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Article

High NH4+/NO3− Ratio Inhibits the Growth and Nitrogen Uptake of Chinese Kale at the Late Growth Stage by Ammonia Toxicity

by
Yudan Wang
,
Xiaoyun Zhang
,
Houcheng Liu
,
Guangwen Sun
,
Shiwei Song
* and
Riyuan Chen
*
College of Horticulture, South China Agricultural University, Guangzhou 510642, China
*
Authors to whom correspondence should be addressed.
Horticulturae 2022, 8(1), 8; https://doi.org/10.3390/horticulturae8010008
Submission received: 24 November 2021 / Revised: 16 December 2021 / Accepted: 20 December 2021 / Published: 22 December 2021
(This article belongs to the Special Issue Greenhouse Management for Better Vegetable Quality, Higher Nutrient Use Efficiency and Healthier Soil)
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Abstract

:
The aim of this study was to determine the effects of various NH4+/NO3− ratios in a nutrient solution on the growth and nitrogen uptake of Chinese kale under hydroponic conditions. The four NH4+/NO3− ratios in the nutrient solution were CK (0/100), T1 (10/90), T2 (25/75), and T3 (50/50). An appropriate NH4+/NO3− ratio (10/90, 25/75) promoted the growth of Chinese kale. T2 produced the highest fresh and dry weight among treatments, and all indices of seedling root growth were the highest under T2. A high NH4+/NO3− ratio (50/50) promoted the growth of Chinese kale seedlings at the early stage but inhibited growth at the late growth stage. At harvest, the nutrient solution showed acidity. The pH value was the lowest in T3, whereas NH4+ and NH4+/NO3− ratios were the highest, which caused ammonium toxicity. Total N accumulation and N use efficiency were the highest in T2, and total N accumulation was the lowest in T3. Principal component analysis showed that T2 considerably promoted growth and N absorption of Chinese kale, whereas T3 had a remarkable effect on the pH value. These findings suggest that an appropriate increase in NH4+ promotes the growth and nutrient uptake of Chinese kale by maintaining the pH value and NH4+/NO3− ratios of the nutrient solution, whereas excessive addition of NH4+ may induce rhizosphere acidification and ammonia toxicity, inhibiting plant growth.

1. Introduction

Nitrogen is an essential nutrient in plant growth. It is the main component of many important organic compounds and participates in many physiological and biochemical processes in plants [1]. The forms of nitrogen that plants can absorb and utilize include ammonium (NH4+), nitrate (NO3−), nitrite (NO2−), soluble protein, and free amino acids; higher plants mainly absorb NH4+ and NO3− [2]. However, the processes of absorption, storage, transportation, and assimilation of the two types of N in plants are very different. The different forms of N affect the growth and development of plants and ultimately affect their yield and quality.
Most crops prefer to absorb NH4+ rather than NO3− under the condition of hydroponics because a single NO3− nutrient consumes a large amount of energy during the reduction process. The absorption of NO3− increases the pH value of the solution, which leads to an insufficient supply of iron and other trace elements and decreases the content of chlorophyll, thus affecting the yield and quality [3]. The energy cost of NH4+ absorption and assimilation is lower than that of NO3− [4]. However, single NH4+ nutrition causes many problems, such as ammonium toxicity, blocked leaf expansion, reduced organic acid synthesis, and decreased osmotic regulation [5].
An increasing number of studies have shown that adding a mixture of NH4+ and NO3− in appropriate proportions is more advantageous for crop growth and development and that NH4+ and NO3− can interact when both N forms are provided together [4,6]. Compared with the addition of NH4+ or NO3− alone, appropriate NH4+/NO3− ratio nutrition can significantly promote plant growth, increase plant biomass, soluble sugar, soluble protein, and vitamin C content, and reduce nitrate content in strawberry [7], mini-Chinese cabbage [8], flowering Chinese cabbage [9], and Chinese kale [10]. In addition, it is well-known that the absorption of NH4+ can induce net release of H+ and acidify the rhizosphere, whereas the absorption of NO3− can increase H+ uptake through the H+ cotransport system in PM and alkalize the rhizosphere [11,12]. A plant’s uptake of different forms of N and its transport and assimilation mechanisms depend on its NH4+/NO3− ratios. Our recent research further showed that an appropriate NH4+/NO3− ratio triggers plant growth and nutrient uptake of flowering Chinese cabbage by optimizing pH value in nutrient solution [13].
Chinese kale (Brassica alboglabra L. H. Bailey) is an important vegetable in south China. The flower stalk and leaves of Chinese kale are rich in anticarcinogenic compounds and antioxidants, including glucosinolates, carotenoids, vitamin C, and total phenolics [14,15]. Chinese kale best absorbs NO3− under hydroponic conditions and easily accumulates nitrate. In our previous study, an appropriate increase of NH4+ in nutrient solution enhancement improved the yield and quality of Chinese kale and significantly reduced the nitrate content in its product organs [16]; however, the physiological mechanism of this regulation is still unclear.
Based on previous research, this study further investigates the effects of different NH4+/NO3− ratios on plant growth, seedling root morphology, nutrient solution composition, and plant nutrient absorption to reveal the physiological mechanism by which different NH4+/NO3− ratios regulate the growth and N uptake of Chinese kale.

2. Materials and Methods

2.1. Plant Material

The experiment was conducted in a greenhouse at the College of Horticulture, South China Agricultural University from March 2013 to January 2014. The average temperature from colonization to the end of the experiment was 24–30/20–24 °C (day/night). Chinese kale seeds ‘lvbao’ were provided by Guangzhou Academy of Agriculture Science. Chinese kale seeds were sown in a perlite medium. Seedlings with one developed true leaf and one core were watered with a 1/4 dose of Hoagland nutrient solution every 4 days. After 1 month, three consistent seedlings with three developed leaves and one core were selected and transplanted into hydroponic containers with 5.5 L of nutrient solution. There were 10 replications in each treatment arranged in a randomized complete block design.

2.2. Treatments

In this experiment, four different NH4+/NO3− ratios were set based on 1/2 dose of Hoagland sloe NO3− nutrient solution formula (Table 1): CK, 0/100; T1, 10/90; T2, 25/75; and T3, 50/50. General formula for mineral elements: B, 0.5 mg L−1; Mn, 0.5 mg L−1; Zn, 0.05 mg L−1; Cu, 0.02 mg L−1; Mo, 0.01 mg L−1. Fe was supplied by EDTANaFe at a concentration of 50 mg L−1. Additionally, 0.2 g L−1 ampicillin (excellent grade pure) was added to inhibit microbial activity. Chinese kale seedlings were transplanted and watered with a 1/4 dose of Hoagland nutrient solution (adjusted according to Table 1), adding 3/4 dose of mother liquor after 12 days, and adding pure water to the original volume of 5.5 L. Pure water was added to the original volume every 3 days. Electrical conductivity and pH were measured during the experiment. In nutrient solutions with different NH4+/NO3− ratios, NH4+ was supplied by NH4Cl. KCl or CaCl2 was added to maintain a constant concentration of K+ and Ca2+ among the treatments. All nutrient solutions were aerated for 15 min per hour using a controlled pump.
The seeds of Chinese kale were sown in a medium containing 0.5% agar. After 5 days, seedlings with a radicle length of 1.5 cm were transplanted into hydroponic containers with 1.1 L of nutrient solution for different NH4+/NO3− ratio treatments.

2.3. Parameter Measurements

Chinese kale seedlings were harvested when they reached marketable maturity, plant height, and stem diameter, and their fresh and dry weight (determined after 1 h at 120 °C and 48 h at 75 °C in a drying oven) were measured (3 biological replicates per treatment, 12 plants per replicate). The fresh weight of the product organ (flower stalk above the 4th node) is called the economic yield. The fresh and dry weight were measured at 9, 15, 21, and 27 days after treatment to calculate the growth rate. The growth rate was measured by dividing the difference in fresh weight before and after sampling by the number of days.
The seeds of Chinese kale were accelerated to bud on a medium containing 0.5% agar. After 5 days, seedlings with a radicle length of 1.5 cm were selected and treated with different NH4+/NO3− ratios. After 2 weeks, the root morphological indices were analyzed (3 biological replicates per treatment, 12 plants per replicate). The root samples were stained with 0.16% neutral red solution, scanned using an applied digital scanner (LA2400), and quantitatively analyzed using the WinRHIZO Pro LA2400 software (Regent Instruments, Canada) for total root length, root surface area, root volume, and average root diameter.
Total N content was determined according to the method suggested by Avery and Rhodes [17], and total N content was multiplied by the dry weight of the whole plant to calculate N accumulation. N loss (NL), N loss rate (NLR), mean residence time of N (MRT), N productivity (NP), and N use efficiency (NUE) were calculated as described by Eckstein and Karlsson [18] using the following formulae: NL = [(NSapplied − NSremain) − (Nharvest − Ntransplant) × n]/n; NLR = NL/(NSapplied − NSremain); MRT = (Nharvest − Ntransplant)/[(lnNharvest − lnNtransplant) × (NL/t)]; NP = [(Wharvest − Wtransplant)/(Tharvest − Ttransplant)] × [(lnNharvest − lnNtransplant)/(Nharvest − Ntransplant)]; NUE = NP ×MRT. In the above formulae, W represents the dry weight of the plant, T represents the sampling time, N represents the amount of N absorbed by seedlings, NS represents the amount of N in nutrient solution, n represents the number of seedlings in each hydroponic bucket, and t represents the number of days in the whole growth period. Total P and K were determined at 660 nm using a spectrophotometer and atomic absorption spectrophotometer [19].

2.4. Data Analysis

The data were analyzed by one-way analysis of variance (ANOVA) using SPSS 19.0. The differences between treatments were compared using the least significant difference (LSD) with a significance level of p < 0.05. The tables and figures were created using Excel 2013 and SigmaPlot 11.0, respectively. Multivariate principal component analysis (PCA) was performed using OriginPro 9.0.

3. Results

3.1. Growth and Biomass

The growth of Chinese kale was significantly affected by the different NH4+/NO3− ratios (Figure 1 and Figure S1). Compared with CK, plant height increased by 18.89% and 24.70% in T1 and T2, respectively (Figure 1A). Similarly, the stem diameter was the highest in T2, increasing by 13.89%, whereas there was no significant difference between CK and T3 (Figure 1B). The economic yield was the highest in T2 and lowest in T3 at the harvest stage of Chinese kale (Figure 1C). To further study the dynamic changes in Chinese kale growth under different NH4+/NO3− ratios, fresh and dry weights were measured at 9, 15, 21, and 27 days after treatment. T1, T2, and T3 significantly increased the biomass of Chinese kale during the growth stage (0–21 d) compared to the control. However, in contrast to T1 and T2, the fresh weight and dry weight of T3 at harvest time decreased by 17.57% and 12.60%, respectively, compared with CK (Figure 1D,E). This result is consistent with economic yield. At the early stage of Chinese kale growth (0–15 d), the root/shoot ratio was the highest in CK, followed by T1, and the difference between T2 and T3 was not significant, indicating that the treatment of increasing NH4+ in the nutrient solution would reduce the dry matter distribution of the roots. At the harvest stage of Chinese kale (27d), the root/shoot ratio of T3 was 1.13, 1.24, and 1.12 times that of CK, T1, and T2, respectively, indicating that the effect of high NH4+/NO3− ratio treatment on the shoot was greater than that on the root at the late growth stage of Chinese kale (Figure 1F).
Furthermore, we analyzed the effects of different NH4+/NO3− ratios on the growth rate of Chinese kale seedlings and found that the growth of Chinese kale was slow in the early growth stage and fast in the late growth stage (Table 2). During the period of 0–9 d after treatment, seedling growth rates were highest in T2 and T3, with no significant difference between them, followed by T1, and were the lowest in the control. During the period of 9–15 d after treatment, the change trend of the four treatments was consistent with that of 0–9 days. During the period of 15–21 d after treating, the growth rates of seedlings reached the maximum in T2 and T3, which were 519.6 mg d−1 plant−1 and 388.4 mg d−1 plant−1, respectively. During the period of 21–27 d after treatment, the seedling growth rates reached the maximum in CK and T1, which were 656.1 mg d−1 plant−1 and mg d−1 plant−1, respectively. In conclusion, at 0–21 d, the growth rate of seedlings was the highest in T2, followed by T3. However, the difference between them was not significant: at 0–27 d, the growth rate of seedlings was the lowest in T3, which was only 87.45%, 79.47%, and 73.08% that of the control, T1, and T2, respectively, indicating that the growth was significantly inhibited.
To study the effects of different NH4+/NO3− ratios on the root growth of Chinese kale seedlings, we measured the main root length, root total length, root surface area, root volume, and average root diameter (Table 3, Figure S2). The main root length of Chinese kale seedlings in T1 and T2 was slightly higher than that in CK, and that of T3 was slightly lower than that of CK. Compared with CK, the total root lengths of Chinese kale seedlings in T1 and T2 were 1.38 and 1.91 times than those of CK, respectively. Root volumes of Chinese kale seedlings in T1 and T2 were 1.74 and 2.87 times that of CK, respectively. The root surface area and average root diameter of Chinese kale seedlings were maximum in T2. We concluded that the optimal root growth and root indices of Chinese kale seedlings occurred under T2 (NH4+/NO3− = 25/75).. However, a high NH4+/NO3− ratio (50/50) may inhibit the main root elongation of Chinese kale seedlings to a certain extent. In addition, root activity showed no significant difference between the control, T1, and T2; however, it decreased by 20.85% in T3 compared with the control. (Figure S3).

3.2. Dynamic Changes in Nutrient Solution Composition

To elucidate the mechanism by which different NH4+/NO3− ratios affect the growth of Chinese kale, we conducted dynamic monitoring of the physicochemical properties of the nutrient solution and N content (Figure 2). The initial electrical conductivity (EC) value of the nutrient solution increased as the NH4+ proportion increased. The EC values were 629, 673, 732, and 879 µs cm−1 in the control, T1, T2, and T3, respectively (Figure 2A). With the growth of Chinese kale, both the EC value and ion concentration of the nutrient solution gradually decreased. During the entire growth period of the plant, the decrease in EC value in T2 was the largest, and the decrease in T1 and T3 was also greater than that of the control, but the decrease in EC value in T3 was the lowest during the harvest period. This indicates that an appropriate NH4+/NO3− ratio could promote the ion absorption of Chinese kale plants, and the NH4+/NO3− ratio (50/50) could promote ion absorption of plants at the early and middle stages but significantly inhibit ion absorption of plants at the late growth stage.
The initial pH value of the nutrient solution decreased as the NH4+ proportion increased; however, the difference was not significant, both were at approximately 6.75 (Figure 2B). During the entire growth period, the pH value in the CK was mostly weakly alkaline. Before and after the replenishment of the nutrient solution, the average pH of the nutrient solution showed a gradual increase and reached 8.15 at harvest time. The nutrient solution in T1 was weakly acidic at the early stages, and the pH value was stable at approximately 6.5. At 21 d, the pH value was greater than 7.0, the nutrient solution became weakly alkaline, and the pH of the nutrient solution further increased to 8.20 at harvest time. The nutrient solution in T2 was always weakly acidic, and the pH value decreased gradually at the early stage and reached the lowest value at 5.24 at 18 d. The pH value gradually increased and reached 6.73 at harvest time. The nutrient solution in T3 was acidic during the entire growth period, the pH of the nutrient solution decreased gradually, and the pH of the nutrient solution was 3.63 at the harvest stage. In combination with plant biomass, Chinese kale was found to be insensitive to environmental pH and could grow normally in a nutrient solution pH range of 4.73–8.15. An appropriate acidic environment was more conducive to the growth of Chinese kale; however, an over-acidic environment (pH < 4) could significantly inhibit the growth of Chinese kale and reduce the growth rate of plants.
During the plant growth period, the NO3− content in the four treatments decreased gradually as NH4+ proportion increased (Figure 2C). After 12 d of treatment, the NO3− content in the control, T1, T2, and T3 decreased by 45.74, 43.99, 37.38, and 25.12 mg L−1, respectively, compared with that before treatment. After the replenishment of nutrient solution, the NO3− content in the control, T1, T2, and T3 was 164.26, 145.01, 120.12 and 79.88 mg L−1, respectively. At harvest, the NO3− content in the control, T1, T2, and T3 decreased by 154.00, 145.00, 120.05, and 79.77 mg L−1, respectively, compared with that after the replenishment of nutrient solution. The proportions of NO3− absorbed by the four treatments (CK, T1, T2, and T3) to the total NO3− were 95.11%, 99.99%, 99.96%, and 99.90%, respectively, indicating that the three treatments (T1, T2, and T3) all promoted NO3− uptake by Chinese kale plants, and there was no significant difference between the different treatments. Similarly, with an increase in NH4+ proportion, the NH4+ content in the three treatments also decreased gradually (Figure 2D). After 12 d of treatment, the NH4+ content in T1, T2, and T3 decreased by 4.94, 12.26, and 14.74 mg L−1, respectively, compared with that before treatment. After nutrient solutions were added, the NH4+ content in T1, T2, and T3 were 16.06, 40.24, and 90.26 mg L−1, respectively. After 3 d, they decreased by 9.53, 9.52, and 37.55 mg L−1, respectively. Thereafter, they slowly decreased to 0.03, 0.01, and 34.77 mg L−1, respectively, at harvest. The proportions of NH4+ absorbed by the three treatments to the total NH4+ were 99.86%, 99.98%, and 66.89%, respectively, indicating that low and medium NH4+/NO3− ratios could significantly promote the absorption of NH4+ by Chinese kale compared with the high NH4+/NO3− ratio.
With the growth of the plants, the total N content in the four treatments decreased gradually with an increase in NH4+ proportion (Figure 2E). At harvest, the total N content in the control, T1, T2, and T3 was decreased by 154.00, 161.03, 160.28, and 135.26 mg L−1, respectively, compared with that after the replenishment of nutrient solution. The greatest reduction in total N content was observed in T1 and T2, and the final content at harvest was 0.04 and 0.08 mg L−, respectively. This indicates that a low NH4+/NO3− ratio (10/90) significantly promoted the absorption of total N by Chinese kale, whereas a high NH4+/NO3− ratio inhibited the absorption of total N. In addition, the three treatments (T1, T2, and T3) promoted the absorption of p by Chinese kale, whereas the high NH4+/NO3− ratio significantly inhibited the absorption of K by Chinese kale at the late growth stage (Figure S4).
We further analyzed the NH4+/NO3− ratio in the four treatments (Figure 2F). Before and after the replenishment of the nutrient solution, the NH4+/NO3− ratio in T1 showed a decreasing and then an increasing trend. It decreased to a minimum of 0.001 at 21 d and increased to a maximum of 0.445 at the harvest stage. The NH4+/NO3− ratio in T2 remained between 0.243 and 0.435, which decreased significantly to 0.003 at 24 d of treatment and then increased to 0.214 at the harvest stage. The NH4+/NO3− ratio in T3 gradually increased during plant growth, and it increased rapidly after the replenishment of nutrient solution and reached a maximum of 95.144 at the harvest stage.

3.3. N Content and N Use Efficiency

The total N content of Chinese kale first increased and then decreased during the growth period (Figure 3A). The N content of Chinese kale increased rapidly from 0 d to 9 d of growth, and T2 and T3 were significantly higher than those of the control and T1. The N content of Chinese kale increased slowly from 9 d to 15 d of growth, and T3 was higher than that of the other three treatments. Except for the control, the N content of Chinese kale plants decreased significantly from 15 to 21 d of growth. The N content in T3 increased by 5.40%, 5.40%, and 6.93% compared with CK, T1, and T2, respectively, at 27 d. In addition to total N content, seedling dry weight also had a significant effect on total N accumulation. Total N accumulation in Chinese kale increased continuously during the growth period (Figure 3B). In the middle and late periods of plant growth, the total N accumulation was the highest in T2, and the total N accumulation of control plants was the lowest in the period from 0 d to 25 d of growth, whereas the total N accumulation of T3 plants was the lowest at 27 d, which was reduced by 7.88%, 16.13%, and 21.62% compared with CK, T1, and T2, respectively.
To further study the N utilization of Chinese kale plants in response to different NH4+/NO3− ratios, we analyzed the N loss, N productivity, N residence time, and N use efficiency (Table 4). We found that there was a certain amount of N loss in Chinese kale production under hydroponic conditions. Compared with the control, N loss in T1, T2, and T3 was reduced by 7.37%, 27.40%, and 23.71%, respectively, and the N loss rate was reduced by 11.83%, 30.90%, and 12.97%, respectively, with significant differences between treatments. N retention time was prolonged in all three treatments; however, it was most significant in T2. N productivity was the highest in T2, followed by T1, and lowest in T3; however, there was no significant difference between the different treatments. Owing to the difference in N loss rate, N productivity, and N retention time, N use efficiency was significantly different between the four treatments. N use efficiency was the highest in T2, followed by T1; however, there was no significant difference between T1 and T3. The results showed that an appropriate NH4+/NO3− ratio (25/75) significantly reduced N loss, prolonged N retention time, and improved N productivity and N use efficiency compared with the control.

3.4. Principal Component Analysis

Principal component analysis (PCA) was used to visualize the effects of different NH4+/NO3− ratios on the growth and N uptake of Chinese kale (Figure 4). The computed model captured 84.5% of the total observed variance with the first two principal components (PCs). Four treatments (CK, T1, T2, and T3) were distributed in distinct quadrants in the PCA scatter plot. All indexes of plant growth and N uptake were the best in the T2 treatment, and biomass and root morphology were strongly correlated with N use efficiency. In addition, the NH4+/NO3− ratio in the nutrient solution and root/shoot ratio were the highest in T3 and were significantly negatively correlated with the pH value.

4. Discussion

The main forms of inorganic N, NH4+ and NO3− can be absorbed and utilized by plants [20,21]. To date, there have been many reports on the effects of different N forms and ratios on crop biomass [22]. Our previous study showed that the biomass of Chinese kale was largest when the nutrient solution increased NH4+ by 25% to 30%; when the nutrient solution increased NH4+ by 45% to 50%, the biomass of kale was significantly lower than that of the control treatment with only NO3− [9]. In this study, the high NH4+/NO3− ratio (50/50) significantly increased the biomass of Chinese kale and promoted plant growth at the early stage; however, it showed a strong inhibitory effect at the late growth stage (21–27 d). During this period, the plant growth rate was 304.9 mg d−1 plant−1, which was only 46.5% of plant growth in the control with only NO3− (Figure 1, Table 2). This showed that the effects of different NH4+/NO3− ratios on plant growth could also be closely related to the duration of treatment and growth stage of plants, and that a high concentration of NH4+ applied for a short time would not cause ammonium toxicity [23,24]. In this study, 2.25, 5.60, and 11.23 mmol L-1 Cl− was added to the nutrient solution of T1, T2, and T3, respectively, being less than the salt-osmotic stress threshold level of approximately 40 mmol L−1 NaCl for most plants [25]. Therefore, the amount of Cl− in the nutrient solution used in this study was insufficient for salt stress.
Plants mainly absorb nutrients through their roots. Of all mineral nutrients, nitrogen has the greatest influence on root morphology, growth, and distribution in the medium [26]. The absorption of NO3− by plants results in rhizosphere alkalization, while the absorption of NH4+ results in rhizosphere acidification [27]. In the present study, the nutrient solution was weakly acidic under a medium NH4+/NO3− ratio (25/75), and the root morphology index was the highest (Table 3). Root morphology and biomass were significantly positively correlated with pH under a medium NH4+/NO3− ratio (Figure 4). Appropriate ratios of NH4+/NO3− promote root growth and increase root dry weight [28,29]. Pepper treated with a 25:75 ratio increased root length, surface area, and root volume and tips [30]. Therefore, an appropriate NH4+/NO3− ratio (25/75) may promote root growth by maintaining the pH value, thereby increasing biomass. The pH of the rhizosphere also affects the absorption of NH4+ and NO3− by plants [31]. With the growth and development of plants, the pH value of the nutrient solution gradually decreased under a medium NH4+/NO3− ratio (25/75). The NO3− was quickly and completely absorbed, and only NH4+ remained in the nutrient solution at the late growth stage of Chinese kale (Figure 2). When the proportion of NH4+ in the nutrient solution was more than 75%, cabbage growth was reduced by 87% due to the accumulation of a large amount of free ammonia in the leaves [32]. The pH value and NH4+ proportion showed a significant negative correlation under a high NH4+/NO3− ratio (50/50) (Figure 4). However, the pH value was acidic, which was not conducive to the root development of Chinese kale seedlings. In addition, the accumulation of large amounts of NH4+ in Chinese kale leaves resulted in ammonium toxicity, which inhibits plant growth.
The change in pH value in the rhizosphere results in different absorption of NH4+ and NO3−, which affects the content and accumulation of N in plants [9]. In this study, the total N content of the three treatments (T1, T2, and T3) was significantly increased at 0–15 d after treatment compared to that of the control treatment with NO3− alone (Figure 3A). This is consistent with previous studies on Chinese flowering cabbage [13]. Total N accumulation increased continuously throughout the growth period of the Chinese kale. At the late plant growth stage, the total N accumulation of the high NH4+/NO3− ratio (50/50) was the lowest (Figure 3B). This is similar to the results of previous studies [33]. There was a negative correlation between N accumulation and biomass under high NH4+/NO3− ratios (Figure 4). NH4+ at higher concentrations caused toxicity in bamboo, as it inhibits root growth and N accumulation [34]. Therefore, a high NH4+/NO3− ratio reduced the uptake and accumulation of N in plants at the late growth stage of Chinese kale, thus inhibiting plant growth. Different NH4+/NO3− ratios also significantly affect the absorption of other nutrients [35]. In this study, a high concentration of NH4+ promoted the absorption of P but inhibited the absorption of K by Chinese kale at the late stage (Figure S4). There is a strong correlation between pH change in a solution and net cation or anion uptake in geranium and petunia [36]. The elevation of the NH4+ ratio in the fertilizer solution decreased the soil solution pH at 35 days after sowing, resulting in an increase in tissue P and a decrease in K content in French marigold “Orange Boy” [37]. This may be caused by the interaction between ions and the pH change in the rhizosphere.
This study adopts the definition of nutrient use efficiency by Berendse and Aerts [38], and divides nitrogen use efficiency into N productivity and average retention time of N. N productivity reflects a plant’s rapid growth strategy. The average retention time of nitrogen reflects a plant’s nutrient retention strategy [39]. In this study, N loss in the nutrient solution increased by NH4+ treatment was significantly lower than that of the control with NO3− alone (Table 4). In our recent research, the contents of NH4+, NO3−, and total N in the nutrient solution without plant culture were almost constant during the growth period [13]. Therefore, in a closed hydroponic system, the loss of N may be related to the N metabolism of plants or caused by changes in the nutrient solution composition during plant cultivation. Combined with the experimental conditions, this part of the N loss in this experiment should be attributed to gaseous loss. The volatile forms of gaseous nitrides include NH3, N2O, and NO. Previous studies have found that, compared with NH4+, when NO3− is used as the nitrogen source, the volatilization of N2O in wheat and of NO in rice is enhanced [40,41,42]. However, the main loss forms of nitrides during kale production are still unclear, and further experiments are needed. In this study, the medium NH4+/NO3− ratio (25/75) had the highest N use efficiency, unlike Brassica napus, which had the highest N use efficiency with a high NH4+/NO3− ratio (75/25) [43]. We observed that the NH4+/NO3− ratio in T2 was maintained at approximately 0.15 (Figure 2D), which may have contributed to balanced N absorption. The NH4+/NO3− ratio in T3 increased rapidly at the late stage of plant growth (Figure 2D), which may have caused insufficient assimilation of NH4+ after its absorption or protein degradation owing to NH4+ toxicity, thereby reducing N productivity. Thus, applying appropriate ratios of NH4+/NO3− is an important way to improve plant N use efficiency [44].

5. Conclusions

An appropriate NH4+/NO3− ratio (25/75) increased biomass and promoted the growth of Chinese kale, whereas high NH4+/NO3− (50/50) promoted the growth of Chinese kale seedlings at the early growth stage but inhibited growth at the late growth stage. With the prolongation of treatment time, the pH value of T3 nutrient solution decreased continuously, whereas the NH4+/NO3− ratio was the highest in T3 at the harvest stage. In addition, T2 had the highest total N accumulation and N use efficiency, whereas total N accumulation was lowest in T3. Thus, an appropriate NH4+/NO3− ratio (25/75) promotes the growth and N uptake of Chinese kale by maintaining the pH value of the nutrient solution, whereas excessive addition of NH4+ may induce rhizosphere acidification and ammonia toxicity, thereby inhibiting plant growth. This study provides a theoretical basis for the effects of different NH4+/NO3− ratios on plant growth and N absorption and utilization.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/horticulturae8010008/s1, Figure S1: Plant morphology of Chinese kale treated with different NH4+/NO3− ratios; Figure S2: The root morphology of Chinese kale seedlings treated with different NH4+/NO3− ratios; Figure S3: The root activity of Chinese kale under different NH4+/NO3− ratios; Figure S4: Effect of different NH4+/NO3− ratios on the content and accumulation of total K (A,B) and P (C,D) in the growth period of Chinese kale.

Author Contributions

R.C. and S.S. conceived and designed the study X.Z. carried out the experiments. Y.W. analyzed the data and wrote the manuscript. H.L. and G.S. reviewed and edited the manuscript. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by the Key-Area Research and Development Program of Guangdong Province (2020B0202010006), the Guangdong Provincial Special Fund for Modern Agriculture Industry Technology Innovation Teams (2021KJ131), and the China Agriculture Research System of MOF and MARA.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest.

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Horticulturae 08 00008 g001 550
Figure 1. Effect of different NH4+/NO3− ratios on the growth and biomass of Chinese kale. (A) plant height at the harvest stage. (B) stem diameter at the harvest stage. (C) economical plant yield at the harvest stage. (D) dynamic changes in fresh weight. (E) dynamic changes in dry weight. (F) dynamic changes in the ratio of root to shoot fresh weight. CK = 0/100, T1 = 10/90, T2 = 25/75, T3 = 50/50. DAT, days after treatment. The data represent mean ± SE (n = 3). Different letters in Figure 1C–F indicate significant differences at p < 0.05.
Figure 1. Effect of different NH4+/NO3− ratios on the growth and biomass of Chinese kale. (A) plant height at the harvest stage. (B) stem diameter at the harvest stage. (C) economical plant yield at the harvest stage. (D) dynamic changes in fresh weight. (E) dynamic changes in dry weight. (F) dynamic changes in the ratio of root to shoot fresh weight. CK = 0/100, T1 = 10/90, T2 = 25/75, T3 = 50/50. DAT, days after treatment. The data represent mean ± SE (n = 3). Different letters in Figure 1C–F indicate significant differences at p < 0.05.
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Figure 2. Changes in electrical conductivity value (A), pH value (B), NO3− content (C), NH4+ content (D), total N content (E), and NH4+/NO3− ratios (F) in nutrient solution under different NH4+/NO3− ratios. CK = 0/100, T1 = 10/90, T2 = 25/75, T3 = 50/50. DAT, days after treatment. The data represent mean ± SE (n = 3).
Figure 2. Changes in electrical conductivity value (A), pH value (B), NO3− content (C), NH4+ content (D), total N content (E), and NH4+/NO3− ratios (F) in nutrient solution under different NH4+/NO3− ratios. CK = 0/100, T1 = 10/90, T2 = 25/75, T3 = 50/50. DAT, days after treatment. The data represent mean ± SE (n = 3).
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Figure 3. The content (A) and accumulation (B) of total N affected by different NH4+/NO3− ratios during the growth period of Chinese kale. CK = 0/100, T1 = 10/90, T2 = 25/75, T3 = 50/50. DW, dry weight; DAT, days after treatment. The data represent mean ± SE (n = 3).
Figure 3. The content (A) and accumulation (B) of total N affected by different NH4+/NO3− ratios during the growth period of Chinese kale. CK = 0/100, T1 = 10/90, T2 = 25/75, T3 = 50/50. DW, dry weight; DAT, days after treatment. The data represent mean ± SE (n = 3).
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Figure 4. Principal component analysis showing differences and correlations in the investigated parameters of Chinese kale under different NH4+/NO3− ratio.
Figure 4. Principal component analysis showing differences and correlations in the investigated parameters of Chinese kale under different NH4+/NO3− ratio.
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Table
Table 1. Nutrient solution with different NH4+/NO3− ratios (Unit: mM).
Table 1. Nutrient solution with different NH4+/NO3− ratios (Unit: mM).
TreatmentsNH4+/NO3−KNO3Ca(NO3)2·4H2OKH2PO4MgSO4·7H2O(NH4)2SO4K2SO4CaCl2
CK0/1002.52.50.51.4---
T110/901.752.50.51.40.3750.375-
T225/750.6252.50.51.40.93750.9375-
T350/50-1.8750.51.41.8751.250.625
Table
Table 2. Effects of different NH4+/NO3− ratios on the growth rate of Chinese kale (Unit: mg d−1 plant−1).
Table 2. Effects of different NH4+/NO3− ratios on the growth rate of Chinese kale (Unit: mg d−1 plant−1).
TreatmentsNH4+/NO3−0~99~1515~2121~270~210~27
CK0/10027.7 ± 2.8 b141.8 ± 4.9 c237.5 ± 47.5 c656.1 ± 17.0 a120.2 ± 15.3 c239.0 ± 8.1 bc
T110/9033.7 ± 2.0 ab167.1 ± 17.5 b341.3 ± 65.9 b625.1 ± 27.0 a159.7 ± 22.2 bc263.0 ± 22.3 ab
T225/7540.5 ± 3.9a197.2 ± 4.2 a519.6 ± 156.0 a509.0 ± 76.4 b222.2 ± 47.7 a286.0 ± 21.4 a
T350/5039.9 ± 5.3 a186.8 ± 9.3 a388.4 ± 17.5 ab304.9 ± 57.7 c181.4 ± 9.7 ab209.0 ± 20.4 c
Data are presented as mean ± SE (n = 3). Different letters indicate significant differences at p < 0.05.
Table
Table 3. Effects of different NH4+/NO3− ratios on root morphological indices of Chinese kale seedlings.
Table 3. Effects of different NH4+/NO3− ratios on root morphological indices of Chinese kale seedlings.
TreatmentsNH4+/NO3−Main Root Length
(cm plant−1)		Root Total Length
(cm plant−1)		Root Surface Area
(cm2 plant−1)		Root Volume
(cm3 plant−1)		Average Root Diameter
(mm)
CK0/1006.91 ± 0.77 ab65.8 ± 11.5 c13.7 ± 3.2 c0.23 ± 0.07 cd0.66 ± 0.04 b
T110/907.23 ± 0.38 ab90.8 ± 2.7 b20.9 ± 5.1 b0.40 ± 0.19 b0.73 ± 0.16 ab
T225/757.72 ± 0.84 a126.0 ± 8.9 a31.9 ± 4.2 a0.66 ± 0.16 a0.81 ± 0.09 a
T350/506.63 ± 0.49 b61.4 ± 12.4 c14.5 ± 3.7 c0.28 ± 0.09 bc0.75 ± 0.07 ab
Data are presented as mean ± SE (n = 3). Different letters indicate significant differences at p < 0.05.
Table
Table 4. Rate of N loss, N residence time, N productivity, and N use efficiency in nutrient solutions with different NH4+/NO3− ratios during the growth period of Chinese kale.
Table 4. Rate of N loss, N residence time, N productivity, and N use efficiency in nutrient solutions with different NH4+/NO3− ratios during the growth period of Chinese kale.
TreatmentsNH4+/NO3−N Loss
(mg Plant−1)		Rate of N Loss (%)N Residence Time (d)N Productivity (mg mg−1 d−1)N Use Efficiency (mg mg−1)
CK0/100102.1 ± 5.1 a27.9 ± 1.2 a13.9 ± 0.1 c4.6 ± 0.6 a63.3 ± 1.7 c
T110/9094.6 ± 1.5 b24.6 ± 0.4 b16.1 ± 0.4 b4.7 ± 0.2 a75.1 ± 5.4 b
T225/7574.1 ± 3.2 c19.3 ± 0.8 c21.8 ± 0.3 a4.8 ± 0.7 a104.1 ± 4.1 a
T350/5077.9 ± 3.3 c24.3 ± 0.9 b17.0 ± 0.4 b4.3 ± 0.6 a72.3 ± 4.2 b
Data are presented as mean ± SE (n = 3). Different letters indicate significant differences at p < 0.05. Significant differences among the treatments were determined using SPSS 17.0.
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Wang, Y.; Zhang, X.; Liu, H.; Sun, G.; Song, S.; Chen, R. High NH4+/NO3− Ratio Inhibits the Growth and Nitrogen Uptake of Chinese Kale at the Late Growth Stage by Ammonia Toxicity. Horticulturae 2022, 8, 8. https://doi.org/10.3390/horticulturae8010008

AMA Style

Wang Y, Zhang X, Liu H, Sun G, Song S, Chen R. High NH4+/NO3− Ratio Inhibits the Growth and Nitrogen Uptake of Chinese Kale at the Late Growth Stage by Ammonia Toxicity. Horticulturae. 2022; 8(1):8. https://doi.org/10.3390/horticulturae8010008

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Wang, Yudan, Xiaoyun Zhang, Houcheng Liu, Guangwen Sun, Shiwei Song, and Riyuan Chen. 2022. "High NH4+/NO3− Ratio Inhibits the Growth and Nitrogen Uptake of Chinese Kale at the Late Growth Stage by Ammonia Toxicity" Horticulturae 8, no. 1: 8. https://doi.org/10.3390/horticulturae8010008

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