morphology

Nanoscience

Nano-Mo

Nanotechnology

Physiology

Principal Component Analysis

staple food

Photosynthesis

Nanotechnology applications in the agricultural sectors are developing rapidly, especially in nano-fertilizers (Adisa et al., 2019). The nano-materials can be applied to large leaf surfaces to attach fertilizers and facilitate controlled delivery of targeted nutrients to promote vegetative growth, reproduction, flowering, and crop protection, thus improving crop yield and productivity (Shang et al., 2019; Bindraban et al., 2020; Zahedi et al., 2020). Activating nanoparticles (NPs) in plants can produce a variety of responses by causing electron transfer, including an increase in enzyme activity, an acceleration of ammonia production, an intensification of respiration, an increase in photosynthesis, the creation of enzymes and amino acids, and the production of carbon and nitrogen (N) nutrients in different parts of the plants (Sutulienė et al., 2021; Moussa et al., 2022a; 2022b). Additionally, the characteristics of this nano-fertilizer are an option for reducing the loss of nutrients to the broader environment caused by traditional fertilizers (Chaudhuri and Malodia, 2017; Singh et al., 2017; Kopittke et al., 2019). Previous studies suggested that the research conducted on nano-fertilizers can provide various essential micronutrients to the plants such as iron (Fe), manganese (Mn), zinc (Zn), copper (Cu), and molybdenum (Mo) (Liu and Lal, 2015). Positive impacts of nano-fertilizer reported by Dapkekar et al. (2018) indicated that the nano-Zn application enhanced grain Zn content without affecting grain yield, protein content, spikelet per spike, and thousand kernel weight of wheat. It was also reported that the nano-Mn applied as foliar promoted higher shoot and grain Mn contents, lower soil nitrate, and higher soil and shoot phosphorus (P) in T. aestivum (Dimkpa et al., 2018). The foliar nano-Cu application has beneficial effects on the accumulation of bioactive compounds in leaves, increased the antioxidant capacity [such as superoxidase dismutase (SOD) and peroxidase (POD)], carotenoid and chlorophyll contents in the leaves of Moringa oleifera Lam (Juárez-Maldonado et al., 2018). However, the effect of nano-fertilizer on plants can be more dramatic due to the high reactivity of their materials compared to non-nano fertilizers (Dimkpa et al., 2018). The nano-cerium oxide (CeO₂) application on T. aestivum did not affect biomass, yield, cerium concentration in shoots, sugar, and starch content in grains while leading to reducing the photosynthetic pigments, seed protein, and antioxidant enzyme activities upregulated (Du et al., 2015). The nano-Fe application positively influences plant growth and low-dose development by altering leaf organization and increasing the chloroplast number and grana stacking. Nano-Fe will harm plants in high doses by blocking the nutrient transfer through the xylem tissues (Yuan et al., 2018). In addition, nano-fertilizers are potentially a risk to human health and ecosystems due to their gross contamination of plant-based materials if accumulated in the plants (Larue et al., 2018).

Mo is a micronutrient essential and plays a vital role in some enzymes related to plant growth, such as nitrate reductase, xanthine dehydrogenase, aldehyde oxidase, and sulfite oxidase, to carry out redox reactions (Kaiser et al., 2005). Mo is required by plants at extremely low levels, about 0.1 mg kg^-1 dry weight critical deficiency level (Marschner, 1995). Mo deficiency in plants can interfere with growth such as yellowing and etiolating leaves, inhibit chlorophyll biosynthesis, ultra-structure, and chloroplast configuration changes abnormally, and interrupt flowering, leading to yield decreases (Agarwala et al., 1978, 1979; Sun et al., 2009; Yu et al., 2005, 2006). Conversely, Mo supplementation in Mo-deficient soils can increase plant growth and maximize” plant biomass production, chlorophyll content, grain yield, and Mo uptake by the different plant organs (Liu et al., 2005; Tejakhod et al., 2018; Imran et al., 2019; Rana et al., 2020). However, Mo availability for plant uptake depends on pH, the concentration of adsorbing oxides, the extent of water drainage, and organic compounds found in the soil colloids (Kaiser et al., 2005).

To boost crop productivity and quality, smart agriculture must employ modern approaches such as nano-fertilizer technology. As a result, Mo nano-fertilizer is innovative and promotes demand due to cost-effectiveness. Previous studies reported that nano-Mo applications have positive impacts on plant growth and eco-physiology of Cicer arietinum (Taran et al., 2014; Taran et al., 2016; Thomas et al., 2017), Oryza sativa (Li et al., 2018; Zhang et al., 2022), pea (Sutulienė et al., 2021), and Spinacia oleracea, as well as the yield (Abbasifar et al., 2020). To the best of our knowledge, the evaluation of the application of nano-Mo on the yield of wheat has not been well-studied. Winter wheat is a globally important crop and provides the necessary calories and proteins. However, to understand and confirm the possible benefits of nano-Mo application applied to the agriculture sector, it should be to analyze their behavior and transport to the plants. Their control release for reducing the risk of nutrient leaching and helping avoid nutrient wastage could adversely affect potential environmental impacts such as soil, water systems, and non-target organism. Therefore, this study tested the hypothesis that nano-Mo might enhance Mo uptake, photosynthetic machinery, growth, wheat yield, and physiological attributes. Confirmation of this hypothesis may further highlight the potential use of nano-Mo in promoting modern sustainable agriculture to reduce environmental pollution. The study's specific objectives are to evaluate the efficiency of nano-Mo applied foliar to plant growth, yield, and Mo uptake.

2.1 Experiment setup

The experiment was carried out between October 2018 and May 2019 in a greenhouse of Huazhong Agricultural University, Wuhan, China (30°28′26″N, 114°20′51″E, and 30 m above sea level). Ten winter wheat (Triticum aestivum L.) seeds (a 97014 cultivar) were sown in pots (55 cm x 23 cm) filled with 6 kg of soils, and plants were thinned down to four after seed germination (14 days after sowing). The soil used for the study was collected from Xinzhou District, Hubei, China. The soil was acidic yellow-brown and Mo-deficient with pH 5.64 (soil-water ratio of 1:5), organic matter 15.5 g kg^-1, alkaline hydrolysis N 80.50 mg kg^-1, available phosphorus (Olsen-P) 8.11 mg kg^-1, available potassium (K) 120.63 mg kg^-1, and effective molybdenum (Mo) 0.082 mg kg^-1. The soil was air-dried, ground, and sieved through a 2-mm sieve and then weighed 6 kg out to fill each pot. Details of the treatments are explained in Table 1.

Table 1

Details of various treatments
No	Treatment	Marked
1	Spraying 10 mL deionized water (control)	Control
2	Spraying the 10 mL nano-potassium molybdate solution (nano-K₂MoO₄) with 0.50 g Mo L^-1	NMoK
3	Spraying the 10 mL bulk potassium molybdate solution (K₂MoO₄) with 0.50 g Mo L^-1	MoK
4	Spraying the 10 mL ammonium molybdate solution ((NH₄)₆Mo₇O₂₄) with 0.50 g Mo L^-1	MoA

The 0.5 g Mo L^− 1 was carried out based on a previous study (Hugar and Kurdikeri, 2000). Zhongao Nano Tech Co., Ltd kindly provided the nano-potassium molybdate (nano-K₂MoO₄) with 99.99% purity. Foliar spraying was conducted manually at 45, 75, and 105 days after planting. Each treatment replicated six times, with four plants were grown in each pot. The basic fertilizers were applied at 0.25 g N, 0.15 g P₂O₅, and 0.20 g K₂O per kg soil supplied with chemical reagents (NH₄)₂SO₄, KH₂PO₄, and KCl, respectively (Zhang et al., 2016). The modified non-Mo Arnon nutrient solution consisted of 2.86 mg L^− 1 H₃BO₃, 1.81 mg L^− 1 MnCl₂.4H₂O, 0.22 mg L^− 1 ZnSO₄·7H₂O, 0.08 mg L^− 1 CuSO₄·5H₂O, 18.35 mg L^− 1 FeNaEDTA.

The plants were irrigated two times per week (500 mL per pot) till maturity. Then, in May 2019, plants were removed from the pot and split into roots, stems, leaves, spikes, and seeds. After that, these tissues were washed with distilled water and dried at 75ºC until the weight became constant. The oven-dried samples were also used for the measurement of Mo concentration from the different parts of the plants. In addition, for each treatment, three replicate pots were used to determine gas exchange attributes and chlorophyll contents at vegetative stages, and the remaining three to measure yields and yield components of winter wheat.

2.2 Determination of gas exchange attributes

The top three or four leaves of the wheat plants were selected one week after the third Mo application to determine the net photosynthetic rate (Pn), stomatal conductance (Gs), intercellular CO₂ concentration (Ci), and transpiration rate (Tr) measured using a portable photosynthesis system (CIRAS-3, PP-system, Amesbury, MA, USA). All measurements were conducted between 8:00 and 11:00 AM on a sunny day with a clear sky without damaging the plants.

2.3 Determination of chlorophyll contents

The chlorophyll contents (chlorophyll a, chlorophyll b, and carotenoids) were determined in the same leaf tissues as selected for gas exchange measurements described by Wu et al. (2014). The four leaves (0.25 g) were extracted by 95% alcohol, and then absorbance was measured at 665, 649, and 470 nm by a spectrophotometer (Infinite M200 PRO plate reader). Chlorophyll contents were calculated using the equations described by Arnon (1949): C_a = 13.95A₆₆₅ – 6.88A₆₄₉, C_b = 24.96A₆₄₉ – 7.32A₆₆₅, total chlorophyll = C_a + C_b, C_x.c = (100A₄₇₀ – 2.05C_a – 114.8C_b)/245. The results are expressed as mg of chlorophyll g^-1 fresh weight.

2.4 Determination of Mo content

The Mo content determined in the root, stem, leaves, spikes, and seed of wheat according to Ismael et al. (2018) and Moussa et al. (2022a) using the inductively coupled plasma mass spectroscopy (ICP-MS), EXPEC 7000 (FPI, Hangzhou, China).

2.5 Statistical analysis

Statistical analysis was carried out using SPSS version 25 (SPSS, Chicago, IL, USA). First, the one-way variance analysis (ANOVA) was carried out, followed by Duncan’s multiple range test (p < 0.05). Then, principal component analysis was computed using the PCA() function FactoMine(), computed K-means using stats(), and visualized using the factoextra() function in R Studio and Adobe Photoshop CS.

3.1. Mo uptake and accumulation

All plants sprayed with MoK and NMoK had a significantly (p < 0.05) higher Mo content across the tissues of wheat than that in control, except stem for MoK (Fig. 1). The NMoK and MoK showed similarly across the tissues. This result indicated that nano and non-nano Mo enhanced Mo uptake to wheat organs while their performance was similar.

The MoK had a higher Mo accumulation in the leaves, spikes, and seeds than in the control (Fig. 2). The NMoK increased Mo accumulation significantly (p < 0.05) across the tissues compared with the plants grown without the application of Mo treatment. Again, Mo accumulated in the seed was higher when NMoK was used in comparison to the control and MoK.

3.2. Chlorophyll content and gas exchange

All plants sprayed with MoK and NMoK had a higher content of chlorophyll a, chlorophyll b, total chlorophyll, and carotenoids than those in control (Fig. 3), and the NMoK performed similarly with the MoK. The means of gas exchange, a net photosynthesis rate, stomatal conductance, intercellular CO₂ concentration, and transpiration rate of MoK were generally like those of the control. However, nano-Mo application, NMoK significantly increased Gs and Tr by 162.7% and 49.3%, respectively, compared with the control (Fig. 4). The NMoK increased Gs significantly compared with the MoK.

3.3. Dry weights and yield components

Plants sprayed with MoK had a significantly higher dry weight in leaves and spikes than the control (Fig. 5). The NMoK provided a significantly higher dry weight of roots, stems, and leaves concerning the control. The NMoK increased the dry weight of roots compared with the MoK. Also, all plants sprayed with MoK had significantly higher yield, number of grains per pot, and harvest index than the control. The NMoK had a significantly higher yields, number of spikes per pot, number of spikes per pot, and harvest index than the control. The NMoK had a significantly higher yield and number of spikes per pot than the MoK (Table 2).

Table 2

Effects of Mo application on yield component of winter wheat (*Triticum aestivum*). C: Control, NMoK: Nano Molybdate Potassium, MoK: Potassium Molybdate, MoA: Ammonium Molybdate. *
Treatment	Yield (g pot^-1)	Thousand grains weight (g)	Number of grains per pot	Number of spikes per pot	Harvest Index (%)
C	18.32 ± 0.17c	25.33 ± 0.20a	575.67 ± 29.90b	19.67 ± 0.33b	25.74 ± 0.04b
NMoK	26.80 ± 0.55a	30.33 ± 3.64a	951.00 ± 97.17a	23.33 ± 0.33a	28.42 ± 0.50a
MoK	23.52 ± 0.09b	28.63 ± 0.99a	914.33 ± 66.68a	20.33 ± 0.33b	28.20 ± 0.49a
MoA	22.77 ± 0.16b	29.37 ± 0.26a	846.00 ± 26.95a	20.67 ± 0.67b	27.34 ± 0.25a

*: Different letters represent significant differences according to Duncan multiple range test (n = 3).

3.4. Principal component analysis

The two-dimensional score plots of the principal component analysis (PCA) demonstrated that three clusters of applications were separated, each representing NMoK, MoK, and MoA, and control, respectively (Fig. 6), indicating that NMoK had a more substantial effect on the variables. Thus, the first cluster is the three replicates for nano-Mo (NMoK), the second cluster is the three replicates for non-nano-Mo (MoK) and MoA, and the third cluster is the three replicates for control. In addition, the negatively correlated variables, i.e. Mo accumulation percentages of root (MPR), Mo accumulation percentages of stem (MPST), Mo accumulation percentages of seed (MPSE), and Mo accumulation percentages of spikes (MPSP), were on the left of the Biplot in Fig. 6 and were clearly separated from those positively correlated variables on the right of Biplot, i.e. dry weight of root (DR), dry weight of stem (DST), dry weight of leaves (DL), dry weight of spikes (DSP), yield (YIL), 1000 grains weight (TGW), number grains per pot (NGP), number spikes per pot (NSP), harvest index (HI), chlorophyll a (CLA), chlorophyll b (CLB), total chlorophyll (CLT), carotenoids (CAR), intercellular CO₂ concentration (CI), stomatal conductance (GS), net photosynthesis rate (PN), transpiration rate (TR), Mo concentration of root (MCR), Mo concentration of stem (MCST), Mo concentration of leaves (MCL), Mo concentration of spikes (MCSP), Mo concentration of seed (MCSE), Mo accumulation of root (MAR), Mo accumulation of stem (MAST), Mo accumulation of leaves (MAL), Mo accumulation of spikes (MASP), Mo accumulation of seed (MASE), and Mo accumulation percentages of leaves (MPL).

Nano fertilizer allows for precise targeting of nutrients to specific plant tissue, but we should consider concerns about their potential environmental impacts. Plants require tiny amounts of Mo, through using nanotechnology can improve nutrient absorption and utilization by plants, leading to higher crop yields and reduced fertilizer usage. Therefore, this study explored the effectiveness nano-Mo fertilizer application on winter wheat’s growth and profit. This study implied that the nano-Mo outperformed non-nano-Mo in seed Mo accumulation (Fig. 2). This may be owing to seeds acting as strong sinks for nutrients during seed growth (Bennett et al., 2011) and transport mechanisms in seeds that accelerate the movement of nano-Mo into this storage organ, resulting in increased accumulation. However, non-nano-Mo and nano-Mo performed similarly on Mo content across winter wheat tissues (Fig. 1). Our non-nano-Mo application results were consistent with earlier studies that found that non-nano-Mo applications increased the Mo content of winter wheat (Wu et al., 2017, 2018; Imran et al., 2019; Moussa et al., 2021). It might be because the soil used in the study is Mo deficient, and the Mo applications were foliar-applied (Steiner et al., 2018).

Mo is essential for the action of N-metabolizing enzymes; therefore, a sufficient supply of Mo can improve N uptake and assimilation (Alam et al., 2015), enhancing growth performance. This study showed that the nano-Mo application of winter wheat effectively improved physiological response and productivity and was superior to non-nano-Mo applications in most cases, i.e., stomatal conductance, dry weight of root, yield, and the number of spikes per pot (Figs. 4 to 5, Table 2). The previous observations of increased chlorophyll content by nano-Mo (Taran et al., 2016; Li et al., 2018; Abbasifar et al., 2020) and by non-nano-Mo (Zhang et al., 2014; Ali et al., 2019a; Chen et al., 2019a; Imran et al., 2019) reported. However, nano-Mo and non-nano-Mo performed similarly in the chlorophyll content might be due to the same response of accumulating Mo in the leaves as confirmed by the result of the Mo content and accumulation (Fig. 1–2). Thus, Mo might influence various enzymatic reactions and biochemical processes (Imran et al., 2019) that impact similar photosynthesis and stomatal functioning performance. Mo application can influence stomatal conductance through guard cell regulation and nitric oxide production mechanisms (Alamri et al., 2022). Furthermore, the nano-Mo significantly improved stomatal conductance but not the non-nano-Mo applications, which slightly disagrees with previous observations (Masi and Boselli, 2011; Qin et al., 2017; Imran et al., 2019). These results are likely due to the small samples used here and photosynthetic processes influenced by nutrients, light, temperature, and water (Yamori, 2016). Furthermore, our findings that nano-Mo increased root dry weight, yield, and the number of spikes per pot of winter wheat are consistent with previous observations of nano-Mo application in other plants (Thomas et al., 2017; Li et al., 2018; Abbasifar et al., 2020; Moussa et al., 2022a).

The observed advantage of nano-Mo in treating winter wheat may be that nanoparticles are tiny and thus can translocate Mo efficiently across the plant’s natural transportation systems (Wang et al., 2013; Karny et al., 2018), as reflected in our results of Mo accumulation in the seed (Fig. 2) and even alter photosynthesis in plants (Ali et al., 2019b; Chen et al., 2019b; Rizwan et al., 2019; Rossi et al., 2019). The nano-Mo possibly penetrated the leaf cuticle of the winter wheat, then into palisade and spongy mesophyll through the epidermis layer and finally into vascular bundles (Usman et al., 2020), affected the stomatal conductance (Fig. 4), as evidenced in substantial corrections between the relevant measures (Fig. 6). Mo has essential roles in the chlorophyll biosynthesis pathway for the photosynthetic process and in metabolic N enzymes, which correlated with chlorophyll pigment content (Yu et al., 2006; Iobbi-Nivol and Leimkuhler, 2013; Li et al., 2018; Liu et al., 2019; Abbasifar et al., 2020) as the results of chlorophyll content (Fig. 3). Chlorophyll content a and b are crucial intermediaries in plants in transforming the absorbed solar energy and activity into the process of photosynthesis and synthesis of organic substances (Pavlovic et al., 2014). Enhanced Mo quantity may elevate nitrate reductase activity (Alam et al., 2015), promoting growth and nutrient accumulation, leading to increased dry weights and grain yield (Liu et al., 2019).

The nano-Mo was superior over non-nano-Mo in dry weight of root (Fig. 5), yield, and the number of spikes per pot of winter wheat (Table 2) here could also attribute to the improved N-assimilation as a result of a simultaneous increase in the activities of the two molybdo-enzymes, xanthine dehydrogenase, and nitrate reductase (Ventura et al., 2010; Hippler et al., 2017). Besides, Mo-enhanced leaf photosynthesis may increase yield (Long et al., 2006; Ventura et al., 2010). In addition, the yield of winter wheat treated with non-nano-Mo are less than optimal might be due to non-nano-Mo does not have a large surface area, adhesives easily, and a fast mass transfer like nano-Mo so that it is unable to transmit nutrients to plants effectively (Ghormade et al., 2011). Based on the principal component analysis showing that there was a strong relationship between Mo content, Mo accumulation, chlorophyll content a and b, carotenoids, intercellular CO₂ concentration, stomatal conductance, net photosynthesis rate, transpiration rate, dry weight, and yield of winter wheat, it also confirmed the hypothesis of the current study. Among the three clusters obtained by the PCA biplot (Fig. 6), nano-Mo, located on the right of the Biplot, stood out as the most potent application for winter wheat. However, this study has some limitations, such as the fact that it was only conducted in a greenhouse, used only one level of Mo, and omitted the information value temperature. Therefore, further investigations using different amounts of nano-Mo may be essential to evaluate the accuracy of current research findings.

This study explored the effectiveness of nano-Mo fertilizer application on winter wheat’s growth and productivity. Statistically, the nano-Mo performed like non-nano-Mo application in some variables, such as Mo accumulation percentages in leaves, and the majority of chlorophyll content and gas exchange attributes be due to the soil used with Mo deficiency and only one Mo level in this study.

However, this study sheds light on the potential of nano-Mo as a valuable alternative to non-nano-Mo fertilizers for winter wheat cultivation, especially in improving Mo accumulation in seeds and enhancing various growth-related parameters, such as stomatal conductance, the dry weight of root, yield, and the number of spikes per pot.

It is essential to acknowledge the limitations of this pilot study, which was conducted in a greenhouse with a small sample size and reliant on descriptive measures. Despite these limitations, the principal component analysis supported the positive impact of nano-Mo application, as it influenced 28 out of 32 variables favorably. Further tests in different environments and with larger sample sizes are warranted to validate and expand upon these promising findings. Lastly, further studies are required to determine how nano-Mo fertilizer affects crop production economically.

Acknowledgments

We thank Dr. Songwei Wu for his critical reading of the manuscript. We thank Kailing Shou and Songlan Hao for their technical assistance. Wenhua Wei and Chengxiao Hu acknowledge support from New Zealand – China Water Research Centre. Muhamad Syaifudin acknowledges Huazhong Agricultural University for his master’s scholarship during his study.

Conflict of interest

The authors declare no conflicts of interest related to this article.

Funding

This work supported by the National Natural Science Foundation of China (Program No. 41771329), the National Key Research and Development Program of China (2016YFD0200108), and the 948 Project from the Ministry of Agriculture of China (2016-X41).

Author statement

M.S., X.S., and C.H. conceived and designed the experiment; M.S., Y.W., and M.G.M. conducted the experiment; W.W, M.G.M, M.S.R, and Y.W helped to analyze the data; M.S. wrote the manuscript; W.W., M.G.M., M.S.R., Y.W., and X.S provided statistical guidance and revised the manuscript.

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Nano-Molybdenum is a valuable alternative to non-nano-Molybdenum fertilizers for winter wheat grown in acidic soil

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Abstract

Figures

1. Introduction

2. Material and methods

2.1 Experiment setup

2.2 Determination of gas exchange attributes

2.3 Determination of chlorophyll contents

2.4 Determination of Mo content

2.5 Statistical analysis

3. Results

3.1. Mo uptake and accumulation

3.2. Chlorophyll content and gas exchange

3.3. Dry weights and yield components

3.4. Principal component analysis

4. Discussion

5. Conclusions

Declarations

References

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