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Article

The Influence of the Hybrid Compound Nd(NO3)3@Zn-MOF on the Growth of Vanilla (Vanilla planifolia Jacks. ex Andrews) Cultured In Vitro: A Preliminary Study

by
Carlos Alberto Cruz-Cruz
1,
Xóchitl De Jesús García-Zárate
1,
José Luis Spinoso-Castillo
2,
Rodolfo Peña-Rodríguez
1,
Raúl Colorado-Peralta
1,
Ricardo Sánchez-Páez
2,* and
Jericó Jabín Bello-Bello
3,*
1
Facultad de Ciencias Químicas, Universidad Veracruzana, Prolongación de Oriente 6, No. 1009, Orizaba 94340, Veracruz, Mexico
2
Colegio de Postgraduados Campus Córdoba, Carretera Federal Córdoba Veracruz, Amatlán de los Reyes 94953, Veracruz, Mexico
3
CONAHCYT-Colegio de Postgraduados Campus Córdoba, Carretera Federal Córdoba Veracruz, Amatlán de los Reyes 94953, Veracruz, Mexico
*
Authors to whom correspondence should be addressed.
Agronomy 2024, 14(9), 1880; https://doi.org/10.3390/agronomy14091880 (registering DOI)
Submission received: 12 July 2024 / Revised: 16 August 2024 / Accepted: 21 August 2024 / Published: 23 August 2024
(This article belongs to the Special Issue Modern In Vitro Technologies for Developing Horticulture)
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Abstract

:
Hybrid compounds have a significant impact on agriculture as slow macro- and micronutrient administration systems. This study aimed to evaluate the synthesis and effect of the hybrid compound Nd(NO3)3@Zn-MOF in different concentrations on the in vitro growth of vanilla (Vanilla planifolia Jacks. ex Andrews). A total of 13 vanilla plantlets per treatment were cultivated in test tubes with semi-solid Murashige and Skoog (MS) medium and without growth regulators and treated with 0, 5, 10, 15, and 30 mg L−1 of Nd(NO3)3@Zn-MOF. After 60 days of culture, we evaluated different morphological and biochemical parameters, such as shoot length, root length, the number of roots, the number of leaves, total chlorophyll and carotenoid content, antioxidant capacity, and phenolic compound content. Our results showed that the Nd(NO3)3@Zn-MOF at 10 mg L−1 concentration increased plantlet length. Furthermore, we observed an increase in root length and number with the 5 and 10 mg L−1 concentrations, and a decrease in these same parameters with the 15 and 30 mg L−1 Nd(NO3)3@Zn-MOF concentrations. There were no significant differences regarding the number of leaves or total chlorophyll content. As for the antioxidant capacity, we observed an increase with 5, 10, and 15 mg L−1 of Nd(NO3)3@Zn-MOF and a decrease with the highest concentration. Finally, the phenolic and carotenoid content decreased with the 15 and 30 mg L−1 Nd(NO3)3@Zn-MOF concentrations compared to the control. In conclusion, the hybrid compound Nd(NO3)3@Zn-MOF showed beneficial effects on the growth, physiology, and biochemistry of V. planifolia in vitro when plants were treated at low concentrations. Additionally, the high concentrations used in this study did not induce toxicity. Our findings suggest that Nd(NO3)3@Zn-MOF could be used as a biostimulant in vanilla during its in vitro culture. However, due to the hormetic effect and the possible different reactions of different genotypes, this requires further detailed research.

1. Introduction

Metal–organic frameworks (MOFs) are formed by cationic metals bound to polydentate organic ligands. Their coordinated covalent bonds result in crystalline structures with uniform and adjustable pores that render multifunctional properties, such as high porosity, a specific surface area, and a controllable structure [1]. These characteristics are useful for drug administration, environmental remediation, energy sensors, and photocatalysis [2]. Because MOFs possess a prolonged-release system, the agricultural sector is interested in their use as carriers for agrochemical fertilizers and pesticides to increase crop productivity [3,4]. Various studies have demonstrated the efficiency of MOFs in enabling agrochemical release. For example, MOF-ethylene was used to stimulate banana and avocado ripening [5], MOF-1201(Ca2+ acetate and lactic acid) was used as a pesticide [6], Fe-MOF-EDTA was used for fertilization in hydroponic bean cultures (Phaseolus vulgaris L.) [7], and β-CD-MOF-NPC, a β-cyclodextrin-based porous carbon, was used as a potassium precursor in rice seedlings (Oryza sativa L.) [8]. Other agrochemical-related studies have reported the degradation of a MOF consisting of iron, nitrogen, and phosphorus in rice [9]. MOFs based on Zr, UiO-60, UiO-66-NH2, and UiO-67 were used in the slow release of the herbicide 2-methyl-4-chlorophenoxyacetic acid [10], and a MOF-Fe was used as a micronutrient in Tebuconazole degradation in wheat seedlings (Triticum aestivum L.) [11].
On the other hand, lanthanide-based MOFs have been useful in luminescent and/or gas storage applications [12]. Lanthanides have been described as inorganic biostimulants which induce growth in crops such as corn (Zea mays L.), sorghum (Sorgo bicolor (L.) Moench), rye (Secale cereale L.), and water lettuce (Pistia stratiotes L.) [13,14]. To date, some of the lanthanide elements, like Gadolinium [15], Cerium [16], Europium [17], and Lanthanum [18], have improved nutrient efficiency, which contributes to crop production and quality. Among them, neodymium-Nd(III) stands out. This element acts in the development of leaves and roots through the endocytic activation of plant cells [19,20]. Various studies have demonstrated the positive effects of neodymium on in vitro cultures such as dendrobium (Dendrobium densiflorum Lindl.) [21], Chinese cabbage (Brassica chinensis L.), and sunflower (Helianthus annus L.) [22]; under ex vitro conditions it has been evaluated in species such as rice (O. sativa L.) [23]. Vanilla (Vanilla planifolia Jacks. ex Andrews) is a Mexican orchid belonging to the family Orchidaceae. The characteristic aroma of its fruit is due to its vanillin content [24], which is the most in-demand scent in the agri-food sector [25]. It is commonly used in the pharmaceutical [26], cosmetic, and tobacco industries [27]. Unfortunately, V. planifolia faces various threats that endanger our vanillin supply. V. planifolia has been classified as Endangered B2ab (iii, V) by the International Union for Conservation of Nature (IUCN) [28,29]. Conventional propagation via stem cuttings and seed germination limits its production due to its slow growth and susceptibility to pests and diseases [30,31]. Biotechnological tools represent a valuable alternative for increasing vanilla production. One of the plant tissue culture techniques used as a biotechnological alternative is in vitro conservation and propagation. This technique consists of propagating vigorous plants homogeneously and with high phytosanitary quality under aseptic and controlled conditions [32,33]. This study aimed to evaluate the synthesis and effect of the hybrid compound Nd(NO3)3@Zn-MOF in different concentrations on the in vitro growth of vanilla (Vanilla planifolia Jacks. ex Andrews).

2. Materials and Methods

2.1. Zn-MOF Synthesis

A metal–organic framework based on zinc(II) was used as the metal cation. The formatted anion was used as an organic ligand and was obtained by heating under reflux. For this purpose, the precursors Zn(NO3)2 6H2O (Merck KGaA®, Darmstadt, Germany, 2.7760 g, 9.3315 mmol, ≤99.0%) and formic acid (Merck KGaA®,1.2886 mL, 27.9947 mmol, 95–98%) were mixed following a 1:3 ratio (metal: ligand) and 5 mL of N,N-dimethylformamide (DMF) was added using a 10 mL graduated pipette. This mixture was then heated in a reflux condenser (Kimax®, Millville, NJ, USA No. 18140) for 6 h at 120 °C. The obtained crystalline solids were collected by vacuum filtration in a 250 mL Büchner funnel and Double-Rings® filter paper, grade Media 102 (pore size of 8 to 10 μm), washed with methanol, and placed in a drying oven at 80 °C overnight, resulting in a 70% stoichiometric yield. All reagents were commercially purchased from Merck KGaA®. The solvents and reagents used were analytical-grade.

2.2. Nd(NO3)3@Zn-MOF Synthesis and Mechanochemical Doping

The 5% (w/w) doping of the Zn-MOF with neodymium(III) salt (Nd(NO3)3·6H2O) was performed by mechanical milling in a mortar and pestle using a mixture of Zn-MOF (95 mg) and Nd(NO3)3·6H2O (5 mg). A few drops of acetonitrile were added to promote maceration for 40 min. Finally, the mixture was left to dry in an air oven at 80 °C for 2 h and characterized by X-ray powder diffraction.

2.3. X-ray Powder Diffraction (XRD)

Powder X-ray diffractograms were acquired at room temperature employing the D2 Phaser benchtop analyzer (Bruker®, Billerica, MA, USA) and processed with the DIFFRAC.SUITE software version Part 11 provided with the equipment.

2.4. In Vitro Establishment and Multiplication

For the in vitro establishment of vanilla (V. planifolia Jacks. ex Andrews) cultures, we used tillers 20 cm in length obtained from greenhouse mother plants in Fortín, Veracruz, Mexico (18°54′16″ N 96°59′21″ W/18.90448, −96.98906). For the in vitro establishment of axillary buds, the disinfection method used by [28] was followed. Axillary buds were cut into 2 cm nodal segments that were used as explants and were washed for 30 min with running water and Tween-20® (Merck KGaA®). The explants were submerged for 15 min in a solution containing 1 g L−1 of Promyl® Benomil 50% fungicide (Promotora técnica industrial, S.A. de S.V.) and AGRI-MYCIN® 100 bactericide (Pfizer, S.A. de C.V., Mexico). Then, in a laminar flow hood, the explants were washed with a 5% (v/v) (0.25% de i.a.) sodium hypochlorite solution (Cloralex TM, Industrias Alen, S.A. de S.V., NL, Mexico) and rinsed with a 0.1 mg L−1 mercury chloride solution (HgCl2). Lastly, the explants were rinsed three times with sterile distilled water and cultivated in test tubes with 10 mL of semi-solid MS medium [34] supplemented with 2 mg L−1 of BAP (6- benzylaminopurine, Merck KGaA®) and 30 g L−1 of sucrose. The pH of the culture medium was adjusted to 5.8, and 2.2 g L−1 of Phytagel™ (Merck KGaA®) was used as a gelling agent. The test tubes containing the medium were autoclaved for 15 min at 120 °C. Cultures were transferred to an incubation room maintained at 24 ± 2 °C with an artificial white LED lamp with an irradiance of 40 ± 5 µmol m−2 s−1 under a photoperiod of 16 h of light and 8 h of dark. After four weeks, the shoots were transferred to 500 mL flasks with 30 mL of MS semi-solid medium supplemented with 2 mg L−1 of BAP and 30 g L−1 of sucrose for multiplication. These cultures were incubated under the same temperature and irradiance conditions as previously described.

2.5. Effect of Nd(NO3)3@Zn-MOF on the In Vitro Growth of V. planifolia

After three 60-day subcultures, apices measuring 2 cm in length were collected for each Nd(NO3)3@Zn-MOF treatment. A total of 13 test tubes, each containing one apex, were used per treatment. Apices were cultivated in test tubes with a polypropylene cap containing 20 mL of semi-solid MS medium without growth regulators and supplemented with 30 g L−1 of sucrose. Finally, a stock solution of 100 mg of the compound was prepared by dissolving Nd(NO3)3@Zn-MOF in 100 mL of distilled water. Then, different concentrations of the compound (0, 5, 10, 15, and 30 mg L−1) were added to the MS culture medium for each treatment. The pH of the medium was adjusted to 5.8, and 2.2 g L−1 of Phytagel™ (Merck KGaA®) was used as a gelling agent. The shoots were cultivated under the irradiance and temperature conditions previously described. After 60 days, we evaluated the following morphological variables: shoot length, root length, the number of roots, and the number of leaves. We also determined the content of total chlorophyll and carotenoids, the antioxidant capacity, and the phenolic content.

2.6. Determination of Chlorophyll and Carotenoid Content

Total chlorophyll was determined following the [35] methodology. For each sample, 0.25 g of fresh leaf material was weighed and macerated using 2.5 mL of 80% acetone. The samples were left to rest for 24 h in the dark at −4 °C. Then, this extract was filtered and made up to 6.25 mL with 80% acetone. Its absorbance was determined at 645 and 663 nm in a spectrophotometer (Thermo Scientific Genesys 10S; Madison, WI, USA) against an 80% acetone blank. The carotenoid content was determined following the methodology described by [36]. Readings were carried out using a spectrophotometer at 450 nm.

2.7. Determination of Phenolic Compounds and Antioxidant Capacity

The phenolic content was determined according to [37]. The extract was obtained by macerating 0.25 g of a sample with 5 mL of 80% methanol. This extract was centrifuged at 300 rpm for 10 min at 10 °C. The supernatant (0.150 mL) was then mixed with 0.75 mL of 10% Folin–Ciocalteu reagent (Merck KGaA®) and left to rest for 3 min. Finally, 0.6 mL of 20% sodium carbonate (Merck KGaA®) was added and left to stand in the dark for 2 h. The phenolic content was determined at 765 nm.
The antioxidant capacity was expressed as DPPH (2,2-diphenyl-1-picrylhydrazyl) and was established using the methodology described by [38]. The extract was obtained by macerating 0.25 g of a sample with 2.5 mL of 80% methanol. The extract was centrifuged at 3000 rpm for 10 min at 10 °C. Subsequently, the supernatant (100 µL) was mixed with 290 mL of DPPH and left incubating for 1 h. Finally, the absorbance was read at 515 nm.

2.8. Experimental Design and Statistical Analysis

All experiments were carried out following a completely randomized design in triplicate. Data were analyzed with an analysis of variance test followed by Tukey’s mean comparison (p ≤ 0.05) using the Statistical Package for the Social Sciences for Windows, version 23.

3. Results

3.1. Characterization of the Nd(NO3)3@Zn-MOF by X-ray Powder Diffraction (XRD)

Symmetrical crystal clusters were observed from the synthesis of Zn-MOF (Figure 1a). We also observed crystals with amorphous dimensions corresponding to the hybrid compound Nd(NO3)3@Zn-MOF (Figure 1b). The peaks in the experimental diffractogram of the Zn-MOF were observed at 14.8°, 21°, 22°, 24°, 26°, 29.8°, 33°, and 34°. Although a slight shift to the left is exhibited, the experimental diffractogram is similar to that obtained from the single-crystal X-ray structure reported by [39] (Figure 1c). Additionally, the diffraction pattern of Zn-MOF doped with neodymium nitrate hexahydrate shows that most of the peaks correspond to the crystalline phase of Zn-MOF. The remaining peaks correspond to the crystal lattice generated by the presence of Nd(NO3)3·6H2O. The peaks at 16°, 18°, and 35° in the diffractogram of Nd(NO3)3@Zn-MOF correspond to the planes generated by Nd(NO3)3·6H2O. This diffraction pattern results from a mixture of the crystalline phases of its components. Furthermore, superimposing the diffractogram of Nd(NO3)3·6H2O onto the diffractogram of the hybrid compound confirms the presence of the inorganic salt. Incorporating Nd(III) ions into the Zn-MOF caused the hybrid compound to lose crystallinity relative to the undoped Zn-MOF. Additionally, the loss of crystallinity led to broader peaks and the greater absorption and scattering of light. This is attributed to the embedding of Nd(III) ions in the crystal lattice and a decrease in particle size (Figure 1d). Fourier transform infrared spectroscopy (FT-IR) data obtained from the PerkinElmer® FTIR/FTNIR model Spectrum 100 spectrophotometer with an attenuated total reflection accessory confirmed the presence of the doping of Zn-MOF with Nd(NO3)3·6H2O (Figure 1e). The three-dimensional structure of the empty pore of the Zn-MOF, where the electrostatic interactions with the Nd(III) ions take place, is presented in Figure 1f.

3.2. Effect of Nd(NO3)3@Zn-MOF on the In Vitro Growth of V. planifolia

The maximum shoot length (3.5 ± 0.11 cm) was obtained using 10 mg L−1 of Nd(NO3)3@Zn-MOF. It was significantly longer than those obtained from other tested media, except those supplemented with 15 mg L−1. Significant differences in the size of shoots growing in most media have not been proven (Figure 2a). The plantlets with the greatest number of roots (2.54 ± 0.20) were obtained using 10 mg L−1 of Nd(NO3)3@Zn-MOF (Figure 2b). The maximum root lengths (3.25 ± 0.28 cm and 3.45 ± 0.20 cm) were obtained with treatment concentrations of 5 and 10 mg L−1 of Nd(NO3)3@Zn-MOF. Conversely, the shortest root lengths (2.37 ± 0.13 cm and 2.33 ± 0.12 cm) were observed with 15 and 30 mg L−1 concentrations of Nd(NO3)3@Zn-MOF (Figure 2c). There were no significant differences regarding the number of leaves (Figure 2d). The appearances of plantlets treated with different concentrations of Nd(NO3)3@Zn-MOF are shown in Figure 3.

3.3. Effect of Nd(NO3)3@Zn-MOF on Biochemical Parameters of In Vitro Plantlets of V. planifolia

The maximum total chlorophyll content was observed in the control treatment, which was 0.34 ± 0.02 mg g−1 of fresh weight (FW), while the lowest content was observed in the concentrations of 15 and 30 mg L−1 of Nd(NO3)3@Zn-MOF, which was 0.23 and 0.20 mg g−1 FW, respectively (Figure 4a). The maximum β-carotene content was observed in the control, 3.67 ± 0.14 µg mg−1 FW, while the lowest level was observed in the concentrations of 15 and 30 mg L−1 of Nd(NO3)3@Zn-MOF, 3.05 ± 0.11 and 2.63 ± 0.06 µg mg−1 FW, respectively (Figure 4b). The highest antioxidant capacity was observed in the 5 and 10 mg L−1 Nd(NO3)3@Zn-MOF treatments, yielding 47.75 ± 0.23 TE g−1 FW and 47.69 ± 0.32 TE g−1 FW, respectively. They were significantly higher than those obtained on other tested media except those supplemented with 15 mg L−1 of Nd(NO3)3@Zn-MOF. The lowest antioxidant capacity (38.85 ± 0.95 TE g−1 FW) was observed in the highest concentration treatment (Figure 4c). Regarding phenolic content, the control treatment yielded the highest content: 122.32 ± 4.49 mg GAE g−1 FW. However, the highest concentration treatments (15 and 30 mg L−1 Nd(NO3)3@Zn-MOF) decreased the phenolic content to 33.43 ± 1.23 mg GAE g−1 FW and 32.74 ± 0.84 mg GAE g−1 FW, respectively (Figure 4d).

4. Discussion

4.1. Evaluating the Effect of Nd(NO3)3@Zn-MOF on the In Vitro Growth of V. planifolia

In this study, we obtained Nd(NO3)3@Zn-MOF via mechanochemical synthesis, which consisted of the breaking and reforming of the covalent bond through the adsorption of energy by solid reagents, thus reducing particle size, which increased pore size and surface area, allowing the incorporation of secondary components [40,41,42]. The findings in this study suggest that MOFs could function as carriers of culture media components, resulting in the gradual and efficient release of nutrients, growth regulators, vitamins, and other organic compounds. Several studies have demonstrated the ability of MOFs to release secondary components in response to stimuli like temperature [43], light [44], water amount [45], and pH [46]. To improve the response of MOFs to these stimuli, molecules have been included to modify their topology, with the aim of allowing their biodegradation and biocompatibility [47,48]. Some studies have reported the effect of MOFs on the growth of hydroponic cultures and fruit ripening, such as banana (Persea americana) and avocado (Musa acuminata) [5], rice (O. sativa L.) [8], bean (P. vulgaris) [7], and wheat seedlings (T. aestivum) [11]. The present study shows the effect of the hybrid compound Nd(NO3)3@Zn-MOF on the in vitro growth of V. planifolia. We observed an increase in shoot length, root length, and the number of roots at a concentration of 10 mg L−1 of Nd(NO3)3@Zn-MOF. Lanthanides are metallic ions, so they tend to bind to the carboxylate groups of the cell wall, as is the case with pectin, which stimulates plant development and participates in biotic and abiotic stress [49,50]. The absorption of these metals occurs through their interaction with polymer chains through hydrogen bonds, hydrophobic interactions, or divalent cation bridges (Ca2+) [51,52]. The authors of [53] claim that lanthanide transport occurs ionically in plants. The distribution of metals will depend on the plant species. However, most lanthanides are absorbed through an apoplastic pathway based on the concentration gradient [54,55]. The stimulating response of the plant varies according to the accumulation of metals. That is, at low concentrations, they have beneficial effects, and, at high concentrations, they have toxic effects; this is known as hormesis [56,57,58]. In this study, when exceeding the hormetic zone, Nd could hinder plant growth, inducing a loss of tissue turgor due to an excessive accumulation of Nd in the cell, and thus decreasing the extensibility of the cell wall.
To date, there are few reports on Nd(NO3)3·6H2O and its stimulating effect in plants. The authors of [22], using in vitro sunflower (H. annus) and Chinese cabbage (B. chinensis) seedlings, observed a hormetic effect on the stem and roots at concentrations lower than 100 mg of Nd(NO3)3·6H2O. However, Nd(NO3)3·6H2O in higher concentrations (200 and 335 mg L−1) caused toxicity and inhibited the growth of both species. Similarly, in the case of rice seedlings (O. sativa), the authors of [23] reported greater longitudinal growth with 0.5 and 5 mg L−1 of Nd(NO3)3·6H2O. However, the studied substance in higher concentrations (50 and 500 mg L−1) had toxic effects. In this study, low treatment concentrations (5 and 10 mg L−1 of Nd(NO3)3@Zn-MOF) are associated with lower toxicity in V. planifolia. However, in the case of concentrations higher than 10 mg L−1 of Nd(NO3)3@Zn-MOF, we observed hormesis. The purpose of this prolonged delivery system is to use it as a carrier of Nd(NO3)3·6H2O within the plant metabolism of V. planifolia. Thus, Zn-MOF has a degree of chemical stability, which could gradually degrade via the breaking of its electrostatic interactions in the culture medium due to the influence of pH and water, releasing the molecule of interest, in this case, Nd(NO3)3·6H2O, and entering the plant cell of V. planifolia (Figure 5). The MOF used in this study slowly supplies its culture medium component based on the culture requirements while avoiding toxicity at low doses and without affecting the tissues.

4.2. Effect of Nd(NO3)3@Zn-MOF on Biochemical Parameters of In Vitro Plantlets of V. planifolia

The different Nd(NO3)3@Zn-MOF treatments had significantly different effects on chlorophyll and carotenoid content. The authors of [22] reported an increase in chlorophyll content when using 200 mg L−1 of Nd(NO3)3·6H2O in in vitro Chinese cabbage seedlings (B. chinensis). The authors of [59] reported increased chlorophyll content in the hydroponic culture of sugarcane seedlings (Saccharum spp. hybrids) following treatment with 37.5 mg L−1 of NdCl3. Regarding the carotenoid content, they observed an increase at 25 mg L−1 of NdCl3 and a decrease at 37.5 mg L−1 of NdCl3. Although lanthanides could contribute to photosynthetic processes for plant development and growth, at high concentrations they can be toxic and act as stressors [60]. Similarly, carotenoids increase plant tolerance to the oxidative stress caused by biotic stress [61]. According to the authors of [59], Nd could play an indirect role in the formation of photosynthetic pigments such as chlorophyll. Due to a catalytic function, this element probably enters the chloroplasts by joining the chlorophyll, interacting with Mg2+. The decrease in chlorophyll and carotenoid content observed with high concentrations of Nd(NO3)3@Zn-MOF could alter chlorophyll biosynthesis due to lipid peroxidation or damage the chloroplast and trigger the accumulation of ROS in plant cells, promoting an oxidative stress environment and inhibiting photosynthesis [62].
In plants, antioxidant capacity protects against the reactive oxygen species that accumulate under stress. Phenolic compounds also have antioxidant properties and can influence oxidative damage. The authors of [23] used in vitro rice seedlings and found that Nd(NO3)3·6H2O, at low concentrations (0.5 and 5 mg L−1 of Nd(NO3)3·6H2O), decreases oxidative damage by inhibiting reactive oxygen species. However, the use of the studied substance in higher concentrations (500 mg L−1 of Nd(NO3)3·6H2O) increased the content of reactive oxygen species. The authors of [21] confirmed that 0.25 mg L−1 of Nd(NO3)3·6H2O increases the proportion of reduced glutathione (GSH) and oxidated glutathione (GSSG) in in vitro D. densiflorum shoots. According to [55], lanthanides can significantly reduce free radicals. That is, an adequate concentration of lanthanides accelerates antioxidant activity. In this study, we observed an increase in antioxidant capacity with 5, 10, and 15 mg L−1 of Nd(NO3)3@Zn-MOF. However, the DPPH content decreased at 0 and 30 mg L−1 of Nd(NO3)3@Zn-MOF. This effect confirms that a plant’s antioxidant capacity is a tolerance mechanism against oxidative stress. However, there was no correlation with the increase in soluble phenols. The increase in phenolic content at 5 and 10 mg L−1 of Nd(NO3)3@Zn-MOF could be associated with a tolerance mechanism against oxidative damage, which could explain the hormetic effect seen at these concentrations. According to [63], Nd(NO3)3·6H2O could activate antioxidant enzymes, such as catalase, which is related to the delay in the onset of leaf senescence, and peroxidase, which degrades H2O2. These enzymes use peroxides as electron acceptors to reduce oxidative damage [64,65]. This ROS-induced hormetic effect promotes the production of non-enzymatic scavengers such as glutathione, ascorbate, phenolic compounds, and antioxidant enzymes like catalase (CAT), superoxide dismutase (SOD), glutathione peroxidase (GSH-PX), and ascorbate peroxidase (APX). Therefore, antioxidants exhibit a biphasic response characterized by inducing a tolerance mechanism at low levels of ROS and inhibition or cell death at high concentrations of ROS [66,67,68].
Finally, this study shows that Nd(NO3)3@Zn-MOF stimulates growth and antioxidant responses during the in vitro culture of V. planifolia without causing phytotoxicity at high concentrations due to the prolonged release of Nd(III) from Zn-MOF. This hybrid compound could trigger advances in optimizing plant nutrition, as a biostimulant agent, and could represent a significant advance in crop productivity and sustainability. However, further research is required to validate its feasibility.

5. Conclusions

In this study, we obtained a hybrid compound and used it as a prolonged delivery system for neodymium nitrate in V. planifolia plantlets grown in vitro. We demonstrated that 10 mg L−1 of Nd(NO3)3@Zn-MOF stimulates the growth and antioxidant response of V. planifolia. At this concentration, the MOF can gradually release neodymium ions without causing phytotoxicity at high concentrations. To date, the synthesis of Nd(NO3)3@Zn-MOF has not been previously reported. Thus, integrating these materials into in vitro propagation would represent a novel approach to inducing biological activity, reducing costs, and supplying molecules of long-term interest. Finally, the possibility of using Nd(NO3)3@Zn-MOF in agriculture is promising. However, further studies are required to determine the viability of this compound in crops.

Author Contributions

Conceptualization, C.A.C.-C. and X.D.J.G.-Z.; methodology, X.D.J.G.-Z.; validation, J.L.S.-C., R.S.-P., R.C.-P. and R.P.-R.; formal analysis, J.L.S.-C.; investigation, X.D.J.G.-Z.; project administration, J.J.B.-B.; data interpretation and writing—original draft preparation, C.A.C.-C.; writing—review and editing, X.D.J.G.-Z.; validation, J.J.B.-B.; resources, J.J.B.-B. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by Consejo Veracruzano de Investigación Científica y Desarrollo Tecnológico (CP 2710 1427/2023).

Data Availability Statement

The original contributions presented in the study are included in the article, further inquiries can be directed to the corresponding authors.

Conflicts of Interest

The authors declare no conflicts of interest.

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Figure 1. Micrographs obtained using a stereoscope, X-ray powder diffractograms, and the proposed interaction of Nd(NO3)3@Zn-MOF. (a) Micrograph of the Zn-MOF crystals obtained from the stereoscope at 10× magnification, (b) micrograph of the Nd(NO3)3@Zn-MOF hybrid obtained from the stereoscope at 20× magnification, (c) experimental X-ray powder diffraction pattern of Zn-MOF crystals compared to the simulated pattern reported by [39], (d) experimental X-ray powder diffraction pattern of the Nd(NO3)3@Zn-MOF hybrid, (e) comparison of the spectra obtained from Nd(NO3)3@Zn-MOF by the Fourier transform infrared spectroscopy of the precursors and product, where the red row indicates a stretching vibration of the N-O bond in the nitrate ion and the blue row indicates a symmetric stretching vibration of the NO3 group, and (f) the pore structure of empty Zn-MOF. Viewer, Mercury 2022.2.0. Bar = 10 μm.
Figure 1. Micrographs obtained using a stereoscope, X-ray powder diffractograms, and the proposed interaction of Nd(NO3)3@Zn-MOF. (a) Micrograph of the Zn-MOF crystals obtained from the stereoscope at 10× magnification, (b) micrograph of the Nd(NO3)3@Zn-MOF hybrid obtained from the stereoscope at 20× magnification, (c) experimental X-ray powder diffraction pattern of Zn-MOF crystals compared to the simulated pattern reported by [39], (d) experimental X-ray powder diffraction pattern of the Nd(NO3)3@Zn-MOF hybrid, (e) comparison of the spectra obtained from Nd(NO3)3@Zn-MOF by the Fourier transform infrared spectroscopy of the precursors and product, where the red row indicates a stretching vibration of the N-O bond in the nitrate ion and the blue row indicates a symmetric stretching vibration of the NO3 group, and (f) the pore structure of empty Zn-MOF. Viewer, Mercury 2022.2.0. Bar = 10 μm.
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Figure 2. Effect of Nd(NO3)3@Zn-MOF on the in vitro development of plantlets of V. planifolia Jacks. ex Andrews. (a) Shoot length, (b) number of roots, (c) root length, and (d) number of leaves per shoot. Mean ± standard error (SE); different letters indicate statistical significance (Tukey, p ≤ 0.05).
Figure 2. Effect of Nd(NO3)3@Zn-MOF on the in vitro development of plantlets of V. planifolia Jacks. ex Andrews. (a) Shoot length, (b) number of roots, (c) root length, and (d) number of leaves per shoot. Mean ± standard error (SE); different letters indicate statistical significance (Tukey, p ≤ 0.05).
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Figure 3. Effect of Nd(NO3)3@Zn-MOF on the morphological development of vanilla plantlets (V. planifolia Jacks ex Andrews); (a–e) 0, 5, 10, 15, and 30 mg L−1 of Nd(NO3)3@Zn-MOF. Bar = 2 cm.
Figure 3. Effect of Nd(NO3)3@Zn-MOF on the morphological development of vanilla plantlets (V. planifolia Jacks ex Andrews); (a–e) 0, 5, 10, 15, and 30 mg L−1 of Nd(NO3)3@Zn-MOF. Bar = 2 cm.
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Figure 4. Effect of Nd(NO3)3@Zn-MOF on biochemical parameters of in vitro plantlets of vanilla (V. planifolia Jacks ex Andrews). (a) Chlorophyll, (b) β-carotene content, (c) antioxidant capacity expressed as TE (Trolox equivalents per g of fresh weight), and (d) phenolic content expressed as GAE (mg of gallic acid equivalent per g of fresh weight). Mean ± standard error (SE); different letters indicate statistical significance (Tukey, p ≤ 0.05).
Figure 4. Effect of Nd(NO3)3@Zn-MOF on biochemical parameters of in vitro plantlets of vanilla (V. planifolia Jacks ex Andrews). (a) Chlorophyll, (b) β-carotene content, (c) antioxidant capacity expressed as TE (Trolox equivalents per g of fresh weight), and (d) phenolic content expressed as GAE (mg of gallic acid equivalent per g of fresh weight). Mean ± standard error (SE); different letters indicate statistical significance (Tukey, p ≤ 0.05).
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Figure 5. Schematic representation showing the transport mechanisms and action sites of Nd(NO3)3@Zn-MOF in plantlets.
Figure 5. Schematic representation showing the transport mechanisms and action sites of Nd(NO3)3@Zn-MOF in plantlets.
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Cruz-Cruz, C.A.; De Jesús García-Zárate, X.; Spinoso-Castillo, J.L.; Peña-Rodríguez, R.; Colorado-Peralta, R.; Sánchez-Páez, R.; Bello-Bello, J.J. The Influence of the Hybrid Compound Nd(NO3)3@Zn-MOF on the Growth of Vanilla (Vanilla planifolia Jacks. ex Andrews) Cultured In Vitro: A Preliminary Study. Agronomy 2024, 14, 1880. https://doi.org/10.3390/agronomy14091880

AMA Style

Cruz-Cruz CA, De Jesús García-Zárate X, Spinoso-Castillo JL, Peña-Rodríguez R, Colorado-Peralta R, Sánchez-Páez R, Bello-Bello JJ. The Influence of the Hybrid Compound Nd(NO3)3@Zn-MOF on the Growth of Vanilla (Vanilla planifolia Jacks. ex Andrews) Cultured In Vitro: A Preliminary Study. Agronomy. 2024; 14(9):1880. https://doi.org/10.3390/agronomy14091880

Chicago/Turabian Style

Cruz-Cruz, Carlos Alberto, Xóchitl De Jesús García-Zárate, José Luis Spinoso-Castillo, Rodolfo Peña-Rodríguez, Raúl Colorado-Peralta, Ricardo Sánchez-Páez, and Jericó Jabín Bello-Bello. 2024. "The Influence of the Hybrid Compound Nd(NO3)3@Zn-MOF on the Growth of Vanilla (Vanilla planifolia Jacks. ex Andrews) Cultured In Vitro: A Preliminary Study" Agronomy 14, no. 9: 1880. https://doi.org/10.3390/agronomy14091880

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