1. Introduction
Soil is the basis for plant growth, and the soil-plant system is the basic structural unit of the biosphere, which provides strong productivity for human beings. Soil is often limited by a low level of available nutrients, so fertilization is often necessary to replenish them. But, fertilization can introduce heavy metals into the soil [
1]. Excessive use of fertilizers can lead to a decrease in soil pH, increase the availability of natural heavy metal lead (Pb) in soil, cause harm to soil physical properties, and then affect plant growth and development [
2]. Lead from anthropogenic sources typically builds up mostly in the top layer of soil, and as depth increases, its concentration declines and only limited amounts of the lead in soil are thought to be soluble and hence available for plant uptake because of its high binding [
3]. Due to the detrimental effects on soil microbiology, food safety and crop growth, lead accumulation in soils is a severe concern in agricultural production [
4]. Lead’s speciation in soil has a significant impact on its bioavailability and, consequently, its toxicity to plants and microorganisms [
5]. Studies have found that even short-term exposure of plants to the toxic effects of the heavy metal lead can lead to a significant reduction in their microbial activity; to counteract these effects, many plants and microorganisms have evolved detoxification mechanisms using organic colloidal components [
6,
7,
8].
Nitrogen fertilizer is the most widely used fertilizer in agricultural production and plant cultivation, and can directly affect plant yield and quality. Through the root box test, it was found that ammonium nitrogen fertilizer could reduce the pH value of the foundation soil, improve the activity of Pb in the rhizosphere soil, and promote the absorption of Pb by maize, while the effect of nitrate nitrogen is the opposite [
9]. Phosphorus is the second macronutrient necessary for plant growth. Existing studies indicate that phosphorus compounds could reduce the absorption of Pb by plants by enhancing the adsorption and complexation of soil colloid surfaces, on the other hand, the application of ammonium phosphorus fertilizer and calcium-phosphorus fertilizer would reduce soil pH value, and the decrease of pH value would increase the solubility and mobility of heavy metals, improve their bioavailability and toxicity, and promote the absorption of heavy metals by plants [
10]. Potassium is also one of the essential nutrient elements for plant growth, mainly used to improve crop quality [
11]. The research showed that K
+ could compete with Pb
2+ for adsorption sites on the surface of soil particles to increase the content of water-soluble and exchangeable Pb, thus increasing the content of its available state [
12,
13]. Organic fertilizer can not only improve soil fertility but also affect the form of heavy metals in soil and their absorption by plants [
14,
15]. Studies have shown that both the available Pb content and wheat absorption were significantly negatively correlated with the application of organic fertilizer, while the available Pb content in soil was significantly positively correlated with the amount of Pb absorbed by wheat [
15,
16]. The application of organic fertilizer could inhibit the absorption of Pb in soil by wheat [
17]. Therefore, it is of great significance for the safe and sustainable development of agricultural products to understand the effects of nitrogen, phosphorus, potassium and organic fertilizers on the content of heavy metals in soil and plants [
18,
19].
Urumqi is the most distant inland city from the ocean in the world, with an average altitude of 680~920 m. It has a semi-arid continental climate with a large temperature difference between day and night, abundant solar and thermal resources, and its terrain and soil types are suitable for growing vegetables, rice and other crops [
20]. The research showed that the average contents of Cd, Pb and Hg in farmland soil in Urumqi exceed the soil background value in Urumqi, of which the Pb content (24.83 mg·kg
−1) is about the soil background value (17.95 mg·kg
−1) 1.4 times, which has not yet exceeded the limit requirements in the “Evaluation Standards for Environmental Quality of Edible Agricultural Products Origin” (HJ 332-2006) (Pb ≤ 50 mg·kg
−1), and is far lower than the “Soil Environmental Quality” (GB 15618-2018) The control standards (6.5 < pH ≤ 7.5, Pb ≤ 120 mg·kg
−1) but there have been occurrences of Pb exceeding the standard in locally produced vegetables in Urumqi [
21]. The previous data of our research group showed that when the lead content in the soil of Urumqi did not exceed the standard, improper fertilization would lead to excessive lead in the edible part of the radish. Therefore, exploring the effect of fertilization on the growth and Pb content of vegetables in Urumqi City can provide the theoretical basis for safe and reasonable fertilization. In this study, the common solanaceous vegetable pepper was taken as the object, and the effects of different levels of nitrogen, phosphorus and potassium fertilizer and organic fertilizer on the growth and Pb content of pepper under Pb stress were studied by pot orthogonal experiment in the shed [
22].
3. Results
3.1. Effects of Fertilization on Plant Height and Fruit Weight of PLI under Pb Stress
As can be seen from
Figure 1, The highest PLI plant height in the 8th group was 49.87 cm, while the lowest PLI plant height in the 11th group was 27.83 cm; the highest number of PLI fruits in the 2nd group was 20, and the lowest number of PLI fruits in the 13th group was 7; the highest PLI fruit weight in the 12th group was 165.47 g, and the lowest PLI fruit weight in the 13th group was 67.50 g. Most of the soil pH was weakly acidic except for groups 1, 3 and 4.
According to
Table 3, the factors affecting the plant height of PLI in order of importance were: A (N) > B (P
2O
5) > C (K
2O) > E (Pb
2+) > D (sheep manure), and N fertilizer has the greatest influence on PLI plant height. It can be seen from the K value that the level combination of factors that promote PLI plant height to reach the maximum is: A2 B4 C2 D1 E3, namely N (0.15 g·kg
−1), P
2O
5 (0.225 g·kg
−1), K
2O (0.15 g·kg
−1), sheep manure (0 g·kg
−1), Pb
2+ (100 mg·kg
−1); The level combination of factors contributing to the minimum plant height of PLI was as follows: A3 B3 C4 D3 E4, namely N (0.3 g·kg
−1), P
2O
5 (0.15 g·kg
−1), K
2O (0.45 g·kg
−1), sheep manure (6 g·kg
−1), Pb
2+ (350 mg·kg
−1).
The main and secondary influencing factors of different fertilizer applications on PLI fruit weight were as follows: B (P2O5) > D (sheep manure) > A (N)> C (K2O) > E (Pb2+), phosphorus fertilizer had the greatest effect on PLI fruit weight. The horizontal combination of factors that promote the maximum fruit weight of PLI is: A2 B4 C2 D4 E3, namely N (0.15 g·kg−1), P2O5 (0.225 g·kg−1), K2O (0.15 g·kg−1), sheep manure (9 g·kg−1), Pb2+ (100 mg·kg−1); The horizontal combinations of factors that promoted PLI fruit weight to reach the minimum value were: A4 B1 C4 D2 E4, namely N (0.45 g·kg−1), P2O5 (0 g·kg−1), K2O (0.45 g·kg−1), sheep manure (3 g·kg−1), Pb2+ (350 mg·kg−1).
As can be seen from
Figure 2, nitrogen fertilizer was positively correlated with PLI plant height, phosphorus fertilizer was significantly positively correlated with PLI fruit weight (
p < 0.05), and nitrogen fertilizer was significantly negatively correlated with soil pH value (
p < 0.05).
3.2. Analysis of Pb Content in PLI
The results of Pb content determination in PLI were shown in
Table 4. As can be seen from
Table 4, the Pb content range of different parts of PLI in each treatment was generally in the order of root (0.104~1.086 mg·kg
−1) > stem (0.032~0.298 mg·kg
−1) > leaf (0.022~0.072 mg·kg
−1), indicating that Pb was mainly concentrated in the root. Pb content in fruits ranged from 0.011 mg·kg
−1 to 0.085 mg·kg
−1, among which the highest Pb content in fruits treated 16 was 0.085 mg·kg
−1, but it did not exceed the limit (0.1 mg·kg
−1) in the “National Standard for Food Safety-Limit of Pollutants in Food” (GB 2762-2017).
The variance analysis of Pb content in different parts of PLI applied with different kinds of fertilizer is shown in
Figure 3. The difference in Pb content in different parts of PLI under different treatments shows that there is no significant difference in Pb content in different parts of PLI in groups 1, 7, 15 and 16. Pb content in the roots and stems of PLI in groups 3, 5 and 11 was significantly different from that in the leaves and fruits. The Pb content in the roots of PLI in groups 2 and 6 was significantly different from that in the leaves and fruits. Pb content in the roots of PLI seedlings in groups 4 and 13 was significantly different from that in stems, leaves and fruits. The Pb content in the roots of group 14 was significantly higher than that in stems, leaves and fruits, and the Pb content in stems, leaves and fruits also showed significant differences, The content of Pb in roots was significantly different from that in stems, leaves and fruits.
In addition, the difference between groups in the same part of PLI under different treatments was as follows: the Pb content of group 14 in the root was significantly different from that of group 7 and group 15; Pb content in the stems of group 11 was significantly different from that in the stems of group 4. Pb content in leaf group 7 was significantly different from that in groups 1, 2, 3, 5, 6, 8, 9, 10, 11, 12, 13 and 15. Pb content in fruit group 7 was significantly different from that in groups 2, 3, 8, 9, 12, 13, 14, 15 and 16.
3.3. Effects of Fertilization on Pb Content in PLI under Pb Stress
According to the R-value in
Table 5, the main and secondary influencing factors of different fertilizers on Pb content in PLI roots were as follows: E (Pb
2+) > A (N) > C (K
2O) > B (P
2O
5) > D (sheep manure), and Pb
2+ had the greatest influence on Pb content in PLI roots. It can be seen from the K value that the combination of factors that promote the maximum Pb content in PLI root is as follows: A4 B1 C4 D1 E4, namely N (0.45 g·kg
−1), P
2O
5 (0 g·kg
−1), K
2O (0.45 g·kg
−1), sheep manure (0 g·kg
−1), Pb
2+ (350 mg·kg
−1); The level combination of factors to promote the minimum Pb content in PLI root was as follows: A3 B3 C1 D3 E1, namely N (0.3 g·kg
−1), P
2O
5 (0.15 g·kg
−1), K
2O (0 g·kg
−1), sheep manure (6 g·kg
−1), Pb
2+ (0 mg·kg
−1).
The main and secondary influencing factors on Pb content in PLI fruit were as follows: E (Pb2+) > C (K2O) > A (N) = D (sheep manure) > B (P2O5), and Pb2+ had the greatest influence on Pb content in PLI fruit. The combination of factors that promote the maximum Pb content of PLI fruit is as follows: A2 B1 C4 D3 E4, namely N (0.15 g·kg−1), P2O5 (0 g·kg−1), K2O (0.45 g·kg−1), sheep manure (6 g·kg−1), Pb2+ (350 mg·kg−1); The combination of factors that promote the minimum Pb content of PLI fruit is as follows: A4 B4 C3 D1 E3, namely N (0.45 g·kg−1), P2O5 (0.225 g·kg−1), K2O (0.3 g·kg−1), sheep manure (0 g·kg−1), Pb2+ (100 mg·kg−1).
3.4. Effect of Fertilization Level on Pb Content in PLI under Pb Stress
The correlation analysis of various indicators of soil and PLI is shown in
Figure 4. The Pb content of PLI roots is significantly positively correlated with the Pb content of leaves, and the Pb content of PLI stems and fruits is significantly positively correlated. The ratio of PLI stem to root and shoot showed a significant negative correlation; soil Pb content was significantly positively correlated with plant height, and plant height was significantly positively correlated with fruit weight.
The linear relationship between Pb content in different parts of PLI and different fertilizer applications is shown in
Table 6. The variation trend of lead content in each part of PLI is shown in
Figure 5. According to
Table 6 and
Figure 5, we can find that there was a significant negative correlation between sheep manure and Pb content in PLI stems (r =−0.990,
p = 0.010). Pb
2+ was positively correlated with Pb content in root (r = 0.993,
p = 0.007), and Pb content in leaf (r = 0.979,
p = 0.021). There was no significant correlation between Pb content in different parts of PLI and other fertilizers.
4. Discussion
Fertilization is one of the important agricultural measures to ensure the increase of agricultural production and income, and it also affects the adsorption and resolution of heavy metals in soil, the physicochemical properties of rhizosphere soil and the absorption of heavy metals by crops [
23]. Pb is a non-essential element for plants, thus it is hazardous even in low quantities. It easily passes from the soil and atmosphere to plants [
2].
Nitrogen is an essential element for plant growth and is contained in the composition of vitamins and energy systems in plants [
24]. In this experiment, there was a positive correlation between nitrogen fertilizer and plant height of PLI, that is, the increase of nitrogen fertilizer would promote the growth of plant height. The study showed that the average growth rate and plant height of plants increased when the nitrogen supply of plants increased, which was consistent with the results of this experiment. However, nitrogen application is considered to be the main driving factor of soil acidification, because the input of nitrogen fertilizer will make the nitrogen in the soil easy to nitrate, and the generated NO
3− will produce H
+, which is easy to leach out of the soil with base ions [
25]. The study showed that the nitrification of nitrogen in the soil would produce a large number of protons and lead to a decrease in soil pH, while the addition of fertilizer nitrogen in the soil would lead to more significant soil acidification [
25]. In this experiment, there was a significant negative correlation between nitrogen fertilizer and soil pH value, that is, the increase of nitrogen fertilizer led to the decrease of soil pH value. The decrease in soil pH can increase the content of extractable heavy metal elements in soil, improve the bioavailability of heavy metals, and enable plants to enrich more heavy metals [
26]. Therefore, attention should be paid to the decrease in soil pH value caused by nitrogen fertilizer application.
Rational application of phosphorus fertilizer can increase crop yield, improve crop quality, promote flowering and fruit of jacket vegetables, and improve results. The research showed that after applying phosphorus fertilizer, the yield of PLI increased with the increase of phosphorus application, and the yield was the highest at the highest phosphorus application [
18,
27]. In this experiment, there was a significant positive correlation between phosphorus fertilizer and PLI fruit weight, that is, the increase of phosphorus fertilizer would increase PLI fruit weight, possibly because phosphorus would participate in the metabolism and transportation of PLI carbohydrates, which is conducive to the growth of PLI fruit.
Organic fertilizer can not only improve soil fertility but also affect the form of heavy metals in soil and their absorption by plants [
15,
28]. In this experiment, the content of organic fertilizer was negatively correlated with the Pb content in the roots of PLI and significantly negatively correlated with the Pb content in the stems. Pb intake studies in plants revealed that roots have the ability to absorb large amounts of Pb while limiting their translocation to higher parts of the plant [
9,
29]. This may be because organic fertilizer has a fixed effect, including the adsorption of heavy metals by macromolecules of solid organic matter and clay minerals in the soil, limiting its mobility and reducing the availability of heavy metals [
30]. Moreover, after entering the root, ions are transported to the xylem through both ectoplasmic and symplast pathways, and then to the aboveground part. However, the low permeability of the ectoplasmic barrier to heavy metal ions makes it difficult for Pb to transfer to the stem of PLI [
2].
In this experiment, the Pb content in the roots of group 14 was significantly higher than that in stems, leaves and fruits, and the Pb content in stems, leaves and fruits also showed significant differences, which may be because high levels of Pb2+ were enriched in PLI roots through cation adsorption, oxidation and reduction reactions of exchange complexes and because heavy metals in roots were not easily transported upward from stems. Pb content in the stems of group 11 was significantly different from that in the stems of group 4, which may be due to the application of high-concentration organic fertilizer, which resulted in the chelation of Pb2+ with organic matter and other metal oxides, which restricted its mobility and reduced the absorption and transport capacity of Pb in the stems of PLI. Pb content in fruit group 7 was significantly different from that in groups 2, 3, 8, 9, 12, 13, 14, 15 and 16, which may be because potassium plays an important role in plant energy metabolism, acting as a cofactor or activator of many enzymes in carbohydrate and protein metabolism. In addition to helping the roots to absorb Pb from the soil and transfer it from the stem to the leaves, it can also accelerate the process of Pb absorption by the leaf surface itself.
According to the statistics of soil census data, the total nitrogen content of cultivated soil in Urumqi city was 1.13 g·kg
−1, the total phosphorus content was above 0.8 g·kg
−1 and the total potassium content was about 19.28g·kg
−1, showing the phenomenon of nitrogen deficiency, phosphorus deficiency and potassium enrichment [
31]. Pb content in soil is relatively low, generally < 100 mg·kg
−1.In view of the fact that the Pb content of all PLI fruits treated in this experiment is not beyond the standard, the optimal fertilizer application can be recommended according to the factor level combination (A2 B4 C2 D4) that promotes the maximum fruit weight of PLI: N (330 kg·hm
−2), P
2O
5 (495 kg·hm
−2), K
2O (330 kg·hm
−2), sheep manure (19,800 kg·hm
−2); Or according to the combination of treatment 12 with the maximum fruit weight (A3 B4 C2 D1), namely N (660 kg·hm
−2), P
2O
5 (495 kg·hm
−2), K
2O (330 kg·hm
−2), sheep manure (0 kg·hm
−2), both of which were treated with high-level phosphorus fertilizer and low-level potassium fertilizer. medium level of nitrogen fertilizer (or low level of nitrogen fertilizer + high level of organic fertilizer) can achieve a higher yield and not exceed the standard of Pb in fruit.
5. Conclusions
(1) The Pb content in PLI fruit ranged from 0.011 mg·kg−1 to 0.085 mg·kg−1, which did not exceed the limit (0.1 mg·kg−1) in the National Standard for Food Safety-Limit of Pollutants in Food (GB 2762-2017).
(2) The effect order of fertilization on fruit weight of PLI was P2O5 > sheep manure > N > K2O > Pb2+; The horizontal combination of factors that promoted PLI fruit weight to reach the maximum value were N (0.15 g·kg−1), P2O5 (0.225 g·kg−1), K2O (0.15 g·kg−1), sheep manure (9 g·kg−1), Pb2+ (100 mg·kg−1).
(3) The effects of fertilization on Pb content in PLI fruit were as follows: Pb2+ > K2O > N = sheep manure > P2O5; The level combination of factors that promoted the maximum Pb content in PLI fruit was N (0.15 g·kg−1), P2O5 (0 g·kg−1), K2O (0.45 g·kg−1), sheep manure (6 g·kg−1), Pb2+ (350 mg·kg−1). There was a significant negative correlation between sheep manure and Pb content in PLI stem (r = −0.990, p = 0.010). There was a significant positive correlation between Pb2+ and Pb content in the root (r = 0.993, p = 0.007) and in the leaf (r = 0.979, p = 0.021). There was no significant correlation between Pb content in different parts of PLI and other fertilizers.
(4) Recommended optimal fertilizer application: high-level phosphorus fertilizer P2O5 (495 kg·hm−2), low-level potassium fertilizer K2O (330 kg·hm−2), medium-level nitrogen fertilizer N (660 kg·hm−2) (or low-level nitrogen fertilizer N (330 kg·hm−2) + high-level organic manure sheep manure (19,800 kg·hm−2), Can achieve high yield and fruit Pb does not exceed the standard.