Research Article

Horticultural Science and Technology. August 2021. 413-423
https://doi.org/10.7235/HORT.20210037

ABSTRACT


MAIN

  • Introduction

  • Materials and Methods

  •   Plant Material and Growth Conditions

  •   Treatments with Beneficial Elements

  •   Measurements of Growth Parameters

  •   Contents of Leaf Photosynthetic Pigments

  •   Statistical Analyses

  • Results

  •   Effect of Beneficial Elements on Seedling Growth

  •   Effect of Beneficial Elements on Biomass Production

  •   Effect of Beneficial Elements on Leaf Photosynthetic Pigments

  •   Correlation Among Parameters by Effect of Beneficial Elements

  • Discussion

  • Conclusions

Introduction

When supplied in small doses, the beneficial elements have positive effects on plants, such as promoting growth and development, stimulating resistance and tolerance mechanisms to biotic and abiotic stress factors, improving the use of other nutrients, and compensating for or remedying toxic effects caused by other elements (Pilon-Smits et al., 2009). The beneficial effects of these elements are determined by a series of factors, such as the concentration and speciation of the element, the plant species, the growth phase, the method of application (foliar or rooting), and the exposure time, all of which play an important role at the time of use (León-Morales et al., 2019). Elements that have been described as beneficial for plants include iodine (I), lanthanum (La), titanium (Ti), aluminum (Al), cobalt (Co), sodium (Na), selenium (Se), silicon (Si), cerium (Ce), and vanadium (V) (Gómez-Merino and Trejo-Téllez, 2018).

Vanadium is a transition metal that was initially classified as a highly toxic element for plants. However, low concentrations of this element can positively affect plant growth (Larsson et al., 2013). The toxicity of V is associated with its different oxidation states (+2, +3, +4, and +5), with the pentavalent form (+5) being the most toxic and its tetravalent form (+4) the least toxic (Akoumianaki-Ioannidou et al., 2016). In pennyroyal plants (Mentha pulegium L.), an increase in the dry weight of the roots was observed with doses of 340 µM V (Akoumianaki-Ioannidou et al., 2015). In tomato (Solanum lycopersicum L.) and bell pepper (Capsicum annuum L.) plants, doses of 3, 5, and 10 µM promoted the growth of both roots and shoots as well as the dry biomass of the seedlings (Saldaña-Sánchez et al., 2019).

Selenium is an essential element for mammals and some microorganisms (Hernández-Díaz et al., 2020). In plants, Se is considered a beneficial element and is found in four different oxidation states in the soil: selenate (SeO42-), selenite (SeO32-), Se elemental (Se0), and selenide (Se2-); selenate and selenite are the most common and available species for plants (Li et al., 2015). The application of Se in fava bean plants (Vicia faba L.) along with lead (Pb) induced oxidative stress and increased the content of chlorophyll a and b and carotenoids (Mroczek-Zdyrska et al., 2017). The application of Se in turnip plants (Brassica rapa L.) increased seed production by 43% (Lyons et al., 2009). In addition, the application of Se increased the yield of fresh biomass, leaf area, and quality of strawberry (Fragaria × ananassa Duch.) fruit (Mimmo et al., 2017) as well as the height of the seedlings and the growth of the roots of serrano bell pepper (Capsicum annuum L.) and radish (Raphanus sativus L.) plants (León-Morales et al., 2019).

Cerium is a rare earth metal that is present in two oxidation states: +3 and +4 (Rajeshkumar and Naik, 2018). In agriculture, Ce has been documented to have beneficial effects on plants (Ramírez-Olvera et al., 2018). For example, Hong et al. (2002) reported that Ce application led to the increased growth of spinach (Spinacia oleracea L.) plants as well as the proportion of chlorophyll. In addition, Ce has been shown to affect the germination rate, germination index, and vigor index of rice (Oryza sativa L.) seeds (Fashui, 2002). The application of Ce has also been correlated with greater growth, root volume, biomass weight, yield, total sugar content, and nutritional state of several cultivations (Hu et al., 2002; Ramírez-Olvera et al., 2018). In addition, the use of Ce nanoparticles has been suggested to increase the height, photosynthetic pigments, and antioxidant activity in marigold (Calendula officinalis L.) plants (Jahani et al., 2019).

Although I is essential for animals and accumulates strongly in seaweed, this element is considered beneficial for higher plants. In soil, I can be found in inorganic forms, such as iodide (I-) and iodate (IO3- ions), or in organic form, such as methyl iodide (CH3I) (Medrano-Macías et al., 2016). Positive effects of I have been described for celery (Apium graveolens L.) (Dai et al., 2004), lettuce (Lactuca sativa L.) (Smolen et al., 2011), and radish (Strzetelski et al., 2010). In contrast, high concentrations of I have been observed to induce biomass losses in potato (Solanum tuberosum L.) (Mao et al., 2014) and tobacco (Nicotiana tabacum L.) (Caffagni et al., 2011) and to cause phytotoxic symptoms, including chlorosis and necrosis, in lettuce (Lawson et al., 2015).

Marigold is an annual herbaceous plant belonging to the family Asteraceae. It is native to the Mediterranean area and currently occurs in various parts of the world because of its adaptability. Aside from being cultivated for ornamental purposes, it has many other uses because of its chemical composition, which includes terpenes, flavonoids, tannins, coumarins, and essential oils (Ashwlayan et al., 2018). Consequently, marigold is a valuable plant for the cosmetic, food, and pharmaceutical industries (Bragueto et al., 2019). Despite being a species of ornamental and industrial importance, little research has assessed the ability of different elements to promote its growth, development, and quality.

The aim of this study was to evaluate the effects of different concentrations of V, Se, Ce, and I on the growth, biomass accumulation, and concentration of photosynthetic compounds in marigold plants. Our findings could be used to obtain better quality seedlings and ensure the success of marigold cultivation.

Materials and Methods

Plant Material and Growth Conditions

A commercial variety of marigold (Calendula officinalis) (Hortaflor, Mexico) was used; the seeds were sown in flexible polyethylene germination trays with 98 cavities with commercial substrate for germination consisting of peat moss (0-7 mm fiber), wetting agent, dolomite, and NPK fertilizer (20-10-18, 1 kg per 1,000 L of substrate). The trays with the seeds were kept in the dark for 5 days. Afterwards, the experiment was conducted in a greenhouse with a plastic cover under natural light (509 W/m2 in average), with a 12-h photoperiod. The average temperatures during the day and night were 31°C and 16°C, respectively, and the relative humidity ranged from 42-69% (Onset, MX2301, USA).

Marigold seedlings were watered with tap water four days a week and three days a week with 50% Hoagland nutrient solution [0.5 mM (NH4) H2PO4, 2. 5 mM Ca (NO3)2 4H2O, 1 mM MgSO4 7H2O, 3 mM KNO3, 10 µM Fe-EDTA, and microelements (0.1 µM Na2MoO4 2H2O, 0.3 µM CuSO4 5H2O, 0.77 µM ZnSO4 7H2O, 9.1 µM MnCl2 4H2O and 46 µM H3BO3]. Distilled water was used for the preparation of the nutritive solution, and the pH was adjusted to 5.5 using NaOH or HCl.

Treatments with Beneficial Elements

Three concentrations of NH4VO3 (3, 5, and 10 µM V), Na2SeO3 (5, 10, and 20 µM Se), and CeCl3 (25, 50, and 100 µM Ce) and two concentrations of KI (5 and 10 µM I) were evaluated, in addition to the control (0 µM). All of the beneficial elements used were reactive grade (Sigma-Aldrich). The application of treatments began 20 days after sowing by supplying weekly irrigations applied to the root together with the nutritive solution for 26 days, with a total of four applications. Three 98-cavity trays were used per treatment. A completely randomized experimental design was used.

Measurements of Growth Parameters

The plants were measured at the seedling stage. Plant height was measured from the base of the plant to the apex of growth, and the root length from the base of the plant to the tip of the largest root. The root volume was established by the displacement of water with a 50-mL graduated glass probe. The stem diameter was measured at the base of the plant with digital Vernier calipers (Surtek, Urrea, Mexico). The number of leaves per plant was determined. The leaf area was also estimated by digitizing the leaves of each plant in a scanner (MPC3055P Lanier, Ricoh, USA) and measuring the leaf area with Image Processing and Analysis in Java (ImageJ). The weight of fresh biomass from roots, stems, and leaves was determined; the weight of dry biomass was obtained after drying the tissue in an oven (Yamato Scientific, DX402C, Japan) at 70°C for 48 h. Ten plants were measured per tray; the exception was for leaf area, where only five plants were measured per tray.

Contents of Leaf Photosynthetic Pigments

The fourth leaf from three plants was selected per treatment. The tissue was cut into small segments; 100 mg of fresh leaves was weighed and then immediately placed in 5 mL of acetone (80%, v/v). The samples were then placed at 4°C for 24 h. Chlorophyll and carotenoid concentration was determined following the methods of Arnon (1949) and Davies (1976). The absorbance of the supernatant was measured in a spectrophotometer (Thermo Scientific™, GENESYS 10uv, USA) at 645, 663, and 480 nm following the procedure of Saldaña-Sánchez et al. (2019).

Statistical Analyses

Analysis of variance was performed, and the difference between means was evaluated by Duncan's multiple range tests (p < 0.05). A Pearson's correlation analysis was performed using the SAS 9.1 statistical package (SAS Institute, Cary NC, USA). The heat map was created in Microsoft Excel (Microsoft Office Professional Plus, 2010).

Results

Effect of Beneficial Elements on Seedling Growth

The beneficial effects of V, Se, and Ce on the growth of marigold seedlings were reflected by increases in plant height under the concentrations of 5 and 10 µM V, 5 and 20 µM Se, and 50 and 100 µM Ce relative to the control. The two I treatments did not result in statistically significant increases in plant height. The concentration of 25 µM Ce reduced the height of marigold plants by 9.2% (Fig. 1).

/media/sites/kshs/2021-039-04/N0130390401/images/HST_39_04_01_F1.jpg
Fig. 1.

Marigold seedling height. The seedlings were watered with different concentrations of vanadium (V), selenium (Se), cerium (Ce), and iodine (I). Mean values ± SD. Different letters in each element section denote statistically significant differences according to Duncan's test (α = 0.05), p < 0.0001.

Most treatments did not significantly differ from the control in root length. In addition, a negative effect on root length was observed for the three concentrations of V and the highest concentrations of Ce (100 µM) and I (10 µM) (Table 1). The root volume did not significantly differ from the control under all of the treatments of V and 50 µM Ce; for the rest of the treatments, a reduction in root volume was observed relative to the control. There were no significant differences observed in the diameter of the stem between all of the treatments evaluated (Table 1).

Table 1.

Root length, root volume, and stem diameter of marigold seedlings with weekly applications of different concentrations of vanadium (V), selenium (Se), cerium (Ce), and iodine (I)

Beneficial elements Concentration (µM) Root length (cm) Root volume (mL) Stem diameter (mm)
Control 0 13.0 ± 1.4 ab 2.8 ± 0.3 a 2.58 ± 0.14 ab
V 3 11.2 ± 0.5 cd 2.3 ± 0.3 a-c 2.64 ± 0.16 ab
5 11.0 ± 0.4 cd 2.5 ± 0.2 ab 2.70 ± 0.13 a
10 10.4 ± 0.7 d 2.8 ± 0.4 a 2.70 ± 0.14 a
Se 5 12.7 ± 0.9 a-c 2.1 ± 0.3 b-d 2.58 ± 0.17ab
10 12.5 ± 0.9 bc 1.6 ± 0.2 e 2.34 ± 0.15 b
20 13.6 ± 1.0 ab 1.8 ± 0.2 de 2.79 ± 0.19 a
Ce 25 13.6 ± 1.1 ab 1.8 ± 0.2 de 2.73 ± 0.23 a
50 12.7 ± 0.6 a-c 2.7 ± 0.3 a 2.54 ± 0.11 ab
100 11.0 ± 0.8 cd 2.0 ± 0.2 b-e 2.85 ± 0.19 a
I 5 14.4 ± 1.0 a 1.7 ± 0.2 de 2.69 ± 0.17 a
10 11.2 ± 0.7 cd 1.9 ± 0.2 c-e 2.78 ± 0.16 a

Mean values ± SD, different letters in each section denote statistically significant differences according to Duncan's test (α = 0.05), root length and volume: p < 0.0001, stem diameter: p < 0.05.

The leaf area increased under the three concentrations of V, 20 µM Se, and 100 µM Ce; the rest of the treatments did not significantly differ from the control. Treatments with 3 and 10 µM V, 20 µM Se, three concentrations of Ce, and 5 µM I showed an increase in the number of leaves per marigold seedling relative to the control. Specifically, 5 µM I and 10 µM V produced 28.2 and 20.5% more leaves than the control, respectively (Fig. 2).

/media/sites/kshs/2021-039-04/N0130390401/images/HST_39_04_01_F2.jpg
Fig. 2.

The effect of the beneficial elements used on the leaf area (A) and the number of leaves (B) of marigold seedlings. Mean values ± SD. different letters in each element section denote statistically significant differences according to Duncan's test (α = 0.05), p < 0.0001.

Effect of Beneficial Elements on Biomass Production

The dry root biomass in marigold seedlings was greater under the application of 3 µM V; the rest of the treatments did not significantly differ from the control. The dry stem biomass of the seedlings followed a similar trend to that observed for dry root biomass; the use of 3 µM V increased the dry stem biomass by 62.5% compared with the control, and treatment with 5 µM I was also significantly higher than the control. The rest of the treatments evaluated did not significantly differ from the control. The percentage of dry leaf biomass of 20 µM Se, 100 µM Ce, and 5 µM I increased by 44.4, 41.6, and 39.4%, respectively, relative to the control. The dry leaf biomass increased as the dose of Ce increased; specifically, from 25 to 100 µM Ce, there was an increase from 11.1 to 41.6% in the dry weight of leaves (Fig. 3).

/media/sites/kshs/2021-039-04/N0130390401/images/HST_39_04_01_F3.jpg
Fig. 3.

Dry biomass of the root, stem, and leaves of marigold seedlings watered with different concentrations of vanadium (V), selenium (Se), cerium (Ce), and iodine (I). Mean values ± SD. Different letters in each element section denote statistically significant differences according to Duncan's test (α = 0.05), root: p < 0.05, stem: p < 0.05, leaves: p < 0.05.

Effect of Beneficial Elements on Leaf Photosynthetic Pigments

The evaluated treatments did not show significant changes in the chlorophyll concentration relative to the control; however, 25 µM Ce had a negative effect and led to decreases of 16.6 and 17.0% in the content of chlorophyll a and total chlorophyll, respectively. Chlorophyll b, total chlorophyll, and carotenoids responded positively to the application of 10 µM V and showed increases of 35.1, 20.5, and 20.4%, respectively, compared with the control. The photosynthetic pigments at all doses of Se and I did not significantly differ from the control (Table 2).

Table 2.

Chlorophyll and carotenoid content in leaves of marigold seedlings watered with different concentrations of vanadium (V), selenium (Se), cerium (Ce), and iodine (I)

Beneficial elements Concentration (µM) Chlorophyll content (µg·g-1 FW) Carotenoids
(ng·g-1 FW)
Chl a Chl b Chl total
Control 0 16.17 ± 1.01 a 4.83 ± 0.37 bc 21.00 ± 1.36 b 0.44 ± 0.02 bc
V 3 16.45 ± 0.97 a 5.18 ± 0.52 b 21.63 ± 1.45 ab 0.50 ± 0.03 ab
5 18.33 ± 0.39 a 5.74 ± 0.15 ab 24.07 ± 0.48 ab 0.49 ± 0.01 ab
10 18.80 ± 0.50 a 6.53 ± 0.26 a 25.32 ± 0.72 a 0.53 ± 0.02 a
Se 5 18.19 ± 0.86 a 5.58 ± 0.51 ab 23.77 ± 1.37 ab 0.49 ± 0.03 ab
10 16.77 ± 0.53 a 5.17 ± 0.22 b 21.93 ± 0.71 ab 0.46 ± 0.01 ab
20 16.75 ± 0.76 a 5.13 ± 0.26 bc 21.87 ± 0.99 ab 0.49 ± 0.02 ab
Ce 25 13.48 ± 1.58 b 3.96 ± 0.44 c 17.43 ± 2.01 c 0.39 ± 0.03 c
50 18.10 ± 0.34 a 5.44 ± 0.30 ab 23.54 ± 0.53 ab 0.52 ± 0.03 ab
100 17.41 ± 0.74 a 5.21 ± 0.12 b 22.61 ± 0.81 ab 0.48 ± 0.02 ab
I 5 18.57 ± 1.28 a 5.06 ± 0.58 bc 23.62 ± 1.19 ab 0.51 ± 0.02 ab
10 17.30 ± 0.70 a 5.04 ± 0.37 bc 22.33 ± 0.99 ab 0.51 ± 0.03 ab

Mean values ± SD, different letters confined to the same column show statistically significant differences according to Duncan’s test (α= 0.05), Chl a: p < 0.05, Chl: p < 0.05, b and Chl total: p < 0.01, Carotenoids: p < 0.01, FW: fresh weight.

Correlation Among Parameters by Effect of Beneficial Elements

The correlation analysis revealed significant and highly significant correlations between growth and biomass production parameters, whereas photosynthetic pigments were weakly correlated with the rest of the variables. Specifically, there was a highly significant correlation between the leaf area (LA) and all of the evaluated variables, including photosynthetic pigments. There was a negative correlation between root length (RL) and chlorophylls a (Chla) and b (Chlb), total chlorophyll (Chlt), and carotenoids (Car); however, only the correlation between RL and Chlb was significant. A highly significant positive correlation was also observed between chlorophylls and carotenoids (Fig. 4).

/media/sites/kshs/2021-039-04/N0130390401/images/HST_39_04_01_F4.jpg
Fig. 4.

Pearson’s correlations between the growth, biomass production, and photosynthetic pigment parameters of marigold seedlings in response to the application of vanadium (V), selenium (Se), cerium (Ce), and iodine (I). PH: plant height, RL: root length, SD: stem diameter, RV: root volume, FRW: fresh root weight, FSW: fresh stem weight, FLW: fresh leaf weight, DRW: dry root weight, DSW: dry stem weight, DLW: dry leaf weight, Chla: chlorophyll a, Chlb: chlorophyll b, Chlt: total chlorophyll, Car: carotenoids, LA: leaf area, NL: number of leaves. *p < 0.05, **p < 0.01.

Discussion

Currently, marigold production faces several challenges ranging from nutrient deficiency to biotic and abiotic factors that limit overall plant development. Beneficial elements such as V, Se, Ce, and I provide an alternative method for helping plants achieve greater height, leaf area, and dry biomass production of the root, stem, and leaf. The growth of the seedlings was enhanced under the application of 5 µM V (Fig. 1). Saldaña-Sánchez et al. (2019) applied the same concentration of V and observed an even greater growth of tomato and bell pepper plants. In addition, an increase in the foliar area of marigold plants at the three concentrations of V was observed. These results are inconsistent with previous findings in chili plants, where the foliar area of 5 and 10 µM V treatments did not significantly differ from the control (García-Jiménez et al., 2018). The positive effect of V on plant growth may stem from the synergistic effect of V with nitrogen metabolism, as V participates in the accumulation of nitrogen in plants (Grzanka et al. 2020).

The dry biomass of marigold root and stem was higher in seedlings treated with 3 µM V (Fig. 3). In pennyroyal, concentrations from 0 to 340 µM V stimulated the accumulation of dry root biomass (Akoumianaki-Ioannidou et al., 2016). In contrast, dry biomass and root length in rice can be reduced under concentrations of 128-590 µM V (Altaf et al., 2020). This finding can be attributed to mitotic cell division, which could restrict root tip development. Similarly, doses of 1.7-8.54 µM V have been reported to reduce fresh and dry root and shoot biomass of lettuce plants (Gil et al., 1995). In general, the application of 10 µM V increased leaf area (Fig. 2A), the number of leaves, and the amount of chlorophyll b, total chlorophyll, and carotenoids (Fig. 2B and Table 2) in marigold seedlings. In contrast, García-Jiménez et al. (2018) found that 5 µM V increased plant height and the number of leaves and flowers and induced chlorophyll synthesis in bell pepper. Thus, the effect of V depends on its concentration and plant species.

There are three possible ways in which V might influence the chlorophyll content. Firstly, V might act as an inducer at one or more sites in the chlorophyll biosynthetic pathway; secondly, V might have a synergistic effect on the bioavailability of Fe and Mg and support chlorophyll biosynthesis; and thirdly, V might prevent the degradation of chlorophylls by affecting certain enzyme systems in plants (Aihemaiti et al., 2020). There is currently no information on the effect of V on marigold plants. Nevertheless, V has been used as an elicitation strategy in in vitro cultures for the synthesis of secondary metabolites (Siatka and Kasparová, 2007). Therefore, the use of V during marigold culture could contribute to the biosynthesis of a greater number of bioactive compounds that are naturally found in low concentrations. This property could be exploited by the food industry in fortified foods, such as yogurt (Bragueto et al., 2019).

In this study, 5 and 20 µM Se resulted in increases in the height of marigold seedlings, which might be related to the capacity of Se to improve the antioxidant activities in plants and thus improve their growth (Boldrin et al., 2016). At the same time, 20 µM Se resulted in greater leaf area of marigold seedlings (Fig. 2A). This finding is consistent with Mimmo et al. (2017), who used concentrations of 0, 10, and 100 µM Se to achieve a higher percentage of leaf area in strawberry plants. Likewise, a positive effect was observed under the application of 20 µM Se on the dry biomass of marigold leaves (Fig. 3). Similar results were observed in turnip (Brassica rapa), where 2.89 µM promoted the accumulation of dry leaf biomass (Li et al., 2018). In some cases, the positive effect of Se is attributed to an increase in the antioxidant activity of plant tissues as well as to the control of reactive oxygen species (ROS) originating from photosynthesis (Thavarajah et al., 2015). In contrast, Se had negative effects on root volume, which might stem from morphological changes in the root system and thus negatively affect the efficiency of water and nutrient uptake (Hartikainen et al., 2001).

The three concentrations of Se did not significantly differ from the control in the concentration of chlorophylls and carotenoids (Table 2). In contrast, with doses of 200 µM of Se, the content of these photosynthetic pigments in Ulva australis increased greatly; this effect was related to Se toxicity, suggesting that it might be a mechanism of tolerance for this type of toxicity (Schiavon et al., 2016). However, D’Amato et al. (2018) noted that low concentrations of Se could have a positive effect on chlorophyll and carotenoid biosynthesis. To date, there are no studies that have examined the possible effects of Se on marigold production. One study reported a low Se content in marigold plants (Sotek et al., 2018); thus, studies on Se supplementation would be highly relevant to this plant species.

The application of 50 and 100 µM Ce in marigold increased the height of the seedlings (Fig. 1). In other crops, doses of 50 and 100 µM Ce increased the height of tomato plants by 15% (Saldaña-Sánchez et al., 2019). In marigold roots, 100 µM Ce reduced root length and root volume (Table 1). Similarly, Ramírez-Olvera et al. (2018) indicated that doses of 100 µM Ce affected root length in rice. In contrast, root growth inhibition caused by Ce might be attributed to various factors, such as loss of cell turgor or decreased cell wall extensibility, which might be related to deficiencies in certain enzymes involved in energy utilization (Shyam and Aery, 2012). D’Aquino et al. (2009) attributed the reduction in roots after Ce treatment to a low rate of cell division.

However, 25 µM Ce reduced the chlorophyll a and total chlorophyll content of marigold seedlings (Table 2). These results are consistent with those of Zicari et al. (2018) for water lentil (Lemna minor L.), where concentrations of 500 µM Ce decreased the concentration of chlorophyll a and b. This pattern might stem from the fact that high concentrations of Ce can be associated with losses in the proportion of chlorophyll a induced by the activation of chlorophyllase, an enzyme responsible for the degradation of chlorophyll (Shyam and Aery, 2012). In the case of marigold, information is lacking on the possible effect that this element might have on photosynthetic parameters, given that these are smaller doses than those reported by Zicari et al. (2018) However, there is evidence that the use of Ce nanoparticles at concentrations of 290-581 µM increased the fresh and dry biomass of leaves as well as the foliar area and chlorophyll content in marigold plants (Jahani et al., 2019). Although Ce doses were higher than the concentrations used in this study in this last case, nanoparticles have drastically different effects, including reduced toxicity, compared with ionic forms of elements (Hernández-Díaz et al., 2020).

Finally, with the treatment of 5 µM I, marigold plants developed a greater number of leaves (Fig. 2B). In contrast, 10 µM I had a negative effect on root length and root volume (Table 1). Consistent with these results, Zhu et al. (2003) reported that concentrations greater than 10 µM I had detrimental effects on spinach plant growth. This phenomenon has been suggested to occur because of the excessive accumulation of I in plant tissues. In contrast, a synergistic effect was recently reported using 10 µM I combined with 0.1 µM V in corn plants, which led to an increase in plant height by 12% (Grzanka et al., 2020). The application of 5 µM I significantly increased the dry biomass of the stem and leaves (Fig. 3). Similar results were observed for dried cabbage leaf biomass, but these data contrast with data from tomato where no significant differences were observed under concentrations of 0.4-2.33 µM I (Dobosy et al., 2020). This finding is also consistent with results obtained in marigold at concentrations of 10 µM I (Fig. 3). In marigold, no studies to date have established beneficial or harmful effects of I application during its cultivation.

Conclusions

The results of this study indicate that the application of low concentrations of I, Se, and V, as well as high concentration of Ce, had a positive effect on the growth, biomass accumulation, and content of photosynthetic compounds during the initial stage of marigold growth. Low doses of these beneficial elements could be applied throughout the crop cycle to improve the growth of marigold plants, as well as to promote the biosynthesis of bioactive compounds. To our knowledge, this is the first study to examine the use of beneficial elements such as V, Se, and I in marigold, a species of great importance to the cosmetic, food, and pharmaceutical industries.

Acknowledgements

This work was supported by the Consejo Nacional de Ciencia y Tecnología (CONACYT, Mexico) under Grant PlanTECC 314926-2020. The authors would like to thank the CONACYT for the MSc Scholarship of JA Hernández-Díaz (717214) and JJO Garza-García (717217).

References

1
Aihemaiti A, Gao Y, Meng Y, Chen X, Liu J, Xiang H, Xu Y, Jiang J (2020) Review of plant-vanadium physiological interactions, bioaccumulation, and bioremediation of vanadium-contaminated sites. Sci Total Environ 712:135637. doi:10.1016/j.scitotenv.2019.135637 10.1016/j.scitotenv.2019.13563731810710
2
Akoumianaki-Ioannidou A, Barouchas PE, Ilia E, Kyramariou A, Moustakas NK (2016) Effect of vanadium on dry matter and nutrient concentration in sweet basil (Ocimum basilicum L.). Aust J Crop Sci 10:199-206
3
Akoumianaki-Ioannidou A, Barouchas PE, Kyramariou A, Ilia E, Moustakas NK (2015) Effect of vanadium on dry matter and nutrient concentration in pennyroyal (Mentha pulegium L). Bull UASVM Hortic 72:295-298. doi:10.15835/buasvmcn-hort:11348 10.15835/buasvmcn-hort:11348
4
Altaf MM, Diao XP, Rehman A, Imtiaz M, Shakoor A, Altaf MA, Younis H, Fu P, Ghani MU (2020) Effect of vanadium on growth, photosynthesis, reactive oxygen species, antioxidant enzymes, and cell death of rice. J Soil Sci Plant Nutr 20:2643-2656. doi:10.1007 /s42729-020-00330-x 10.1007/s42729-020-00330-x
5
Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1-15. doi:10.1104/pp.24.1.1 10.1104/pp.24.1.1
6
Ashwlayan VD, Kumar A, Verma M, Garg VK, Gupta SK (2018) Therapeutic potential of Calendula officinalis. Pharm Pharmacol Int J 6:149-155. doi:10.15406/ppij.2018.06.00171 10.15406/ppij.2018.06.00171
7
Boldrin PF, de Figueiredo MA, Yang Y, Luo H, Giri S, Hart JJ, Faquin V, Guilherme LRG, Thannhauser TW, et al. (2016) Selenium promotes sulfur accumulation and plant growth in wheat (Triticum aestivum). Physiol Plant 158:80-91. doi:10.1111/ppl.12465 10.1111/ppl.12465
8
Bragueto EG, Cardoso BLC, Sousa SJ, Mendanha CT, Boscacci MM, Araújo VM, Azevedo L, Furtado MM, Sant'Ana AS, et al. (2019) From the field to the pot: Phytochemical and functional analyses of Calendula officinalis L. flower for incorporation in an organic yogurt. Antioxidants 8:559. doi:10.3390/antiox8110559 10.3390/antiox8110559
9
Caffagni A, Arru L, Meriggi P, Milc J, Perata P, Pecchioni N (2011) Iodine fortification plant screening process and accumulation in tomato fruits and potato tubers. Commun Soil Sci Plant Anal 42:706-718. doi:10.1080/00103624.2011.550372 10.1080/00103624.2011.550372
10
D'Amato R, Fontanella MC, Falcinelli B, Beone GM, Bravi E, Marconi O, Benincasa P, Businelli D (2018) Selenium biofortification in rice (Oryza sativa L.) sprouting: effects on Se yield and nutritional traits with focus on phenolic acid profile. J Agric Food Chem 66:4082-4090. doi:10.1021/acs.jafc.8b00127 10.1021/acs.jafc.8b00127
11
D'Aquino L, de Pinto MC, Nardi L, Morgana M, Tommasi F (2009) Effect of some light rare earth elements on seed germination, seedling growth and antioxidant metabolism in Triticum durum. Chemosphere 75:900-905. doi:10.1016/j.chemosphere.2009.01.026 10.1016/j.chemosphere.2009.01.026
12
Dai JL, Zhu YG, Zhang M, Huang YZ (2004) Selecting iodine-enriched vegetables and the residual effect of iodate application to soil. Biol Trace Elem Res 101:265-276. doi:10.1385/BTER:101:3:265 10.1385/BTER:101:3:265
13
Davies B (1976) Carotenoids. In TW Goodwin, ed, Chemistry and biochemistry of plant pigments. Academic Press, London, UK, pp 38-165
14
Dobosy P, Vetési V, Sandil S, Endrédi A, Kröpfl K, Óvári M, Takács T, Rékási M, Záray G (2020) Effect of irrigation water containing iodine on plant physiological processes and elemental concentrations of cabbage (Brassica oleracea L. var. capitata) and tomato (Solanum lycopersicum L.) cultivated in different soils. Agronomy 10:720. doi:10.3390/agronomy10050720 10.3390/agronomy10050720
15
Fashui H (2002) Study on the mechanism of cerium nitrate effects on germination of aged rice seed. Biol Trace Elem Res 87:191-200. doi:10.1385/BTER:87:1-3:191 10.1385/BTER:87:1-3:191
16
García-Jiménez A, Trejo-Téllez LI, Guillén-Sánchez D, Gómez-Merino FC (2018) Vanadium stimulates pepper plant growth and flowering, increases concentrations of amino acids, sugars and chlorophylls, and modifies nutrient concentrations. PLoS ONE 13:e0201908. doi:10.1371/journal.pone.0201908 10.1371/journal.pone.020190830092079PMC6085002
17
Gil J, Alvarez CE, Martinez MC, Pérez N (1995) Effect of vanadium on lettuce growth, cationic nutrition, and yield. J Environ Sci Health A 30:73-87. doi:10.1080/10934529509376186 10.1080/10934529509376186
18
Gómez-Merino FC, Trejo-Téllez LI (2018) The role of beneficial elements in triggering adaptive responses to environmental stressors and improving plant performance. In S Vats, ed, Biotic and abiotic stress tolerance in plants. Springer, Singapore, pp 137-172. doi:10.1007/978-981-10-9029-5_6 10.1007/978-981-10-9029-5_6
19
Grzanka M, Smoleń S, Kováčik P (2020) Effect of vanadium on the uptake and distribution of organic and inorganic forms of iodine in sweetcorn plants during early-stage development. Agronomy 10:1666. doi:10.3390/agronomy10111666 10.3390/agronomy10111666
20
Hartikainen H, Pietola L, Simojoki A (2001) Quantification of fine root responses to selenium toxicity. Agric Food Sci 10:53-58. doi:10.23986/afsci.5679 10.23986/afsci.5679
21
Hernández-Díaz JA, Garza‐García JJO, Zamudio‐Ojeda A, León-Morales JM, López-Velázquez JC, García‐Morales S (2020) Plant‐mediated synthesis of nanoparticles and their antimicrobial activity against phytopathogens. J Sci Food Agric (in press). doi:10.1002/jsfa.10767 10.1002/jsfa.10767
22
Hong F, Wang L, Meng X, Wei Z, Zhao G (2002) The effect of cerium (III) on the chlorophyll formation in spinach. Biol Trace Elem Res 89:263-276. doi:10.1385/BTER:89:3:263 10.1385/BTER:89:3:263
23
Hu X, Ding Z, Wang X, Chen Y, Dai L (2002) Effects of lanthanum and cerium on the vegetable growth of wheat (Triticum aestivum L.) seedlings. Bull Environ Contam Toxicol 69:727-733. doi:10.1007/s00128-002-0121-7 10.1007/s00128-002-0121-7
24
Jahani S, Saadatmand S, Mahmoodzadeh H, Khavari-Nejad RA (2019) Effect of foliar application of cerium oxide nanoparticles on growth, photosynthetic pigments, electrolyte leakage, compatible osmolytes and antioxidant enzymes activities of Calendula officinalis L. Biologia 74:1063-1075. doi:10.2478/s11756-019-00239-6 10.2478/s11756-019-00239-6
25
Larsson MA, Baken S, Gustafsson JP, Hadialhejazi G, Smolders E (2013) Vanadium bioavailability and toxicity to soil microorganisms and plants. Environ Toxicol Chem 32:2266-2273. doi:10.1002/etc.2322 10.1002/etc.232223832669
26
Lawson PG, Daum D, Czauderna R, Meuser H, Härtling JW (2015) Soil versus foliar iodine fertilization as a biofortification strategy for field-grown vegetables. Front Plant Sci 6:450. doi:10.3389/fpls.2015.00450 10.3389/fpls.2015.0045026157445PMC4477264
27
León-Morales JM, Panamá-Raymundo W, Langarica-Velázquez EC, García-Morales S (2019) Selenium and vanadium on seed germination and seedling growth in pepper (Capsicum annuum L.) and radish (Raphanus sativus L.). Bio Ciencias 6:e425. doi:10.15741/revbio.06.e425 10.15741/revbio.06.e425
28
Li J, Liang D, Qin S, Feng P, Wu X (2015) Effects of selenite and selenate application on growth and shoot selenium accumulation of pak choi (Brassica chinensis L.) during successive planting conditions. Environ Sci Pollut Res Int 22:11076-11086. doi:10.1007/s11356-015-4344-7 10.1007/s11356-015-4344-7
29
Li X, Wu Y, Li B, Yang Y, Yang Y (2018) Selenium accumulation characteristics and biofortification potentiality in turnip (Brassica rapa var. rapa) supplied with selenite or selenate. Front Plant Sci 8:2207. doi:10.3389/fpls.2017.02207 10.3389/fpls.2017.02207
30
Lyons GH, Genc Y, Soole K, Stangoulis JCR, Liu F, Graham RD (2009) Selenium increases seed production in Brassica. Plant Soil 318:73-80. doi:10.1007/s11104-008-9818-7 10.1007/s11104-008-9818-7
31
Mao H, Wang J, Wang Z, Zan Y, Lyons G, Zou C (2014) Using agronomic biofortification to boost zinc, selenium, and iodine concentrations of food crops grown on the loess plateau in China. J Soil Sci Plant Nutr 14:459-470. doi:10.4067/S0718-95162014005000036 10.4067/S0718-95162014005000036
32
Medrano-Macías J, Leija-Martínez P, González-Morales S, Juárez-Maldonado A, Benavides-Mendoza A (2016) Use of iodine to biofortify and promote growth and stress tolerance in crops. Front Plant Sci 7:1146. doi:10.3389/fpls.2016.01146 10.3389/fpls.2016.0114627602033PMC4993787
33
Mimmo T, Tiziani R, Valentinuzzi F, Lucini L, Nicoletto C, Sambo P, Scampicchio M, Pii Y, Cesco S (2017) Selenium biofortification in fragaria × ananassa: implications on strawberry fruits quality, content of bioactive health beneficial compounds and metabolomic profile. Front Plant Sci 8:1887. doi:10.3389/fpls.2017.01887 10.3389/fpls.2017.01887
34
Mroczek-Zdyrska M, Strubińska J, Hanaka A (2017) Selenium improves physiological parameters and alleviates oxidative stress in shoots of lead-exposed Vicia faba L. minor plants grown under phosphorus-deficient conditions. J Plant Growth Regul 36:186-199. doi:10.1007/s00344-016-9629-7 10.1007/s00344-016-9629-7
35
Pilon-Smits EAH, Quinn CF, Tapken W, Malagoli M, Schiavon, M (2009) Physiological functions of beneficial elements. Curr Opin Plant Biol 12:267-274. doi:10.1016/j.pbi.2009.04.009 10.1016/j.pbi.2009.04.00919477676
36
Rajeshkumar S, Naik P (2018) Synthesis and biomedical applications of Cerium oxide nanoparticles-A Review. Biotechnol Rep 17:1-5. doi:10.1016/j.btre.2017.11.008 10.1016/j.btre.2017.11.008
37
Ramírez-Olvera SM, Trejo-Téllez LI, García-Morales S, Pérez-Sato JA, Gómez-Merino FC (2018) Cerium enhances germination and shoot growth, and alters mineral nutrient concentration in rice. PLoS ONE 13:e0194691. doi:10.1371/journal.pone.0194691 10.1371/journal.pone.019469129579100PMC5868810
38
Saldaña-Sánchez WD, León-Morales JM, López-Bibiano Y, Hernández-Hernández M, Langarica-Velázquez EC, García-Morales S (2019) Effect of V, Se, and Ce on growth, photosynthetic pigments, and total phenol content of tomato and pepper seedlings. J Soil Sci Plant Nutr 19:678-688. doi:10.1007/s42729-019-00068-1 10.1007/s42729-019-00068-1
39
Schiavon M, Pilon-Smits EAH, Citta A, Folda A, Rigobello MP, Vecchia FD (2016) Comparative effects of selenate and selenite on selenium accumulation, morphophysiology, and glutathione synthesis in Ulva australis. Environ Sci Pollut Res 23:15023-15032. doi:10.1007/s11356-016-6649-6 10.1007/s11356-016-6649-6
40
Shyam R, Aery NC (2012) Effect of cerium on growth, dry matter production, biochemical constituents and enzymatic activities of cowpea plants [Vigna unguiculata (L.) Walp.]. J Soil Sci Plant Nutr 12:1-14. doi:10.4067/S0718-95162012000100001 10.4067/S0718-95162012000100001
41
Siatka T, Kasparová M (2007) Effect of vanadium compounds on the growth and production of coumarins in the suspension culture of Angelica archangelica L. Ceska Slov Farm 56:230-234.
42
Smolen S, Rozek S, Ledwozyw-Smolen I, Strzetelski P (2011) Preliminary evaluation of the influence of soil fertilization and foliar nutrition with iodine on the efficiency of iodine biofortification and chemical composition of lettuce. J Elem 16:613-622. doi:10.5601/jelem.2011.16.4.10 10.5601/jelem.2011.16.4.10
43
Sotek Z, Białecka B, Pilarczyk B, Kruzhel B, Drozd R, Tomza-Marciniak A, Pilarczyk R, Lysak H, Bąkowska M, et al.(2018) The content of selenium, polyphenols and antioxidative activity in selected medicinal plants from Poland and Western Ukraine. Acta Pol Pharm Drug Res 75:1107-1116. doi:10.32383/appdr/82775 10.32383/appdr/82775
44
Strzetelski P, Smoleń S, Rozek S, Sady W (2010) The effect of diverse iodine fertilization on nitrate accumulation and content of selected compounds in radish plants (Raphanus sativus L.). Acta Sci Pol 9:65-73.
45
Thavarajah D, Thavarajah P, Vial E, Gebhardt M, Lacher C, Kumar S, Combs GF (2015) Will selenium increase lentil (Lens culinaris Medik) yield and seed quality? Front Plant Sci 6:356. doi:10.3389/fpls.2015.00356 10.3389/fpls.2015.00356
46
Zhu YG, Huang YZ, Hu Y, Liu YX (2003) Iodine uptake by spinach (Spinacia oleracea L.) plants grown in solution culture: effects of iodine species and solution concentrations. Environ Int 29:33-37. doi:10.1016/S0160-4120(02)00129-0 10.1016/S0160-4120(02)00129-0
47
Zicari MA, d'Aquino L, Paradiso A, Mastrolitti S, Tommasi F (2018) Effect of cerium on growth and antioxidant metabolism of Lemna minor L. Ecotoxicol Environ Saf 163:536-543. doi:10.1016/j.ecoenv.2018.07.113 10.1016/j.ecoenv.2018.07.113
페이지 상단으로 이동하기