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Effects of nano-molybdenum fertilizers on mo-inefficient winter wheat

grown in acidic soil

Article in Journal of Plant Nutrition · January 2024

DOI: 10.1080/01904167.2023.2280146

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ISSN: (Print) (Online) Journal homepage: https://www.tandfonline.com/loi/lpla20

Effects of nano-molybdenum fertilizers on mo-

inefficient winter wheat grown in acidic soil

Muhamad Syaifudin, Mohamed G. Moussa, Yiwen Wang, Muhammad Shoaib

Rana, Wenhua Wei, Chengxiao Hu & Xuecheng Sun

To cite this article: Muhamad Syaifudin, Mohamed G. Moussa, Yiwen Wang, Muhammad
Shoaib Rana, Wenhua Wei, Chengxiao Hu & Xuecheng Sun (2024) Effects of nano-molybdenum
fertilizers on mo-inefficient winter wheat grown in acidic soil, Journal of Plant Nutrition, 47:5,
762-775, DOI: 10.1080/01904167.2023.2280146

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JOURNAL OF PLANT NUTRITION
2024, VOL. 47, NO. 5, 762–775
https://doi.org/10.1080/01904167.2023.2280146

Effects of nano-molybdenum fertilizers on mo-inefficient

winter wheat grown in acidic soil
Muhamad Syaifudina,b,� , Mohamed G. Moussaa,b,c,# , Yiwen Wanga,b ,
Muhammad Shoaib Ranaa,b , Wenhua Weid , Chengxiao Hua,b , and
Xuecheng Suna,b,‡,¶
a
Microelement Research Center, College of Resources and Environment, Huazhong Agricultural University,
Wuhan, Hubei, P.R. China; bHubei Provincial Engineering Laboratory for New-Type Fertilizers, Huazhong
Agricultural University, Wuhan, P.R. China; cSoil and Water Research Department, Nuclear Research Center,
Egyptian Atomic Energy Authority, Cairo, Egypt; dDepartment of Biochemistry, School of Biomedical Sciences,
University of Otago, Dunedin, New Zealand

ABSTRACT ARTICLE HISTORY

Due to the essential role of nano-fertilizers in crop production, studies have Received 29 April 2021
yet to be conducted to evaluate nano-molybdenum (Mo) application on win­ Accepted 31 October 2023
ter wheat (Triticum aestivum L.). The present study assessed the efficacy of
KEYWORDS
nano-Mo on the Mo-uptake, plant growth, and winter wheat yield. Wheat
Nano-Mo; nanotechnology;
was grown in the pot experiment using four experimental groups (deionized photosynthesis; physiology;
water: C, nano potassium molybdate: NMoK, potassium molybdate: MoK, principal component
and ammonium molybdate: MoA), each with six replicate samples applied- analysis; staple food
foliar three times in a 30-day interval. The results revealed that NMoK
improved Mo accumulation in grains, stomatal conductance, root dry weight,
yield, and the number of spikes per pot of wheat compared with MoK.
Additionally, NMoK treatment significantly increased wheat grain yield by
46.29%, 13.94%, and 17.70% compared with C, MoK, and MoA treatments,
respectively. These results demonstrated that the nano-Mo application may
enhance Mo-inefficient wheat growth, thus, increasing its productivity under
acidic soil conditions. The principal component analysis (PCA) elucidates that
all variables reside within the positively correlated variable domain. This
encompasses parameters related to yield, photosynthetic machinery, and Mo
uptake by various plant organs. Through cluster analysis, the nano-Mo group
exhibited a more pronounced influence on the variables than the without-
Mo and non-nano-Mo groups. Based on our findings, nano-Mo could be a
suitable alternative to non-nano molybdenum fertilizers. This recommenda­
tion is particularly relevant for enhancing the growth of winter wheat crops
cultivated in acidic soil conditions.

Introduction
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

CONTACT Xuecheng Sun sxccn@mail.hzau.edu.cn Microelement Research Center, College of Resources and Environment,
Huazhong Agricultural University, Wuhan, Hubei, 430070, P.R. China.
�Current address: Research Faculty of Agriculture, Hokkaido University, Kita-9, Nishi-9, Kitaku, Sapporo 060-8589, Japan.
#
International Center for Biosaline Agriculture, ICBA, Dubai, P.O. Box 14660, United Arab Emirates.
‡
Shenzhen Institute of Nutrition and Health, Huazhong Agricultural University, Wuhan 430070, China.
¶
Shenzhen Branch, Guangdong Laboratory for Lingnan Modern Agriculture, Genome Analysis Laboratory of the Ministry of
Agriculture, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen 518000, China.
� 2023 Taylor & Francis Group, LLC
 JOURNAL OF PLANT NUTRITION 763

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, Dimkpa, and Pandey 2020; Zahedi, Karimi, and da Silva 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 (Sutulien_e et al.
2022; 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 fertil­
izers (Chaudhuri and Malodia 2017; Singh et al. 2017; Kopittke et al. 2019). Previous studies sug­
gested 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 con­
tent, 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 antioxi­
dant capacity [such as superoxidase dismutase (SOD) and peroxidase (POD)], carotenoid and
chlorophyll contents in the leaves of Moringa oleifera Lam (Ju�arez-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-fertil­
izers 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 1955). 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, Yu, Hu, and Wang 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, Hammond, and Ellis 2018; Imran et al. 2019; Rana et al. 2020). However, Mo avail­
ability 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 posi­
tive impacts on plant growth and eco-physiology of Cicer arietinum (Taran et al. 2014; Taran
et al. 2016; Thomas, Rathore, and Tarafdar 2017), Oryza sativa (Li et al. 2018; Zhang et al. 2022),
pea (Sutulien_e et al. 2022), and Spinacia oleracea, as well as the yield (Abbasifar, ValizadehKaji,
and Iravani 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
764 M. SYAIFUDIN ET AL.

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 leach­
ing 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.

Material and methods

Experiment setup
The experiment was carried out between October 2018 and May 2019 in a greenhouse at the
Micro-element Research Center, Huazhong Agricultural University, Wuhan, China (30� 280 2500 N,
114� 200 5000 E, and 30 m above sea level). Ten winter wheat (Triticum aestivum L.) seeds (97014 culti­
var) were sown in pots (55 cm � 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 adequate molyb­
denum (Mo) 0.082 mg kg−1. The soil contained 20.32% clay, 5.45% silt, and 74.23% sand, and was
classified as a light loam according to Kachinsky’s classification (Moussa et al. 2022b). The soil was
air-dried, ground, and sieved through a 2-mm sieve and then weighed 6 kg out to fill each pot.
The experimental treatments comprised four applications of Mo: without-Mo (C), nano-potas­
sium molybdate solution (nano-K2MoO4; NMoK), potassium molybdate solution (K2MoO4;
MoK), and ammonium molybdate solution ((NH4)6Mo7O24; MoA). Details of the treatments are
explained in Table 1. The 0.5 g Mo L−1 was used in this study, based on a previous study (Hugar
and Kurdikeri 2000). Zhongao Nano Tech Co., Ltd kindly provided the nano-potassium molyb­
date (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 sup­
plied 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 grains.
After that, these tissues were washed with distilled water and dried at 75 � C until the weight
became constant. The oven-dried samples were also used for the measurement of Mo concentra­
tion 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.

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 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
 JOURNAL OF PLANT NUTRITION 765

Determination of gas exchange attributes

The top three or four leaves of the wheat plants were selected one week after the third Mo appli­
cation 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.

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): Ca ¼ 13.95 A665 − 6.88 A649, Cb
¼ 24.96 A649 − 7.32 A665, total chlorophyll ¼ Ca þ Cb, Cx.c ¼ (100 A470 − 2.05 Ca − 114.8 Cb)/
245. The results are expressed as mg of chlorophyll g−1 fresh weight.

Determination of Mo content
The Mo content was determined in the root, stem, leaves, spikes, and wheat grains, according to
Ismael et al. (2018) and Moussa et al. (2022a). The dried-plant materials (300 mg) were digested
in 10 mL of HNO3/HClO4 (9:1 (v/v) at 190 � C for two h and then at 205 � C till the sample turned
white with volume of about 1 mL. Once digestion was complete, the samples were cooled, shaken,
and filtered. The filtrate was then dissolved in 50 mL of deionized water. The quantification of
Mo concentrations was analyzed using an inductively coupled plasma mass spectroscopy (ICP-
MS), EXPEC 7000; FPI, Hangzhou, China. Overall plant Mo accumulation was calculated by mul­
tiplying the dry mass by the tissue Mo concentration.

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). The principal component analysis (PCA) was performed in R studio using the
FactoMineR package (Husson, L^e, and Pag�es 2017). The cluster package was used for clustering
analysis (Maechler et al. 2022). The factoextra package was used to visualize results (Kassambara
and Mundt 2020) and was modified using Adobe Photoshop CS.

Results
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 (Figure 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 grains than in the control
(Figure 2). The NMoK increased Mo accumulation significantly (p < 0.05) across the tissues com­
pared with the plants grown without the application of Mo treatment. Again, Mo accumulated in
the grains was higher when NMoK was used in comparison to the control and MoK.
766 M. SYAIFUDIN ET AL.

Figure 1. Effects of Mo application on Mo content of winter wheat (Triticum aestivum L.). Vertical bar above indicates standard
error of three replicates. Different letters (a, b, c, etc.) represent significant differences according to Duncan multiple range test
(n ¼ 3). C: Control, NMoK: Nano Molybdate Potassium, MoK: Potassium Molybdate, MoA: Ammonium Molybdate.

Figure 2. Effects of Mo application on Mo accumulation of winter wheat (Triticum aestivum L.). Vertical bar above indicates
standard error of three replicates. Different letters (a, b, c, etc.) represent significant differences according to Duncan multiple
range test (n ¼ 3). Description of applications is mentioned in Figure 1.

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 (Figure 3), and the NMoK performed
similarly with the MoK. The means of gas exchange, Pn, Gs, Ci, and Tr 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 (Figure 4). The NMoK increased
Gs significantly compared with the MoK.
 JOURNAL OF PLANT NUTRITION 767

Figure 3. Effects of Mo application on chlorophyll content of winter wheat (Triticum aestivum L.). Vertical bar above indicates
standard error of three replicates. Different letters (a, b, c, etc.) represent significant differences according to Duncan multiple
range test (n ¼ 3). Description of applications is mentioned in Figure 1.

Figure 4. Effects of Mo application on net photosynthesis rate (Pn), stomatal conductance (Gs), intercellular CO2 concentration
(Ci), and transpiration rate (Tr) of winter wheat (Triticum aestivum L.). Vertical bar above indicates standard error of three repli­
cates. Different letters (a, b, c, etc.) represent significant differences according to Duncan multiple range test (n ¼ 3). Description
of applications is mentioned in Figure 1.

Dry weights and yield components

Plants sprayed with MoK had a significantly higher dry weight in leaves and spikes than the con­
trol (Figure 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.
768 M. SYAIFUDIN ET AL.

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).

Principal component analysis and clustering analysis

All the variables were loaded into two-dimensional score plots of the principal component ana­
lysis (PCA), explaining 74.3% of the total variance (Figure 6a). Dim1 discriminated all the varia­
bles and thus explained by the more significant proportion of variance (64.1%), while Dim2
indicated a lower proportion of variance (10.2%). According to Dim1, 27 variables had positive
loadings on this component, 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), chloro­
phyll b (CLB), total chlorophyll (CLT), carotenoids (CAR), intercellular CO2 concentration (CI),
stomatal conductance (GS), net photosynthesis rate (PN), transpiration rate (TR), Mo concentra­
tion of root (MCR), Mo concentration of stem (MCST), Mo concentration of leaves (MCL), Mo
concentration of spikes (MCSP), Mo concentration of grains (MCG), Mo accumulation of root
(MAR), Mo accumulation of stem (MAST), Mo accumulation of leaves (MAL), Mo accumulation
of spikes (MASP), and Mo accumulation of grains (MAG). Therefore, cluster analysis separated
the treatment groups into three clusters: (i) without-Mo application (C), (ii) nano-Mo (NMoK),
and (iii) non-nano-Mo (MoK and MoA), as shown in Figure 6b. Thus, nano-Mo application had
a more substantial effect on the variables than without-Mo and non-nano-Mo application.

Discussion
Nano fertilizer allows for precise targeting of nutrients to specific plant tissue, but we should con­
sider concerns about their potential environmental impacts. Plants require tiny amounts of Mo,

Figure 5. Effects of Mo application on dry weight of winter wheat (Triticum aestivum L.). Vertical bar above indicates standard
error of three replicates. Different letters (a, b, c, etc.) represent significant differences according to Duncan multiple range test
(n ¼ 3). Description of applications is mentioned in Figure 1.
 JOURNAL OF PLANT NUTRITION 769

Table 2. Effects of Mo application on yield component of winter wheat (Triticum aestivum L.).
Thousand grains Number of grains Number of Harvest
Treatment Yield (g pot−1) weight (g) per pot spikes per pot 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
C: Control, NMoK: Nano Molybdate Potassium, MoK: Potassium Molybdate, MoA: Ammonium Molybdate�.
�Different letters represent significant differences according to Duncan multiple range test (n ¼ 3).

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 grains Mo accumulation (Figure 2). This may be owing
to grains acting as strong sinks for nutrients during grains growth (Bennett, Roberts, and
Wagstaff 2011) and transport mechanisms in grains 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 (Figure 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, 2019; 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. sto­
matal conductance, dry weight of root, yield, and the number of spikes per pot (Figures 4 to 5,
Table 2). The previous observations of increased chlorophyll content by nano-Mo (Taran et al.
2016; Li et al. 2018; Abbasifar, ValizadehKaji, and Iravani 2020) and by non-nano-Mo (Zhang
et al. 2014; Ali, Hadi, and Ali 2019a; Chen, Meng, and Chen 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 (Figures 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,
Rathore, and Tarafdar 2017; Li et al. 2018; Abbasifar, ValizadehKaji, and Iravani 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, Tarafdar, and Biswas 2013; Karny et al. 2018), as reflected in our results of Mo accumula­
tion in the grains (Figure 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 (Figure 4), as
770 M. SYAIFUDIN ET AL.

Figure 6. Principal component analysis (PCA) biplot of variables and individuals (A) and clustering analysis (B). 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 grains (MCG), Mo accumulation of root (MAR), Mo accumulation
of stem (MAST), Mo accumulation of leaves (MAL), Mo accumulation of spikes (MASP), and Mo accumulation of grains (MAG). C:
Control, NMoK: Nano Molybdate Potassium, MoK: Potassium Molybdate, MoA: Ammonium Molybdate.

evidenced in substantial corrections between the relevant measures (Figure 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, Hu, and Wang 2006; Iobbi-
Nivol and Leimk€ uhler 2013; Li et al. 2018; Liu et al. 2019; Abbasifar, ValizadehKaji, and Iravani
2020) as the results of chlorophyll content (Figure 3). Chlorophyll content a and b are crucial
 JOURNAL OF PLANT NUTRITION 771

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 quan­
tity 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 (Figure 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, Deshpande, and Paknikar
2011). Based on the principal component analysis (Figure 6a) showing that there was a strong rela­
tionship between Mo content, Mo accumulation, chlorophyll content a and b, carotenoids, intercellu­
lar 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 (Figure 6b), 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.

Conclusions
Our results indicated that the nano-Mo fertilizer higher increased the dry weight of root, stem,
leaves, spikes, and grain yield more than the non-nano-Mo fertilizer, which suggested that nano-
Mo fertilizer is a valuable alternative to non-nano-Mo fertilizer when applied as a foliar fertilizer
on wheat grown in acidic soil conditions. The nano-Mo fertilizer enhanced the photosynthesis
rate and stomatal conductance compared to the control and non-nano-Mo fertilizer. Meanwhile,
it significantly increased the intercellular CO2 concentration and transpiration rate of winter
wheat, suggesting that nano-Mo fertilizer may increase the efficiency of the photosynthesis pro­
cess and enhance the carbon metabolism in Mo-inefficient wheat. However, our study concluded
that the nano-Mo fertilizer is a valuable alternative to non-nano-Mo fertilizer for winter wheat,
especially in improving Mo accumulation in grain and enhancing various growth-related parame­
ters, such as chlorophyll content and gas exchange stomatal conductance, dry weight, and grain
yield. Further tests in different environments and with larger sample sizes are warranted to valid­
ate 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.

Authors’ contributions
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.
772 M. SYAIFUDIN ET AL.

Disclosure statement
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. 42077095 and No.
41771329) and the National Key Research and Development Program of China (2022YFD1701004).

ORCID
Muhamad Syaifudin http://orcid.org/0000-0002-2256-0995
Mohamed G. Moussa http://orcid.org/0000-0003-3492-5071
Yiwen Wang http://orcid.org/0009-0004-8688-2047
Muhammad Shoaib Rana http://orcid.org/0009-0009-0740-970X
Wenhua Wei http://orcid.org/0000-0001-5774-5941
Chengxiao Hu http://orcid.org/0000-0001-7081-0162
Xuecheng Sun http://orcid.org/0000-0001-7377-8225

References
Abbasifar, A., B. ValizadehKaji, and M. A. Iravani. 2020. Effect of green synthesized molybdenum nanoparticles on
nitrate accumulation and nitrate reductase activity in spinach. Journal of Plant Nutrition 43 (1):13–27. doi:10.
1080/01904167.2019.1659340.
Adisa, I. O., V. L. R. Pullagurala, J. R. Peralta-Videa, C. O. Dimkpa, W. H. Elmer, J. L. Gardea-Torresdey, and
J. C. White. 2019. Recent advances in nano-enabled fertilizers and pesticides: A critical review of mechanisms of
action. Environmental Science: Nano 6 (7):2002–30. doi:10.1039/C9EN00265K.
Agarwala, S. C., C. P. Sharma, S. Farooq, and C. Chatterjee. 1978. Effect of molybdenum deficiency on the growth
and metabolism of corn plants raised in sand culture. Canadian Journal of Botany 56 (16):1905–8. doi:10.1139/
b78-227.
Agarwala, S. C., C. Chatterjee, P. N. Sharma, C. P. Sharma, and N. Nautiyal. 1979. Pollen development in maize
plants subjected to molybdenum deficiency. Canadian Journal of Botany 57 (18):1946–50. doi:10.1139/b79-244.
Alam, F., T. Y. Kim, S. Y. Kim, S. S. Alam, P. Pramanik, P. J. Kim, and Y. B. Lee. 2015. Effect of molybdenum on
nodulation, plant yield and nitrogen uptake in hairy vetch (Vicia villosa Roth). Soil Science and Plant Nutrition
61 (4):664–75. doi:10.1080/00380768.2015.1030690.
Alamri, S., M. H. Siddiqui, S. Mukherjee, R. Kumar, H. M. Kalaji, M. Irfan, T. Minkina, and V. D. Rajput. 2022.
Molybdenum-induced endogenous nitric oxide (NO) signaling coordinately enhances resilience through chloro­
phyll metabolism, osmolyte accumulation and antioxidant system in arsenate stressed-wheat (Triticum aestivum
L.) seedlings. Environmental Pollution (Barking, Essex: 1987) 292 (Pt A):118268. doi:10.1016/j.envpol.2021.
118268.
Ali, N., F. Hadi, and M. Ali. 2019a. Growth stage and molybdenum treatment affect cadmium accumulation, anti­
oxidant defence and chlorophyll contents in Cannabis sativa plant. Chemosphere 236:124360. doi:10.1016/j.che­
mosphere.2019.124360.
Ali, S., M. Rizwan, S. Noureen, S. Anwar, B. Ali, M. Naveed, E. F. Abd Allah, A. A. Alqarawi, and P. Ahmad.
2019b. Combined use of biochar and zinc oxide nanoparticle foliar spray improved the plant growth and
decreased the cadmium accumulation in rice (Oryza sativa L.) plant. Environmental Science and Pollution
Research International 26 (11):11288–99. doi:10.1007/s11356-019-04554-y.
Arnon, D. I. 1949. Copper enzymes in isolated chloroplasts. polyphenoloxidase in Beta Vulgaris. Plant Physiology
24 (1):1–15. doi:10.1104/pp.24.1.1.
Bennett, E. J., J. A. Roberts, and C. Wagstaff. 2011. The role of the pod in seed development: Strategies for manip­
ulating yield. The New Phytologist 190 (4):838–53. doi:10.1111/j.1469-8137.2011.03714.x.
Bindraban, P. S., C. O. Dimkpa, and R. Pandey. 2020. Exploring phosphorus fertilizers and fertilization strategies
for improved human and environmental health. Biology and Fertility of Soils 56 (3):299–317. doi:10.1007/
s00374-019-01430-2.
Chaudhuri, S. K., and L. Malodia. 2017. Biosynthesis of zinc oxide nanoparticles using leaf extract of Calotropis
gigantea: Characterization and its evaluation on tree seedling growth in nursery stage. Applied Nanoscience 7
(8):501–12. doi:10.1007/s13204-017-0586-7.
 JOURNAL OF PLANT NUTRITION 773

Chen, D., Z. Meng, and Y. Chen. 2019a. Toxicity assessment of molybdenum slag as a mineral fertilizer : A case
study with pakchoi (Brassica chinensis L.) Chemosphere 217 (97):816–24. doi:10.1016/j.chemosphere.2018.10.216.
Chen, L., C. Wang, S. Yang, X. Guan, Q. Zhang, M. Shi, S. T. Yang, C. Chen, and X. L. Chang. 2019b. Chemical
reduction of graphene enhances: In vivo translocation and photosynthetic inhibition in pea plants.
Environmental Science: Nano 6 (4):1077–88. doi:10.1039/C8EN01426D.
Dapkekar, A., P. Deshpande, M. D. Oak, K. M. Paknikar, and J. M. Rajwade. 2018. Zinc use efficiency is enhanced
in wheat through nanofertilization. Scientific Reports 8 (1):6832. doi:10.1038/s41598-018-25247-5.
Dimkpa, C. O., U. Singh, I. O. Adisa, P. S. Bindraban, W. H. Elmer, J. L. Gardea-Torresdey, and J. C. White.
2018. Effects of manganese nanoparticle exposure on nutrient acquisition in wheat (Triticum aestivum L.).
Agronomy 8 (9):158. doi:10.3390/agronomy8090158.
Du, W., J. L. Gardea-Torresdey, R. Ji, Y. Yin, J. Zhu, J. R. Peralta-Videa, and H. Guo. 2015. Physiological and bio­
chemical changes imposed by CeO2 nanoparticles on wheat: A life cycle field study. Environmental Science &
Technology 49 (19):11884–93. doi:10.1021/acs.est.5b03055.
Ghormade, V., M. V. Deshpande, and K. M. Paknikar. 2011. Perspectives for nano-biotechnology enabled protec­
tion and nutrition of plants. Biotechnology Advances 29 (6):792–803. doi:10.1016/j.biotechadv.2011.06.007.
Hippler, F. W. R., R. M. Boaretto, V. L. Dovis, G. O. F. Gomes, J. A. Quaggio, A. Qui~ nones, and D. Mattos. Jr.,
2017. Revisiting nutrient management for Citrus production: To what extent does molybdenum affect nitrogen
assimilation of trees? Scientia Horticulturae 225:462–70. doi:10.1016/j.scienta.2017.06.049.
Hugar, A. B., and M. B. Kurdikeri. 2000. Effect of application methods and levels of zinc and molybdenum on field
performance and seed yield in soybean. Karnataka Journal of Agricultural Sciences 13:439–41.
Husson, F., S. L^e, and J. Pag�es. 2017. Exploratory Multivariate Analysis by Example Using R. 2nd edn. New York:
Chapman and Hall/CRC. doi:10.1201/b21874.
Imran, M., C. X. Hu, S. Hussain, M. S. Rana, M. Riaz, J. Afzal, O. Aziz, A. M. Elyamine, M. A. F. Ismael, and
X. C. Sun. 2019. Molybdenum-induced effects on photosynthetic efficacy of winter wheat (Triticum aestivum L.)
under different nitrogen sources are associated with nitrogen assimilation. Plant Physiology and Biochemistry:
PPB 141:154–63. doi:10.1016/j.plaphy.2019.05.024.
Iobbi-Nivol, C., and S. Leimk€ uhler. 2013. Molybdenum enzymes, their maturation and molybdenum cofactor biosyn­
thesis in Escherichia coli. Biochimica et Biophysica Acta 1827 (8-9):1086–101. doi:10.1016/j.bbabio.2012.11.007.
Ismael, M. A., A. M. Elyamine, Y. Y. Zhao, M. G. Moussa, M. S. Rana, J. Afzal, M. Imran, X. H. Zhao, and C. X.
Hu. 2018. Can selenium and molybdenum restrain cadmium toxicity to pollen grains in brassica napus?
International Journal of Molecular Sciences 19 (8):2163. doi:10.3390/ijms19082163.
Ju�arez-Maldonado, A., H. Ortega-Ort�ız, G. Cadenas-Pliego, J. Vald�es-Reyna, J. M. Pinedo-Espinoza, C. U. L� opez-
Palestina, and A. D. Hern�andez-Fuentes. 2018. Foliar application of Cu nanoparticles modified the content of
bioactive compounds in Moringa oleifera Lam. Agronomy 8 (9):167. doi:10.3390/agronomy8090167.
Kaiser, B. N., K. L. Gridley, J. N. Brady, T. Phillips, and S. D. Tyerman. 2005. The role of molybdenum in agricul­
tural plant production. Annals of Botany 96 (5):745–54. doi:10.1093/aob/mci226.
Karny, A., A. Zinger, A. Kajal, J. Shainsky-Roitman, and A. Schroeder. 2018. Therapeutic nanoparticles penetrate
leaves and deliver nutrients to agricultural crops. Scientific Reports 8 (1):7589. doi:10.1038/s41598-018-25197-y.
Kassambara, A., and F. Mundt. 2020. Factoextra: Extract and Visualize the Results of Multivariate Data Analyses.
R Package Version 1.0.7. https://CRAN.R-project.org/package=factoextra
Kopittke, P. M., E. Lombi, P. Wang, J. K. Schjoerring, and S. Husted. 2019. Nanomaterials as fertilizers for improv­
ing plant mineral nutrition and environmental outcomes. Environmental Science: Nano 6 (12):3513–24. doi:10.
1039/C9EN00971J.
Larue, C., C. Baratange, D. Vantelon, H. Khodja, S. Surble, A. Elger, and M. Carriere. 2018. Influence of soil type
on TiO2 nanoparticle fate in an agro-ecosystem. The Science of the Total Environment 630:609–17. doi:10.1016/j.
scitotenv.2018.02.264.
Li, Y. D., Q. Jin, D. S. Yang, and J. H. Cui. 2018. Molybdenum sulfide induce growth enhancement effect of rice
(Oryza sativa L.) through regulating the synthesis of chlorophyll and the expression of aquaporin gene. Journal
of Agricultural and Food Chemistry 66 (16):4013–21. doi:10.1021/acs.jafc.7b05940.
Liu, C. K., C. X. Hu, Q. L. Tan, X. C. Sun, S. W. Wu, and X. H. Zhao. 2019. Co-application of molybdenum and
zinc increases grain yield and photosynthetic efficiency of wheat leaves. Plant, Soil and Environment 65 (10):
508–15. doi:10.17221/508/2019-PSE.
Liu, P., Y. S. Yang, G. D. Xu, Y. H. Fang, Y. A. Yang, and R. M. Kalin. 2005. The effect of molybdenum and boron
in soil on the growth and photosynthesis of three soybean varieties. Plant, Soil and Environment 51 (5):197–205.
doi:10.17221/3574-PSE.
Liu, R. Q., and R. Lal. 2015. Potentials of engineered nanoparticles as fertilizers for increasing agronomic produc­
tions. The Science of the Total Environment 514:131–9. doi:10.1016/j.scitotenv.2015.01.104.
Long, S. P., X. G. Zhu, S. L. Naidu, and D. R. Ort. 2006. Can improvement in photosynthesis increase crop yields?
Plant, Cell & Environment 29 (3):315–30. doi:10.1111/j.1365-3040.2005.01493.x.
774 M. SYAIFUDIN ET AL.

Maechler, M., P. Rousseeuw, A. Struyf, M. Hubert, and K. Hornik. 2022. cluster: Cluster Analysis Basics and
Extensions. R package version 2.1.4—For new features, see the ’Changelog’ file (in the package source), https://
CRAN.R-project.org/package=cluster
Marschner, M. 1955. Mineral nutrition of higher plants. 2nd edn. London: Academic Press.
Masi, E., and M. Boselli. 2011. Foliar application of molybdenum: Effects on yield quality of the grapevine
Sangiovese (Vitis vinifera L.). Advances in Horticultural Science 25 (1):37–43. doi:10.13128/ahs-12783.
Moussa, M. G., C. X. Hu, A. M. Elyamine, M. A. Ismael, M. S. Rana, M. Imran, M. Syaifudin, Q. L. Tan, C.
Marty, and X. C. Sun. 2021. Molybdenum-induced effects on nitrogen uptake efficiency and recovery in wheat
(Triticum aestivum L.) using 15N-labeled nitrogen with different N forms and rates. Journal of Plant Nutrition
and Soil Science 184 (6):613–21. doi:10.1002/jpln.202100040.
Moussa, M. G., X. C. Sun, M. A. Ismael, A. M. Elyamine, M. S. Rana, M. Syaifudin, and C. X. Hu. 2022a.
Molybdenum-induced effects on grain yield, macro-micro-nutrient uptake, and allocation in Mo-inefficient win­
ter wheat. Journal of Plant Growth Regulation 41 (4):1516–31. doi:10.1007/s00344-021-10397-0.
Moussa, M. G., X. Sun, S. El-Tohory, A. Mohamed, M. H. Saleem, M. Riaz, Z. Dong, L. He, C. Hu, and M. A.
Ismael. 2022b. Molybdenum role in nitrogen bioavailability of wheat-soil system using the natural 15N abun­
dance technique. Journal of Soil Science and Plant Nutrition 22 (3):3611–24. doi:10.1007/s42729-022-00913-w.
Pavlovic, D., B. Nikolic, S. Djurovic, H. Waisi, A. Andjelkovic, and D. Marisavljevic. 2014. Chlorophyll as a meas­
ure of plant health: Agroecological aspects. Pesticidi i Fitomedicina 29 (1):21–34. doi:10.2298/PIF1401021P.
Qin, S. Y., C. X. Hu, Q. L. Tan, and X. C. Sun. 2017. Effect of molybdenum levels on photosynthetic characteris­
tics, yield and seed quality of two oilseed rape (Brassica napus L.) cultivars. Soil Science and Plant Nutrition 63
(2):137–44. doi:10.1080/00380768.2017.1286232.
Rana, M. S., X. C. Sun, M. Imran, Z. Khan, M. G. Moussa, M. Abbas, P. Bhantana, M. Syaifudin, I. U. Din, M.
Younas, et al. 2020. Mo-inefficient wheat response toward molybdenum supply in terms of soil phosphorus
availability. Journal of Soil Science and Plant Nutrition 20 (3):1560–73. doi:10.1007/s42729-020-00298-8.
Rizwan, M., S. Ali, B. Ali, M. Adrees, M. Arshad, A. Hussain, M. Z. U. Rehman, and A. A. Waris. 2019. Zinc and
iron oxide nanoparticles improved the plant growth and reduced the oxidative stress and cadmium concentra­
tion in wheat. Chemosphere 214:269–77. doi:10.1016/j.chemosphere.2018.09.120.
Rossi, L., L. N. Fedenia, H. Sharifan, X. M. Ma, and L. Lombardini. 2019. Effects of foliar application of zinc sul­
fate and zinc nanoparticles in coffee (Coffea arabica L.) plants. Plant Physiology and Biochemistry: PPB 135:160–
6. doi:10.1016/j.plaphy.2018.12.005.
Shang, Y. F., M. K. Hasan, G. J. Ahammed, M. Q. Li, H. Q. Yin, and J. Zhou. 2019. Applications of nanotechnol­
ogy in plant growth and crop protection: A review. Molecules (Basel, Switzerland) 24 (14):2558. doi:10.3390/
molecules24142558.
Singh, A., N. B. Singh, I. Hussain, and H. Singh. 2017. Effect of biologically synthesized copper oxide nanoparticles
on metabolism and antioxidant activity to the crop plants Solanum lycopersicum and Brassica oleracea var.
botrytis. Journal of Biotechnology 262:11–27. doi:10.1016/j.jbiotec.2017.09.016.
Steiner, F., T. Zoz, A. M. Zuffo, P. Pereira-Machado, J. Zoz, and A. Zoz. 2018. Foliar application of molybdenum
enhanced quality and yield of crispleaf lettuce (Lactuca sativa L., cv. Grand Rapids). Acta Agron�omica 67 (1):
73–8. doi:10.15446/acag.v67n1.59272.
Sun, X. C., C. X. Hu, Q. L. Tan, J. S. Liu, and H. G. Liu. 2009. Effects of molybdenum on expression of cold-
responsive genes in abscisic acid (ABA)-dependent and ABA-independent pathways in winter wheat under low-
temperature stress. Annals of Botany 104 (2):345–56. doi:10.1093/aob/mcp133.
Sutulien_e, R., L. Ragelien_e, P. Duchovskis, and J. Miliauskien_e. 2022. The effects of nano-copper, -molybdenum,
-boron, and -silica on pea (Pisum sativum L.) growth, antioxidant properties, and mineral uptake. Journal of
Soil Science and Plant Nutrition 22 (1):801–14. doi:10.1007/s42729-021-00692-w.
Taran, N., L. Batsmanova, O. Kosyk, O. Smirnov, M. Kovalenko, L. Honchar, and A. Okanenko. 2016. Colloidal
nanomolybdenum influence upon the antioxidative reaction of chickpea plants (Cicer arietinum L.). Nanoscale
Research Letters 11 (1):476. doi:10.1186/s11671-016-1690-4.
Taran, N. Y., O. M. Gonchar, K. G. Lopatko, L. M. Batsmanova, M. V. Patyka, and M. V. Volkogon. 2014. The
effect of colloidal solution of molybdenum nanoparticles on the microbial composition in rhizosphere of Cicer
arietinum L. Nanoscale Research Letters 9 (1):289. doi:10.1186/1556-276x-9-289.
Tejakhod, S., J. P. Hammond, and R. H. Ellis. 2018. Foliar application of molybdenum reduces yield loss and pre-
harvest sprouting in Japonica rice seeds subjected to simulated flooding during seed development and matur­
ation. Seed Science and Technology 46 (1):175–89. doi:10.15258/sst.2018.46.1.17.
Thomas, E., I. Rathore, and J. C. Tarafdar. 2017. Bioinspired production of molybdenum nanoparticles and its
effect on chickpea (Cicer arietinum L). Journal of Bionanoscience 11 (2):153–9. doi:10.1166/jbns.2017.1425.
Usman, M., M. Farooq, A. Wakeel, A. Nawaz, S. A. Cheema, H. U. Rehman, I. Ashraf, and M. Sanaullah. 2020.
Nanotechnology in agriculture: Current status, challenges and future opportunities. The Science of the Total
Environment 721:137778. doi:10.1016/j.scitotenv.2020.137778.
 JOURNAL OF PLANT NUTRITION 775

Ventura, Y., W. A. Wuddineh, Y. Ephrath, M. Shpigel, and M. Sagi. 2010. Molybdenum as an essential element for
improving total yield in seawater-grown Salicornia europaea L. Scientia Horticulturae 126 (3):395–401. doi:10.
1016/j.scienta.2010.07.015.
Wang, W. N., J. C. Tarafdar, and P. Biswas. 2013. Nanoparticle synthesis and delivery by an aerosol route for
watermelon plant foliar uptake. Journal of Nanoparticle Research 15 (1):1–13. doi:10.1007/s11051-013-1417-8.
Wu, S. W., C. X. Hu, Q. L. Tan, Z. J. Nie, and X. C. Sun. 2014. Effects of molybdenum on water utilization, anti­
oxidative defense system and osmotic-adjustment ability in winter wheat (Triticum aestivum) under drought
stress. Plant Physiology and Biochemistry: PPB 83:365–74. doi:10.1016/j.plaphy.2014.08.022.
Wu, S. W., C. X. Hu, Q. L. Tan, S. J. Xu, and X. C. Sun. 2017. Nitric oxide mediates molybdenum-induced anti­
oxidant defense in wheat under drought stress. Frontiers in Plant Science 8:1085. doi:10.3389/fpls.2017.01085.
Wu, S. W., X. C. Sun, Q. L. Tan, and C. X. Hu. 2019. Molybdenum improves water uptake via extensive root
morphology, aquaporin expressions and increased ionic concentrations in wheat under drought stress.
Environmental and Experimental Botany 157:241–9. doi:10.1016/j.envexpbot.2018.10.013.
Yamori, W. 2016. Photosynthetic response to fluctuating environments and photoprotective strategies under abiotic
stress. Journal of Plant Research 129 (3):379–95. doi:10.1007/s10265-016-0816-1.
Yu, M., C. Hu, W. Xiao, and Y. Hua. 2005. Effect of Mo deficiency on the concentration of chlorophyll and the
ultrastructure of chloroplast in winter wheat cultivars. J Huazhong Agric Univ 24:465–9. (in Chinese)
Yu, M., C. X. Hu, and Y. H Wang. 2006. Effects of molybdenum on the intermediates of chlorophyll biosynthesis
in winter wheat cultivars under low temperature. Agricultural Sciences in China 5 (9):670–7. doi:10.1016/S1671-
2927(06)60109-0.
Yuan, J. X., Y. Chen, H. S. Li, J. Y. Lu, H. Zhao, M. Liu, G. S. Nechitaylo, and N. N. Glushchenko. 2018. New
insights into the cellular responses to iron nanoparticles in Capsicum annuum. Scientific Reports 8 (1):3228. doi:
10.1038/s41598-017-18055-w.
Zahedi, S. M., M. Karimi, and J. A. T. da Silva. 2020. The use of nanotechnology to increase quality and yield of
fruit crops. Journal of the Science of Food and Agriculture 100 (1):25–31. doi:10.1002/jsfa.10004.
Zhang, H., R. Wang, Z. Chen, J. Pu, J. Wang, H. Zhang, and Y. Yang. 2022. Nanoscale molybdenum oxide
improves plant growth and increases nitrate utilisation in rice (Oryza sativa L. Food and Energy Security 11 (2):
e383. doi:10.1002/fes3.383.
Zhang, M., C. X. Hu, X. C. Sun, X. H. Zhao, Q. L. Tan, Y. Zhang, and N. Li. 2014. Molybdenum affects photosyn­
thesis and ionic homeostasis of chinese cabbage under salinity stress. Communications in Soil Science and Plant
Analysis 45 (20):2660–72. doi:10.1080/00103624.2014.941855.
Zhang, M., C. Hu, X. Zhao, Q. Tan, and X. Sun. 2016. Co-application of molybdenum and selenium fertilizers
increase uptake, recovery and harvest index of molybdenum and selenium in pepper crop. Journal of Plant
Nutrition 39 (2):244–51. doi:10.1080/01904167.2015.1105970.

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