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Article

Effect of Zinc Excess on Some Physiological Parameters and on the Fatty Acids Profile of Sinapis alba L. and Brassica juncea L. (Czern)

by
Natalia Repkina
*,
Svetlana A. Murzina
,
Viktor P. Voronin
and
Natalia Kaznina
Institute of Biology of the Karelian Research Centre of the Russian Academy of Sciences (IB KarRC RAS), 11 Pushkinskaya St., Petrozavodsk185910, Russia
*
Author to whom correspondence should be addressed.
Horticulturae 2023, 9(9), 1002; https://doi.org/10.3390/horticulturae9091002
Submission received: 7 August 2023 / Revised: 30 August 2023 / Accepted: 2 September 2023 / Published: 5 September 2023
(This article belongs to the Special Issue Horticultural Crop Physiology under Biotic and Abiotic Stresses)
Browse Figure
Versions Notes

Abstract

:
Zinc (Zn) is a vital micronutrient for all living organisms, but in high concentrations, it is a major anthropogenic pollutant. In this study, it was investigated the effect of zinc excess concentrations (50, 100, and 150 mg kg−1) in the substrate on some physiological parameters and the dynamics of fatty acid (FA) content in yellow mustard (Sinapis alba L. cv. Belgia) and oriental mustard (Brassica juncea L. (Czern) cv. Slavanka). The Zn concentration of 50 mg kg−1 did not affect the physiological parameters of yellow mustard, whereas some physiological parameters slightly decreased in oriental mustard. Moreover, this concentration stimulated an increase in total and unsaturated FAs content in leaves of both species, along with high Zn accumulation by both species. The Zn concentrations of 100 and 150 mg kg−1 in substrate had a negative effect on the state of plants as measured by the studied physiological parameters and caused different changes in FAs content in yellow and oriental mustard. Particularly, the total amount of FA increased in comparison to the control, but this increase was due to an elevation in saturated FA (SFA) content. At the same time, the total FA content in oriental mustard slightly decreased while the proportion of unsaturated FAs to SFA kept rising. According to the present data and analysis of the available literature, two strategies of adaptation to heavy metals were suggested through the changes in FAs: height-resistant horticultural plant species on the one side and sensitive species on the other.

1. Introduction

The gradual buildup of pollution with heavy metals, especially in agricultural areas, is one of the greatest worldwide concerns due to the hazards of pollutants for all living organisms [1,2]. Heavy metals include elements with an atomic mass greater than 40 Da and a density of 5.31–22.0 g cm−3 [3]. Some of these elements are essential for plants’ metabolism, whereas others are non-essential and can be toxic even at low concentrations [4]. Among metals, zinc (Zn) is an essential micronutrient required at low concentrations (up to 150 ppm) for the growth and development of the majority of plant species [5]. Zn is a valuable element for the metabolism of all living organisms [6]. For instance, Zn is a structural component of a number of proteins. Among the structural domains of proteins, Zn finger domains have a major physiological relevance [7,8]. Zn-binding enzymes (RNA polymerase, alcohol dehydrogenase, carbonic anhydrase, and Cu/Zn-superoxide dismutase) are involved in translation, transpiration, photosynthesis, and the metabolism of reactive oxygen species [9]. In addition to this, the role of Zn in cell proliferation, membrane stabilization, prevention of oxidative stress, regulation of transcription, and autophagy has also been reported [10,11]. Although Zn is an essential microelement, elevated concentrations (more than 100 mg kg−1) of this metal in soils can lead to toxicity symptoms in plants [5].
The source of heavy metal contamination can be natural or anthropogenic as a result of agricultural activities [3,4]. Particularly, oversupplementation of Zn-containing fertilizers into soils causes a higher Zn ion concentration and affects crop yield is affected [2,12]. However, plants have a wide range of mechanisms of tolerance for preventing the damage effect of metal excess [3]. The defense reactions include: an increase in lignification of the cell wall for prevention of the transport of metal ions into the cell; the synthesis of chelating agents that are conjugated with ions, further inactivating them; a rise in the activity of antioxidant enzymes, preventing the development of oxidative stress, etc. [3,13,14]. It should be noted that data about the effects of heavy metals on fatty acid (FA) profiles is practically nonexistent. Furthermore, quality and quantity changes of FAs are important for maintaining the structure of membranes at the cellular level under optimum and stress growth conditions [15,16]. It is well known that FAs are constituents of lipids, which play various roles in cells as essential and basement components of membrane structure and participate in various signaling pathways [17]. Moreover, the content of FAs is important in estimating food’s nutritional value [18]. According to this, the study of changes in FAs profile under heavy metal influence is important for the assessment of agricultural crops. Sinapis alba (yellow mustard) and Brassica juncea (oriental mustard) plants belong to the Brassicaceae family. Some plant species from this family are capable of accumulating metal ions in high amounts and are used in phytoremediation (the technology of cleaning up the substrate by plants) [19,20,21,22]. Usually, B. juncea is classified as a “hyperaccumulator” (a group of plant species that accumulate high concentrations of metal ions in their aboveground parts) [23,24]. partly due to the fact that oriental mustard is able to accumulate high concentrations of metals and has a high activity of transport proteins involved in the translocation of ions through the plasmalemma to the root and further to the aboveground organs [25]. It was also demonstrated that B. juncea has higher levels of salicylic and glutamic acids, which facilitate the effective binding of metal ions and further sequester them into vacuoles [26]. At the same time, there are opposite data that demonstrate no significant metal ion accumulation by oriental mustard in comparison to other species of the Brassicaceae family [27,28]. With respect to yellow mustard, the data is limited, but some fragmentary research showed its capability to accumulate significant metal ions [29]. Both plant species are valuable for the food industry [30]. So the accumulation of heavy metal ions will have important consequences. Yellow and oriental mustard is a source for oil and spice [31], fodder [32], as well as biofuel production [33,34]. One of the key criteria for assessing the quality of plant raw materials is the determination of the qualitative and quantitative characteristics of the FA profile. Nowadays, there are a few reports demonstrating the changes in FAs profiles in plants under heavy metal effects, but the role of FAs in mechanisms of adaptation to heavy metals is still poorly studied.
The present study was undertaken to evaluate the response of yellow mustard and oriental mustard, particularly changes in FAs profiles under growing at high Zn concentrations in substrate. It has been suggested that, like any stressor, an excess of zinc can lead to quantitative changes in the composition of FAs, which can improve or worsen the nutritional value of plant raw materials. At the same time, a change in the composition of FAs, as one of the mechanisms of adaptation, can be implemented differently in two ways under the influence of excess zinc.

2. Materials and Methods

2.1. Plant Material, Growth Conditions, and Organization of the Experiment

Seeds of yellow mustard (Sinapis alba L. cv. Belgia) and oriental mustard (Brassica juncea L. (Czern) cv. Slavyanka) were acquired from the Federal Research Center N. I. Vavilov All-Russian Institute of Plant Genetic Resources (VIR), Ministry of Science and Higher Education, Russia. This study was conducted at the research base of the Agricultural Experiment Station (61°45′6″ N, 119°25′10.9″ E) (WGS84), Petrozavodsk, Republic of Karelia, Russia. The day before sowing, mustard seeds were soaked in distilled water. Two-day-old seedlings (12 seedlings per pot) were placed in plastic pots (1 L). Each pot contains 0.8 kg of pure quartz sand. Appropriate amounts of the sulfate salt of Zn (ZnSO4 × H2O) were once added to the sand to maintain the required level of Zn: 5 (control), 50, 100, and 150 mg kg−1 of the substrate. These concentrations are in comparison to the optimum, which is two-foldhigher than maximum allowable concentrations (MAC), four-foldhigher than MAC, and six-foldhigher than MAC in sand. The standards of MAC were published by the Ministry of Agriculture (GN 2.1.7.2041-06 from 2006). Before the seeds were sown, the sand in the pots was mixed in order to ensure a uniform distribution of the elements. During the growing period, pots have been irrigated with Hoagland-Arnon nutrient solution (pH 6.2), excluding Zn addition. All pots were placed in a greenhouse under natural day/night conditions with a day/night temperature of 21/14 ± 2 °C and 77 ± 5% relative humidity during the growing period. The experimental design was completely randomized with three replications. Plants were harvested and analyzed after 3 weeks (stage of 3–4 true leaves).

2.2. Parameters Determined

2.2.1. Determination of Zinc Content

An inductively coupled plasma-mass spectrometry (ICP-MS) (Agilent 7900, Santa Clara, CA, USA) analysis was performed to determine the concentration of Zn in the roots and shoots of plants. The samples were digested by microwave using the Speedwave Digestion System (Berghof, Eningen, Germany). The extraction was performed in a solution of nitric acid. The data was expressed as mg kg−1DW, where DW is the dry weight that was evaluated after drying the aboveground parts of plants to a constant weight at 80 °C.

2.2.2. Growth-Related Parameters and Photosynthetic Rate Measurement

Fresh weight (FW) (g) was measured immediately after harvest and the separation of plants into shoots and roots. The leaf area was analyzed by AreaS 2.01 (Gust, Moscow, Russia). The net photosynthetic rate (Pn) (µmol CO2 m−2s−1) was measured on the first true leaves using the portable photosynthesis system HCM-1000 (Walz, Effeltrich, Germany).

2.2.3. Analysis of Relative Electrolyte Leakage

The relative electrolyte leakage (REL) was measured by the electrical conductivity method as described by [35] with slight modifications. Fresh leaves were cut into pieces of 0.5 cm2 square, rinsed with deionized water, and put into 30 mL of deionized water in a test tube. After vacuuming for 10 min, tubes were stored at room temperature for 4 h. The initial electrolyte leakage (EL0) was measured using a conductometer (HANNA, Woonsocket, Italy). The tubes were subsequently boiled at 100 °C for 30 min to release all the electrolytes into the solution, cooled to 25 °C, and the final electrolytic leakage (EL1) was measured. REL was calculated according to the following formula: (EL0/EL1) × 100 and expressed as a percentage of total conductivity.

2.2.4. Photosynthetic Pigments Content Measurement

Chlorophyll a (Chla), chlorophyll b (Chlb), total chlorophylls, and carotenoids were determined spectrophotometrically on an SF2000 spectrophotometer (Spectrum, Moscow, Russia) [36]. For the extraction of assimilatory pigments, 85% (v/v) aqueous acetone was used. The absorbance of the supernatant was measured at 665, 649, and 440.5 nm alongside a blank of untainted 85% liquid acetone. Photosynthetic pigment concentrations were analyzed using known formulas [36]. The percentage of Chl in light harvesting complex II (LHCII) was calculated by accepting that almost all Chlb is in LHCII and that the ratio of Chla and Chlb in LHCII is 1.2 [37].

2.2.5. Lipids Extraction and Fatty Acids Analysis

The total lipids (TL) from 0.2 g of fresh leaves (a mixed sample from 10 leaves of seedlings) were extracted using the Folch method with a mixture of chloroform and methanol (2:1 v/v) [38]. In brief, the samples were filtered using a paper filter, Red Ribbon (pore size 5–8 μm) with 20 mL of the mixture, after which the precipitate on the filter was washed with 10 mL of pure chloroform. To remove water-soluble impurities, 10 mL of purified deionized water (Simplicity, Millipore, Merck, Darmstadt, Germany) was added to the filtered mixture and left for 2 h in separating funnels (Schott Duran, Mainz, Germany) until the organic phases were completely separated. Lipids remained in the lower chloroform layer, whereas non-lipid substances moved to the upper aqueous methanol phase. Then, the chloroform layer was withdrawn to evaporate under a vacuum on a rotary evaporator—Hei-VAP Advantage HL/G3 (Heidolph, Schwalbach, Germany)—and dried in a vacuum over phosphoric anhydride to a constant weight. The dried samples were redissolved with chloroform-methanol (1:1, v/v) and stored at −20 °C until further processing.
The qualitative and quantitative fatty acid (FA) profile of the TL was analyzed through gas chromatography coupled with mass spectrometry (GC–MS); we had previously subjected the TL mixture to acid methylation. To obtain the fatty acid methyl esters (FAMEs) from the TLs, 0.2 mL of a solution of TLs, 2 mL of methanol, and 0.2 mL of chlorate acetyl (CH3COCl) as catalyst were added to a glass retort (Schott Duran, Mainz, Germany). The obtained solution was heated for 90 min at a fixed temperature of 70–80 °C. After methylation (followed by cooling), the hexane was poured into 5 mL of each sample. For phase separation, 2 mL of deionized water was poured into each glass retort and transferred into the separatory glass funnels for 15 min. FAMEs remained in the upper hexane layer, while residue substances were concentrated in the lower aqueous phase. The hexane layer was evaporated using a rotary evaporator, Hei-VAP Advantage HL/G3 (Heidolph, Schwabach, Germany), to collect pure FAMEs. Then, 1 mL of hexane for GC (Sigma Aldrich, St. Louis, MO, USA) was added to the collected FAMEs in glass retorts, and the gathered and final solutions were accumulated in GC vials for the following GC analysis.
FAMEs were separated using GC with a mono-quadrupole mass-selective detector–α-Maestro (Saitegra, Moscow, Russia). The separation of FAs was carried out in a gradient thermal configuration (tstart = 140 °C—hold 5 min; increase in t from 140 °C to 240 °C at a rate of 4 °C per min; and tfinal = 240 °C—hold 2 min) with an HP-88 (60 m × 0.25 mm × 0.20 µm) capillary column (Agilent Technologies, Santa Clara, CA, USA) using helium as a mobile phase. FAMEs were detected in SCAN and SIM modes. The SCAN mode was used for searching and identifying FAs (qualitative analysis) with scan parameters of 50 to 400 mz−1. The SIM mode was used for FAs according to analytical standards with Supelco 37 (Sigma Aldrich, St. Louis, MO, USA), with subsequent quantitative analysis of the components that make up the mixture of Supelco 37. Quantitative individual FAs in the samples were detected using the calibration method using the Supelco 37 mixture (Sigma Aldrich, St. Louis, MO, USA). The data were analyzed using Maestro Analytic v. 1.026 software (Saitegra, Moscow, Russia) with the NIST library.

2.3. Statistical Analysis

All experiments were repeated three times. The data were subjected to an analysis of variance (ANOVA). The data were processed using Excel 2007 (Microsoft Corp., Redmond, WA, USA) and analyzed with Statgraphics Plus 5.0 (Statgraphics Technologies, Inc., The Plains, VA, USA) statistical software. The normality of the distribution was tested using the Shapiro-Wilk test. Data are presented as mean values ± standard error (SE). The Fisher’s least significant difference (LSD) test was used to compare the treatment means. Differences at p< 0.05 were considered statistically significant. The statistical analysis of FA content was made using the GC-MSD method (n = 3) with high precision and convergence.

3. Results

3.1. Amount of Zn in the Roots and Shoots of S. alba and B. juncea Seedlings

Along with the increase in concentration of Zn in the substrate, its content increased in the roots and shoots of both S. alba and B. juncea seedlings (Table 1). The yellow mustard seedlings subjected to 50 mg kg−1of Zn mostly accumulated the metal ions in shoots, whereas under higher concentrations of Zn (100 and 150 mg kg−1), their content between shoots and roots was similar. The oriental mustard seedlings at Zn concentrations of 50 and 100 mg kg−1 accumulated Zn ions in roots, while at Zn concentrations of 150 mg kg−1, there was no statistical difference in this metal content between shoots and roots (Table 1).

3.2. Effect of Zn Excess on Leaf Area, Fresh Weight, and Relative Electrolyte Leakage in S. alba and B. juncea Seedlings

Height Zn concentrations led to a decrease in leaf areas of S. alba and B. junceaseedlings (Table 2). It was noted that a Zn concentration of 50 mg kg−1stimulated the leaf area of yellow mustard (Table 2). The Zn concentration of 150 mg kg−1caused almost twice as much leaf area loss in yellow mustard and even more leaf area loss in oriental mustard. The fresh weight (FW) of both plant species decreased only at 100 and 150 mg kg−1 Zn concentrations (Table 2). The most negative effect of Zn excess on FW was observed under a 150 mg kg−1Zn concentration in both S. alba and B. juncea seedlings. However, the relative electrolyte leakage was not significantly different at exposure to all Zn concentrations in S. alba and B. juncea seedlings (Table 2).

3.3. Effect of Zn Excess on Some Photosynthesis Parameters of S. alba and B. juncea Seedlings

At a Zn concentration of 50 mg kg−1 the rate of photosynthesis (Pn) of yellow mustard and oriental mustard was not significantly different in comparison to the control (Figure 1). At the higher Zn concentrations (100 and 150 mg kg−1), Pn decreased, which was observed to a greater extent in yellow mustard.
The Zn excess also caused a decrease in photosynthetic pigment content in S. alba and B. juncea (Table 3). Particularly in yellow mustard, the decrease in total chlorophylls and carotenoids content was observed at 100 and 150 mg kg−1 Zn concentration impacts, whereas in oriental mustard seedlings, the drop in photosynthetic pigment content was caused by 50 mg kg−1 Zn concentration. Similar changes were detected for chlorophyll content in LHCII in both plant species.

3.4. Fatty Acids Content in S. alba and B. juncea Seedlings under Exposure to Zn Excess

Along with the rise in Zn ion concentration, the content of palmitic acid (PA) and stearic acid (SA) in yellow mustard increased, as did the total content of saturated fatty acids (SFA) (Table 4). For instance, the total content of SFA increased by 8 and 59% at 50 and 100 mg kg−1 Zn concentrations, respectively, compared with control. However, the influence of 150 mg kg−1 Zn concentration on seedlings of yellow mustard caused a rise in SFA content about 2.5-fold (Table 4).
The changes in unsaturated fatty acid (USFA) content were not as marked in yellow mustard compared with control (Table 4). The 100 mg kg−1 Zn concentration caused a slight decrease in all detected USFA, but under the influence of other Zn concentrations (50 and 150 mg kg−1), the total content of USFAs was similar to the control. Approximate 70% of all USFA is presented by α-linolenic (ALA) FA in yellow mustard under exposure to all concentrations of Zn. Also, in control plants of yellow mustard and seedlings subjected to 50 mg kg−1of Zn, the total content of USFAs was higher than SFAs. However, in seedlings of yellow mustard treated with 100 and 150 mg kg−1 of Zn, the content of SFAs was higher than USFAs.
The content of SFAs in oriental mustard slightly dropped at 50 mg kg−1 of Zn impact, whereas under higher Zn concentration influences (100 and 150 mg kg−1), the total content of SFAs was similar to control (Table 5). During exposure to Zn excess, the content of myristic acid (MA) increased while the PA content slightly dropped in oriental mustard. The content of SA stayed the same (Table 5). The influence of 50 mg kg−1 of Zn concentration caused a significant increase in the content of total USFAs, whereas at higher Zn concentrations (100 and 150 mg kg−1), the amount of total content dropped compared with control (Table 5). The increase in total USFA content at a Zn concentration of 50 mg kg−1 mostly depends on the rise of ALA FA. It is necessary to note that despite the decrease in USFA’s total content at high concentrations of Zn impact, its amount was higher than the total SFA’s content. This proportion was also observed in control plants and seedlings of oriental mustard treated by Zn excess (50 mg kg−1) (Table 5).

4. Discussion

It is well known that different plant species absorb and accumulate metal ions in organs and tissues [29,39]. Particularly, plants that are “hyperaccumulators” intake a high amount of metal ions and mostly keep them in the aboveground part, whereas plants that are “excluders” absorb less concentrations of metals and accumulate them mostly in the roots [40]. In the present study, it was demonstrated that both yellow and oriental mustards accumulated Zn proportionally to the concentrations in the substrate and that both species contain similar amounts of Zn ions. At the same time, the Zn content in yellow mustard at a metal concentration of 50 mg kg −1 of substrate was higher in shoots, and at the higher Zn concentrations (100 and 150 mg kg−1), it turned out to be almost equal in underground and aboveground organs. In contrast, in oriental mustard, at a zinc concentration of 50 and 100 mg kg−1 of substrate, the metal accumulated mainly in the roots, and with an increase in the metal concentration to 150 mg kg−1 of substrate, it accumulated in the roots and shoots almost equally. It is correlated with data demonstrated previously on yellow mustard [29] and oriental mustard [28]. Despite the rather large amount of data on the high ability of oriental mustard to accumulate metal ions [25,41], their content is significantly lower than in “hyperaccumulator” species, such as Thlaspi caerulescens and Arabidopsis halleri, which accumulate up to 9000 mg kg−1 DW of Zn [42,43]. There are practically no data on yellow mustard; however, a fragmentary work demonstrated its ability to accumulate metal ions no less than oriental mustard [44] that corresponded with present data.
In addition to differences in the accumulation of heavy metals, different plant species also have different metal tolerances, which, as a rule, are assessed by growth and photosynthesis activity. As with other heavy metals, Zn has a negative effect on plant growth [45]. Under Zn excess, a decrease in growth was observed in plants: B. juncea and B. napus [28], Zea mays [46], Polypogon monspeliensis [47], Ocimum basilicum [48]. In the present study, the Zn concentration of 50 mg kg−1 caused a slightly stimulated effect on the growth of yellow mustard. whereas the increase in Zn concentration in substrate to 100 and 150 mg kg−1 resulted in a negative effect on the growth of both plant species. It is suggested that growth inhibition under Zn excess concentration can be a result of limiting cell division due to an increase in the duration of mitotic phases as well as the full mitotic cycle [49], impaired cell elongation due to a decrease in the elasticity of cell walls, or a decrease in their turgor [39].
In addition, the inhibition of plant growth under these conditions can be a result of changes in the photosynthesis activity of plants, leading to the inhibition of photosynthesis. The present study showed that zinc at a concentration of 50 mg kg−1 of substrate had no effect on the photosynthesis rate, while at higher concentrations (100–150 mg kg−1 of substrate), the rate of photosynthesis significantly decreased in both species, but a more pronounced effect was noted in yellow mustard, indicating its lower tolerance to metal influence. One of the reasons for the drop in photosynthesis activity is a decrease in photosynthetic pigment content, which we also observed in other species such as wheat [50], Polypogon monspeliensis [47], Ocimum basilicum [48], etc. On the other hand, the slowdown in the rate of photosynthesis under stress conditions can be a result of a decrease in the activity of carbonic anhydrase. Carbonic anhydrase (EC: 2.4.1.1) catalyzes the rapid conversion of carbon dioxide plus water into a proton and the bicarbonate ion (HCO 3−)and provides the RuBisCO with CO2 molecules [51]. There are no available data about the effect of Zn at high concentrations on the activity of carbonic anhydrase in plants. Whereas, the negative effect of an excess of these metal ions on the other enzymes’ activity that participate in photosynthesis, for instance, RuBisCO, was demonstrated [52,53] as well as a decrease in the activity of photosystems [50,54]. Moreover, Segardoy et al. [55] showed the effect of excess zinc on carboxylate metabolism, which leads to an increase in respiration due to using the carboxylates from roots as a substrate, in parallel with a decrease in photosynthesis rate.
To ensure the process of photosynthesis, it is necessary to maintain the integrity of chloroplast membranes. One of the main roles in membrane stability is played by the USFAs. In the present study, it was shown that the Zn concentration of 50 mg kg−1 stimulated the accumulation of total FAs, including USFA. Whereas, despite the drop in total FAs content in oriental mustard under Zn concentration (100 and 150 mg kg−1) influence, the content of USFAs was higher than SFA. At the same time, the photosynthesis rate decreased slightly in comparison to yellow mustard. It was assumed that the higher USFA content pointed to a compensatory rearrangement of membrane structure, which was also suggested by the absence of electrolyte leakage. The functioning of membrane-bound enzymes and processes in membrane is maintained by an increase in the unsaturation of FAs, one of the mechanisms of adaptation in living systems, resulting in a change in the structure and physicochemical properties of membrane [56]. Due to this, it is possible to suggest that maintenance of unsaturation of lipids by accumulation of USFAs in the thylakoids membrane of oriental mustard provides for optimal activity of photosystem II under Zn excess. Also, it was shown that the chlorophyll content in LCH II remained stable in oriental mustard at Zn concentrations of 100 and 150 mg kg−1. Moreover, the connection between USFA accumulation and photosystem II functioning in oriental mustard under cadmium (Cd) influence was previously observed [57].
More recently, it was demonstrated the increase in USFAs content in “hyperaccumulator” plant species, such as Noccaea caerulescens under Cd ions [58] and Arabidopsis halleri under Zn ions [59]. The accumulation of high amounts of USFAs is an important mechanism that determines the tolerance of these species and their ability to grow in conditions of high concentrations of metals in the substrate. Probably, it is associated with the multifunctional activity of USFAs in cells, particularly those involved in maintaining membrane permeability. It was discussed that USFAs protect cells from reactive oxygen species, and these FAs are precursors for the manifestation of secondary metabolites [60]. More USFAs are known as “signal messengers” because they consist of nitro-FAs, which are the donors of nitrogen dioxide (NO2) [60,61]. As a constituent of triacylglycerides, USFAs are deposited in their structure (the energy cost of such TAGs is high) and actively used in energy-dependent processes under changing environments; thus, fast-growing plants are able to react to stressconditions [62]. It is interesting that a similar mechanism of biochemical adaptation was described for animals (fish) [17,63] At this point, it is possible to discuss the general patterns—evolutionarily determined ones—of stress-induced reactions.
It is necessary to note that changes in FAs content in yellow mustard under the Zn excess effect were unlike those in oriental mustard. In particular, as the proportion of zinc in the substrate increased, the total content of FAs in the aerial parts of plants rose. The Zn concentration of 50 mg kg−1increased the total amount of SFAs but was lower than the USFAs content. At a zinc concentration of 150 mg kg−1, the total content of FAs increased by 60% compared to the control. But in this case, this increase was a result of a rise in SFAs, particularly palmitic and stearic acids. The increase in palmitic acid concentration under heavy metal influence was reported in several articles [59,64,65,66]. Moreover, the possible role of palmitic acid in the stress tolerance of plants was described by Zhukov [67]. The accumulation of SFAs is characteristic of plants that mainly accumulate metals in the roots (excluders), for example, wheat under Cd ions [66], caraway [68], coriander [64], and Arabidopsis lyrata under Zn ions [59].
The data from the present study demonstrated that both species (yellow and oriental mustard) accumulate significant Zn concentrations and maintain the capability for growth and development under this condition. This indicates successful adaptation of both species to high concentrations of Zn in the substrate, despite different changes in the FA composition. Probably, the accumulation of SFAs is an alternative way of adapting plants (which are not hyperaccumulators or more sensitive species to metal ions’ influence). This also supports the fact that caraway plants under Zn excess in parallel with SFA accumulation are capable of forming natural seeds [68]. Earlier, we already made this assumption when studying changes in the FA composition of wheat under the influence of Cd ions [66]. Probably the increase in particularly palmitic and stearic acids caused a “raft” formation that leads to obturating membranes that prevent the overintake of metal ions into cells. At the same time, one of the possible functions of palmitic acid is “anchorage” in membrane transporter proteins to optimize their activity [67]. In addition, an increase in the total content of fatty acids is possibly associated with the creation of energy storage, which can subsequently be spent on energy-consuming cell reactions to maintain vital activity.

5. Conclusions

Both species (S. alba and B. juncea) are capable of accumulating sufficient amounts of Zn ions. Zn concentrations of 100 and 150 mg kg−1 caused the most negative effect on the physiological and biochemical parameters of mustard. The greater negative effect of Zn excess observed in yellow mustard, particularly in photosynthesis rate, in comparison with oriental mustard The changes in the quantity content of FAs in two plant species were different under the Zn effect. The Zn concentration of 50 mg kg−1 caused a stimulated effect on the total content of FAs and the amount of USFA to SFA, while the FAs content changes were rather different under higher Zn concentrations. Particularly in yellow mustard, the total content of FAs increased due to a rise in SFA content, whereas in oriental mustard, the total content of FAs decreased but the ratio of USFAs to SFAs was maintained. According to the present data and some recently available data, it is possible to conclude that there are two ways of adapting to heavy metal influences. On the one hand, there is an increase in USFAs content by “hyperaccumulators”, or highly resistant plants to metal stress, and on the other hand, there is an increase in SFAs content by “excluders”, or sensitive plant species to metal stress.

Author Contributions

Conceptualization, N.R. and S.A.M.; Methodology, N.R. and S.A.M.; Investigation, N.K. and V.P.V.; Data Curation, N.R. and S.A.M.; Writing—Original Draft Preparation, N.R.; Writing—Review and Editing, N.K. and S.A.M. All authors have read and agreed to the published version of the manuscript.

Funding

The study was carried out with the financial support of RSF (project No. 22-24-00668). This study was carried out using the equipment of the Core Facility of the Institute of Biology at KarRC RAS.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

All data and tables in this manuscript are original.

Conflicts of Interest

The authors declare no conflict of interest.

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Horticulturae 09 01002 g001
Figure 1. Effect of Zn excess on photosynthesis rate (Pn) of S. alba and B. juncea. Different letters indicate significant differences between treatments (p < 0.05), determined by Fisher’s least significant difference (LSD) test.
Figure 1. Effect of Zn excess on photosynthesis rate (Pn) of S. alba and B. juncea. Different letters indicate significant differences between treatments (p < 0.05), determined by Fisher’s least significant difference (LSD) test.
Horticulturae 09 01002 g001
Table 1. The Zn content in S. alba and B. juncea seedlings under exposure to Zn excess.
Table 1. The Zn content in S. alba and B. juncea seedlings under exposure to Zn excess.
Plant SpeciesZn Concentration, mg kg−1 SubstrateZn Content, mg kg−1 DW
ShootRoot
S. alba5187.32 ± 20.60 f115.01 ± 14.80 f
502505.31 ± 206.02 c1504.60 ± 125.96 e
1002620.35 ± 215.22 b2708.28 ± 222.26 b
1503118.52 ± 311.08 a3340.07 ± 272.80 a
B. juncea577.48 ± 10.78 g170.59 ± 19.25 f
501450.23 ± 121.62 e2169.80 ± 179.18 c
1001849.71 ± 153.58 d2174.27 ± 179.54 c
1502239.21 ± 184.74 c2379.11 ± 195.93 c
Values are means ± SE (n = 3). Different letters indicate significant differences between treatments (p < 0.05), determined by Fisher’s least significant difference (LSD) test.
Table 2. Effect of Zn excess on leaf area, fresh weight (FW), and relative electrolyte leakage (REL) in S. alba and B. juncea seedlings.
Table 2. Effect of Zn excess on leaf area, fresh weight (FW), and relative electrolyte leakage (REL) in S. alba and B. juncea seedlings.
Plant SpeciesZn Concentration, mg kg−1 SubstrateLeaf Area, cm2FW, gREL, %
S. alba54.00 ± 0.61 b1.27 ± 0.14 a10.78 ± 0.82 a
505.70 ± 0.17 a1.36 ± 0.15 a11.33 ± 0.77 a
1002.70 ± 0.55 d0.46 ± 0.04 b13.51 ± 1.23 a
1501.99 ± 0.48 e0.27 ± 0.03 c12.29 ± 0.06 a
B. juncea54.09 ± 0.34 b1.28 ± 0.07 a12.52 ± 0.64 a
503.13 ± 0.22 c1.09 ± 0.12 a13.00 ± 0.81 a
1001.77 ± 0.22 e0.67 ± 0.10 b14.61 ± 1.59 a
1501.35 ± 0.20 f0.39 ± 0.05 c14.00 ± 1.67 a
Values are means ± SE (n = 30). Different letters indicate significant differences between treatments (p < 0.05), determined by Fisher’s least significant difference (LSD) test.
Table 3. Effect of Zn excess on photosynthetic pigments content in S. alba and B. juncea.
Table 3. Effect of Zn excess on photosynthetic pigments content in S. alba and B. juncea.
Plant SpeciesZn Concentration, mg kg−1 SubstrateTotal Chl (a + b), mg g−1 FWCarotenoids,
mg g−1 FW		Chl b LHCII, %
S. alba51.36 ± 0.04 a0.28 ± 0.01 a0.18 ± 0.02 a
501.35 ± 0.04 a0.25 ± 0.01 a0.20 ± 0.01 a
1000.88 ± 0.03 bc0.18 ± 0.01 b0.09 ± 0.01 b
1500.53 ± 0.03 e0.13 ± 0.01 c0.03 ± 0.01 d
B. juncea51.37 ± 0.02 a0.25 ± 0.01 a0.20 ± 0.01 a
500.94 ± 0.03 b0.18 ± 0.01 b0.09 ± 0.01 b
1000.71 ± 0.03 d0.15 ± 0.01 c0.05 ± 0.01 dc
1500.84 ± 0.01 c0.18 ± 0.01 b0.07 ± 0.01 c
Values are means ± SE (n = 12). Different letters indicate significant differences between treatments (p < 0.05), determined by Fisher’s least significant difference (LSD) test.
Table 4. The fatty acids content in S. alba under Zn excess.
Table 4. The fatty acids content in S. alba under Zn excess.
Fatty Acids, µL mg−1Zn Concentration in Substrate, mg kg−1p Value
550100150
Saturated
Myristic C 14:08.428.788.319.230.05
Palmitic C 16:084.3790.11120.64145.01≤0.05
Stearic C 18:029.6633.9767.21153.99≤0.05
Total content122.45132.86196.16308.23≤0.05
Unsaturated
Oleic C 18:1n-920.3618.4013.4416.71≤0.05
Linoleic C 18:2n-625.4128.2526.9037.83≤0.05
Linolenic C 18:3n-3147.66141.24112.74145.860.05
Total content193.43187.89153.08200.40≤0.05
Unsturated/Saturated FAs1.581.410.780.65≤0.05
Values are presented as means, the SE were low and approximately 0.003–0.009 since the analysis was made using GC-MSD method (n = 3) with high precision and convergence.
Table 5. The fatty acid content in B. juncea under Zn excess.
Table 5. The fatty acid content in B. juncea under Zn excess.
Fatty Acids, µL mg−1Zn Concentration in Substrate, mg kg−1p Value
550100150
Saturated
Myristic C 14:05.818.1911.489.10≤0.05
Palmitic C 16:0100.0588.3198.1194.17≤0.05
Stearic C 18:036.5733.5033.4934.550.05
Total content142.43130.00143.08137.82≤0.05
Unsaturated
Oleic C 18:1n-921.2617.0925.0518.73≤0.05
Linoleic C 18:2n-624.2927.4728.1432.31≤0.05
Linolenic C 18:3n-3174.81271.57123.76118.39≤0.05
Total content220.36316.13176.95169.43≤0.05
Unsturated/Saturated FAs1.552.431.241.23≤0.05
Values are presented as means, the SE were low and approximately 0.003–0.009 since the analysis was made using GC-MSD method (n = 3) with high precision and convergence.
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Repkina, N.; Murzina, S.A.; Voronin, V.P.; Kaznina, N. Effect of Zinc Excess on Some Physiological Parameters and on the Fatty Acids Profile of Sinapis alba L. and Brassica juncea L. (Czern). Horticulturae 2023, 9, 1002. https://doi.org/10.3390/horticulturae9091002

AMA Style

Repkina N, Murzina SA, Voronin VP, Kaznina N. Effect of Zinc Excess on Some Physiological Parameters and on the Fatty Acids Profile of Sinapis alba L. and Brassica juncea L. (Czern). Horticulturae. 2023; 9(9):1002. https://doi.org/10.3390/horticulturae9091002

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Repkina, Natalia, Svetlana A. Murzina, Viktor P. Voronin, and Natalia Kaznina. 2023. "Effect of Zinc Excess on Some Physiological Parameters and on the Fatty Acids Profile of Sinapis alba L. and Brassica juncea L. (Czern)" Horticulturae 9, no. 9: 1002. https://doi.org/10.3390/horticulturae9091002

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