Next Article in Journal
Fermented Apple Pomace Improves Plasma Biochemical and Antioxidant Indicators and Fecal Microbiota of Weaned Pigs
Previous Article in Journal
Estimation of Technical, Allocative, and Economic Efficiencies for Smallholder Broiler Producers in South Africa
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Agriculture
Volume 12
Issue 10
10.3390/agriculture12101602
agriculture-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Differences in Nitrogen and Phosphorus Removal under Different Temperatures in Oenanthe javanica Cultivars

by
Linhe Sun
1,2,†,
Wei Wang
1,2,†,
Fengjun Liu
3,
Jixiang Liu
1,2,
Fengfeng Du
1,2,
Xiaojing Liu
1,2,
Yajun Chang
1,2 and
Dongrui Yao
1,2,*
1
Jiangsu Key Laboratory for the Research and Utilization of Plant Resources, Institute of Botany, Jiangsu Province and Chinese Academy of Sciences (Nanjing Botanical Garden Memorial Sun Yat-Sen), Nanjing 210014, China
2
Jiangsu Engineering Research Center of Aquatic Plant Resources and Water Environment Remediation, Institute of Botany, Jiangsu Province and Chinese Academy of Sciences (Nanjing Botanical Garden Memorial Sun Yat-Sen), Nanjing 210014, China
3
Suzhou Academy of Agricultural Sciences, Suzhou 215000, China
*
Author to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Agriculture 2022, 12(10), 1602; https://doi.org/10.3390/agriculture12101602
Submission received: 24 August 2022 / Revised: 30 September 2022 / Accepted: 30 September 2022 / Published: 3 October 2022
(This article belongs to the Topic Innovation and Solution for Sustainable Agriculture)
Browse Figures
Versions Notes

Abstract

:
Plant selection plays a critical role in phytoremediation. However, previous research has focused on comparing different plant species but has ignored different cultivars. Here, a laboratory experiment was performed to analyze the nitrogen (N) and phosphorus (P) removal performance of different cultivars of Oenanthe javanica, which are widely employed for phytoremediation in China. Seven cultivars were planted on simulated livestock wastewater with high N and P content prepared with compounds for 22 days in two artificial climate chambers with different temperatures. N and P contents were monitored to estimate the nutrient removal performance of the cultivars. ‘Suzhou Yuanye’ had the highest N removal ability at room temperature (45.33 ± 1.92%) and under cold stress (39.63 ± 2.15%) in 22 days, and it could also remove P effectively (99.32 ± 0.33% at room temperature and 77.50 ± 0.08% under cold stress). ‘Yixing Yuanye’ performed the best in P removal (97.90 ± 2.89% at room temperature and 99.57 ± 0.61% under cold stress). ‘Liyang Baiqin’ performed well in N removal only at room temperature (44.30 ± 1.03%). ‘Suqian Jianye’ had low removal efficiencies for both N and P. From the biomass and N content, we could conclude that the high N removal efficiency of ‘Suzhou Yuanye’ is due to high N assimilation of the plant. However, ‘Yixing Yuanye’ did not show higher P assimilation ability than other cultivars. Taken together, the selection of cultivars is important for phytoremediation projects using O. javanica, and ‘Suzhou Yuanye’ is much more suitable for phytoremediation than other cultivars.

1. Introduction

As a valuable resource, global surface freshwater availability is facing significant pressure due to increasing demand, resource reduction, and increasing pollution, driven by enormous population and economic growth [1]. Freshwater can easily be contaminated, but difficult and expensive to restore [2]. Aquatic phytoremediation is a nature-based solution that facilitates the removal of contaminants in water using the ability of macrophytes to take up, sequester, and degrade pollutants [3,4]. This approach is efficient, spatially adaptable, multi-targeted, environmentally friendly, energy-saving, and inexpensive [5,6,7]. Plant selection has a key role in phytoremediation due to the different growth features of different plant species. Thus, we need to consider not only the phytoremediation features, such as high tolerance, high contaminate removal efficiency, fast growth, high biomass, extensive rhizosphere, and easy management, but also the biomass utilization value [8,9,10]. Thus, economic plants with high purification performance, which is beneficial to the reuse of plant biomass and ensures the sustainable utilization of the nutrients in the wastewater, have become preferable for surface water phytoremediation [4,11].
Economic plants, such as ornamental plants and vegetables, often have different cultivars due to breeders’ work. Different cultivars of one plant species can have different features, growth patterns, and tolerances, which may affect the phytoremediation performance. Iris sp. and Canna sp. are widely employed in constructed wetlands (CWs) for wastewater treatment [12]. However, not all Canna cultivars are suitable as plants in wetlands. Furthermore, not only flower type or leaf color, but also waterlogging tolerance can be significantly different between cultivars. For example, the waterlogging injury index of Canna ‘RLRF’ was the highest in 11 cultivars and twice higher than that of Canna ‘Mohong’, indicating that Canna ‘RLRF’ may not be suitable for freshwater phytoremediation [13]. In addition, different Iris cultivars can show significant differences in plant height, leaf length, and flower shoot length, leading to biomass differences, which is the key feature affecting phytoremediation performance [14]. Salinity tolerance, which affects the phytoremediation application, of I. germanica cultivars is also diverse [15]. However, research on plant selection and performance has focused only on the plant species and has ignored cultivar differences [3,7,8].
As a traditional aquatic vegetable species, Oenanthe javanica (Blume) DC is an ideal plant for wastewater phytoremediation due to its economic value, rapid growth in polluted water, high contaminant removal efficiency, allelopathy, and cold tolerance [3,16,17]. O. javanica is widely cultivated in East Asia, supported by decades of cultivars [18,19]. However, different studies have reported different removal abilities of O. javanica [17,20,21]. Different experimental set-ups may be the main reason for the different performances; however, none of the reports employed O. javanica cultivars, which should not be ignored as there are differences between cultivars. Furthermore, cultivars cannot be distinguished easily by the plant height, stem length, branch number, or leaf color [22].
To further study the purification performance of different O. javanica cultivars, a simulation experiment was performed to evaluate the removal abilities of nitrogen (N) and phosphorus (P) from simulated livestock wastewater of seven different O. javanica cultivars (‘Meinan Shuiqin’, ‘Yuqi Baiqin’, ‘Jiangyin Baiqin’, ‘Liyang Baiqin’, ‘Yixing Yuanye’, ‘Suzhou Yuanye’, and ‘Suqian Jianye’) both at room temperature and under cold stress. The seven cultivars were bred and cultivated in Jiangsu, which is one of the main provinces cultivating O. javanica, and they are common vegetables available at most markets. Here, we hypothesize that: (a) different O. javanica cultivars have significantly different removal abilities of N and P; (b) different cultivars have different responses against cold stress; and (c) the removal ability is correlated with N and P accumulation in plants. This study provides new insights on the selection of plants for phytoremediation, emphasizes the importance of cultivar differences, and proposes a plant configuration for wastewater treatment using economic plants.

2. Materials and Methods

2.1. Experimental Design and Set-Up

Seven common O. javanica cultivars from Jiangsu Province bred or collected by the Suzhou Academy of Agricultural Sciences were used for this study (Figure 1). The cultivars were planted in pots with soil for reproduction in a greenhouse at the Institute of Botany of Jiangsu Province and the Chinese Academy of Sciences. Juvenile plant samples with similar biomass from each cultivar were collected, washed, and placed in aerated tap water for 1 week and then transferred to 500-mL beakers (two individuals for each beaker with a total biomass of 10–12 g) with simulated livestock wastewater for 22 days. The formula of the simulated wastewater is listed in Table 1 and is reflective of the data presented in [8]. The control (CK) contained simulated wastewater without plants. The beakers were placed into two artificial climate chambers (DGZL-P1000-E3, Liance Co., Nanjing, China) with a light intensity of 24,000 Lx for 14 h per day and a relative humidity of 65%. One chamber was set at 25 °C to simulate a suitable growth environment (room temperature), and the other one was set at 8 °C in light and 4 °C in dark to simulate the winter season in Jiangsu Province (subtropical monsoon climate) and to induce cold stress. Three replicates were established for each treatment of each cultivar (Table 2).

2.2. Sampling and Determination Methods

In brief, 10-mL water samples were collected on day 1, day 3, day 5, day 7, day 12, day 17, and day 22 at 10:00 a.m. The samples were stored at 4 °C and analyzed within 48 h. To estimate the pollutant removal efficiency of each cultivar, TN, NH4+-N, and TP were analyzed. The concentrations were analyzed following the methods of a previously published study [11]. TN was determined using alkaline potassium persulfate digestion UV spectrophotometry (HJ636-2012), TP was determined using ammonium molybdate spectrophotometry (GB11893-89), and the NH4+-N concentration was measured using Naismith spectrophotometry with medium-range parameters (HI96715) (HANNA Instruments, Woonsocket, RI, USA). Fresh plant samples were weighed, dried at 65 °C, and re-weighed to determine the dry biomass and moisture content. Dried plant samples were then used to determine the N and P contents in plants following the methods of a previously published study [20]. The N content was determined using the Kjeldahl method after digestion with H2SO4-K2SO4-CuSO4-Se, and the P content was determined using ammonium molybdate spectrophotometry after digestion with H2O2-H2SO4. Water quality parameters (electrical conductivity, pH, temperature, salinity, and dissolved oxygen) were measured in situ using a YSI Pro Plus multi-parameter meter (YSI Inc., Yellow Springs, OH, USA) prior to water sampling.

2.3. Data Analysis

Statistical analysis was performed using SPSS 26.0 software (SPSS Inc., Chicago, IL, USA). One-way analysis of variance (ANOVA) and Tukey HSD test were performed to determine statistically significant differences (p < 0.05). Two-way ANOVA was performed to assess the relationship between temperature and cultivar (p < 0.05). Pearson’s correlation coefficient was calculated for correlation analysis using the data from day 22. Figures were constructed using Origin 2021 software (OriginLab Co., Northampton, MA, USA) and R (R Core Team, Vienna, Austria).

3. Results

3.1. O. javanica Cultivars Could Tolerate More than 400 mg/L NH4+-N Both at Room Temperature and under Cold Stress

The NH4+ content of the simulated wastewater was set to 400 mg/L due to the high NH4+-N content of livestock wastewater, which is harmful to plant growth. All the plants survived after 22 days, suggesting that O. javanica could tolerate more than 400 mg/L NH4+-N. Only ‘Suqian Jianye’ started to wither and perish after 22 days of cold treatment, indicating that cold stress could affect the phenotypes of O. javanica (Figure 2a). The chlorophyll synthesis pathway was inhibited under cold stress, as evidenced by the pale red and red leaf color of the plants (Figure 2a). For most cultivars, cold stress increased the plant height, especially for ‘Jiangyin Baiqin’ and ‘Liyang Baiqin’. ‘Suqian Jianye’ was the only cultivar with a significantly lower plant height under cold stress (Figure 2b). However, a higher plant height did not lead to a higher biomass. After 22 days of growth, the plant biomass of all the cultivars under cold stress increased but showed no significant difference compared with that of day 0. On the other hand, the plant biomass of all the cultivars significantly increased after 22 days of growth at room temperature, except for ‘Yixing Yuanye’ (Figure 2b–d), indicating that cold stress inhibited the growth of O. javanica.
The dry matter content was determined after the experiment. The results indicated that after 22 days of growth only ‘Suqian Jianye’ and ‘Suzhou Yuanye’ showed significantly higher dry matter biomass at room temperature than that under cold stress (Figure 2d). In addition, it was demonstrated that a higher fresh matter did not lead to a higher dry matter, and the moisture content was the major contributor to the high fresh matter of most O. javanica cultivars. Thus, most cultivars did not show significantly different growth patterns under the same temperature. The temperature mainly affected the fresh matter biomass of O. javanica. ‘Suzhou Yuanye’ showed fast growth under both temperature conditions and accumulated the most biomass, which may lead to better nutrient removal efficiency in phytoremediation.

3.2. ‘Suzhou Yuanye’ and ‘Liyang Baiqin’ Showed the Best N Removal Ability at Room Temperature, but Cold Stress Inhibited the N Removal Ability of ‘Liyang Baiqin’

To investigate the TN removal performance of the seven O. javanica cultivars grown in simulated livestock wastewater, the concentrations of TN and NH4+-N in the water were monitored on day 1, day 3, day 5, day 7, day 12, day 17, and day 22 (Figure 3). At room temperature, ‘Suzhou Yuanye’ and ‘Liyang Baiqin’ showed the strongest N removal efficiency. After 22 days of growth, the TN and NH4+ contents in beakers with ‘Suzhou Yuanye’ were 282.71 ± 3.74 mg/L and 265.67 ± 4.19 mg/L, respectively, and the contents in beakers with ‘Liyang Baiqin’ were 278.50 ± 5.14 mg/L and 275.00 ± 2.94 mg/L, respectively. There were no significant differences between the TN contents of the beakers with ‘Suzhou Yuanye’ and ‘Liyang Baiqin’ at room temperature on day 5, day 12, day 17, and day 22. After 22 days, ‘Liyang Baiqin’ removed the most TN with a reduction rate of 44.30 ± 1.03%, which was 1.3 times the reduction rate of ‘Suqian Jianye’ (34.67 ± 1.87%), with a significant difference. The N removal performance at room temperature indicated that the N removal efficiency was significantly different between cultivars, and cultivar differences should be considered before employing O. javanica for livestock wastewater phytoremediation applications. ‘Liyang Baiqin’ and ‘Suzhou Yuanye’ were more suitable for N purification from wastewater than the other cultivars in spring or autumn, which are the optimum growing seasons for O. javanica, while ‘Suqian Jianye’ and ‘Yixing Yuanye’ had the worst N removal efficiency and should be avoided for this purpose.
Under cold stress, ‘Suzhou Yuanye’ showed strong N removal efficiency; however, the removal efficiency of ‘Liyang Baiqin’ was suppressed. After 22 days of growth, TN and NH4+-N contents in the beakers with ‘Suzhou Yuanye’ were 301.87 ± 10.75 mg/L and 281.00 ± 11.00 mg/L, respectively, and the contents in the beaker with ‘Liyang Baiqin’ were 319.16 ± 12.15 mg/L and 292.33 ± 11.15 mg/L, respectively. Thus, ‘Suzhou Yuanye’ is more suitable for N purification from wastewater than ‘Liyang Baiqin’ and can be employed for all-year-round phytoremediation projects. Two-way ANOVA results showed that the cultivar was the main effect that could explain a significant amount of variation in both TN and NH4+-N content (Table 3). The effect of temperature on the N content was limited. There was no interaction between temperature and cultivar on TN or NH4+-N removal.

3.3. ‘Yixing Yuanye’ Had the Best P Removal Ability Both at Room Temperature and under Cold Stress

To investigate the TP purification performance of the seven O. javanica cultivars, the concentration of TP in the simulated wastewater from all the beakers were monitored. The TP concentration decreased rapidly in all the beakers after planting O. javanica (Figure 4). At room temperature, the TP content in all the beakers reached nearly 0 mg/L on day 17, indicating that all the cultivars could remove P in wastewater efficiently. However, the TP content in the beakers with ‘Yuqi Baiqin’ and ‘Liyang Baiqin’ started to increase after 17 days, which may be caused by rotten roots. The TP content reached 1.02 ± 0.65 mg/L in the beaker with ‘Yixing Yuanye’ in 5 days, while the beakers with other cultivars needed approximately 12 days to reach a similar TP content, indicating that ‘Yixing Yuanye’ was more suitable for P purification from wastewater than the other cultivars in spring or autumn. Under cold stress, the TP content decreased much slower than that at room temperature, which may be due to the slow growth of the plants at low temperature. After 22 days of growth, the TP content in the beakers with ‘Jiangyin Baiqin’, ‘Meinan Shuiqin’, ‘Suqian Jianye’, ‘Suzhou Yuanye’, and ‘Yixing Yuanye’ reached less than 5.0 mg/L, with reduction rates higher than 66.7%. There were no significant differences between the reduction rates of the beakers with ‘Jiangyin Baiqin’, ‘Meinan Shuiqin’, ‘Suqian Jianye’, and ‘Suzhou Yuanye’. Only ‘Yixing Yuanye’ showed a significantly stronger removal ability of TP, with a reduction rate of 99.57 ± 0.61%. In addition, ‘Yixing Yuanye’ was more suitable for P purification in winter than the other cultivars, as the cold stress conditions were set to simulate the winter of a subtropical monsoon climate (Jiangsu Province). Two-way ANOVA results showed that both temperature and cultivar could explain a significant amount of variation in the TP content, but there was no interaction between temperature and cultivar on TP removal (Table 4).
Although ‘Yixing Yuanye’ performed the best in terms of P removal ability, the N removal ability of ‘Yixing Yuanye’ was not impressive, which may limit its application in the phytoremediation of livestock wastewater containing massive amounts of N. ‘Suzhou Yuanye’, which showed the highest N reduction rate, also performed well in P removal. The TP content in the beaker with ‘Suzhou Yuanye’ reached 0.07 ± 0.01 mg/L in 12 days at room temperature and reached 3.35 ± 0.67 mg/L in 22 days under cold stress. ‘Jiangyin Baiqin’ performed similarly to ‘Suzhou Yuanye’ in P removal but did not perform well in N removal. Taken together, ‘Suzhou Yuanye’ was suitable for nutrient purification from livestock wastewater at room temperature conditions. In winter, ‘Suzhou Yuanye’ and ‘Yixing Yuanye’ could be employed together to achieve an ideal removal efficiency of both N and P.
‘Yuqi Baiqin’ performed the worst in P removal and did not show better N removal efficiency in both normal and cold conditions, indicating that ‘Yuqi Baiqin’ was not suitable for phytoremediation and should be avoided in CWs or other water purification projects. However, it is difficult to distinguish ‘Yuqi Baiqin’ from other cultivars using the plant traits of different cultivars (Figure 1). Thus, it is important to identify the cultivars before commencing the phytoremediation project using O. javanica as the main plant to ensure a high removal efficiency.

3.4. Correlation Analysis of Plant Biomass, Nutrients Accumulation, Multiple Water Quality Parameters, and Removal Efficiencies

To further investigate the mechanism on the removal efficiency of macronutrients by O. javanica, the TN and TP contents in O. javanica cultivars were determined (Figure 5). At room temperature, there was no significant difference in the TN content among all the cultivars. ‘Suzhou Yuanye’, which showed the highest dry matter biomass, assimilated more N from the water body than the other cultivars. It could be demonstrated that plant uptake may be the main factor affecting the N removal efficiency at room temperature. Cold stress significantly decreased the TN content in all the cultivars, especially ‘Jiangyin Baiqin’, ‘Liyang Baiqin’, and ‘Yuqi Baiqin’. This could be the reason why the N removal rates of all the cultivars under cold stress were much lower. Cold stress affected the N uptake of ‘Suzhou Yuanye’ the most, possibly due to the significantly lower TN content and dry matter biomass. However, ‘Suzhou Yuanye’ still performed well in terms of the N removal efficiency under cold stress, indicating that the rhizosphere microorganisms of ‘Suzhou Yuanye’ play critical roles in N removal under cold stress.
In contrast to N uptake, different O. javanica cultivars showed different P uptake patterns. At room temperature, ‘Suqian Jianye’ showed the highest TP content, while ‘Suzhou Yuanye’ showed the lowest. However, there was no significant difference in the P removal efficiency of the two cultivars. Different cultivars also showed different responses to cold stress in P accumulation. Cold stress increased the P content of ‘Suqian Jianye’, ‘Suzhou Yuanye’, and ‘Yixing Yuanye’, but decreased the P content of ‘Jiangyin Baiqin’. The TP content of ‘Meinan Shuiqin’, ‘Yuqi Baiqin’, and ‘Liyang Baiqin’ was not affected by cold stress. In addition, cold stress decreased the biomass of the plants, and ‘Suqian Jianye’ and ‘Suzhou Yuanye’ under cold stress did not assimilate more P. The lower P assimilation may be one of the reasons for the lower TP removal efficiency under cold stress. ‘Yixing Yuanye’, which performed the best in both normal and cold conditions, did not show the highest TP content or P assimilation among the seven cultivars on day 22.
To further investigate the effects of the water quality parameters on the removal efficiency, several water quality parameters, including electrical conductivity, pH, temperature, salinity, and dissolved oxygen, were measured using a portable meter prior to water sampling (Table S1). The correlation between various water quality parameters and removal efficiencies is presented in Figure 6. Temperature was significantly positively correlated with nutrient removal and fresh weight, indicating that cold stress suppressed plant growth and removal ability. Salinity was significantly negatively correlated with removal efficiency due to the decreasing concentrations of nutrients in the simulated wastewater. The TN removal efficiency was significantly positively correlated with TN bioaccumulation and plant fresh weight, indicating that plant assimilation was one of the primary mechanisms for N removal in the phytoremediation system using O. javanica. Interestingly, TP removal efficiency was not significantly correlated with TP bioaccumulation. In theory, pH can affect N and P forms in solution and may impede or facilitate the bioavailability of these species. The pH of all the water samples decreased after planting O. javanica, indicating that the growth of O. javanica could affect the H+ ion concentration. Significant correlations were found between pH and the other water quality parameters; however, no significant correlations were found between pH and removal efficiency.

4. Discussion

4.1. Ammonia Tolerance of O. javanica Was Important for Livestock Wastewater Phytoremediation

A high ammonia level is a feature of livestock wastewater [23,24]. As an odor-causing substance, ammonia in livestock wastewater not only leads to serious air pollution, but also inhibits both plant and microbe activities, leading to the instability of the wastewater treatment [25,26]. Thus, a high tolerance for NH4+-N is one of the key features to consider when selecting plants for the phytoremediation of livestock wastewater. Furthermore, NH4+-N is a universal abiotic stress for plant growth that can affect virtually every plant species through ammonium toxicity [25]. In this study, all the cultivars could survive for 22 days in the simulated livestock wastewater with high NH4+-N content both at room temperature and under cold stress, indicating that O. javanica was not sensitive to 400 mg/L NH4+-N and suitable for phytoremediation of livestock wastewater. The decreased pH and acidic stress caused by ammonium assimilation were the primary causes of ammonium toxicity in plants [27]. The pH of all the water samples also decreased after planting O. javanica; however, O. javanica did not show ammonium toxicity-related phenomena such as stunted root growth or leaf chlorosis at room temperature, indicating that O. javanica could adapt to acidic water environments, and this could be the primary mechanism for the high-level ammonium tolerance of O. javanica. Under cold stress, the plants showed leaf chlorosis (pale red leaf color), revealing that low temperature can affect the ammonium tolerance of O. javanica. Although suppressed by cold stress, O. javanica could survive and remove the nutrients from the simulated livestock wastewater. Thus, O. javanica has great potential for phytoremediation of livestock wastewater in winter.

4.2. Differences between Cultivars Were One of the Main Reasons for Challenges in Comparing Optimal Plant Accumulator Species

Studies on plant species often vary in the removal efficiency of macronutrients, which makes it challenging to compare optimal plant accumulator species [3]. The mechanism of N and P removal in phytoremediation is complicated by the crosstalk of multiple pathways, namely sedimentation [28,29], direct uptake via the roots [29,30], nitrification–denitrification and plant P uptake by rhizosphere microbes, and interactions between plants and microbes [11,31,32]. The phytoremediation potential of plants is influenced by both plant status and abiotic factors such as temperature, pH, and light. However, few studies have focused on cultivar differences, which may affect the removal efficiency of a plant species due to the uptake ability of macronutrients. Interactions with microbes can also significantly vary among cultivars of one species [33,34]. From this study, different O. javanica cultivars showed significant N and P removal differences on simulated livestock wastewater. For example, at room temperature, the TN reduction rate of ‘Liyang Baiqin’ was 28% higher than that of ‘Suqian Jianye’ in 22 days, and the TP reduction rate of ‘Yixing Yuanye’ was 3 times that of ‘Meinan Shuiqin’ in 5 days. Chen et al. reported that there was no significant difference in the N removal efficiency between Oryza sativa and Lactuca sativa in 13 days [30], while Sun et al. reported that there was no significant difference in the TP removal efficiency of high concentrate simulated water of Lythrum salicaria, Sagittatia trifolia, and Typha prientalis in 7 days [11]. Thus, the removal efficiency differences on macronutrients among different species may be less significant than the differences among cultivars, indicating that ignoring cultivar differences may be a major loophole in studies on plant selection for phytoremediation.

4.3. Convenient Methods to Distinguish Different Cultivars Were Important to Phytoremediation Using O. javanica

From the results, we demonstrated that ‘Suzhou Yuanye’ was suitable for the purification of N and P both at room temperature and under cold stress from wastewater, especially for livestock wastewater with high NH4+-N content. This cultivar removed 45.33 ± 1.92% of TN and 99.32 ± 0.33% of TP at room temperature and removed 39.63 ± 2.15% of TN and 74.50 ± 0.08% of TP under cold stress. ‘Yixing Yuanye’ would be preferable for rapid P removal projects, as it had a high TP removal efficiency in 7 days at room temperature and 22 days under cold stress. At room temperature, ‘Liyang Baiqin’ could be an alternative for ‘Yixing Yuanye’ because of the similar removal rates of TN and TP in 17 days, but cold stress slowed down the removal efficiency of ‘Liyang Baiqin’. Thus, the selection of cultivars is important for phytoremediation projects using O. javanica.
In addition, there were significant differences in macronutrient removal efficiency, while the plant architectures and leaf colors of the cultivars were similar (Figure 1 and Figure 2a). This introduces a challenge to the selection of O. javanica cultivars for scientists in the field of environmental science or designers working on phytoremediation projects, both of which are not O. javanica breeders. The selection of the wrong cultivar can delay purification and cause economic loss. Thus, convenient methods to distinguish between the different O. javanica cultivars need to be established. Plant morphology characteristics are not suitable for the identification of O. javanica cultivars because of similarities in the plant architecture of the different cultivars. On the other hand, isozymes can be used for the identification of different cultivars. However, this approach associates with issues such as lack of sensitivity and specificity at different developmental stages and environmental factors [35]. Molecular biology methods are more reliable due to genetic stability. DNA fingerprints based on simple sequence repeat (SSR) markers have several advantages, including reproducibility, ease of genotyping, extensive polymorphisms, and short determination time [36,37]. In recent years, single-nucleotide polymorphisms (SNPs) have been proved to be more powerful, abundant, and stable but not cost-effective [38]. With the rapid development of next-generation sequencing, the sequence information of O. javanica was obtained, and 1233 SSR markers were identified using transcriptome sequencing [39], while 11,493 SNPs were identified using restriction site-associated DNA sequencing [40]. Given that countless molecular markers have already been identified and characterized from O. javanica, the screening of different cultivars using these markers and the selection of optimal SSR markers or SNPs for cost-effective O. javanica cultivar identification should be established in the near future to assure that suitable cultivars are chosen for wastewater treatment.

5. Conclusions

In the simulation experiment, all the O. javanica cultivars could tolerate 400 mg/L NH4+-N. ‘Suzhou Yuanye’ was suitable for the purification of N and P in both normal and cold conditions from simulated livestock wastewater, with reduction rates of 45.33 ± 1.92% TN and 99.32 ± 0.33% TP at room temperature, and 39.63 ± 2.15% TN and 74.50 ± 0.08% TP under cold stress. ‘Liyang Baiqin’ performed well in TN removal (44.30 ± 1.03%) at room temperature. ‘Yixing Yuanye’ could remove more than 98% of TP in 5 days at room temperature and in 22 days under cold stress, indicating that it is an ideal cultivar for P removal. Cold stress inhibited the nutrient removal ability, but ‘Suzhou Yuanye’ and ‘Yixing Yuanye’ still had potential phytoremediation applications in winter. Thus, the selection of cultivars is important for phytoremediation projects using O. javanica. To minimize the chance of N and P overload in colder periods, applications of different cultivars should be investigated in future studies.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/agriculture12101602/s1, Table S1: Water quality parameters of the samples.

Author Contributions

Conceptualization, D.Y. and Y.C.; methodology, L.S. and W.W.; validation, Y.C. and F.L.; formal analysis, W.W. and F.L.; investigation, W.W. and J.L.; resources, Y.C. and J.L.; data curation, W.W. and L.S.; writing—original draft preparation, L.S. and W.W.; writing—review and editing, Y.C., F.D. and D.Y.; visualization, J.L.; supervision, X.L. and D.Y.; project administration, D.Y. and Y.C.; and funding acquisition, L.S., D.Y. and Y.C. All authors have read and agreed to the published version of the manuscript.

Funding

This work was financially supported by the National Natural Science Foundation of China (32000270), the Six Talent Peaks Project in Jiangsu Province (TD-JNHB-008), the Projects of Independent Development (BM2018021-7) of the Jiangsu Provincial Department of Science and Technology of China, and the Foundation for Doctor Talents (JSPKLB202022) in the Institute of Botany, Jiangsu Province and Chinese Academy of Sciences, China.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

Acknowledgments

We thank breeders from the Suzhou Academy of Agricultural Sciences for the assistance with O. javanica cultivar collection. We are grateful to all lab members for their suggestions, support, and encouragement.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Boretti, A.; Rosa, L. Reassessing the Projections of the World Water Development Report. NPJ Clean Water 2019, 2, 15. [Google Scholar] [CrossRef] [Green Version]
  2. Walker, D.B.; Baumgartner, D.J.; Gerba, C.P.; Fitzsimmons, K. Chapter 16—Surface Water Pollution. In Environmental and Pollution Science, 3rd ed.; Brusseau, M.L., Pepper, I.L., Gerba, C.P., Eds.; Academic Press: Cambridge, MA, USA, 2019; pp. 261–292. [Google Scholar]
  3. Fletcher, J.; Willby, N.; Oliver, D.M.; Quilliam, R.S. Phytoremediation Using Aquatic Plants. In Phytoremediation; Shmaefsky, B.R., Ed.; Concepts and Strategies in Plant Sciences; Springer International Publishing: Cham, Switzerland, 2020; pp. 205–260. [Google Scholar]
  4. Rai, P.K. Phytoremediation of Emerging Contaminants in Wetlands, 1st ed.; CRC Press: Boca Raton, FL, USA, 2018; pp. 31–45. [Google Scholar]
  5. Luo, L.; He, H.; Yang, C.; Wen, S.; Zeng, G.; Wu, M.; Zhou, Z.; Lou, W. Nutrient Removal and Lipid Production by Coelastrella Sp. in Anaerobically and Aerobically Treated Swine Wastewater. Bioresour. Technol. 2016, 216, 135–141. [Google Scholar] [CrossRef]
  6. Markou, G.; Wang, L.; Ye, J.; Unc, A. Using Agro-Industrial Wastes for the Cultivation of Microalgae and Duckweeds: Contamination Risks and Biomass Safety Concerns. Biotechnol. Adv. 2018, 36, 1238–1254. [Google Scholar] [CrossRef]
  7. Wei, Z.; Van Le, Q.; Peng, W.; Yang, Y.; Yang, H.; Gu, H.; Lam, S.S.; Sonne, C. A Review on Phytoremediation of Contaminants in Air, Water and Soil. J. Hazard. Mater. 2021, 403, 123658. [Google Scholar] [CrossRef]
  8. Hu, H.; Li, X.; Wu, S.; Yang, C. Sustainable Livestock Wastewater Treatment via Phytoremediation: Current Status and Future Perspectives. Bioresour. Technol. 2020, 315, 123809. [Google Scholar] [CrossRef]
  9. Ali, S.; Abbas, Z.; Rizwan, M.; Zaheer, I.E.; Yavaş, İ.; Ünay, A.; Abdel-DAIM, M.M.; Bin-Jumah, M.; Hasanuzzaman, M.; Kalderis, D. Application of Floating Aquatic Plants in Phytoremediation of Heavy Metals Polluted Water: A Review. Sustainability 2020, 12, 1927. [Google Scholar] [CrossRef] [Green Version]
  10. Ting, W.H.T.; Tan, I.A.W.; Salleh, S.F.; Wahab, N.A. Application of Water Hyacinth (Eichhornia crassipes) for Phytoremediation of Ammoniacal Nitrogen: A Review. J. Water Process Eng. 2018, 22, 239–249. [Google Scholar] [CrossRef]
  11. Sun, L.; Liu, J.; Zhao, H.; Wang, Z.; Liu, X.; Chang, Y.; Yao, D. Phytoremediation Performance of Three Traditional Ornamental Hydrophytes and the Structure of Their Rhizosphere Microorganism Populations. Environ. Sci. Pollut. Res. 2022, 29, 50727–50741. [Google Scholar] [CrossRef]
  12. Sandoval, L.; Zamora-Castro, S.; Vidal-Álvarez, M.; Marín-Muñiz, J. Role of Wetland Plants and Use of Ornamental Flowering Plants in Constructed Wetlands for Wastewater Treatment: A Review. Appl. Sci. 2019, 9, 685. [Google Scholar] [CrossRef] [Green Version]
  13. Zhao, T.; Pan, X.; Ou, Z.; Li, Q.; Zhang, W. Comprehensive Evaluation of Waterlogging Tolerance of Eleven Canna Cultivars at Flowering Stage. Sci. Hortic. 2022, 296, 110890. [Google Scholar] [CrossRef]
  14. Yu, F.; Xiao, Y.; Cheng, L.; Feng, S.; Zhang, L. Four New Early Spring-flowering Evergreen Iris Cultivars. HortScience 2020, 55, 103–105. [Google Scholar] [CrossRef] [Green Version]
  15. Zhao, Z.; Li, T.; Cheng, Y.; Wang, F.; Zhao, X. Morphological and Metabolic Responses of Four Iris germanica Cultivars under Salinity Stress. Sci. Hortic. 2021, 30, 109960. [Google Scholar] [CrossRef]
  16. Liu, J.; Chang, Y.; Sun, L.; Du, F.; Cui, J.; Liu, X.; Li, N.; Wang, W.; Li, J.; Yao, D. Abundant Allelochemicals and the Inhibitory Mechanism of the Phenolic Acids in Water Dropwort for the Control of Microcystis aeruginosa Blooms. Plants 2021, 10, 2653. [Google Scholar] [CrossRef]
  17. Song, S.; Wang, P.; Liu, Y.; Zhao, D.; Leng, X.; An, S. Effects of Oenanthe javanica on Nitrogen Removal in Free-Water Surface Constructed Wetlands under Low-Temperature Conditions. Int. J. Environ. Res. Public. Health 2019, 16, 1420. [Google Scholar] [CrossRef] [Green Version]
  18. Kumar, S.; Li, G.; Yang, J.; Huang, X.; Ji, Q.; Liu, Z.; Ke, W.; Hou, H. Effect of Salt Stress on Growth, Physiological Parameters, and Ionic Concentration of Water Dropwort (Oenanthe javanica) Cultivars. Front. Plant Sci. 2021, 12, 660409. [Google Scholar] [CrossRef] [PubMed]
  19. Liu, J.-X.; Jiang, Q.; Tao, J.-P.; Feng, K.; Li, T.; Duan, A.-Q.; Wang, H.; Xu, Z.-S.; Liu, H.; Xiong, A.-S. Integrative Genome, Transcriptome, MicroRNA, and Degradome Analysis of Water Dropwort (Oenanthe javanica) in Response to Water Stress. Hortic. Res. 2021, 8, 262. [Google Scholar] [CrossRef] [PubMed]
  20. Sun, L.; Zhao, H.; Liu, J.; Li, B.; Chang, Y.; Yao, D. A New Green Model for the Bioremediation and Resource Utilization of Livestock Wastewater. Int. J. Environ. Res. Public. Health 2021, 18, 8634. [Google Scholar] [CrossRef] [PubMed]
  21. Zhou, X.; Wang, G. Nutrient Concentration Variations during Oenanthe javanica Growth and Decay in the Ecological Floating Bed System. J. Environ. Sci. 2010, 22, 1710–1717. [Google Scholar] [CrossRef]
  22. Kumar, S.; Li, G.; Huang, X.; Ji, Q.; Zhou, K.; Hou, H.; Ke, W.; Yang, J. Phenotypic, Nutritional, and Antioxidant Characterization of Blanched Oenanthe javanica for Preferable Cultivar. Front. Plant Sci. 2021, 12, 639639. [Google Scholar] [CrossRef] [PubMed]
  23. Cheng, D.; Ngo, H.H.; Guo, W.; Chang, S.; Nguyen, D.D.; Kumar, S.M. Microalgae Biomass from Swine Wastewater and Its Conversion to Bioenergy. Bioresour. Technol. 2019, 275, 109–122. [Google Scholar] [CrossRef]
  24. Lv, J.; Liu, Y.; Feng, J.; Liu, Q.; Nan, F.; Xie, S. Nutrients Removal from Undiluted Cattle Farm Wastewater by the Two-Stage Process of Microalgae-Based Wastewater Treatment. Bioresour. Technol. 2018, 264, 311–318. [Google Scholar] [CrossRef]
  25. Marino, D.; Moran, J.F. Can Ammonium Stress Be Positive for Plant Performance? Front. Plant Sci. 2019, 10, 1103. [Google Scholar] [CrossRef] [Green Version]
  26. Lee, G.; Kim, K.; Chung, J.; Han, J. Electrochemical Ammonia Accumulation and Recovery from Ammonia-Rich Livestock Wastewater. Chemosphere 2021, 270, 128631. [Google Scholar] [CrossRef] [PubMed]
  27. Hachiya, T.; Inaba, J.; Wakazaki, M.; Sato, M.; Toyooka, K.; Miyagi, A.; Hawai-Yamada, M.; Sugiura, D.; Nakagawa, T.; Kiba, T.; et al. Excessive Ammonium Assimilation by Plastidic Glutamine Synthetase Causes Ammonium Toxicity in Arabidopsis thaliana. Nat. Commun. 2021, 12, 4944. [Google Scholar] [CrossRef] [PubMed]
  28. Abe, K.; Komada, M.; Ookuma, A.; Itahashi, S.; Banzai, K. Purification Performance of a Shallow Free-Water-Surface Constructed Wetland Receiving Secondary Effluent for about 5 Years. Ecol. Eng. 2014, 69, 126–133. [Google Scholar] [CrossRef]
  29. Tyler, H.L.; Moore, M.T.; Locke, M.A. Influence of Three Aquatic Macrophytes on Mitigation of Nitrogen Species from Agricultural Runoff. Water. Air. Soil Pollut. 2012, 223, 3227–3236. [Google Scholar] [CrossRef]
  30. Chen, C.; Zhao, T.; Liu, R.; Luo, L. Performance of Five Plant Species in Removal of Nitrogen and Phosphorus from an Experimental Phytoremediation System in the Ningxia Irrigation Area. Environ. Monit. Assess. 2017, 189, 497. [Google Scholar] [CrossRef]
  31. Müller, L.M.; Flokova, K.; Schnabel, E.; Sun, X.; Fei, Z.; Frugoli, J.; Bouwmeester, H.J.; Harrison, M.J. A CLE–SUNN Module Regulates Strigolactone Content and Fungal Colonization in Arbuscular Mycorrhiza. Nat. Plants 2019, 5, 933–939. [Google Scholar] [CrossRef]
  32. Smith, S.E.; Smith, F.A. Roles of Arbuscular Mycorrhizas in Plant Nutrition and Growth: New Paradigms from Cellular to Ecosystem Scales. Annu. Rev. Plant Biol. 2011, 62, 227–250. [Google Scholar] [CrossRef] [Green Version]
  33. Edwards, J.; Johnson, C.; Santos-Medellín, C.; Lurie, E.; Podishetty, N.K.; Bhatnagar, S.; Eisen, J.A.; Sundaresan, V. Structure, Variation, and Assembly of the Root-Associated Microbiomes of Rice. Proc. Natl. Acad. Sci. USA 2015, 112, E911–E920. [Google Scholar] [CrossRef]
  34. Zhang, J.; Liu, Y.-X.; Zhang, N.; Hu, B.; Jin, T.; Xu, H.; Qin, Y.; Yan, P.; Zhang, X.; Guo, X.; et al. NRT1.1B Is Associated with Root Microbiota Composition and Nitrogen Use in Field-Grown Rice. Nat. Biotechnol. 2019, 37, 676–684. [Google Scholar] [CrossRef] [PubMed]
  35. Lumaret, R.; Ouazzani, N.; Michaud, H.; Vivier, G.; Deguilloux, M.-F.; Di Giusto, F. Allozyme Variation of Oleaster Populations (Wild Olive Tree) (Olea europaea L.) in the Mediterranean Basin. Heredity 2004, 92, 343–351. [Google Scholar] [CrossRef] [PubMed]
  36. Ercisli, S.; Ipek, A.; Barut, E. SSR Marker-Based DNA Fingerprinting and Cultivar Identification of Olives (Olea europaea). Biochem. Genet. 2011, 49, 555. [Google Scholar] [CrossRef] [PubMed]
  37. Kalia, R.K.; Rai, M.K.; Kalia, S.; Singh, R.; Dhawan, A.K. Microsatellite Markers: An Overview of the Recent Progress in Plants. Euphytica 2011, 177, 309–334. [Google Scholar] [CrossRef]
  38. Wu, D.; Liang, Z.; Yan, T.; Xu, Y.; Xuan, L.; Tang, J.; Zhou, G.; Lohwasser, U.; Hua, S.; Wang, H.; et al. Whole-Genome Resequencing of a Worldwide Collection of Rapeseed Accessions Reveals the Genetic Basis of Ecotype Divergence. Mol. Plant 2019, 12, 30–43. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  39. Jiang, Q.; Wang, F.; Tan, H.; Li, M.; Xu, Z.; Tan, G.; Xiong, A. De Novo Transcriptome Assembly, Gene Annotation, Marker Development, and miRNA Potential Target Genes Validation under Abiotic Stresses in Oenanthe javanica. Mol. Genet. Genom. 2015, 290, 671–683. [Google Scholar] [CrossRef]
  40. Ji, Q.; Zhu, H.; Huang, X.; Zhou, K.; Liu, Z.; Sun, Y.; Wang, Z.; Ke, W. Uncovering phylogenetic relationships and genetic diversity of water dropwort using phenotypic traits and SNP markers. PLoS ONE 2011, 16, e0249825. [Google Scholar] [CrossRef]
Agriculture 12 01602 g001 550
Figure 1. Seven common O. javanica cultivars tested in this study.
Figure 1. Seven common O. javanica cultivars tested in this study.
Agriculture 12 01602 g001
Agriculture 12 01602 g002a 550Agriculture 12 01602 g002b 550
Figure 2. Architecture and biomass assimilation of O. javanica cultivars in different temperatures. Different letters with the same color indicate the significance of the difference at the same temperature. Asterisk indicates the significance of the difference of a different temperature on the same cultivar. * significant differences, p < 0.05; ** extremely significant differences, p < 0.01. (a) Architecture of different O. javanica cultivars after 22 days of growth in the simulated livestock wastewater at different temperatures. Normal: room temperature; Cold: cold stress. (b) Plant height of different O. javanica cultivars after 22 days of growth. (c) Fresh matter biomass of different O. javanica cultivars after 22 days of growth. (d) Dry matter biomass of different O. javanica cultivars after 22 days of growth. MS: ‘Meinan Shuiqin’; YB: ‘Yuqi Baiqin’; JB: ‘Jiangyin Baiqin’; LB: ‘Liyang Baiqin’; YY: ‘Yixing Yuanye’; SY: ‘Suzhou Yuanye’; SJ: ‘Suqian Jianye’.
Figure 2. Architecture and biomass assimilation of O. javanica cultivars in different temperatures. Different letters with the same color indicate the significance of the difference at the same temperature. Asterisk indicates the significance of the difference of a different temperature on the same cultivar. * significant differences, p < 0.05; ** extremely significant differences, p < 0.01. (a) Architecture of different O. javanica cultivars after 22 days of growth in the simulated livestock wastewater at different temperatures. Normal: room temperature; Cold: cold stress. (b) Plant height of different O. javanica cultivars after 22 days of growth. (c) Fresh matter biomass of different O. javanica cultivars after 22 days of growth. (d) Dry matter biomass of different O. javanica cultivars after 22 days of growth. MS: ‘Meinan Shuiqin’; YB: ‘Yuqi Baiqin’; JB: ‘Jiangyin Baiqin’; LB: ‘Liyang Baiqin’; YY: ‘Yixing Yuanye’; SY: ‘Suzhou Yuanye’; SJ: ‘Suqian Jianye’.
Agriculture 12 01602 g002aAgriculture 12 01602 g002b
Agriculture 12 01602 g003 550
Figure 3. Concentrations of different N forms in the beakers with different O. javanica cultivars at different temperatures. Different letters indicate the significance of the difference of the concentration on the same day. (a) Concentrations of TN at room temperature. (b) Concentrations of NH4+-N at room temperature. (c) Concentrations of TN under cold stress. (d) Concentrations of NH4+-N under cold stress. MS: ‘Meinan Shuiqin’; YB: ‘Yuqi Baiqin’; JB: ‘Jiangyin Baiqin’; LB: ‘Liyang Baiqin’; YY: ‘Yixing Yuanye’; SY: ‘Suzhou Yuanye’; SJ: ‘Suqian Jianye’.
Figure 3. Concentrations of different N forms in the beakers with different O. javanica cultivars at different temperatures. Different letters indicate the significance of the difference of the concentration on the same day. (a) Concentrations of TN at room temperature. (b) Concentrations of NH4+-N at room temperature. (c) Concentrations of TN under cold stress. (d) Concentrations of NH4+-N under cold stress. MS: ‘Meinan Shuiqin’; YB: ‘Yuqi Baiqin’; JB: ‘Jiangyin Baiqin’; LB: ‘Liyang Baiqin’; YY: ‘Yixing Yuanye’; SY: ‘Suzhou Yuanye’; SJ: ‘Suqian Jianye’.
Agriculture 12 01602 g003
Agriculture 12 01602 g004 550
Figure 4. Concentrations of TP in the beakers with different O. javanica cultivars at different temperatures. Different letters indicate the significance of the difference of the concentration on the same day. (a) Concentrations of TP at room temperature. (b) Concentrations of TP under cold stress. MS: ‘Meinan Shuiqin’; YB: ‘Yuqi Baiqin’; JB: ‘Jiangyin Baiqin’; LB: ‘Liyang Baiqin’; YY: ‘Yixing Yuanye’; SY: ‘Suzhou Yuanye’; SJ: ‘Suqian Jianye’.
Figure 4. Concentrations of TP in the beakers with different O. javanica cultivars at different temperatures. Different letters indicate the significance of the difference of the concentration on the same day. (a) Concentrations of TP at room temperature. (b) Concentrations of TP under cold stress. MS: ‘Meinan Shuiqin’; YB: ‘Yuqi Baiqin’; JB: ‘Jiangyin Baiqin’; LB: ‘Liyang Baiqin’; YY: ‘Yixing Yuanye’; SY: ‘Suzhou Yuanye’; SJ: ‘Suqian Jianye’.
Agriculture 12 01602 g004
Agriculture 12 01602 g005 550
Figure 5. N and P assimilation in O. javanica cultivars at room temperature and under cold stress. Different letters with the same color indicate the significance of the difference in the same temperature. Asterisk indicates the significance of the difference of a different temperature on the same cultivar. * significant differences, p < 0.05; ** extremely significant differences, p < 0.01. (a,b) Concentrations of N and P in O. javanica cultivars at room temperature (a) and under cold stress (b) on day 22. (c,d) N and P accumulation amounts in O. javanica cultivars at room temperature (c) and under cold stress (d) on day 22. MS: ‘Meinan Shuiqin’; YB: ‘Yuqi Baiqin’; JB: ‘Jiangyin Baiqin’; LB: ‘Liyang Baiqin’; YY: ‘Yixing Yuanye’; SY: ‘Suzhou Yuanye’; SJ: ‘Suqian Jianye’.
Figure 5. N and P assimilation in O. javanica cultivars at room temperature and under cold stress. Different letters with the same color indicate the significance of the difference in the same temperature. Asterisk indicates the significance of the difference of a different temperature on the same cultivar. * significant differences, p < 0.05; ** extremely significant differences, p < 0.01. (a,b) Concentrations of N and P in O. javanica cultivars at room temperature (a) and under cold stress (b) on day 22. (c,d) N and P accumulation amounts in O. javanica cultivars at room temperature (c) and under cold stress (d) on day 22. MS: ‘Meinan Shuiqin’; YB: ‘Yuqi Baiqin’; JB: ‘Jiangyin Baiqin’; LB: ‘Liyang Baiqin’; YY: ‘Yixing Yuanye’; SY: ‘Suzhou Yuanye’; SJ: ‘Suqian Jianye’.
Agriculture 12 01602 g005
Agriculture 12 01602 g006 550
Figure 6. Correlations among water quality parameters, TN and TP removal rates, TN and TP bioaccumulation, and biomass. Numbers indicate the Pearson’s r between two parameters with significant correlation; * significant correlation, p < 0.05; ** extremely significant correlation, p < 0.01.
Figure 6. Correlations among water quality parameters, TN and TP removal rates, TN and TP bioaccumulation, and biomass. Numbers indicate the Pearson’s r between two parameters with significant correlation; * significant correlation, p < 0.05; ** extremely significant correlation, p < 0.01.
Agriculture 12 01602 g006
Table
Table 1. Formula of the simulated livestock wastewater (1 L).
Table 1. Formula of the simulated livestock wastewater (1 L).
ElementVolume
10 × Hoagland solution without N or P100 mL
KH2PO40.066 g
(NH4)2SO41.886 g
KNO30.722 g
Table
Table 2. Experimental conditions and test designations.
Table 2. Experimental conditions and test designations.
O. javanica CultivarTemperature
Room TemperatureCold Stress
CK3 beakers3 beakers
‘Meinan Shuiqin’3 beakers3 beakers
‘Yuqi Baiqin’3 beakers3 beakers
‘Jiangyin Baiqin’3 beakers3 beakers
‘Liyang Baiqin’3 beakers3 beakers
‘Yixing Yuanye’3 beakers3 beakers
‘Suzhou Yuanye’3 beakers3 beakers
‘Suqian Jianye’3 beakers3 beakers
Table
Table 3. Two-way ANOVA on TN and NH4+-N removal.
Table 3. Two-way ANOVA on TN and NH4+-N removal.
VariableTNNH4+-N
F Valuep ValueF Valuep Value
Temperature00.9931.0260.312
Cultivar2.190.0353.8180.001
Temperature × Cultivar0.5550.7920.7450.634
Table
Table 4. Two-way ANOVA on TP removal.
Table 4. Two-way ANOVA on TP removal.
VariableF Valuep Value
Temperature22.7480
Cultivar7.4090
Temperature × Cultivar1.5120.162
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Sun, L.; Wang, W.; Liu, F.; Liu, J.; Du, F.; Liu, X.; Chang, Y.; Yao, D. Differences in Nitrogen and Phosphorus Removal under Different Temperatures in Oenanthe javanica Cultivars. Agriculture 2022, 12, 1602. https://doi.org/10.3390/agriculture12101602

AMA Style

Sun L, Wang W, Liu F, Liu J, Du F, Liu X, Chang Y, Yao D. Differences in Nitrogen and Phosphorus Removal under Different Temperatures in Oenanthe javanica Cultivars. Agriculture. 2022; 12(10):1602. https://doi.org/10.3390/agriculture12101602

Chicago/Turabian Style

Sun, Linhe, Wei Wang, Fengjun Liu, Jixiang Liu, Fengfeng Du, Xiaojing Liu, Yajun Chang, and Dongrui Yao. 2022. "Differences in Nitrogen and Phosphorus Removal under Different Temperatures in Oenanthe javanica Cultivars" Agriculture 12, no. 10: 1602. https://doi.org/10.3390/agriculture12101602

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop