EFFECT OF THE INTERACTION OF NICKEL STRESS AND SULPHUR SUPPLEMENTATION ON THE CONTENT AND ACCUMULATION OF MACRONUTRIENTS IN WHITE MUSTARD (SINAPIS ALBA L.)
DOI:10.30825/5.EJPAU.24.2017.20.2

Renata Matraszek¹, Barbara Hawrylak-Nowak¹, Mirosława Chwil², Stanisław Chwil³, Michał Rudaś^4
1 Department of Plant Physiology, Faculty of Horticulture and Landscape Architecture, University of Life Sciences in Lublin, Poland
² Department of Botany, Faculty of Horticulture and Landscape Architecture, University of Life Sciences in Lublin, Poland
³ Department of Chemistry, Faculty of Agrobioengineering, University of Life Sciences in Lublin, Poland
⁴ Central Laboratory of Agroecology, University of Life Sciences in Lublin, Poland

ABSTRACT

Nickel in excessive amounts deteriorates the nutritional status in plants, inter alia reduces the level of sulphur. Simultaneously, the common use of NPK fertilizers without sulphates (S-SO₄) together with the progressive process of reducing emissions of S compounds to the natural environment may lead to deficiency of this element involved in stress tolerance. The aim of the studies was to evaluate the changes in the macronutrient contents and accumulation in Sinapis alba L. cv. Rota grown for 2 weeks at different levels of S-SO₄ (S-2-standard dose, 6, 9 mM) and Ni (0, 0.0004, 0.04, 0.08 mM) in modified Hoagland’s nutrient solution. Intensive S-SO₄ nutrition of Ni-exposed mustard seems to improve to some extent the unfavourable macronutrient status. It substantially increased the root macronutrient content drop in the content of this macronutrient. The macronutrient status in shoots remained stable, except for the significant increase in the S content and the rise in Ca accumulation accompanied by an increase in N and K accumulation recorded at the S dose 6 mM. Ni-bioaccumulation did not change markedly with the exception of its increase in roots at the 6 mM S level.

Key words: macronutrient content and accumulation, nickel phytotoxicity, nutrient solution, sulphur level, white mustard.

INTRODUCTION

Mustard is one of the oldest known species. Sinapis alba L. (synonyms: Brassica alba L., Brassica hirta Moench), also known as yellow or English mustard, originates from the Mediterranean region and is now widespread worldwide. This spice plant is widely cultivated in Australia, many countries of Asia (China, Japan), Europe (Italy, Denmark, Netherlands, the UK), North and South America (USA, Canada, Chile), and North Africa [57]. Nowadays, Canada and Nepal are the biggest producers of white mustard 14]. In Poland, it is hard to estimate mustard production because of the predominant cultivation of this plant as a catch crop. Apart from rape, white mustard together with other oil crops, i.e. poppy and sunflower, cover a total area of 994,000 ha [66]. Based on the data published by FAO (Food Agriculture Organization of the United Nations) and Central Statistical Office it may be predicted that the production of this species will increase in the nearest years and that the scope of its application will be extended [14, 66]. White mustard is a multifunctional plant. Its pungent seeds are used in the food industry to produce table mustard, oil, and various kinds of spices. Besides food industry, mustard seeds are used after processing in pharmaceutical and cosmetics industries. Fresh tender mustard greens are eaten raw either as salad or as juice 68, 45]. Mustards are increasingly used as green manure, fodder crop, or winter or rotational cover crops in vegetable and specialty crop production, such as potatoes, fruit trees, and in plantation of grapevines. White mustard is also a useful winter cover at home gardens. White mustard releases metabolic and bio-toxic by-products that inhibit growth of soil-borne pathogen and pests. This suppression is related to degradation of thioether glucosinolate into thiocyanates. Moreover, white mustard provides allelopathic compounds, which are able to control some small annual weeds [38]. White mustard straw may have technological application as a valuable substitute of wood chips in the production of particle boards and interior boards, including furniture [11].

Sulphur (S) is highly and constantly required throughout the growing season by mustard and all the other species of the Brassicaceae family due to oil production and biosynthesis of secondary metabolites with a high nutritional value such as glucosinolates. Especially high S supplementation is necessary at the flowering stage, because this macronutrient is a major constituent of seed protein. Mustard requirements for S are at least twice as high as those of cereal crops, with an optimal range of the N:S ratio from 4:1 to 8:1 [3, 25, 37]. Nowadays, the insufficient S level in the environment and, consequently, reduced yield and quality have become a global problem [42, 47]. Sulphur deficiency results from progressive reduction of emissions of compounds containing this element to the natural environment, extensive use of S-free NPK fertilizers, and intensive crop production. Furthermore, the limited availability of S to plants is related to the fact that sulphate ions easily leach deeper into the soil profile and they are relatively immobile in the soil-plant system [12, 47]. Sulphur is crucial to many processes of growth and development. This element is involved in the synthesis of chlorophyll and pathways of various cellular processes, e.g. the redox cycle, electron transport in iron-sulphur (Fe-S) clusters, protein disulphide bridges, and metabolism of secondary products (allyl Cys sulfoxides and the above-mentioned glucosinolates). First of all, sulphur is a constituent of amino acids (cysteine Cys and methionine Met), which play a central role both as building blocks of proteins and as intermediates in metabolism. This macronutrient is also found in vitamins (thiamine and biotin), and cofactors (coenzyme A CoA and S-adenosyl-Met) [65]. A suitable S level to plants is important not only for proper growth and development, but also for enhanced tolerance to many biotic and abiotic stress factors [13, 17]. It is widely known that ligands containing SH-groups, such as tripeptide glutathione (GSH) or phytochelatins (PCs), form high-strength, durable complexes with heavy metals. It has been found that especially the former compound, besides amino acid histidine, is crucial for Ni tolerance [5, 16, 31]. Various studies demonstrated that S fertilization contributed to a drop in the Ni content of soil and improved the efficiency of the use of other essential plant nutrients, particularly N and P [1, 4, 75, 76].

Nickel (Ni) is among essential nutrients for higher plants involved in many biochemical and physiological processes that are crucial for proper growth and development, such as nitrogen metabolism, iron absorption, and maintenance of proper cellular redox status [10, 32, 40, 56, 60]. Ni deficit is very rare, which is related to the especially low plant requirements for this micronutrient (0.5 mg kg^-1 DW). In turn, the phytotoxic effects of Ni excess are quite commonly found. Due to its high mobility, this element is very easily and rapidly taken up by plants and incorporated into the food chain, causing a serious threat for animals and humans [56, 64]. The main sources of Ni pollution are anthropogenic activities: fossil fuel combustion, smelting and refining, ore mining, metallurgical and electroplating industry, cement and steel manufacturing, municipal refuse incineration, electronic and electrical industry, chemical and food industry, fertilization with sewage sludge, agricultural use of organic and mineral fertilizers containing heavy metals, and many others [8, 23, 77, 83]. The phytotoxicity of excessive Ni amounts is related to alterations in mineral nutrition (uptake, transport, and distribution), photosynthesis, respiration, and water regime. This leads to growth inhibition. Reduced yield and quality have also been observed [10, 22]. Ni phytotoxicity is one of the serious problems that limit agricultural production [35]. Plants from the genus Brassica, among them Indian mustard, may tolerate excessive concentrations of heavy metals, including Ni [58, 79]. Stanisławska-Głubiak and Korzeniowska [78] claim that white mustard is most sensitive to Ni contamination, compared to excess of Cu and Zn. Many reports concerned the Ni phytotoxic effects and tolerance to this metal; nevertheless, our knowledge in this area is incomplete, and the mechanisms involved in the phytotoxic effects and tolerance to Ni are poorly understood [8, 43, 77]. Moreover, it is well documented that Ni-excess unfavourably affects plant nutrient status, but the literature data on the Ni effect on plant mineral nutrition are contradictory [61, 71, 77, 82]. Because of the dual character and complex electronic chemistry of Ni, conducting studies on its biological role and toxicity is very difficult. For this reason, there is less information about Ni phytotoxicity and resistance than for other commonly found toxic trace metals like Cd, Cu, Cr, and Pb [28, 29, 83].

The imbalanced nutritional status in plants occurring under conditions of Ni excess as well as the reduced availability and progressive deficiency of S – a unique essential element involved in stress tolerance – prompted us to undertake research on the effectiveness of macronutrient balance improvement in plants by high S-SO₄ supplementation. The aim of this study was to determine the effects of intensive S nutrition on changes in the macronutrient status in Ni-stressed white mustard (Sinapis alba L.) – a very important agricultural oil seed crop characterised by especially high S requirement. Efforts were undertaken to check whether it is possible to improve macronutrient status of this species imbalanced by the Ni presence with using intensive S-SO₄ supplementation. The studies presented in this manuscript are only part of a huge research project focused on the role of intensive S nutrition in Ni tolerance. It is hoped that our investigations are important for farmers and horticulturalist. It is believed that the results of the presented investigations provide some new and valuable information on the strategies involving mineral nutrition developed by plants to cope with Ni excess and that they may be helpful in further studies on this issue.

MATERIAL AND METHODS

Plant material and growth conditions
The experiment was carried out in the years 2012–2014 in the Plant Physiology Department, University of Life Sciences in Lublin, Poland. White mustard ‘Rota’ was the biological object of the study. The experiment was carried out with the method of water cultures. One-week-old seedlings were transferred to 1 dm3 glass jars (two plants per each) with Hoagland II solution with different concentrations of sulphates (2.00-standard dose, 6.00, or 9.00 mM S) and nickel in the form of NiCl₂ (0, 0.0004, 0.04, and 0.08 mM Ni). The standard S dose 2 mM S was supplied as MgSO₄, but in the high S treatment (6 and 9 mM) the standard level of this macronutrient in the form of MgSO₄ was given and supplemented with appropriate amounts of Na2SO₄. In all experimental treatments, the level of sodium and chlorine was equalized by adding appropriate amounts of NaCl and 1% HCl to the nutrient solution; the pH of the nutritional environment was set at 5.8–6.0. Plant vegetation was conducted in an air-conditioned room (phytotron) under controlled conditions: temperature 25/20ºC (day/night), photoperiod of 14 h, Photosynthetic Photon Flux Density of 400 µmol m^-2 s^-1, and relative air humidity between 60–70%. After two weeks of growth under conditions of different Ni contamination and sulphate nutrition, plants were harvested and the dry mass (data not shown) as well as macronutrient content in roots and aboveground parts was assessed.

Macronutrient content and accumulation
After wet mineralization in H₂SO₄+H₂O₂, the dry plant material (roots and aboveground parts separately) was subjected to chemical analyses by determining the concentrations of the macronutrients. The content of total nitrogen (N) was determined with the classic Kjeldahl method, phosphorus (P) with the vanadium-molybdenum method, potassium (K), calcium (Ca), magnesium (Mg) with the AAS – atomic absorption spectrometry technique and total sulphur (S) with the nephelometric Butters-Chanery method. The results obtained (macronutrients and Ni contents as well as dry biomass of root and shoots) were used to calculate the accumulation of nutrients and nickel [46, 48].

Nickel determination
Analyses of the Ni content in roots and shoots was carried out using the classic AAS method, following prior dry-mineralisation of 5.000 g plant samples at 500°C, dissolved in 20% HNO₃. Ni analyses were performed by an accredited laboratory of the Regional Chemical-Agricultural Station in Lublin. This study presents the data concerning the Ni accumulation.

Statistical analysis
The experimental design was randomised with twelve treatments and twenty replicates per treatment. Each experimental series included 40 plants and the experiment was repeated three times under the same conditions. The results were elaborated with the statistical and analytical software package STATISTICA 9 (StatSoft, Inc. 2009) using a two-factorial analysis of variance (ANOVA). The experimental factors were the level of S nutrition of plants and the Ni concentration in the nutritional environment. Data normality was tested using the Shapiro-Wilk test. The significance of differences was estimated with Tukey’s test at the probability level P ≤ 0.05. The values in the same treatment as well as mean values among each treatment obtained from each of the three independent replicates of the experiment over the time were not significantly different. Thus, the data presented in the tables and in the figures followed by SD values represent means from nine measurements (three measurements per each independent repetition of the experiment over the time).

RESULTS

Macronutrient content and accumulation
Intensive S nutrition (6 and 9 mM) of white mustard ‘Rota’ grown in the nutrient solution without Ni addition markedly increased root N and S content, with no statistically proven changes in P, K, Ca, and Mg content (Tab. 1a). Simultaneously, the shoot contents of all the analysed macronutrients were not substantially affected. An exception was the significantly reduced Mg content in the presence of 6 mM S (Tab. 1b). Furthermore, it was found that high S concentrations in the nutrient solution without Ni markedly elevated root accumulation of all the macronutrients (Fig. 1a). At the same time, the shoot Ca and S accumulation significantly rose, but K accumulation dropped, whilst N, P, and Mg accumulation remained unchanged (Fig. 1b). It is worth stressing that the increase in Ca and S accumulation in the Ni-untreated plants subjected to the intensive S levels was more pronounced in roots than in shoots (Fig. 1a, b).

Table 1a. The content of macronutrients (g kg-1 DM; means ± SD, n = 9)  in the root biomass of white mustard ‘Rota’ exposed to different sulphur (S) and/or nickel (Ni) concentrations in the nutrient solution

Concentration of the element in the nutrient solution		Content of the macronutrient in the root biomass [g kg-1 DM ± SD]
[mM]		N	P	K	Ca	Mg	S
S	Ni
2	0.00	9.28±0.19b-d 11.07±0.33a 10.39±0.21ab	5.94±0.36a-c 5.32±0.25c 6.36±0.17a	18.3±1.05c 20.17±0.75bc 19.57±0.92c	1.72±0.05bc 1.67±0.06cd 1.88±0.04b	1.08±0.10de 0.97±0.05e 1.12±0.07de	12.34±1.22f 20.55±1.36d 21.10±1.09cd
6
9
2	0.0004	8.45±0.43de 8.78±0.25c-e 9.89±0.37a-c	5.29±0.22cd 3.56±0.11g 5.43±0.14c	17.34±1.23c 18.47±1.17c 19.52±0.89c	2.02±0.05a 1.05±0.04g 1.59±0.04d	1.04±0.09de 1.25±0.04b-d 1.37±0.06a-c	13.48±1.18ef 19.58±0.97d 23.37±1.12bc
6
9
2	0.04	7.04±0.33fg 9.67±0.39b-d 10.16±0.45ab	5.53±0.19bc 4.56±0.24de 4.28±0.13e-g	9.78±0.99d 24.78±0.85a 25.64±1.04a	0.84±0.06h 1.00±0.03g 1.35±0.05ef	0.56±0.06f 1.16±0.07c-e 1.54±0.04a	12.19±0.86f 21.05±1.13cd 28.57±0.94a
6
9
2	0.08	5.93±0.27g 7.98±0.51ef 9.82±0.31a-c	6.22±0.29ab 3.70±0.34fg 4.45±0.27ef	11.57±0.96d 23.17±1.24ab 23.36±1.07a	1.28±0.05f 1.45±0.02e 1.43±0.04e	0.39±0.05f 0.98±0.10e 1.40±0.08b	15.90±0.98e 25.40±0.81b 15.39±1.15e
6
9
Main effects
S concentration 2 mM 6 mM 9 mM		7.68±0.24c 9.38±0.31b 10.07±0.25a	5.75±0.17a 4.31±0.11c 5.13±0.14b	14.25±0.68b 21.65±0.57a 22.02±0.70a	1.47±0.03b 1.29±0.02c 1.56±0.03a	0.77 ± 0.04c 1.09±0.06b 1.36±0.06a	13.48±0.54b 21.65±0.68a 22.11±0.59a
Ni concentration 0 0.0004 0.0400 0.0800		10.25±0.21a 9.04±0.29b 8.96±0.15b 7.98±0.19c	5.87±0.12a 5.13±0.08b 4.46±0.17c 4.79±0.11bc	19.35±0.52 18.44±0.78 20.07±0.61 19.37±0.59	1.76±0.02a 1.55±0.02b 1.06±0.03d 1.39±0.02c	1.06±0.02b 1.22±0.03a 1.09±0.03b 0.92±0.1c	18.00±0.43b 18.81±0.23b 20.60±37a 18.90±0.29b
Statistical significance S concentration Ni concentration S×Ni concentration		* * *	* * *	* ns *	* * *	* * *	* * *
Explanations: Different letters within the same column (separately for main effects i.e. Ni and S concentrations and their interactions) indicate significant differences between means of nine replications according to the Tukey's multiple range test (P ≤ 0.05); SD, standard deviation; ns, not significant. Significant effects for the main factors and the interactions between them are also denoted with asterisks. ;

Table 1b. The content of macronutrients (g kg-1 DM; means±SD, n = 9) in the shoot biomass of white mustard ‘Rota’ exposed to different sulphur (S) and/or nickel (Ni) concentrations in the nutrient solution

Concentration of the element in the nutrient solution		Content of the macronutrient in the shoot biomass [g kg-1 DM±SD]
[mM]		N	P	K	Ca	Mg	S
S	Ni
2	0.00	37.13±1.22c-e 29.37±1.47e 31.46±1.03de	0.87±0.04 0.94±0.10 0.89±0.07	29.45±1.53ef 21.78± 1.07f 22.51±1.23f	10.56±0.75ab 12.89±1.12a 13.57±0.58a	2.78±0.14a-c 1.92±0.20de 2.17±0.09b-e	17.35±0.45c 19.68±0.53bc 19.97±0.37bc
6
9
2	0.0004	48.68±1.58ab 42.75±1.34a-c 50.03±1.17a	0.90±0.08 0.97±0.06 0.82±0.09	41.96±0.88b-d 37.89±0.75c-e 34.52±1.39de	5.23±0.62d 7.35±0.95b-d 8.21±0.79b-d	2.15±0.27c-e 2.47±0.11a-d 2.35±0.19a-e	18.88±0.95bc 22.29±1.21ab 17.98±0.63 c
6
9
2	0.04	45.39±0.95a-c 49.4±1.19 ab 42.87±1.32a-c	0.83±0.05 0.79±0.11 0.85±0.09	45.34±0.93a-c 51.89±1.22a 48.61±1.37ab	6.48±0.64 cd 7.69±0.82b-d 6.17±0.73cd	2.80±0.13ab 1.76±0.21e 1.89±0.18de	18.57±1.14c 24.96±0.81a 23.87±0.95 a
6
9
2	0.08	44.26±1.24a-c 46.25±0.87a-c 39.61±1.38b-d	0.85±0.07 0.79±0.08 0.88±0.05	39.56±1.19b-d 42.11±0.79b-d 37.52±1.58c-e	9.44±0.93bc 8.69±0.86b-d 8.17±1.09b-d	2.58±0.25ac 2.86±0.14a 2.39±0.17a-e	19.58±0.54bc 18.72±0.79bc 20.79±0.63c
6
9
Main effects
S concentration2 6 9		43.86±1.24 41.95±0.99 40.99±1.28	0.86±0.03 0.87±0.05 0.86±0.04	39.08±1.39 38.42±1.12 35.79±1.27	7.93±0.87 9.16±0.73 9.03±0.90	2.58 ± 0.11 2.25 ± 0.06 2.20 ± 0.08	18.60±0.74b 21.42±0.56a 20.66±0.61a
Ni concentration 0 0.0004 0.0400 0.0800		32.65±0.87b 47.15±1.16a 45.89±1.38a 43.37±0.91a	0.90±0.04 0.90±0.03 0.82±0.04 0.83±0.04	24.58±0.89c 38.12±1.17b 48.61±1.05a 39.73±1.44b	12.34±0.53a 6.93±0.67c 6.78±0.71c 8.77±0.62b	2.29±0.09ab 2.32±0.14ab 2.15±0.07b 2.61±0.10a	19.00±0.68b 19.72±0.82b 22.47±0.75a 19.70±0.62b
Statistical significance S concentration Ni concentration S×Ni concentration		ns * *	ns ns ns	ns * *	ns * *	ns * *	* * *
Note: See Table 1a for explanations

Fig. 1a. Macronutrient accumulation in the root biomass of white mustard ‘Rota’ grown under different sulphur (S) and/or nickel (Ni) concentrations in the nutrient solution Note. Presented data are mean values ± SD from nine replications. Different letters stand for statistically significant differences at P ≤ 0.05 (Tukey’s test). Asterisks indicate significant effects for main factors and interactions between them.

Fig. 1b. Macronutrient accumulation in the shoot biomass of white mustard ‘Rota’ grown under different sulphur (S) and/or nickel (Ni) concentrations in the nutrient solution. Note: Explanations the same as those under Figure 1a.

The increasing Ni concentration (0.0004–0.08 mM) in the nutrient medium of mustard, irrespective of the S concentration, led to a significant drop in the root N, P, and Ca contents and did not markedly change the root K content (Tab. 1a). At the same time, the N and K contents in shoots were increased, the Ca content was decreased, whilst the P content remained quite stable; it was noticed that the decrease in the Ca content was more pronounced in shoots than in roots (Tab. 1b). Moreover, it was revealed that, depending on the Ni level in the nutrient solution, the root Mg content significantly increased (0.0004), did not change (0.04), or dropped (0.8 mM), whilst the shoot content of this macronutrient in Ni-stressed mustard remained quite stable. Furthermore, it was noticed that Ni contamination did not affect the content of S in the root and shoot biomass, except for the statistically proven increase at the Ni dose 0.04 mM applied in the soil solution and that this increase was more marked in shoots than in roots (Tab. 1 a, b).

In general, the presence of Ni in the nutrient environment of white mustard, under conditions of the standard S dose, substantially reduced the accumulation of all macronutrients in roots and shoots and this decrease was much more pronounced in roots. Only the lowest Ni dose used in the experiment, i.e. 0.0004 mM, markedly raised the Ca and S contents in roots, without substantial changes in the accumulation of the other elements. These changes in roots were accompanied by a significant increase in the shoot N and K contents and a drop in the Ca content (Fig. 1 a, b).

As a result of intensive S nutrition (6 and 9 mM) of Ni-treated mustard (0.0004–0.08 mM), irrespective of the Ni contamination level, a significant increase in the N, K, Ca, Mg, and S contents as well as a decrease in the P content was observed in the root biomass. An exception was the statistically proven drop in Ca recorded at the S level 6 mM S. At the same time, a significant increase in the S content and substantially unchanged contents of all the other macronutrients were found in shoot biomass. The increase in the S content in the high S-supplemented and Ni-stressed mustard was more pronounced in roots than in shoots (Tab. 1 a, b).

High S concentrations (6 and 9 mM) in the nutrient solution containing Ni (0.0004–0.08 mM) substantially enhanced N, K, Ca, Mg, and S accumulation in white mustard roots, and this increase was much more marked at the dose 9 than 6 mM S (Fig. 1 a, b). Furthermore, it was found that P accumulation in the root and shoot biomass was not significantly changed, except for the proven substantial increase at the treatment with 6 mM S/0.04 mM Ni shown in aboveground parts (Fig. 1 a, b). Similarly, there were no significant differences recorded in shoot Mg and S accumulation, except for the S increase at the treatment with 6 mM S/0.04 mM Ni. As a rule, shoot N and K accumulation in Ni-treated mustard supplemented with high S doses significantly increased at 6 mM S and did not substantially change at 9 mM S. At the same time, the increasing S dose in the nutrient solution increased (0.0004 and 0.04 mM Ni) and did not change (0.08 mM Ni) shoot Ca accumulation (Fig. 1 a, b).

The significant effect of the S and Ni interaction on the root and shoot content of macronutrients in mustard, taking into account the Ni-contamination of the nutrient solution with the standard S level and addition of high S doses into the Ni-contaminated nutrient solution, generally corresponded with the above description of this parameter concerning the main effects of Ni and S (Tab. 1 a, b). The main differences involved changes in the root P, K, and Mg contents in Ni-treated mustard supplied with the standard S dose i.e. 2 mM. Namely, the root K content remained quite stable, whilst the K and Mg contents did not change markedly at the lowest (0.0004 mM) and dropped at the higher (0.04 and 0.08 mM) Ni concentrations used in the experiment.

Nickel accumulation
The results obtained indicate that, both at the standard and high S level, Ni accumulation in the white mustard biomass rose together with the increasing concentration of this microelement in the nutrient environment, and that the increase in Ni accumulation was much more pronounced in shoots than in roots (Fig. 2). Under the conditions of the increased S level in the nutrient solution, depending on the Ni-treatment, mustard plants accumulated 1.5–2 (0.0004 mM) and 5–10 times (0.04; 0.08 mM Ni) larger amounts of Ni in shoots than in roots.

Fig. 2. Nickel accumulation in the biomass of white mustard ‘Rota’ grown under different sulphur (S) and/or nickel (Ni) concentrations in the nutrient solution. Note: In control plants (Ni-0 mM) in basic (S-2) and high-S (S-6 or 9 mM) treated plants, only trace amounts of nickel were identified and, hence, accumulations were zero. The remaining explanations are the same as those under Figure 1a.

Intensive sulphate nutrition of Ni-stressed white mustard significantly enhanced (6 mM S) or did not change (9 mM) root Ni-accumulation. Simultaneously, there were no significant changes in the shoot Ni accumulation, except for the statistically proven drop occurring at the treatment with 9 mM S/0.04 mM Ni (Fig. 2).

DISCUSSION

Macronutrient content
Ni concentrations in the nutrient solution used in the present study, ranging between 0.0004 and 0.08 mM. The lower Ni dose is considered to be the maximum acceptable level in ground water and soil solution. Ni level from water in industrial regions is estimated at between 6∙10^-4 and 6∙10^-2 mM [28].

Alterations in the essential element balance and ionic homeostasis were identified as a key mechanism of Ni phytotoxicity. Nickel interferes not only with nutrient uptake but also with nutrient distribution into the particular plant parts. The literature data show an inconclusive impact of Ni on mineral nutrition of plants. Ni excess may cause a drop, rise, or not affect the mineral nutrient content in particular organs. Moreover, the type of changes in the mineral nutrient content may depend on the Ni concentrations in the nutrient environment [6, 30, 69, 77]. The presented studies provide substantive evidence for the decrease in the P and Ca contents in the biomass of Ni-stressed white mustard, although the content of the latter macronutrient in shoots remained quite stable. Simultaneously, the N and K contents in the whole biomass of Ni-exposed mustard were elevated in spite of the markedly decreased root N. In turn, the type of changes in the Mg and S contents varied depending on the Ni level in the nutrient solution. The root Mg content was elevated at the lowest (0.0004), reduced at the highest (0.08), and stable at the medium (0.04 mM) Ni concentration used in the experiment, whereas the shoot Mg content was not substantially affected by the Ni contamination. The S root and shoot content remained unchanged at the lowest and the highest levels, but increased at the medium Ni dose applied. In general, all the above-mentioned changes in the macronutrient content were accompanied by a decrease in accumulation thereof. Investigations conducted by Putnik-Delić et al. [58] on winter and spring varieties of rapeseed, white and black mustard, and turnip revealed that the Ca concentration in leaves of all the mentioned genotypes treated with 0.01 mM Ni decreased, whilst at the same time the Mg content increased. In turn, the concentrations of K varied among the genotypes, but they were generally reduced in the presence of the Ni. Palacios et al. [52] found that N and K contents in tomato significantly increased, whilst Mg, Ca, and P decreased with the increasing Ni treatment with 0.08–0.5 mM, ipso facto showing a synergistic effect between Ni and N and Ni and K, and an antagonistic relationship between Ni and the other macronutrients i.e. Mg, Ca, and P. In turn, Shukla and Gopal [71] recorded increased P and S contents in different plant parts of potato (except for roots) exposed to Ni excess between 0.1 and 0.5 mM. Singh et al. [72] revealed that the Ni amount increased, whilst the excess concentrations of this micronutrient decreased the N content in wheat. In turn, Hunter and Vergnano [21] noted that the toxic effect of Ni was associated with reduced N and raised P contents in oat. The Ni concentrations used in the presented studies (0.0004–0.08 mM) decreased or elevated the N content in mustard roots and shoots, respectively. This rise in the content of this macronutrient in shoots was more pronounced than the drop in roots. Moreover, our findings concerning the P content in mustard were in contrast with the results of Hunter and Vergnano [21] for oat.

The increase in the concentrations of essential elements in Ni-exposed mustard plants supplied with standard S dose, as shown in the presented studies for N and K, may be explained by severe reduction in the productivity. The reduced P and Ca contents recorded in the biomass of Ni-stressed mustard, resulted, inter alia, in cellular respiration disorders and in consequence low status of energy needed for the active uptake and nutrient transport. Especially the former macronutrient, i.e. P, plays a crucial role in cellular energy metabolism. In turn, the latter essential nutrient, i.e. Ca, plays a vital role in stress signalling and tolerance. Moreover, Ca together with Mg – a macronutrient, whose root content decreased in plants grown under conditions of high Ni-contamination – regulates and stabilizes cell membrane structure and permeability. Ni may turn some macronutrients like Ca and Mg and micronutrients like Fe, Zn, and Cu from their physiological function. Its toxicity may be related to the fact that Ni2+ is characterised by ionic radii comparable to the other cations of essential elements; therefore, it may compete with them for common binding sites. The mechanism of Ni toxicity is often attributed to the replacement of essential metals in metalloproteins, binding to catalytic residues of non-metalloenzymes, allosteric inhibition of enzymes due to binding outside their catalytic site, and indirectly to oxidative stress [8, 10, 43, 51, 61]. The presence of Ni influences the cell membrane composition and permeability due to unfavourable changes in sterol and phospholipid levels as well as ATPase conformational and functional disorders. Proton pump H-ATPase coordinates active uptake and transport of essential elements. Enzyme activity may be influenced by Ni indirectly as a consequence of ion-induced imbalances resulting from inhibition of absorption and transport of essential elements or directly due to strong Ni affinity for functional sulfhydryl groups (-SH) of enzymes, which alters the conformation of the enzyme and inhibits its activity, thereby leading to various metabolic disorders. Thus, Ni excess alters -SH homeostasis. GSH depletion and bonding to the protein -SH groups are considered the primary route for Ni toxicity [67, 77]. Nevertheless, our findings (unpublished results) showed reduced and unchanged GSH concentrations at low (0.0004 mM) and high (0.08 mM) Ni levels, respectively, in mustard roots, accompanied by markedly increased synthesis of PCs. It is worth mentioning that, in spite of these significantly increased levels of thiol peptides in mustard roots, our investigations confirmed statement that Ni is a weak inducer of PCs [9].

The S-SO₄ level in the nutrient solution, besides Ni, was the second factor differentiating the conditions of the experiment. The standard S-SO₄ dose (2 mM S) used in the presented studies is recognized as moderate. The S-SO₄2- concentration found in the natural environment, i.e. unpolluted with heavy metals, oscillates between 0.16 and 7, in arid regions between 3 and 16, whilst in soil solutions with residues of sulphide ore mine between 13 and 110 mM [13]. It is well documented that the processes of Ni-resistance and mechanisms of alleviation of the toxicity of this element are associated with S metabolism, chiefly with high levels of O-acetyl-L-serine (OAS), Cys, and GSH in the biomass due to high activity of Ser acetyl transferase (SAT). Ni is classified as a borderline metal able to form durable connections with various types of chelating agents, especially S-donor ligands rich in highly reactive S functional groups [5, 16, 69]. Conducted studies (personal communication) revealed significantly increased GSH content in the Ni-exposed white mustard roots supplied with high S doses (6 and 9 mM), which may indicate activation of defence mechanisms. At the same time, the PC content in intensively S fertilized mustard increased at the lower (0.0004 and 0.04 mM) and decreased at the highest Ni doses (0.08 mM) applied.

Our investigations involve an obvious and widely known rule that available S in the nutrient environment increases with an increasing level of this macronutrient in the nutrient solution [25, 27]. This increase in total S obtained in mustard grown with and without Ni addition was accompanied by an increase in the S-SO₄ form (data not shown) and was more evident in roots than in shoots, whereas it should be stressed that the highest Ni dose used in the experiment did not significantly affect total and sulphate sulphur in shoots. The high concentration of total-S and S-SO₄ was not accompanied by external toxicity symptoms.

Conducted studies revealed that intensive S fertilization generally did not markedly affect the shoot N, P, K, Ca, and Mg contents, and this rule operated in treatments without Ni addition as well as in Ni-exposed objects. In turn, studies carried out by Rahman et al. [62] on rice, Togay et al. [80] on wheat, and Ganie et al. [18] on French bean demonstrated an increase in the contents of N, P, K, Ca, and Mg in shoot together with an increasing S dose in the nutrient environment. It should be stressed, however, that these species are characterised by different S requirements, i.e. mustard and bean need high but wheat and rice low S levels. Podleśna [55] reported that winter oilseed rape plants fertilized with high S doses showed higher concentrations of N, Ca, and K, lower content of P, and slightly changed Mg content. In turn, Lošák et al. [41] and Hřivna et al. [20] found that S fertilization did not affect N, P, Mg, and K concentrations but markedly raised the Ca content. Studies conducted by Jankowski et al. [26] revealed that S fertilization significantly raised S, decreased K, and did not affect N, P, Ca, and Mg contents in white mustard roots, whilst in Indian mustard roots supplied with S, the contents of N, K, Ca, and S increased, the P content decreased, and the Mg content remained unchanged.

At the same time, both these mustard species responded to the intensive S supplementation with decreased N and increased K content in shoots, but the shoot Mg and S contents remained unaffected. Simultaneously, P content rose in white mustard shoots and dropped in Indian mustard shoots. Admittedly, the presented studies in general did not show substantial changes in the macronutrient content except for S in the shoots of white mustard supplemented with high S doses and grown in the nutrient solution without and with Ni addition. Nevertheless, significantly increased contents of all macronutrients, except for the unchanged P content in the Ni-untreated plants and the decreased content of this macronutrient in the Ni-exposed plants, were recorded at the same time in roots. This constitutes evidence that S fertilization improves the nutritional environment both in the rhizosphere and plant system, which leads to increased availability of nutrients in the root zone coupled with enhanced metabolic activity [18, 27].

Macronutrient accumulation
In this paper above of the content, the accumulation i.e. the total amount of macronutrient in the mean biomass of one plant obtained in each treatment was presented. It is documented that sulphur fertilisation induces changes in the anionic composition in plants [7]. Furthermore, sulphur, similar to other essential elements, increases the rate of plant biomass growth, especially in representatives of the family Brassicaceae, which results in a decline or rise in the nutrient concentration in biomass and, consequently, changes in total accumulation thereof [2, 36, 74, 81]. This is important from the point of view of agriculture and horticulture, since the concentration of mineral compounds in tissues is associated not only with the dynamics of plant growth and development but also with enhanced or decreased resistance to various stress factors and, consequently, the quality of crops.

The changes in the macronutrient accumulation shown in the particular treatments of the experiment resulted from the changes in their contents together with changes in productivity (personal communications). The statistically proven rise found in root accumulation of all the analysed macronutrients in white mustard grown without Ni addition and fertilized with high S doses was related to the elevated productivity rather than the different kinds of changes in their content. At the same time, shoot accumulation of Ca and K, unlike that of S, was mainly induced by the changes in the content of the elements rather than the changes in productivity, whereas the N, P, and Mg accumulation was to a similar extent influenced by their contents and changes in productivity.

In turn, the decrease in the root and shoot accumulation of the macronutrients found in Ni-exposed mustard was mainly a consequence of the severe drop in the productivity (personal communications) rather than the different changes in their contents. Only the reduced shoot Ca accumulation was mainly related to the severe drop in the content of this macronutrient.

The quite stable root P accumulation found in Ni-stressed mustard supplied with high S doses was a consequence of the drop in the content of this macronutrient as well as elevated biomass. In turn, the increase in the root accumulation of all the other macronutrients was related both to the significant rise in their contents and to the elevated productivity, wherein K, Mg, and S accumulation was affected mainly by the changes in the content, and N and Ca by the changes in the productivity. The elevated shoot S accumulation shown in Ni-treated mustard supplemented with high S doses resulted from the greater increase in the content than the rise in the productivity. At the same time, the changes in the productivity together with the changes in the Mg and P contents were not big enough to affect significantly the accumulation of these macronutrients in shoots. In turn, the increase in the shoot Ca content and rise in the productivity, although not statistically proven, resulted in a significant increase in the accumulation of this macronutrient in Ni-stressed mustard plants intensively fertilized with S. Similarly, although insignificant, the changes in the shoot N and K contents as well as productivity in Ni-exposed mustard under the presence of 6 mM S were big enough to increase markedly the accumulation of both these macronutrients. However, N and K accumulation in the shoots of Ni-contaminated plants supplied with 9 mM S remained quite stable due to the slightly marked changes in their contents and shoot productivity. In the studies concerning fertilization with sulphur of winter oilseed rape, Podleśna [55] revealed a rise in the macronutrient content coupled with increased dry weight of biomass, which resulted in elevated nutrient accumulation, compared to control treatments.

Nickel accumulation
Our studies revealed that, under conditions of the standard and high S concentrations in the nutrient solution, Ni accumulation in the biomass of white mustard ‘Rota’ rose together with the increasing concentration of this micronutrient in the growth environment, and this increase was more marked in shoots than in roots. The elevated Ni accumulation in the biomass was accompanied by a rise in the Ni content and a decrease in the productivity (personal communication). The increase in the Ni content at the lowest and highest Ni concentrations in the nutrient solution (0.0004 and 0.08 mM) were more marked in shoots, and at the medium Ni dose (0.04 mM) in roots. In turn, the drop in the dry weight of Ni-exposed mustard, irrespective of the S level in the nutrient solution, was more pronounced for roots than shoots. It is quite well documented that growth inhibition and reduced dry biomass due to Ni toxicity are caused by, inter alia, alterations in polysaccharide synthesis and carbohydrate translocation [33], Golgi apparatus damage, disturbances in the ultrastructure of chloroplasts, deregulation of redox homeostasis, damage to nucleic acids, proteins, and lipids, disturbances in cell divisions, suppression of cell elongation, e.g. via stimulation of peroxidase activity, an improper course of meristematic tissue differentiation, and a reduced size of intracellular spaces [34, 39, 49, 53, 54]. Also our previous results (personal communication) obtained for mustard plants indicated oxidative stress, which manifested itself by increased superoxide anion radical (O2-.), and hydrogen peroxide (H2O2) accumulation accompanied by enhanced lipid peroxidation as the causes of suppressed root elongation. A similar pattern of growth reduction and Ni accumulation in under- and aboveground parts of mustard to that found in the presented investigations was shown by Tickoo et al. [79], Gopal and Nautiyal [19], Singh et al. [73], and Maitra and Banerjee [44]. Opposite tendencies in the Ni distribution in mustard were shown by Rajkumar and Freitas [63] as well as Qiu et al. [59]. In turn, Fargašová [15] found higher Ni accumulation in the shoots than in the roots as well as equal accumulation of Ni in both parts of this plant.

It was found that Ni-exposed mustard responded in a different way to both high S doses. Intensive sulphate nutrition of Ni-stressed white mustard, in general, significantly raised root Ni-accumulation at 6 mM S mainly due to the increased productivity and did not change the value of this parameter at 9 mM due to the similar significant increase in the productivity and a decrease in the Ni content. This change in root Ni accumulation was accompanied by reduced markers of oxidative stress (personal communication). Simultaneously, no significant changes were found in the shoot Ni accumulation. Only at the treatment with 9 mM S/0.04 mM Ni, a statistically proven drop in the shoot Ni accumulation occurred as a result of the severe drop in the Ni content.

It should be stressed that in all the experimental treatments, except for those without Ni-addition and those with the lowest Ni dose used in the experiment, the contents of Ni in the biomass (personal communication) exceeded to a great extent the permissible limit of 2 mg kg^-1 mentioned by Shah et al. [70] and Nazir et al. [50] and exceeded the allowable level of Ni (10 mg kg^-1) set by the WHO [24]. Also Singh et al. [73] claimed that mustard seemed to be unsafe and not suitable for cultivation on Ni contaminated soil due to the high Ni content in edible parts.

SUMMARY AND CONCLUSIONS

Our research demonstrated that Ni exposure (0.0004–0.08 mM Ni) of white mustard causes various unfavourable changes in the macronutrient content and, in general, decreases accumulation thereof and raises Ni accumulation in the roots and shoots. Moreover, the results imply that high sulphate supplementation (6 or 9 mM S) of Ni-stressed mustard seems to improve to some extent the macronutrient status in this species. In general, it substantially increases the contents and accumulation of all macronutrients in roots. Simultaneously, the macronutrient content in shoots, as a rule, remains quite stable. Moreover, a rise in Ca accumulation accompanied by an increase in N and K accumulation was recorded at the S dose 6 mM. Furthermore, the data presented in this paper showed quite stable root and shoot Ni accumulation. Only at the S level 6 mM, a statistically proven rise in the root Ni accumulation and content was recorded. So it may be stated that intensive S-SO₄ supplementation may to some extent improve unfavourable macronutrient status of mustard.

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Accepted for print: 17.04.2017

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Renata Matraszek
Department of Plant Physiology, Faculty of Horticulture and Landscape Architecture, University of Life Sciences in Lublin, Poland
Akademicka 15
20-950 Lublin
Poland
email: renata.matraszek@up.lublin.pl

Barbara Hawrylak-Nowak
Department of Plant Physiology, Faculty of Horticulture and Landscape Architecture, University of Life Sciences in Lublin, Poland
Akademicka 15
20-950 Lublin
Poland
email: bhawrylak@yahoo.com

Mirosława Chwil
Department of Botany, Faculty of Horticulture and Landscape Architecture, University of Life Sciences in Lublin, Poland
Akademicka 15
20-950 Lublin
Poland
email: miroslawa.chwil@up.lublin.pl

Stanisław Chwil
Department of Chemistry, Faculty of Agrobioengineering, University of Life Sciences in Lublin, Poland
Akademicka 15
20-950 Lublin
Poland
email: stanislaw.chwil@up.lublin.pl

Michał Rudaś
Central Laboratory of Agroecology, University of Life Sciences in Lublin, Poland
B. Dobrzańskiego 3
20-262, Lublin
Poland
email: erdihl@gmail.com

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