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Effects of Different Inorganic Nitrogen Sources of Iris pseudacorus and Iris japonica on Energy Distribution, Nitrogen, and Phosphorus Removal

Authors:
Rongrong Duan Key Laboratory of Modern Agricultural Equipment and Technology of Ministry of Education, School of Agricultural Engineering, Jiangsu University, Zhenjiang 212013, China

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Deke Xing Key Laboratory of Modern Agricultural Equipment and Technology of Ministry of Education, School of Agricultural Engineering, Jiangsu University, Zhenjiang 212013, China

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Tian Chen Key Laboratory of Modern Agricultural Equipment and Technology of Ministry of Education, School of Agricultural Engineering, Jiangsu University, Zhenjiang 212013, China

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Yanyou Wu State Key Laboratory of Environmental Geochemistry, Institute of Geochemistry, Chinese Academy of Sciences, Guiyang 550081, China

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Article Category:
Research Article
Online Publication Date:
16 May 2022
Page(s):
698–707
Volume/Issue:
Volume 57: Issue 6
Copyright:
© American Society for Horticultural Science 2022
DOI:
https://doi.org/10.21273/HORTSCI16510-22
Open Access
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Abstract

High- and low-affinity transport systems are the main pathways for the transportation of NO3– and NH4+ across intracellular membranes. NO3− and NH4+ are assimilated through different metabolic pathways in plants. Fifteen ATP molecules are hydrolyzed in the metabolic process of NO3–; however, only five ATP molecules are hydrolyzed in that of NH4+. In this research, seedlings of Iris pseudacorus and Iris japonica were used as the experimental materials in the NO3–:NH4+ = 30:0, NO3–:NH4+ = 28:2, NO3–:NH4+ = 27:3, NO3–:NH4+ = 15:15, NO3–:NH4+ = 3:27, and NO3–:NH4+ = 0:30 treatments at the 7.5 mmol·L−1 the total nitrogen content (TN). The intracellular free energy was represented by physiological resistance (R) and physiological impedance (Z) according to the Nernst equation and could conveniently and comprehensively determine the cellular metabolic energy (GB). The maximum absorption rate (Vmax) and Michaelis constant (Km) for NH4+ and NO3– uptake were calculated according to the kinetic equation. The results showed that the cellular metabolic energy (GB) of I. pseudacorus was 1 to 1.5 times lower than that of I. japonica at each treatment on the 10th day. The GB values of I. pseudacorus and I. japonica seedlings increased with increasing NH4+ concentration. However, there was a turning point at the NO3–:NH4+ = 15:15 treatment for the cellular metabolic energy of I. pseudacorus and I. japonica. Correlation analysis showed that the value of cellular metabolic energy was negatively correlated with the Vmax and Km for NO3– uptake, whereas it was positively correlated with that for NH4+ uptake. These results demonstrate that the NO3–:NH4+ = 27:3 treatment level was the most suitable for I. pseudacorus and I. japonica. This indicates that the greater cellular metabolic energy is the most suitable for plant growth when the concentration of ammonium or nitrate had no significant difference at treatment. These results provide a simple and rapid solution for removal of nitrogen by determination of cellular metabolic energy.

Keywords: electrophysiological information; cellular metabolic energy; nitrogen metabolism; nitrogen affinity system; phosphorus affinity system

Nitrate (NO3–) and ammonium (NH4+) are the primary nitrogen sources for higher plants (Cui et al., 2017; Poothong and Reed, 2016; Tho et al., 2017). High- and low-affinity transport systems (HATS and LATS) are the main pathways for the transportation of nitrate across intracellular membranes (Kochian and Jiao, 1985). The Michaelis constant (Km) estimated by using the Michaelis equation can be used to determine the pathway of nitrate transport, and a high value of Km indicates low-affinity NO3– uptake. Conversely, a low value of Km is associated with high-affinity NO3– uptake in plants (Kochian and Jiao, 1985; Siddiqi et al., 1992). HATS in plants is activated when the value of Km is lower than 1 mmol·L−1, whereas LATS is activated when the value of Km is higher than 1 mmol·L−1 (Krapp et al., 2014). The kinetics of NO3– absorption are characterized by a linear unsaturated dependence in high-concentration media (Krapp et al., 2014). The transmembrane transport of NH4+ can also be conducted through HATS or LATS (Kronzucker et al., 1996). It is dominated by HATS when the concentration of NH4+ is lower than 1 mmol·L−1. However, LATS becomes dominant and can be characterized by a linear unsaturated dependence when the concentration of NH4+ is ≥1 mmol·L−1 (Kronzucker et al., 1996). A high concentration of NH4+ will induce HATS and inhibit the activity of ammonium metabolites (Wang et al., 1994).

Phosphorus and phosphorus-containing compounds are not only important constituents of the cytomembrane ATP, nucleic acids, and other living matter but are also necessary participants in the metabolic processes of matter and energy changes; they maintain the normal growth of plants (Hu, 2008). Phosphorus also plays an important role in the utilization of nitrogen by plants. It has been found that the transmembrane transport systems of phosphorus are similar to those of ammonium or nitrate (Hu, 2008). When suffering from phosphorus deficiency, plants absorb phosphorus through HATS, and the unit of Km is always µmol·L−1 (Mei et al., 2012). LATS prevails in plants, and the unit of Km is mmol·L−1 (Muchhal et al., 1996; Nielsen and Barber, 1978). Plants can use alternative transmembrane transport systems to transport ions, and the affinities of those systems are different. As a result, the values of the maximum absorption rate (Vmax) and Km will change correspondingly. Research has proven that the removal of ions could be represented by Km and Vmax (Chen et al., 2013).

NO3− and NH4+ are assimilated by different metabolic pathways in plants. Inorganic nitrogen metabolism in plants is shown diagrammatically in Fig. 1 (Liu and Shang, 2016; Wang et al., 2020). Part of NH4+ is assimilated to form amino acids and finally synthesizes proteins. Five ATP molecules are hydrolyzed in the metabolic process of NH4+. NO3– in plants is reduced into NO2– by nitrate reductase (NR), and NO2– is reduced into NH3 by nitrite reductase (NIR) when it enters the chloroplast through the plasma membrane. Then the synthesis process of amino acids is similar to that using NH4+ (Li et al., 2020; Liu and Shang, 2016; Wang and Lu, 2020). Fifteen ATP molecules are hydrolyzed in the metabolic process of NO3–, which means that the assimilation of NO3− requires more energy consumption than that of NH4+ (Guo et al., 2007). Therefore, we hypothesize that the cellular metabolic energy stored in plants changes when the inorganic nitrogen resources used by plants is altered. The solar energy used by plants is assumed to be Ea, the total energy consumption in the inorganic nitrogen metabolism process is Eb, the cellular metabolic energy stored in plants is GB, and the energy consumption in other metabolic processes (e.g., EMP, HMP) is Ed (Fig. 1). Here we presume that the values of Ea and Ed are constant, but what if the change trend of GB as Eb is altered? The accurate determination of GB is of great importance for the aforementioned investigation.

Fig. 1.
Fig. 1.

Relationship between plant metabolism and energy consumption. Ea represents the plant fixed solar energy, E represents the stable chemical energy in plants, Eb represents the total energy consumed by nitrogen metabolism, GB represents the cellular metabolic energy, and Ed represents the energy consumption by all the other metabolic processes.

Citation: HortScience 57, 6; 10.21273/HORTSCI16510-22

At present, the cellular metabolic energy in plants is traditionally represented by the intracellular energy state (Hardie and Grahame, 2015). The requirement and supply of metabolic energy in many metabolic processes are still unknown when referring to the assimilation and alienation of matter. Therefore, the cellular metabolic energy cannot simply be determined by the intracellular energy and charge state (Reuveni, 1992). In this research, the electrical energy is coupled with the resistance (R), impedance (Z), and capacitor (C) according to the Nernst equation, and the intracellular free energy is represented by R and Z to conveniently and comprehensively determine the cellular metabolic energy (Mwesigwa et al., 2000). The mesophyll cell can be regarded as a concentric sphere capacitor with both inductor and resistor functions. The resistive current is produced when the ion is transported across the cell membrane and is affected by the permeability of the cell membrane and the quantity of permeable ions (Mark et al., 2008; Stitt, 1999). The cell membrane permeability is influenced by the external stimulus, which changes the ion concentrations inside and outside the membrane. The Nernst equation can be applied to the difference in the ion concentrations mentioned earlier (Aoki, 1991; Schönleber and Ivers-Tiffée, 2015). Physiological resistance is inversely proportional to EC, and EC is proportional to the ion concentration in cells. As such, the relationship between physiological R or Z and external stimuli can be derived. Cellular metabolic energy can be more conveniently and comprehensively determined, in a more timely manner, by electrophysiological parameters than by the measurement of intracellular energy and charge state (Anderson, 1980; Ramage, 2002).

Iris pseudacorus and Iris japonica are both fast-growing plants with a strong ability to remove inorganic nitrogen (Chen et al., 2013). I. pseudacorus is a typical plant growing in aquatic and terrestrial environments. Studies have shown that I. pseudacorus grows better than I. japonica in the polluted water (Abe et al., 1991). Currently, most studies focus on the nitrogen absorption and efficiency of the aforementioned plants in water, and the absorption kinetics of NH4+, NO3–, and H2PO4– are also hot topics (Zhu et al., 2020). It has been found that I. pseudacorus had significant advantages in removing high concentration of nitrogen and phosphorus (NH4+: 180–220 mg·L−1, TP: 30–35 mg·L−1) (Feng et al., 2020). Researchers have also reported that the total nitrogen and phosphorus removal rate of I. pseudacorus were 48.84% and 46.13%, and I. pseudacorus has a strong ability to remove nitrogen and phosphorus (Ji et al., 2015; Yang et al., 2017). However, there is little research on the total nitrogen and phosphorus removal of I. japonica. In this research, seedlings of I. pseudocorus and I. japonica were used as the experimental materials, the variation of energy distribution in the two plant species and the removal of nitrogen or phosphorus in water were investigated under different inorganic nitrogen resources, and the relationship between energy distribution and removal of nitrogen or phosphorus was analyzed. This study provides a theoretical basis for improving the removal efficiency of different proportions of nitrogen in water and maintaining ecological balance.

Materials and Methods

Experimental materials.

Seedlings (20–30 cm) of I. pseudacorus and I. japonica were obtained from an online shopping platform in China. They were cultivated in half-strength Hoagland solution for one month before applying inorganic nitrogen treatment.

Experimental design.

The experiment was carried out at the Institute of Agricultural Engineering, Jiangsu University, Jiangsu Province, China. The seedlings of I. pseudacorus and I. japonica were cultivated in water under a 12 h photoperiod (260 ± 20 μmol·m−2·s−1), day/night temperature cycle of 28–30°C and relative humidity of 65% ± 5%. The concentrations of dissolved O2 were constantly supplied and were no less than 0.625 mmol·L−1. The water environment for the treatment was artificially simulated by using Hoagland solution. Each tray contained 10 L modified Hoagland’s solution, and water was added into the tray every day to maintain the content of the solution.

Taking the concentration of the urban pollutant emission standard (GB18918-2002) and the environmental quality standard of the surface water (GB3838-2002) as references, the total nitrogen content (TN) of Hoagland’s solution was calculated to be 7.5 mmol·L−1. Six NO3–/NH4+ proportions (30:0, 28:2, 27:3, 15:15, 3:27, and 0:30) (Table 1) were prepared by adding KNO3, Ca(NO3)2, NH4+NO3– and NH4+SO4– into Hoagland’s solution. The seedlings of I. pseudacorus were subjected to these six levels of treatment and marked as ps-1 (30:0), ps-2 (28:2), ps-3 (27:3), ps-4 (15:15), ps-5 (3:27), and ps-6 (0:30). The seedlings of I. japonica were simultaneously subjected to these six levels of treatment and marked as ja-1 (30:0), ja-2 (28:2), ja-3 (27:3), ja-4 (15:15), ja-5 (3:27), and ja-6 (0:30). The seedlings of I. pseudacorus and I. japonica before the treatment are marked as ps-0 and ja-0, respectively. To prevent the conversion of ammonium to nitrate nitrogen, 0.0035 mmol·L−1 nitrification inhibitor dicyandiamide (C2H4N4) was added to the treatment solution at each level. The treatment lasted for 10 d.

Table 1.

The concentration of NO3–, NH4+, and total nitrogen.
Table 1.

Determination of physiological capacitance, resistance, and impedance.

The third youngest fully expanded leaves from the top (five plants from each treatment group) were chosen for measurements. The leaves were soaked in water for 30 min to ensure that they were saturated. The leaf surface was then immediately sucked up, and the measurement site (10 cm away from the top) on the leaves was marked. The leaf was clamped at the parallel electrode plates of the measurement device, and the clamping force was changed by changing the number of weights (100 g per weight). The physiological C, R, and Z were measured using an LCR tester (Model 3532-50; Hioki, Nagano, Japan), and the frequency and voltage were set as 3 kHz and 1 V, respectively (Fig. 2).

Fig. 2.
Fig. 2.

The parallel-plate capacitor.

Citation: HortScience 57, 6; 10.21273/HORTSCI16510-22

Calculation of leaf cellular metabolic energy based on physiological capacitance, resistance, and impedance.

The mesophyll cells can be regarded as concentric sphere capacitors with both inductor and resistor functions. The leaf was clamped between the two parallel plates of the capacitor to form a parallel plate capacitor. The elasticity and plasticity of the mesophyll cells was changed, further leading to a change in the dielectric constant of the solute in leaf tissue. The physiological capacitance was affected.

The gravity equation is:
F = (M0 + m)g,
where F is gripping force (N), M is the mass of weights (kg), m is the mass of plastic rod and electrode (kg), and g is the gravitational acceleration with a value of 9.8.
The Gibbs’s free energy equation is:
ΔG = ΔH + PV.
The equation for the energy of the capacitor is:
W = 12U2C.

ΔH is the internal energy of the system (plant leaf system composed of cells), P is the pressure imposed on plant cells, V is the volume of plant cells, U is the test voltage, and C is the physiological capacitance of plant leaves.

P can be calculated as follows:
P = FS.
where F is the clamping force and S is the effective area of the leaf in contact with the action capacitor plates.
According to the energy conservation law, a capacitor’s energy is equal to the work converted by Gibbs’s free energy, i.e., W = ΔG. The physiological capacitance (C) is expressed using Eq. [5]:
C = 2ΔHU2+2VSU2F.
Assuming d represents the specific effective thickness of plant leaves, that is d=VS; Eq. [5] is then rewritten as:
C = 2ΔHU2+2dU2F.
Incorporating x0 = 2ΔHU2, h = 2dU2 into Eq. [6], it is then changed to be:
C = x0+hF,
where x0 and h are model parameters.
The d is then calculated as follows:
d = U2h2.
The Nernst equation is:
E−E0 = RTnF0InCiC0,
where E is the electromotive force (V), E0 is the standard electromotive force (V), R is the gas constant (8.31 J·K−1·mol−1), T is the thermodynamic temperature (K), Ci is the intracellular ion concentration (mol·L−1), C0 is the extracellular ion concentration (mol·L−1), F0 is the Faraday constant (9.65 × 104 C·mol−1), and n is the ion transfer amount (mol).

In mesophyll cells, vacuoles and cytoplasm occupy most of the space in the cell. The sum of C0 and Ci is certain for mesophyll cell. It is equal to the total amount of permeable ions (CT) inside and outside the membrane in response to physiological resistance, and Ci is directly proportional to the EC. The conductivity is the reciprocal of resistance (R).

The CiC0 is expressed as follows:
CiC0 = f0RCT−f0R = f0CTR−f0.
The internal energy of the electromotive force (E) can be transformed into work produced by the pressure PV = aE.
PV = aE = aE0+aRTnF0lnCiC0,
where P is the pressure imposed on plant cells; a is the transfer coefficient from electromotive force to energy; and V is the volume of plant cells. Eq. [10] into Eq. [11], and Eq. [12] are then rewritten as follows:
PV = aE = aE0−aRTnRlnCTR−f0f0.
Then:
lnCTRf0 = nF0E0RT−VnF0SARTF.
The logarithmic Eq. [13] written in base e can be solved as follows:
CTR−f0f0 = enF0E0RTe−VnF0FSaRT.
The resistance can be calculated as follows:
R = f0CT+f0CTenF0E0RTe−dnFF0aRT.
Incorporating y = f0CT,k1 = f0CTenF0E0RT,b1 = dnF0RTa into Eq. [15], it is then rewritten as:
R = y0+k1e−b1F.
where y0, k1, and b1 are the parameters.
The equation of unit cellular metabolic energy based on physiological resistance is:
ΔGR−E = aE0d = lnk1−lny0b1.
Then,
ΔGR = ΔGR−E×d.
Similarly,
E−E0 = R0TnZF0lnQiQ0.
The physiological resistance (Z) of plant leaves with increasing clamping force is expressed as follows:
Z = p0+k2e−Fb2,
where p0, k2, and b2 are the parameters.
Therefore, the unit cellular metabolic energy of leaf cells based on physiological impedance is:
ΔGZ−E=aE0d=lnk2—−lnp0b2.
The metabolic energy of plant leaves based on physiological impedance is:
ΔGZ = ΔGZ−E×d.
The equation of cellular metabolic energy (GB) is as follows:
GB = ΔGZ+ΔGR2.

Determination of nitrogen and phosphorus contents.

The water samples (20 mL) at each treatment level were measured on the 10th day. The concentrations of NH4+, NO3– and PO4– in water were determined by the following methods: NH4+-Nessler colorimetric spectrophotometer (Tan and Mao, 1998); NO3–-Thymol spectrophotometry (Sun et al., 2007); PO4–-ammonium molybdate spectrophotometer (Wei, 2003).

Calculation of kinetic parameters.

The contents of NO3–, NH4+, and PO4– in the samples were calculated according to the standard curve.

The equation is:
pN−N0 = mV,
where p(N–N0) is the nitrogen content in the water sample (mg·L−1), m is the value of the nitrogen content calculated according to the standard curve, and v is the volume of the measured water sample (mL).
The kinetic equation is then expressed as follows:
ΔV = VmaxCKm+C,
where V is the absorption rate (mmol·L−1·H−1), Vmax is the maximum absorption rate (mmol·L−1·H−1), C is the ion concentration in the external solution (mmol·L−1), and Km is the Michaelis constant (mmol·L−1).
The correlation between the ion concentration and the absorption time is expressed as follows:
Y = c + bX + aX2,
where Y is the ion concentration; X is the absorption time; and a, b, and c are the fitting parameters.
The derivative of Eq. [25] is as follows:
Y=−bX−aX2.
The Vmax is expressed as follows (where N is absorbed liquid volume):
Vmax=−b×N.

Incorporating Y=Vmax2 into Eq. [26], the X value in the equation seems to be the Km value.

Measurement of growth index.

The heights of plants (three plants from each treatment group) were determined by a ruler. The fresh weights of roots and leaves (three plants from each treatment group) were determined on the 10th day. The dry weights of leaves and roots (three plants from each treatment group) were measured after deactivation at 150 °C and drying blade at 60–70°.

Measurement of photosynthetic parameters.

The second fully expanded leaves were selected for the gas exchange measurement from 9:00 am to 11:30 am on sunny days. A portable LI-6400XT photosynthetic measurement system was used to determine the net photosynthesis rate (PN, µmol·m−2·s−1).

Statistical analysis.

Excel and Origin software were used to analyze the experimental data. Data were analyzed using exploratory data analysis by SPSS software (version 15.0, SPSS Inc.). A correlation matrix was generated by Pearson’s correlation coefficients.

Results

Fitting curves of the relationship between C, R, Z, and F. The linear relationships between C and F of I. pseudacorus (Fig. 3A) and I. japonica (Supplemental Fig. 1) were fitted using Sigmaplot software. Linear curves of the relationship between the C and F of I. pseudacorus (Fig. 3A) and I. japonica (Supplemental Fig. 1A) were fitted through Sigmaplot software. However, the values of R and Z in I. pseudacorus (Fig. 3B and C) and I. japonica (Supplemental Fig. 1B and C) logarithmically decreased as the values of F increased.

Fig. 3.
Fig. 3.

Fitting curves of the relationships among capacitance (C), resistance (R), impedance (Z), and gripping force (F) of I. pseudacorus under different inorganic nitrogen sources. (A) The relationship between the physiological C and F of I. pseudacorus. (B) The relationship between the physiological R and F of I. pseudacorus. (C) The relationship between the physiological Z and F of I. pseudacorus.

Citation: HortScience 57, 6; 10.21273/HORTSCI16510-22

Cellular metabolic energy under different inorganic nitrogen sources.

The values of cellular metabolic energy (GB) of I. pseudacorus and I. japonica were calculated according to Eq. [23]. As shown in Fig. 4A and B, the GB value of I. japonica at ja-0 was higher than that of I. pseudacorus at ps-0. The GB of I. japonica became 1 to 1.5 times higher than that of I. pseudacorus at each treatment level on the 10th day. The GB values of I. pseudacorus and I. japonica increased as the NH4+ concentration increased. However, a significant difference between the values of GB in I. pseudacorus at ps-4 and those in I. japonica at ja-4 was observed.

Fig. 4.
Fig. 4.

Effects of different inorganic nitrogen sources on the cellular metabolic energy of I. pseudacorus and I. japonica on the 10th day. ps-0 and ja-0 are the cellular metabolic energies of I. pseudacorus and I. japonica before the treatment, respectively. The cellular metabolic energy of (A) I. pseudacorus and (B) I. japonica on the 10th day. Different letters appear above the error bars when subsequent values differ significantly at the 5% level (P < 0.05).

Citation: HortScience 57, 6; 10.21273/HORTSCI16510-22

There was no significant difference between the values of GB in I. pseudacorus at ps-0 and ps-2 (Fig. 4A). The GB value of I. pseudacorus at the ps-1 level was the lowest and that at the ps-6 level was the highest (Fig. 4A). The GB values of I. pseudacorus clearly increased at the ps-3 and ps-4 levels compared with the ps-2 or ps-1 level. However, the GB values of I. pseudacorus at the ps-3 and ps-4 levels showed no significant difference. The GB value of I. pseudacorus at ps-5 was lower than that at ps-6 but higher than that at the ps-3 and ps-4 levels.

There was no significant difference between the GB values of I. japonica at the ja-0 and ja-2 levels (Fig. 4B). The GB value of I. japonica at the ja-1 level was ≈120 J, which was the lowest, and the highest GB value of I. japonica was observed at the ja-6 level. The GB values of I. japonica increased with increasing ammonium nitrogen between the levels ranging from ja-1 to ja-6 (Fig. 4B). However, the GB values of I. japonica at the ja-4 and ja-5 levels exhibited no significant difference on the 10th day.

Effects of different nitrogen sources on growth indices.

The leaf fresh weights of I. pseudacorus at the ps-3 and ps-2 levels were significantly higher than other levels on the 10th day (Table 2). The leaf fresh weights of I. pseudacorus at the ps-0, ps-4, ps-5, and ps-6 levels showed no significant difference but were clearly lower than those at the ps-1, ps-2, and ps-3 levels on the 10th day. The root fresh weight of I. pseudacorus on the 10th day increased significantly compared with the ps-0 level, but there was no significant difference between the levels ranging from ps-1 to ps-6. The highest values of leaf and root dry weight of I. pseudacorus were all observed at the ps-2 and ps-3 levels. The values of leaf dry weight and root dry weight showed no significant difference between the levels ranging from ps-4 to ps-6. The lowest value of height of I. pseudacorus was observed at the ps-0 level, and the highest value appeared at the ps-2 and ps-3 levels. The height of I. pseudacorus increased between the levels ranging from ps-0 to ps-3 but decreased between the levels ranging from ps-3 to ps-6.

Table 2.

Effects of different inorganic nitrogen sources on the growth indices of I. pseudacorus and I. japonica.
Table 2.

There was no significant difference between the values of the leaf fresh and dry weight of I. japonica at ja-1, ja-2, and ja-3 (Table 2). However, these values were higher than those at other levels, and the lowest values of leaf fresh and dry weight were all observed at the ja-0 level. A higher value of root fresh and dry weight of I. japonica was associated with increasing ammonium concentration between the levels ranging from ja-1 to ja-3. The root fresh and dry weight of I. japonica decreased between the levels ranging from ja-4 to ja-6. Higher values of plant height of I. japonica were associated with increasing ammonium concentration between the levels ranging from ja-1 to ja-3. The values of plant height at the ja-4, ja-5, and ja-6 levels showed no significant difference.

Kinetic parameters for NH4+, NO3–, and PO4– uptake in I. pseudacorus.

Fitting curves of the relationship between ion concentration and absorption time (h) in I. pseudacorus are shown in Fig. 5. The correlation coefficients (R2) of the fitting equations for I. pseudacorus were 0.93 to 0.99. The kinetic parameters Km and Vmax for NH4+, NO3–, and PO4– uptake were calculated according to Eq. [25] and are shown in Table 3.

Fig. 5.
Fig. 5.

Fitting curves of the relationship between concentrations of NH4+, NO3–, and PO4– and the absorption time in I. pseudacorus. (A) Fitting curves of the relationship between the concentrations of NH4+ and the absorption time in I. pseudacorus. (B) Fitting curves of the relationship between the concentrations of NO3– and the absorption time in I. pseudacorus. (C) Fitting curves of the relationship between the concentrations of PO4– and the absorption time in I. pseudacorus.

Citation: HortScience 57, 6; 10.21273/HORTSCI16510-22

Table 3.

Kinetic parameters for NH4+, NO3–, and PO4– uptake in I. pseudacorus.
Table 3.

As shown in Table 3, the Km for NO3– uptake in I. pseudacorus at the ps-1 and ps-2 levels was significantly higher than that at the ps-3, ps-4, and ps-5 levels and the lowest Km for NO3– uptake in I. pseudacorus at the ps-5 level. The Km for NO3– uptake in I. pseudacorus exhibited no significant differences at the ps-1 and ps-2 and the ps-3 and ps-4 levels. The value of Vmax for NO3– uptake in I. pseudacorus at ps-1 was the highest and then decreased with increasing ammonium concentration between the levels ranging from ps-1 to ps-5.

The Vmax for NH4+ uptake in I. pseudacorus at the ps-2 level was the lowest and then increased with increasing ammonium concentration between the levels ranging from ps-2 to ps-6 (Table 3). The Km for NH4+ uptake in I. pseudacorus at the ps-6 level was the highest. The Km for NH4+ uptake in I. pseudacorus at the ps-4 level was significantly higher than those at the ps-3 and ps-2 levels. However, the Km for NH4+ uptake in I. pseudacorus at the ps-2 level exhibited no significant differences from that at the ps-3 level.

The higher values of Vmax for PO4– uptake in I. pseudacorus at the ps-3, ps-4, and ps-5 levels compared with those at the ps-1, ps-2, and ps-6 levels are shown in Table 3. There was no significant difference between the values of Vmax for PO4– uptake in I. pseudacorus at levels ranging from ps-3 to ps-5. The value of Vmax for PO4– uptake in I. pseudacorus at the ps-2 level was clearly lower than those at the ps-3, ps-4, and ps-5 levels. The values of Vmax for PO4– uptake in I. pseudacorus at the ps-1 and ps-6 levels were lowest. The values of Vmax for PO4– uptake in I. pseudacorus was no significant difference between the values at the ps-1 and ps-6 levels. The values of Km for PO4– uptake in I. pseudacorus at the ps-3 and ps-6 levels were lower than those at other levels, and there was no significant difference between the values at these levels (ps-1, ps-2, ps-4, and ps-5).

Kinetic parameters for NH4+, NO3–, and PO4– uptake in I. japonica.

Lower values of Vmax for NO3– uptake in I. japonica were associated with different inorganic nitrogen sources between the levels ranging from ja-1 to ja-5 (Table 4). However, the values of Vmax for NO3– uptake in I. japonica at the ja-2 and ja-3 levels showed no significant differences. The value of Km for NO3– uptake in I. japonica clearly decreased as inorganic nitrogen sources changed from ja-1 to ja-5.

Table 4.

Kinetic parameters for NH4+, NO3–, and PO4– uptake in I. japonica.
Table 4.

The value of Vmax for NH4+ uptake in I. japonica at the ja-2 level was the lowest and that at the ja-6 level was the highest (Table 4). The values of Vmax for NH4+ uptake (I. japonica) at the ja-4 and ja-5 levels were lower than those at ja-6 and showed no significant difference at the ja-4 and ja-5 levels, whereas the Vmax for NH4+ uptake in I. japonica at the ja-3 level remained relatively low. The Km values for NH4+ uptake in I. japonica at the ja-6 level were the highest, and the values increased with increasing NH4+ concentration between the levels ranging from ja-2 to ja-6.

The lowest value of Vmax for PO4– uptake in I. japonica was observed at the ja-1 and ja-4 levels (Table 4). The value of Vmax for PO4– uptake (I. japonica) at the ja-2 level showed no significant difference from those at the ja-5 and ja-6 levels but was clearly lower than that at the ja-3 level. The Km for PO4– uptake in I. japonica at the ja-1 level was the lowest and increased with increasing ammonium nitrogen between the levels ranging from ja-4 to ja-6. However, the values of Km for PO4– uptake (I. japonica) at the ja-2, ja-3, and ja-4 levels exhibited no significant difference.

Correlation of parameters.

The Pearson correlation coefficients for the relationship of ps-GB, Vmax, and Km for NH4+, NO3–, and PO4– uptake in I. pseudacorus are shown in Table 5. ps-GB had a significant positive correlation with PO4–-Km, NH4+-Vmax, and NH4+-Km and a significant negative correlation with NO3–-Vmax and NO3–-Km. However, ps-GB exhibited no significant correlation with PO4–-Vmax. PO4–-Km was significantly correlated with NH4+-Vmax, NH4+-Km, NO3–-Vmax, and NO3–-Km. PO4–-Vmax exhibited no significant correlation with NH4+-Vmax, NH4+-Km, NO3–-Vmax, and NO3–-Km.

Table 5.

Correlation analysis of the cell metabolic energy and kinetic parameters for NH4+, NO3–, and PO4– uptake in I. pseudocorus.
Table 5.

Table 6 shows that there was a good correlation between ja-GB and the kinetic parameters for NH4+, NO3–, and PO4– uptake in I. japonica, that is, Vmax and Km. ja-GB had a significant positive correlation with PO4–-Km, NH4+-Vmax, and NH4+-Km and a significant negative correlation with NO3–-Vmax and NO3–-Km. However, ja-GB exhibited no significant correlation with PO4–-Vmax. PO4–-Km was significantly correlated with NH4+-Vmax, NH4+-Km, NO3–-Vmax, and NO3–-Km. PO4–-Vmax exhibited no significant correlation with NH4+-Vmax, NH4+-Km, NO3–-Vmax, and NO3–-Km.

Table 6.

Correlation analysis of the cell metabolic energy and kinetic parameters for NH4+, NO3–, and PO4– uptake in I. japonica.
Table 6.

Net photosynthetic rate under different inorganic nitrogen sources.

As shown in Fig. 6A and B, the PN of I. pseudacorus was higher than that of I. japonica at same treatment level. However, the PN of I. pseudacorus at the ja-0, ja-1, and ja-2 levels showed no significant differences. The PN of I. pseudacorus at the ps-3 higher than those at other treatments. The PN of I. pseudacorus at ps-4 to ps-6 were lowest those at the ps-3.

Fig. 6.
Fig. 6.

Effects of different nitrogen sources on the net photosynthetic rate (PN) of I. japonica and I. pseudacorus. a, b, c, d, and e = the mean ± sd and significant differences at the 5% level of I. pseudacorus. A, B, C, and D = the mean ± sd and significant differences at the 5% level of I. japonica.

Citation: HortScience 57, 6; 10.21273/HORTSCI16510-22

The PN of I. japonica at the ps-3 higher than that of other treatments. The PN of I. japonica from ja-4 to ja-6 was lower than the ja-0, ja-1, ja-2, and ja-3. However, the PN of I. japonica at the ja-0, ja-1, and ja-2 levels showed no significant differences.

Discussion

The assimilation and catabolism processes include hydrogen exchange, assimilation, and utilization of inorganic matter, synthesis, and transformation of organic matter and energy, physiological processes, and other biochemical processes (Shu et al., 2016). The activities of those processes can be directly reflected by the cellular metabolic energy in plants (Vanhercke et al., 2014). First, in this study, the cellular metabolic energy stored in I. pseudacorus and I. japonica plants both increased with increasing ammonium concentration (Fig. 4). Nitrogen metabolism, which is an important part of assimilation and catabolism in plants, is closely related to metabolic energy (Wang and Lu, 2020). Compared with the nitrogen metabolism of NH4, that of NO3– requires more energy in the processes of nitrogen metabolism (Guo et al., 2007; Konnerup et al., 2010). The cellular metabolic energy stored in plants is affected by the energy consumption of the nitrogen metabolism of NH4+ and NO3–. When the concentration of the total nitrogen is same, the increase of NH4+ concentration can increase the cellular metabolic energy stored in I. pseudacorus and I. japonica. Second, the cellular metabolic energy stored in I. pseudacorus plants at each level was lower than that of I. japonica (Fig. 4). It indicated that the purification rate of I. japonica was relatively lower compared with I. pseudacorus (Yuan et al., 2018). In other words, I. pseudacorus and I. japonica showed different demands for nitrogen during growth and development (Colmer and Bloom, 1998). The removal of ions could be represented by Km and Vmax (Zhu et al., 2020). A low value of Km and a high value of Vmax indicate a high removal efficiency of ions from wastewater (Zhu et al., 2020). The results shown that the Vmax for NO3– and NH4+ uptake by I. pseudacorus was 1.5 to 2 times higher than that by I. japonica (Tables 3 and 4), which demonstrated that the removal of NO3– and NH4+ by I. pseudacorus was higher than that by I. japonica. Correlation analysis showed that the cellular metabolic energy stored in plants was correlated with the kinetic parameters of NO3– and NH4+ absorption (Tables 5 and 6). The results inferred that the strong removal of NO3– and NH4+ had consumed more energy for nitrogen metabolism. The cellular metabolic energy stored in the I. pseudacorus had reduced.

Third, there was a turning point at the ps-3 and ps-4 levels for the cellular metabolic energy of I. pseudacorus (Fig. 4A). However, that of I. japonica was observed at the ja-4 and ja-5 levels (Fig. 4B). The reasons for this phenomenon were as follows: first, the cellular metabolic energy could affect the phosphate (Guo et al., 2006). The phosphorus increased the activities of NR and glutamine systhetase (GS) in Flag leaves of wheat (Wang et al., 2006). During the nitrogen metabolism, some key enzymes, e.g., NR and GS, participate in these processes (Xu and Zhou, 2004). The results showed that the cellular metabolic energy of I. japonica and I. pseudacorus was positively correlated with the Km values for PO4– uptake (Tables 5 and 6). The Km values for PO4– uptake in I. pseudacorus at the ps-4 level was significantly higher than that at the ps-3 treatment, which indicated that the phosphorus in I. pseudacorus at the ps-4 level was lower than that at the ps-3 treatment level. Phosphorus deficiency could decrease the activities of GS in I. pseudacorus at the ps-4 level. The activities of NR and GS could affect the assimilation process of NO3– and NH4+ (Xu and Zhou, 2004). The cellular metabolic energy stored in I. pseudacorus at the ps-4 level had reduced. Second, nitrate nitrogen would promote photosynthetic carbon assimilation enzymes and chlorophyll synthesis in I. pseudacorus and I. japonica (Fig. 6). Researchers have reported that amount of nitrate nitrogen during the cultivation of Hemarthria altissima was beneficial for the photosynthetic carbon assimilation and chlorophyll synthesis, further the improvement of photosynthesis ability and the promotion of its growth and development (Guo et al., 2007; Wei et al., 2020). The net photosynthetic rates of I. pseudacorus at the ps-3 level were significantly higher than those at the ps-4 level (Fig. 6), which indicated that the solar energy captured by I. pseudacorus at the ps-3 level was greater than that at the ps-4 level. The results showed that amount of nitrate was beneficial to plant growth of I. pseudacorus and I. japonica (Table 2). Researchers have reported that high concentration of ammonium has an apparent toxic effect on the photosynthetic rates in plants (Cumming and Weinstein, 1990). A high concentration of ammonium could decrease the PN of I. japonica at ja-5 and ja-6 levels and those at ja-5 and ja-6 levels. Studies have shown that excessive application of NH4+ inhibited the absorption of potassium (K+) and calcium ions (Ca2+) in plants, resulting in various metabolic disorders and ammonia poisoning in plants (Jampeetong et al., 2012; Li et al., 2006; Wang and Luo, 2009).

A low value of Km and a high value of Vmax indicate a high removal efficiency of ions from wastewater (Zhu et al., 2020). The values of Vmax for NO3–, NH4+, and PO4– uptake in I. pseudacorus were higher than those in I. japonica at each treatment level (Tables 3 and 4). The results shown that removal of nitrogen and phosphorus for I. pseudacorus higher than I. japonica. Studies have shown that HATS for NO3– will be activated when the value of Km is lower than 1 mmol·L−1, whereas LATS will be activated when the value of Km is higher than 1 mmol·L−1 (Krapp et al., 2014). The high-affinity NO3– uptake system would be activated in ps-5 and ja-5 (Tables 3 and 4). The results reflected that NO3– was transported through LATS at the other levels. It is dominated by HATS when the concentration of NH4+ is lower than 1 mmol·L−1 (Kronzucker et al., 1996). However, the LATS will become dominant when the concentration of NH4+ is ≥1 mmol·L−1 (Kronzucker et al., 1996). The results shown that the high-affinity NH4+ uptake system was activated in the intracellular membranes at ps-2, ps-3, ja-2, and ja-3 levels (Tables 3 and 4), but NH4+ was transported through the LATS at ps-4, ps-5, ps-6, ja-4, ja-5, and ja-6 levels. When suffering from phosphorus deficiency, plants absorb phosphorus through HATS, and the unit of Km is always µmol·L−1 (Mei et al., 2012). LATS prevails in plants, and the unit of Km is mmol·L−1 (Muchhal et al., 1996; Nielsen and Barber, 1978). The PO4– was transported through the HATS at ps-6 and ja-1 levels (Tables 3 and 4). The low-affinity PO4– uptake system was activated at other levels.

The absorption and assimilation of phosphate are influenced by inorganic nitrogen in plants (Guo et al., 2006). First, the degree of polarization and structure of the cell membrane are changed by inorganic nitrogen resources (Ai et al., 2009; Zhou et al., 1998). Second, the proteins of phosphate transporters located on the cell membrane are closely related to the nitrogen inside and outside the plant cells (Versaw and Garcia, 2017; Xu et al., 2018). The active transport of nitrogen dominated by the binding proteins is equal to the absorption of nitrogen by plants (Versaw and Garcia, 2017; Xu et al., 2018).

Studies have shown that the NO3– or NH4+ could have similar affinity and absorption rate, and the most suitable environment for plant could not be distinguished when the concentration of ammonium or nitrate have no significant difference between treatments (Wang et al., 2016). In conclusion, high concentration of ammonia (ps-4, ps-5, ps-6 and ja-4, ja-5, ja-6) was not conducive to I. pseudacorus and I. japonica. When there was no significant difference in the concentration of ammonium or nitrate between treatments, the higher value of cellular metabolic energy indicated the better status of plant growth. The results showed that the NO3–:NH4+ = 27:3 treatment level was more suitable for I. pseudacorus and I. japonica compared with other treatment levels.

Conclusion

Overall, the increase of NH4+ concentration could increase the cellular metabolic energy stored in I. pseudocorus and I. japonica when the concentration of total nitrogen was the same. The results indicate that the cellular metabolic energy stored in I. pseudacorus was lower than those in I. japonica, which made the removal for NO3– and NH4+ in I. pseudacorus higher than those in I. japonica. The cellular metabolic energy stored in I. pseudacorus and I. japonica could also affect the phosphate and photosynthetic rate. The results showed that the removal for NO3–, NH4+, and H2PO4– in I. pseudacorus were higher than those in I. japonica at each treatment level. These results demonstrate that the NO3–:NH4+ = 27:3 treatment level was more suitable for I. pseudacorus and I. japonica compared with other treatment levels. This indicates that the higher value of cellular metabolic energy was suitable for plant growth when there was no significant difference in the concentration of ammonium or nitrate between treatments. The results can provide a simple and rapid solution for removal of nitrogen by the determination of cellular metabolic energy.

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Supplemental Fig. 1.
Supplemental Fig. 1.

Fitting curves of the relationships among capacitance (C), resistance (R), impedance (Z), and gripping force (F) of I. japonica under different inorganic nitrogen sources. (A) The relationship between the physiological C and F of I. japonica. (B) The relationship between the physiological R and F of I. japonica. (C) The relationship between the physiological Z and F of I. japonica.

Citation: HortScience 57, 6; 10.21273/HORTSCI16510-22
Received:
26 Jan 2022
|
Accepted:
15 Mar 2022
|
Published online:
16 May 2022
|
Published-print:
01 Jun 2022
Received:
26 Jan 2022
|
Accepted:
15 Mar 2022
|
Published online:
16 May 2022
|
Published-print:
01 Jun 2022
  • Fig. 1.
    View in gallery
    Fig. 1.

    Relationship between plant metabolism and energy consumption. Ea represents the plant fixed solar energy, E represents the stable chemical energy in plants, Eb represents the total energy consumed by nitrogen metabolism, GB represents the cellular metabolic energy, and Ed represents the energy consumption by all the other metabolic processes.

  • Fig. 2.
    View in gallery
    Fig. 2.

    The parallel-plate capacitor.

  • Fig. 3.
    View in gallery
    Fig. 3.

    Fitting curves of the relationships among capacitance (C), resistance (R), impedance (Z), and gripping force (F) of I. pseudacorus under different inorganic nitrogen sources. (A) The relationship between the physiological C and F of I. pseudacorus. (B) The relationship between the physiological R and F of I. pseudacorus. (C) The relationship between the physiological Z and F of I. pseudacorus.

  • Fig. 4.
    View in gallery
    Fig. 4.

    Effects of different inorganic nitrogen sources on the cellular metabolic energy of I. pseudacorus and I. japonica on the 10th day. ps-0 and ja-0 are the cellular metabolic energies of I. pseudacorus and I. japonica before the treatment, respectively. The cellular metabolic energy of (A) I. pseudacorus and (B) I. japonica on the 10th day. Different letters appear above the error bars when subsequent values differ significantly at the 5% level (P < 0.05).

  • Fig. 5.
    View in gallery
    Fig. 5.

    Fitting curves of the relationship between concentrations of NH4+, NO3–, and PO4– and the absorption time in I. pseudacorus. (A) Fitting curves of the relationship between the concentrations of NH4+ and the absorption time in I. pseudacorus. (B) Fitting curves of the relationship between the concentrations of NO3– and the absorption time in I. pseudacorus. (C) Fitting curves of the relationship between the concentrations of PO4– and the absorption time in I. pseudacorus.

  • Fig. 6.
    View in gallery
    Fig. 6.

    Effects of different nitrogen sources on the net photosynthetic rate (PN) of I. japonica and I. pseudacorus. a, b, c, d, and e = the mean ± sd and significant differences at the 5% level of I. pseudacorus. A, B, C, and D = the mean ± sd and significant differences at the 5% level of I. japonica.

  • Supplemental Fig. 1.
    View in gallery
    Supplemental Fig. 1.

    Fitting curves of the relationships among capacitance (C), resistance (R), impedance (Z), and gripping force (F) of I. japonica under different inorganic nitrogen sources. (A) The relationship between the physiological C and F of I. japonica. (B) The relationship between the physiological R and F of I. japonica. (C) The relationship between the physiological Z and F of I. japonica.

Fig. 1.

Relationship between plant metabolism and energy consumption. Ea represents the plant fixed solar energy, E represents the stable chemical energy in plants, Eb represents the total energy consumed by nitrogen metabolism, GB represents the cellular metabolic energy, and Ed represents the energy consumption by all the other metabolic processes.
Fig. 2.

The parallel-plate capacitor.
Fig. 3.

Fitting curves of the relationships among capacitance (C), resistance (R), impedance (Z), and gripping force (F) of I. pseudacorus under different inorganic nitrogen sources. (A) The relationship between the physiological C and F of I. pseudacorus. (B) The relationship between the physiological R and F of I. pseudacorus. (C) The relationship between the physiological Z and F of I. pseudacorus.
Fig. 4.

Effects of different inorganic nitrogen sources on the cellular metabolic energy of I. pseudacorus and I. japonica on the 10th day. ps-0 and ja-0 are the cellular metabolic energies of I. pseudacorus and I. japonica before the treatment, respectively. The cellular metabolic energy of (A) I. pseudacorus and (B) I. japonica on the 10th day. Different letters appear above the error bars when subsequent values differ significantly at the 5% level (P < 0.05).
Fig. 5.

Fitting curves of the relationship between concentrations of NH4+, NO3–, and PO4– and the absorption time in I. pseudacorus. (A) Fitting curves of the relationship between the concentrations of NH4+ and the absorption time in I. pseudacorus. (B) Fitting curves of the relationship between the concentrations of NO3– and the absorption time in I. pseudacorus. (C) Fitting curves of the relationship between the concentrations of PO4– and the absorption time in I. pseudacorus.
Fig. 6.

Effects of different nitrogen sources on the net photosynthetic rate (PN) of I. japonica and I. pseudacorus. a, b, c, d, and e = the mean ± sd and significant differences at the 5% level of I. pseudacorus. A, B, C, and D = the mean ± sd and significant differences at the 5% level of I. japonica.
Supplemental Fig. 1.

Fitting curves of the relationships among capacitance (C), resistance (R), impedance (Z), and gripping force (F) of I. japonica under different inorganic nitrogen sources. (A) The relationship between the physiological C and F of I. japonica. (B) The relationship between the physiological R and F of I. japonica. (C) The relationship between the physiological Z and F of I. japonica.

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Rongrong Duan Key Laboratory of Modern Agricultural Equipment and Technology of Ministry of Education, School of Agricultural Engineering, Jiangsu University, Zhenjiang 212013, China

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Deke Xing Key Laboratory of Modern Agricultural Equipment and Technology of Ministry of Education, School of Agricultural Engineering, Jiangsu University, Zhenjiang 212013, China

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Tian Chen Key Laboratory of Modern Agricultural Equipment and Technology of Ministry of Education, School of Agricultural Engineering, Jiangsu University, Zhenjiang 212013, China

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Yanyou Wu State Key Laboratory of Environmental Geochemistry, Institute of Geochemistry, Chinese Academy of Sciences, Guiyang 550081, China

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Contributor Notes

This work was funded the Support Plan Projects of Science and Technology Department of Guizhou Province [No. (2021) YB453], the National Natural Science Foundation of China (No. U1612441-2), and Priority Academic Program Development (PAPD) of Jiangsu Higher Education Institutions for supporting this research.

Y.W. and D.X. are the corresponding authors. E-mail: wuyanyou@mail.gyig.ac.cn or xingdeke@ujs.edu.cn.

Received:
26 Jan 2022
|
Accepted:
15 Mar 2022
|
Published online:
16 May 2022
|
Published-print:
01 Jun 2022
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