Next Article in Journal
Olive Plant Treated with Different Geo-Material Foliar Film (Zeolite and Kaolin Based): Leaf Characteristics and Oil Quality
Previous Article in Journal
Transmission Route of Airborne Fungal Spores for Cucumber Downy Mildew
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Horticulturae
Volume 11
Issue 3
10.3390/horticulturae11030337
horticulturae-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
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Physiological and Biochemical Adaptation of Common Garden Plants to Inorganic Nitrogen-Laden Fine Particulate Matter Stress

by
Keqin Xiao
1,
Yiying Wang
1,
Rongkang Wang
1,
Zhanpeng Hu
1,
Sili Peng
1,2,
Zimei Miao
1,2,* and
Zhiwei Ge
1,2,*
1
Co-Innovation Center for Sustainable Forestry in Southern China, College of Biology and the Environment, Nanjing Forestry University, Nanjing 210037, China
2
Academy of Chinese Ecological Progress and Forestry Development Studies, Nanjing Forestry University, Nanjing 210037, China
*
Authors to whom correspondence should be addressed.
Horticulturae 2025, 11(3), 337; https://doi.org/10.3390/horticulturae11030337
Submission received: 12 February 2025 / Revised: 7 March 2025 / Accepted: 17 March 2025 / Published: 20 March 2025
(This article belongs to the Section Developmental Physiology, Biochemistry, and Molecular Biology)
Browse Figures
Versions Notes

Abstract

:
Accelerated urbanization has intensified nitrogen deposition and fine particulate matter (PM2.5) pollution. While urban landscape plants play a vital role in atmospheric remediation, systematic exploration of their adaptation strategies to these dual stressors remains limited. This study investigated the dynamic responses of antioxidant defense systems and nitrogen/weight ratios of Iris germanica L. and Portulaca grandiflora Hook. under four nitrogen deposition scenarios (N0, N1, N2, and N4 with nitrogen concentrations of 0, 15, 30, and 60 kg N·hm−2·a−1, respectively) combined with constant PM2.5 exposure (50 μg/m3). Through fumigation experiments, we demonstrated that Iris germanica L. showed higher sensitivity to inorganic nitrogen-laden PM2.5 stress than Portulaca grandiflora Hook. Both species exhibited stronger antioxidant enzyme (SOD, CAT, POD) activities in the high-growth season compared to the low-growth season. Nitrogen allocation analysis revealed that Portulaca grandiflora Hook. maintained stable nitrogen content across treatments, while Iris germanica L. showed progressive nitrogen loss under high nitrogen-laden PM2.5 exposure. These findings establish Portulaca grandiflora Hook.’s superior resilience through two synergistic mechanisms: modulated antioxidant systems and efficient nitrogen remobilization. This comparative study provides actionable insights for selecting pollution-tolerant species in urban green infrastructure planning.

1. Introduction

The concurrent escalation of atmospheric nitrogen deposition and particulate matter (PM) pollution has emerged as a critical environmental stressor driven by global urbanization and industrialization [1,2]. These interconnected phenomena profoundly affect both ecosystem integrity and public health through multiple pathways [3,4,5]. Atmospheric reactive nitrogen (Nr) concentrations exhibit a sustained upward trajectory [6], with excess Nr undergoing heterogeneous chemical transformations that generate nitrogenous compounds adsorbed onto PM surfaces, thereby exacerbating aerosol pollution through secondary formation processes [7].
As an essential macronutrient, nitrogen governs fundamental metabolic pathways in plant systems [8]. While nitrogen has been demonstrated to enhance plant growth and productivity within optimal concentration ranges [9], supra-optimal nitrogen accumulation in plant tissues can exert growth-inhibitory effects upon reaching nitrogen saturation thresholds [10]. Nitrogen deposition-induced excess may adversely affect plant physiology, morphology, and stress tolerance. At the physiological level, excessive nitrogen disrupts nitrogen metabolism, alters nutrient homeostasis, and impairs photosynthetic efficiency, resulting in reduced net photosynthetic rates [11]. In terms of morphology, nitrogen overaccumulation induces foliar abscission and chlorosis [12] while simultaneously compromising plant resilience to environmental stressors, including drought [13], low-temperature conditions, and pest infestation. Notably, plant responses to nitrogen deposition exhibit species-specific variations dependent not only on ambient nitrogen ratios but also on functional group classifications. Of particular significance, divergent nitrogen use efficiencies occur between photosynthetic types, with C4 plants displaying significantly higher nitrogen utilization capacity than C3 species [14]. Correspondingly, nitrogen supplementation exerts more pronounced effects on biomass accumulation and growth rates in C3 plants relative to C4 counterparts [15].
Airborne PM, a critical component of airborne pollutants, is classified as TSP (Total Suspended Particulate, Dp ≤ 100 μm), PM10 (Dp ≤ 10 μm), PM2.5 (Dp ≤ 2.5 μm), etc., according to the aerodynamic diameter of the PM. PM less than 2.5 μm is also known as fine PM. Chemical characterization reveals that water-soluble inorganic ions dominate PM2.5 composition, contributing approximately 50% of its mass fraction [16], with ammonium (NH4+) and nitrate (NO3−) emerging as the predominant ionic species [17].
Plants function as a natural filtration system through foliar PM interception, with plants demonstrating significant capacity for particulate matter absorption and retention. This biological process establishes plants as an essential component in urban PM pollution mitigation strategies [18,19]. However, PM accumulation on phyllosphere surfaces induces detrimental physiological impacts. Mechanistic studies demonstrate dual pathway interference with photosynthesis: (1) surface-deposited particulates attenuate photosynthetically active radiation penetration, and (2) stomatal occlusion by particulate deposits impedes gaseous exchange processes [20]. These synergistic effects depress key photosynthetic parameters, including net photosynthetic rate and stomatal conductance, while simultaneously initiating oxidative stress through reactive oxygen species (ROS) generation, consequently elevating antioxidant enzyme activities [21,22]. However, plant response to PM is highly dependent on particle concentrations and species-specific tolerance thresholds. Comparative studies reveal divergent physiological responses under equivalent PM2.5 exposure: Koelreuteria paniculata demonstrates a 50% enhancement in antioxidant enzyme activity at 200 μg/m3, while Trifolium repens sustains irreversible oxidative damage under identical conditions [23]. Tolerance mechanisms show marked differentiation: Platycladus orientalis (Chinese arborvitae) showed enhanced ROS scavenging capacity at PM2.5 levels > 150 μg/m³, with ascorbic acid (AsA) content increasing by 50% and superoxide dismutase (SOD) activity increasing by 35%. Conversely, sensitive species such as Toxicodendron vernicifluum (Japanese lacquer tree) showed only a 15% increase in AsA, resulting in an air pollution tolerance index (APTI) below 8.0—a threshold indicating low resilience to pollution [24]. Beyond these biochemical strategies, morphological traits critically determine interspecific PM retention efficiency. Evergreen shrubs in Beijing, including Cephalotaxus sinensis and Euonymus japonicus, achieved superior PM2.5 trapping efficiencies (1.5–2.0 μg/cm2) due to rough leaf surfaces and dense trichomes, which enhance particle adhesion [25]. This biomechanical optimization parallels Tectona grandis (teak) specimens in Indian coalfields, which demonstrate exceptional PM resilience (APTI = 17.0) attributed to thick cuticular wax layers that prevent stomatal blockage while maintaining gas exchange efficiency [26].
At present, scholars have made some progress in studying the effects of nitrogen deposition and PM on plants, but most of them have focused on natural ecosystems such as forests and farmlands, and relatively few studies have been conducted on urban landscape plants, and most of these have focused on growth performance or changes in a single physiological index. In addition, due to the complexity and variability of urban environments, the responses of different types of landscape plants to nitrogen-laden PM may differ significantly, further increasing the complexity and challenge of the study.
Iris germanica L. and Portulaca grandiflora Hook. are herbaceous plants renowned for their ornamental and medicinal properties [27,28,29]. They possess remarkable environmental adaptability, which has made them popular choices for urban greening and landscaping. In particular, they are widely used as ground cover in urban green spaces in southern China. Although previous research on their stress resistance has mainly focused on drought and salinity tolerance [30,31,32], the adaptive mechanisms of these two species under nitrogen deposition and atmospheric particulate pollution remain poorly understood.
In this study, we investigated the physiological and biochemical adaptation of Iris germanica L. and Portulaca grandiflora Hook. to inorganic nitrogen-laden fine particulate matter (hereafter abbreviated as nitrogen-laden PM2.5) stress. The main objectives of this study were as follows: (1) to bring new contributions to the regulatory mechanisms of plant nitrogen storage patterns and antioxidant defense systems under varying levels of particulate pollution and (2) to compare the physiological responses of these two representative garden species under identical pollution conditions and explore the reasons and potential mechanisms for the differences in their tolerance. The results of this study are expected to provide a theoretical basis for optimizing plant selection and allocation in urban landscaping against the background of increasing nitrogenous PM2.5 in air pollution. It is also expected to improve our understanding of the response mechanisms by which plants respond to nitrogenous PM2.5 pollution.

2. Materials and Methods

2.1. Study Area

This experiment was carried out at the Jishan Experimental Forestry Farm of the Jiangsu Academy of Forestry in Jiangning District, Nanjing, China (31°32°07′ N, 118°119°06′ E). The experimental site is situated in the north subtropical monsoon climate zone, characterized by an annual average temperature of 15.7 °C and abundant rainfall with an annual average precipitation of 1072.9 mm. The study region experiences extreme temperature fluctuations, with an annual minimum of −13.3 °C and a maximum of 40.4 °C during severe weather events. Between 2009 and 2011, the wet and dry deposition of inorganic nitrogen in Nanjing was 28.7 kg N·hm−2·a−1 and 35.8 kg N·hm−2·a−1, respectively [33]. From 2014 to 2016, the average yearly concentrations of PM2.5 in Nanjing ranged from 43 to 74 μg m−3 [34].

2.2. Experimental Design

The experiment was conducted in an unheated greenhouse at the Jiangsu Academy of Forestry (Nanjing, China), where temperature and humidity conditions mirrored the indoor environment. The natural temperature range was 18–28 °C, and the average relative humidity was 65 ± 10%, which is consistent with local indoor values. Photosynthetically active radiation (PAR) was maintained at 250–400 μmol/m2/s during the day by natural sunlight filtered by polycarbonate panels. Iris germanica L. and Portulaca grandiflora Hook. were sown in February in cylindrical plastic pots (top diameter: 15 cm; bottom diameter: 13 cm; height: 15 cm; approximate volume: 1.7 L) filled with a uniform nursery substrate (Model 422, Klasmann-Deilmann GMBH Incorporated, Geeste, Germany).
Separate fumigation experiments were conducted for the Iris germanica L. and Portulaca grandiflora Hook., with each plant exposed to four distinct fumigation concentration treatments and aerosol levels as follows: N0 (aerosol with an average particle size of 2.5 μm from distilled water, nitrogen concentration = 0 kg N·hm−2·a−1), N1 (aerosol formed from NH4NO3 solution with an average particle size of 2.5 μm, nitrogen concentration = 15 kg N·hm−2·a−1), N2 (same as above, nitrogen concentration = 30 kg N·hm−2·a−1), and N4 (same as above, nitrogen concentration = 60 kg N·hm−2·a−1). The nitrogen concentrations were determined according to the annual nitrogen deposition levels in Nanjing City. For each fumigation concentration, four individual plants with virtually identical growth patterns were selected as subjects for both Iris germanica L. and Portulaca grandiflora Hook., resulting in a total of 32 plants.

2.3. Test Equipment

Utilizing a custom-designed fumigation system (Figure 1) with proprietary intellectual property rights (Patent No: ZL201621111648.7, China) [35], the experimental setup comprises three primary components: a PM2.5 generator, plant chambers, and an exhaust gas recycling device. The PM2.5 generator is composed of an air pump (Model 36-7, Jiebao Incorporated, Shanghai, China) and a six-nozzle aerosol generator (Model: 9306A, TSI Incorporated, Shoreview, MN, USA), which produces NH4NO3 aerosols with a median particle size of 2.5 μm. The particle size is calibrated through the nozzle of the regulator and monitored using a Dusttrak II particulate monitor (Model: 8530, TSI Incorporated, Shoreview, MN, USA), which was only turned on for concentration checking during fumigating. The plant chambers, constructed from Plexiglas, feature a rectangular design measuring 0.3 m × 0.3 m × 0.65 m with a side sliding door. To prevent the absorption of aerosol particles from being absorbed by the soil, a plastic film covers the soil surface. For irrigation purposes, an irrigation tube is inserted into the soil using a PVC pipe and securely capped. The entire apparatus was sealed to facilitate gas circulation, with exhaust gases directed through the exhaust pipe into an exhaust gas collection pool containing NaHCO3 solution to mitigate environmental contamination. Fans were installed both vertically and horizontally in each chamber for the uniform distribution of aerosols, temperature, and CO2.
The experiment operated for 16 h each daily, with a scheduled 1 h break for every 2 h of operation to maintain a consistent PM2.5 concentration within the system at 50 µg m−3 (in accordance with the annual average PM2.5 concentration in Nanjing).

2.4. Sample Collection and Sample Analysis

Sampling was carried out on the 3rd, 8th, 15th, 22nd, and 30th days starting from 1 April (considered the low-growth season of the plants) and 15 July 2018 (the high-growth season of the plants). Subsequently, two leaves exhibiting uniform length, complete shape, good health, and consistent maturity were carefully selected from each potted plant. These carefully selected leaves were then carefully removed and stored in an icebox for transportation to the laboratory for the determination of superoxide dismutase (SOD), peroxidase (POD), and catalase (CAT) activities of the plants. Furthermore, a portion of leaves and roots were harvested from each potted plant for subsequent drying and grinding into a fine powder, passing through a 0.149 mm steel sieve, and then utilized for the assessment of the plants’ total nitrogen/weight ratio using a PE2400II Elemental Analyser (PEKIN-ELMER Co., Ltd., Waltham, MA, USA).
Approximately 0.2 g of fresh leaves were accurately weighed and incised, following which 10 mL of pre-cooled PBS 7.8 solution was sequentially added in two installments. The samples were ground and extracted, followed by centrifugation at 10,500 rpm for 15 min at 4 °C [35]. The resulting supernatant was collected for subsequent enzyme assays and stored at 4 °C. For the assessment of SOD activity measurement, the nitro blue tetrazolium photoreduction method, as described by Giannopolitis and Ries [36], was employed, with 50% inhibition of nitro blue tetrazolium (NBT) photochemical reduction considered as one unit of enzyme activity. POD activity was determined through guaiacol oxidation following the method outlined by Zheng and Van Huystee [37], with an increase of 0.01 per minute in optical density (OD) at 470 nm, defined as one unit of activity. Lastly, CAT activity was evaluated via UV absorption following the method established by Change and Maehly [38], with a decrease of 0.01 per minute in OD at 240 nm considered as one unit of enzyme activity.

2.5. Statistical Analyses

The preliminary data processing was carried out using Excel 2016, followed by the utilization of SPSS 25.0 software (IBM Corp. Released 2017. IBM SPSS Statistics for Windows, Version 25.0. IBM Corp.: Armonk, NY, USA) for performing multifactorial ANOVA on plant antioxidant enzyme activity based on growth period, fumigation time, fumigation concentration, and plant species. Moreover, one-way ANOVA was performed on antioxidant enzyme activity considering fumigation time, nitrogen pattern, and fumigation concentration, while repeated measures ANOVA was employed to analyze antioxidant enzyme activity with respect to fumigation concentration. Prior to the repeated measures ANOVA, Mauchly’s sphericity test [39] was conducted, and the significance of the differences between factors was reported post Mauchly’s sphericity test confirmation. In instances where Mauchly’s sphericity test did not meet the assumptions, the Greenhouse–Geisser was applied. The statistically significance level was established at p < 0.05. Graphical representations were generated utilizing Origin 2021 software (version 2021 for Windows; OriginLab. MAS, Hampton, VA, USA).

3. Results

3.1. Effects of Inorganic Nitrogen-Laden Fine PM on Antioxidant Systems in Iris germanica L. and Portulaca grandiflora Hook.

ANOVA analysis revealed that all four factors of the growth period, fumigation time, fumigation concentration, and plant species significantly influenced the changes in the activities of the three enzymes, while the exception of plant species did not exhibit a significant effect on the changes in POD activities (Table 1). Overall, the analysis highlights complex interdependencies among factors, the combined effects of these factors play important roles in modulating the activity of antioxidant enzyme activities.

3.1.1. Effect of Fumigation Time on Antioxidant Enzyme Activity

The comparison of trends in antioxidant enzyme activities within the same plant across varying fumigation times in different growth periods revealed distinct patterns. A notable observation was the earlier increase in SOD activity for both Iris germanica L. and Portulaca grandiflora Hook. during the high-growth season compared with that in the low-growth season, indicating a more rapid and consistent response to stress in both species during active growth (Figure 2). Moreover, there was no significant downward trend observed in POD activities for both Iris germanica L. and Portulaca grandiflora Hook. towards the latter phase of the fumigation period in the high-growth season (Figure 3). This suggests the plants’ improved capacity to sustain POD activity under stress conditions during the growing phase. The fluctuations in CAT activity of Iris germanica L. and Portulaca grandiflora Hook. were more pronounced during the late fumigation period of the low-growth season while exhibiting a more moderate variation during the fumigation period of the high-growth season (Figure 4). These findings emphasize the plants’ capacity to regulate antioxidant enzymes more consistently during active growth phases, indicating a more stable and resilient response to stress.
Furthermore, it is worth noting that CAT activity exhibited relatively higher levels within the antioxidant enzyme system of Iris germanica L., whereas POD activity was significantly elevated in Portulaca grandiflora Hook. These distinct enzyme profiles indicate that both CAT and POD play critical roles in scavenging hydrogen peroxide (H2O2) ROS, with Iris germanica L. primarily depending on CAT for H2O2 scavenging and Portulaca grandiflora Hook., predominantly utilizing POD for H2O2 detoxification.

3.1.2. Effect of Fumigation Concentration on Antioxidant Enzyme Activity

Both in the non-growing and high-growth season, the SOD activity of Iris germanica L. and Portulaca grandiflora Hook. exhibited a significant decrease in the N4 treatment compared with that in the other treatments (Figure 5A,B). In the low-growth season, Iris germanica L. POD activity displayed significantly higher in the N4 treatment than the other treatments, while in the high-growth season, both the N2 and N4 treatments were significantly higher than the N0 and N1 treatments. Conversely, Portulaca grandiflora Hook. did not demonstrate significant differences in POD activity among other treatments (Figure 5C,D). Furthermore, in the low-growth season, Iris germanica L. CAT activity was significantly elevated in the N1 treatment compared with that in the other treatments, with no significant differences observed in the high-growth season. In contrast, Portulaca grandiflora Hook. did not exhibit significant variations in CAT activity across treatments (Figure 5E,F).
In summary, exposure to inorganic nitrogen-laden PM2.5 fumigation influenced the activities of three antioxidant enzymes in Iris germanica L. and one antioxidant enzyme in Portulaca grandiflora Hook. These results indicated that the response of POD and CAT to different stress levels is more pronounced in Iris germanica L. than in Portulaca grandiflora Hook.

3.2. Effects of Inorganic Nitrogen-Laden PM on Nitrogen Storage Patterns in Iris germanica L. and Portulaca grandiflora Hook.

In the low-growth season, the nitrogen/weight ratio in the leaves of Iris germanica L. exhibited a significant decrease in the N4 treatment compared with that in other treatments. Moreover, the nitrogen/weight ratio in the roots of Iris germanica L. notably decreased in the N2 and N4 treatments compared with that in the N0 and N1 treatments. These findings indicated a substantial reduction in the nitrogen/weight ratio of Iris germanica L. leaves under high-concentration fumigation treatments, with the nitrogen/weight ratio in roots also decreasing at medium and high concentrations. Conversely, there were no significant differences in the nitrogen/weight ratio of Portulaca grandiflora Hook. leaves and roots among all treatments (Figure 6A). Therefore, exposure to PM2.5 fumigation containing inorganic nitrogen resulted in a decrease in the nitrogen/weight ratio in both leaves and roots of Iris germanica L., while no such effect was observed in Portulaca grandiflora Hook.
In the high-growth season, the nitrogen/weight ratio in leaves of Iris germanica L. was significantly lower in the N2 and N4 treatments compared with that in the N0 and N1 treatments. However, the nitrogen/weight ratio in the roots of Iris germanica L., as well as that in the leaves and roots of Portulaca grandiflora Hook., showed no significant differences among all treatments (p > 0.05). Notably, the nitrogen/weight ratios in the leaves and roots of Portulaca grandiflora Hook. were significantly higher than those of Iris germanica L. under all treatment conditions, which indicated a greater nitrogen storage capacity in Portulaca grandiflora Hook. cells compared with that in Iris germanica L. (Figure 6B).
Overall, the data suggest that heavy PM stress generally results in a decrease in the nitrogen/weight ratio in Iris germanica L., whereas no significant reduction in the nitrogen/weight ratio was observed in any parts of Portulaca grandiflora Hook. under intense PM stress. This suggests that Portulaca grandiflora Hook. demonstrates a superior ability to maintain the nitrogen/weight ratio in vivo under the influence of nitrogen-laden PM stress.

4. Discussion

4.1. Antioxidant Response to Inorganic Nitrogen PM2.5 in Iris germanica L. and Portulaca grandiflora Hook.

Under normal physiological conditions, plants maintain a dynamic equilibrium between reactive oxygen species (ROS) production and scavenging. However, adversity stress disrupts this balance by accelerating ROS accumulation [40], triggering the activation of antioxidant enzyme systems to mitigate oxidative damage and sustain growth [41]. Generally, when plants are under mild or moderate adversity stress, the antioxidant system is induced to increase the ability to scavenge ROS; when under severe adversity stress, the balance of the plant’s antioxidant system is disrupted and inhibited, and a large amount of ROS accumulates in the body, resulting in organismal damage [42]. The antioxidant system for scavenging reactive oxygen species consists of antioxidant enzymes and antioxidants. The main antioxidant enzymes are SOD, POD, and CAT [43]. Among them, SOD is the fastest reacting indicator of the antioxidant system to eliminate intracellular oxygen ions to form H2O2 and O2 [44], while CAT and POD function to scavenge high intracellular concentrations of hydrogen peroxide [45]. The activity of antioxidant enzymes is closely related to the antioxidant capacity of plants.
Plant antioxidant enzyme systems exhibit differential responses to stress at various growth stages and development phases [46]. In this study, it was observed that two plant antioxidant enzyme systems demonstrated greater stability during the high-growth season, displaying more rapid and persistent responses to stress. Enzymes in plants are normally made up of proteins, and as ambient temperatures rise during the high-growth season, plant photosynthesis increases [47], and the rate of protein production from photosynthesis is faster. This may explain why plant antioxidant enzyme systems demonstrate heightened activity and stability during the high-growth season [48].
In the conducted experiment, the CAT activity of Iris germanica L. was notably elevated, whereas the POD activity of Portulaca grandiflora Hook. was comparatively heightened. It is worth mentioning that Iris germanica L. is categorized as a C3 plant, while Portulaca grandiflora Hook. is classified as a C4 plant [35]. The distinction in photosynthesis mechanisms between C3 and C4 plants becomes more pronounced when they are exposed to similar stress stimuli, with C4 plants generally demonstrating higher photosynthetic efficiency compared with that observed in C3 plants [14]. The superior photosynthetic efficiency observed in C4 plants is primarily driven by their capacity to minimize photorespiration, a process that becomes markedly amplified in C3 plants under environmental stress [49]. This adaptive advantage stems from the carbon-concentrating mechanism (CCM), a biochemical strategy that spatially segregates photosynthetic phases to elevate CO2 concentrations around ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBisCO) [50]. By suppressing RuBisCO’s oxygenation activity, the CCM effectively enhances carboxylation efficiency, thereby reducing energy losses associated with photorespiration. This not only bolsters photosynthetic performance under optimal conditions but also confers resilience to abiotic stressors such as drought and salinity [51]. Under mild stress conditions, the variance in antioxidant enzyme profiles between C3 and C4 plants may not be very noticeable. However, a more pronounced disparity in H2O2 content emerges under conditions of increased stress intensity. CAT and POD play complementary roles in alleviating environmental stress, with CAT demonstrating superior efficacy in scavenging high concentrations of H2O2, while POD excels in scenarios involving lower H2O2 concentrations [52]. Moreover, Uzilday et al. [53] observed that the increase in POD activity in C4 plants under drought stress was approximately twofold that of C3 plants, with the highest concentration of H2O2 detected in C3 plants based on experimental. This observation helps explain the relatively elevated CAT activity in Iris germanica L. and the comparatively heightened POD activity in Portulaca grandiflora Hook. during the experiment.

4.2. Nitrogen Storage in Iris germanica L. and Portulaca grandiflora Hook. Under Nitrogen-Laden PM2.5 Stress

In this study, the NH4NO3 fumigation experiment was utilized to simulate the effects of atmospheric nitrogen deposition via PM originating from NH4NO3 solution, which can infiltrate plants through the stomata of leaves [54,55] or permeate the plant surface [56]. Inorganic nitrogenous salts enter the plant system, initially being absorbed and transported by the plant and subsequently transforming into organic nitrogen through assimilation [57].
In most experiments, heightened nitrogen-laden PM stress levels have been linked to a decrease in the nitrogen/weight ratio in plants. Generally, as the external nitrogen availability increases, the plant nitrogen/weight ratio tends to elevate [58]. Optimal increases in nitrogen levels can enhance plant N-assimilating enzyme activities [59], while excessively high nitrogen levels may lead to reduced activities of certain N-assimilating enzymes [60], resulting in decreased plant nitrogen content and affect carbon and nitrogen balance in plants [61]. Several studies have documented nitrogen loss from aboveground plant parts upon excessive fertilizer application [62,63,64,65], frequently attributed to nitrogen translocation from aboveground to roots or soil (e.g., nitrate leaching), leaching from leaves, and emission into the atmosphere as gases (e.g., N2O). By contrast, the nitrogen/weight ratio of Portulaca grandiflora Hook. exhibited no significant decrease under severe conditions. This resilience to inorganic nitrogen-laden fumigation in Portulaca grandiflora Hook. suggests a less pronounced response compared to that of Iris germanica L. Building on our research group’s previous experimental work with Portulaca grandiflora Hook. [35], demonstrate that the species employs a compensatory ’over-photosynthesis’ mechanism to counteract reduced leaf nitrogen mass. Fumigation of nitrogen-laden PM2.5 stimulated an increase in stomatal conductance [66,67], contributing to an increase in nitrogen influx through the pores and the sub-pores [68]. This resulted in a temporary but large increase in nitrogen concentration in the gas exchange space in direct contact with chloroplasts. This plasticity of nitrogen storage under PM2.5 stress is consistent with the adaptive strategies of Portulaca grandiflora Hook. to salinity. Under salinity stress (400 mM NaCl), Portulaca grandiflora Hook. maintains nitrogen assimilation efficiency through sustained K+ transport from roots to leaves, stabilizing ion homeostasis and minimizing oxidative damage [31]. In contrast, Iris germanica L. exhibits severe inhibition of nitrogen uptake at 100 mM NaCl, associated with ROS accumulation and reduced SOD activity [69]. These findings highlight that stress tolerance mechanisms are stressor-specific, while Portulaca grandiflora Hook. leverages ion transport for salinity and metabolic plasticity for PM2.5, Iris germanica L.’s sensitivity across stressors stems from its limited antioxidant redundancy and C3 metabolic constraints.
After a month of continuous fumigation with fine PM containing inorganic nitrogen, the results revealed a significantly higher N ratio in all organs of Portulaca grandiflora Hook. compared with that in Iris germanica L. Portulaca grandiflora Hook. may use its higher nitrogen uptake and utilization capacity to convert more inorganic nitrogen into organic nitrogen and store it in its organs, thus responding to stress by increasing nitrogen accumulation, whereas Iris germanica L. may have relatively low nitrogen levels in its organs due to growth restriction or impaired nitrogen metabolism. Morphologically, the main assimilation process of NO3− uptake in herbaceous plants mainly occurs in the chloroplasts, the leaf mesophyll cells of the C4 plant Portulaca grandiflora Hook. exhibit larger and more numerous chloroplasts, in contrast to the smaller vascular sheath cells lacking chloroplasts in the C3 plant Iris germanica L. [70]. Furthermore, enzymes related to nitrogen absorption are predominantly located in the chloroplasts of leaf mesophyll cells [71]. The abundant and large chloroplasts in Portulaca grandiflora Hook. enhance its nitrogen assimilation efficiency, supported by the C4 plant-specific pathway, maintaining increased photosynthetic efficiency and carbon assimilation rates at lower CO2 concentrations [72], thereby augmenting nitrogen uptake and storage capacity [73].

5. Conclusions

Significant disparities in the antioxidant defense mechanisms utilized by Iris germanica L. and Portulaca grandiflora Hook. when confronted with nitrogen-laden PM stress. Iris germanica L. primarily employed CAT to mitigate reactive oxygen species, specifically H2O2, whereas Portulaca grandiflora Hook. primarily depended on POD for H2O2 scavenging. Moreover, Portulaca grandiflora Hook. demonstrated superior preservation of enzyme activities under extended fumigation treatments compared with that in Iris germanica L., indicating a more robust and sustained response to stress. The plant antioxidant enzyme systems exhibited enhanced consistency throughout the high-growth season and responses to stress in both species. The differing adaptive mechanisms employed by Iris germanica L. and Portulaca grandiflora Hook. in response to excess nitrogen led to the observation that severe particulate stress often resulted in decreased nitrogen/weight ratios in Iris germanica L., while Portulaca grandiflora Hook. showed no significant decrease in nitrogen ratios under similar stress conditions. Furthermore, Portulaca grandiflora Hook. demonstrated an ability to adapt to elevated ambient nitrogen concentrations, allowing for moderate nitrogen accumulation within its tissues, thereby enhancing its nitrogen storage capacity. In conclusion, this study confirms that Portulaca grandiflora Hook. exhibited greater resilience to stress throughout the high-growth season, underscoring its superior capacity to withstand the adverse effects of elevated nitrogen deposition and particulate pollution. Our study provides a clearer understanding of the plant response to pollution, as well as theoretical support for future plant screening. Specifically, the robust antioxidant defense system and nitrogen storage capacity of Portulaca grandiflora Hook. suggest its potential as a priority species for green infrastructure in nitrogen-polluted environments, such as industrial zones or traffic-dense urban areas. Future research should explore the scalability of these adaptive traits under field conditions, including long-term monitoring of nitrogen accumulation dynamics and interactions with other environmental stressors (e.g., heavy metals).

Author Contributions

Conceptualization, S.P., Z.G. and Z.M.; methodology, K.X.; validation, S.P.; formal analysis, K.X., Y.W., R.W. and Z.H.; investigation, K.X., Y.W., R.W. and Z.H.; resources, Z.G. and Z.M.; data curation, Z.G. and Z.M.; writing—original draft, K.X.; writing—review and editing, K.X.; visualization, Y.W., R.W. and Z.H.; supervision, S.P., Z.G. and Z.M.; project administration, Z.G. and Z.M.; funding acquisition, S.P., Z.G. and Z.M. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by the Jiangsu Forestry Science & Technology Innovation and Extension Project (Project No: LYKJ [2022]02 & LYKJ [2022]16), Jiangsu Social Development Project (BE2022792), the National Natural Science Foundation of China (grant numbers 31870506, 32271712).

Data Availability Statement

The raw data supporting the conclusions of this article will be made available by the authors upon request.

Conflicts of Interest

The authors declare no conflicts of interest.

References

  1. Ackerman, D.; Millet, D.B.; Chen, X. Global Estimates of Inorganic Nitrogen Deposition Across Four Decades. Glob. Biogeochem. Cycles 2019, 33, 100–107. [Google Scholar]
  2. Song, C.; Wang, K.; Song, Y.; Zhang, N. Effects of nitrogen deposition on soil respiration in regional forests of the central Yunnan Plateau. J. Nanjing For. Univ. (Nat. Sci. Ed.) 2024. [Google Scholar]
  3. Borer, E.T.; Stevens, C.J. Nitrogen deposition and climate: An integrated synthesis. Trends Ecol. Evol. 2022, 37, 541–552. [Google Scholar]
  4. Hong, W.Y. Meteorological variability and predictive forecasting of atmospheric particulate pollution. Sci. Rep. 2024, 14, 14. [Google Scholar]
  5. Zhao, C.; Peng, S.; Ruan, H.; Zhang, Y. Effects of nitrogen deposition on soil microbes. J. Nanjing For. Univ. (Nat. Sci. Ed.) 2015, 39, 149–155. [Google Scholar]
  6. Stevens, C.J. Nitrogen in the environment. Science 2019, 363, 578–580. [Google Scholar] [PubMed]
  7. Wu, L.; Yue, S.; Shi, Z.; Hu, W.; Chen, J.; Ren, H.; Deng, J.; Ren, L.; Fang, Y.; Yan, H.; et al. Source forensics of inorganic and organic nitrogen using δ15N for tropospheric aerosols over Mt. Tai. npj Clim. Atmos. Sci. 2021, 4, 8. [Google Scholar]
  8. Anas, M.; Liao, F.; Verma, K.K.; Sarwar, M.A.; Mahmood, A.; Chen, Z.; Li, Q.; Zeng, X.; Liu, Y.; Li, Y. Fate of nitrogen in agriculture and environment: Agronomic, eco-physiological and molecular approaches to improve nitrogen use efficiency. Biol. Res. 2020, 53, 47. [Google Scholar]
  9. Noor, H.; Yan, Z.; Sun, P.; Zhang, L.; Ding, P.; Li, L.; Ren, A.; Sun, M.; Gao, Z. Effects of Nitrogen on Photosynthetic Productivity and Yield Quality of Wheat (Triticum aestivum L.). Agronomy 2023, 13, 1448. [Google Scholar] [CrossRef]
  10. Cui, X.; Yue, P.; Wu, W.; Gong, Y.; Li, K.; Misselbrook, T.; Goulding, K.; Liu, X. The Growth and N Retention of Two Annual Desert Plants Varied Under Different Nitrogen Deposition Rates. Front. Plant Sci. 2019, 10, 356. [Google Scholar]
  11. Cun, Z.; Zhang, J.-Y.; Wu, H.-M.; Zhang, L.; Chen, J.-W. High nitrogen inhibits photosynthetic performance in a shade-tolerant and N-sensitive species Panax notoginseng. Photosynth. Res. 2021, 147, 283–300. [Google Scholar] [CrossRef]
  12. Yuan, J.; Peng, M.; Tang, G.; Wang, Y. Fine root production, mortality, and turnover in response to simulated nitrogen deposition in the subtropical Abies georgei (Orr) forest. Sci. Total Environ. 2024, 923, 171404. [Google Scholar] [CrossRef] [PubMed]
  13. Khan, A.; Sun, J.; Zarif, N.; Khan, K.; Jamil, M.A.; Yang, L.; Clothier, B.; Rewald, B. Effects of Increased N Deposition on Leaf Functional Traits of Four Contrasting Tree Species in Northeast China. Plants 2020, 9, 1231. [Google Scholar] [CrossRef]
  14. Zhang, L.; He, X. Nitrogen Utilization Mechanism in C3 and C4 Plants. Chin. Bull. Bot. 2020, 55, 228–239. [Google Scholar]
  15. Niu, S.; Liu, W.; Wan, S. Different growth responses of C3 and C4 grasses to seasonal water and nitrogen regimes and competition in a pot experiment. J. Exp. Bot. 2008, 59, 1431–1439. [Google Scholar] [CrossRef]
  16. Lin, G.; Chen, H.; Chen, B.; Yang, Y. Characterization of temporal PM2.5, nitrate, and sulfate using deep learning techniques. Atmos. Pollut. Res. 2022, 13, 101260. [Google Scholar] [CrossRef]
  17. Xie, M.; Feng, W.; He, S.; Wang, Q.G. Seasonal variations, temperature dependence, and sources of size-resolved PM components in Nanjing, east China. J. Environ. Sci. 2022, 121, 175–186. [Google Scholar] [CrossRef]
  18. Luo, W.; Wang, X.; Sardans, J.; Wang, Z.; Dijkstra, F.A.; Lü, X.-T.; Peñuelas, J.; Han, X. Higher capability of C3 than C4 plants to use nitrogen inferred from nitrogen stable isotopes along an aridity gradient. Plant Soil 2018, 428, 93–103. [Google Scholar] [CrossRef]
  19. Xu, X.; Xia, J.; Gao, Y.; Zheng, W. Additional focus on particulate matter wash-off events from leaves is required: A review of studies of urban plants used to reduce airborne particulate matter pollution. Urban For. Urban Green. 2020, 48, 126559. [Google Scholar] [CrossRef]
  20. Lu, T.; Lin, X.; Chen, J.; Huang, D.; Li, M. Atmospheric particle retention capacity and photosynthetic responses of three common greening plant species under different pollution levels in Hangzhou. Glob. Ecol. Conserv. 2019, 20, e00783. [Google Scholar] [CrossRef]
  21. Nawaz, M.F.; Rashid, M.H.U.; Saeed-Ur-Rehman, M.; Gul, S.; Farooq, T.H.; Sabir, M.A.; Iftikhar, J.; Abdelsalam, N.R.; Dessoky, E.S.; Alotaibi, S.S. Effect of Dust Types on the Eco-Physiological Response of Three Tree Species Seedlings: Eucalyptus camaldulensis, Conocarpus erectus and Bombax ceiba. Atmosphere 2022, 13, 1010. [Google Scholar] [CrossRef]
  22. Singh, S.; Pandey, B.; Roy, L.B.; Shekhar, S.; Singh, R.K. Tree responses to foliar dust deposition and gradient of air pollution around opencast coal mines of Jharia coalfield, India: Gas exchange, antioxidative potential and tolerance level. Environ. Sci. Pollut. Res. 2020, 28, 8637–8651. [Google Scholar] [CrossRef] [PubMed]
  23. Peng, L.; Yang, Z.; Liu, M.; Huang, M.; Zhang, C.; Yongli, D. Relationship between Net Photosynthetic Rate of Green Plants and Air Pollutants. Ecol. Environ. Sci. 2015, 24, 1166–1170. [Google Scholar] [CrossRef]
  24. He, C.; Zhang, Z.F.; Wang, Q.; Zhang, Y.P.; Wei, C.H.; Zhang, L.; Li, Z.; Yu, H.Q.; Chang, C.Y.; Zhang, Y.L. Evaluation of air pollution tolerance index of urban roadside young leaf and the correlation with its capturing capacity for water-insoluble fine particulate matters. Air Qual. Atmos. Health 2024, 17, 2675–2691. [Google Scholar] [CrossRef]
  25. Mo, L.; Ma, Z.Y.; Xu, Y.S.; Sun, F.B.; Lun, X.X.; Liu, X.H.; Chen, J.G.; Yu, X.X. Assessing the Capacity of Plant Species to Accumulate Particulate Matter in Beijing, China. PLoS ONE 2015, 10, e0140664. [Google Scholar] [CrossRef]
  26. Singh, S.K.; Singh, R.K.; Singh, R.S.; Pal, D.; Singh, K.K.; Singh, P.K. Screening potential plant species for arresting particulates in Jharia coalfield, India. Sustain. Environ. Res. 2019, 29, 37. [Google Scholar] [CrossRef]
  27. Yuan, Y.; Sun, Y.; Zhao, Y.; Liu, C.; Chen, X.; Li, F.; Bao, J. Identification of Floral Scent Profiles in Bearded Irises. Molecules 2019, 24, 1773. [Google Scholar] [CrossRef]
  28. Budiawan, A.; Purwanto, A.; Puradewa, L.; Cahyani, E.D.; Purwaningsih, C.E. Wound healing activity and flavonoid contents of purslane (Portulaca grandiflora) of various varieties. RSC Adv. 2023, 13, 9871–9877. [Google Scholar] [CrossRef]
  29. Yousefsani, B.S.; Boozari, M.; Shirani, K.; Jamshidi, A.; Dadmehr, M. A review on phytochemical and therapeutic potential of Iris germanica. J. Pharm. Pharmacol. 2021, 73, 611–625. [Google Scholar] [CrossRef]
  30. Zhang, J.W.; Huang, D.Z.; Zhao, X.J.; Zhang, M. Evaluation of drought resistance and transcriptome analysis for the identification of drought-responsive genes in. Sci. Rep. 2021, 11, 16308. [Google Scholar] [CrossRef]
  31. Borsai, O.; Hassan, M.A.; Negrușier, C.; Raigón, M.D.; Boscaiu, M.; Sestraș, R.E.; Vicente, O. Responses to Salt Stress in Portulaca: Insight into Its Tolerance Mechanisms. Plants 2020, 9, 1660. [Google Scholar] [CrossRef] [PubMed]
  32. Zhao, Z.P.; Li, T.Y.; Cheng, Y.F.; Wang, F.J.; Zhao, X.J. Morphological and metabolic responses of four cultivars under salinity stress. Sci. Hortic. 2021, 281, 109960. [Google Scholar]
  33. Sun, L.Y.; Li, B.; Ma, Y.C.; Wang, J.Y.; Xiong, Z.Q. Year-Round Atmospheric Wet and Dry Deposition of Nitrogen and Phosphorus on Water and Land Surfaces in Nanjing, China. Water Environ. Res. 2013, 85, 514–521. [Google Scholar]
  34. JI, Y.; Zhang, J.; Song, J. Analysis of PM2.5 Pollution in Jiangsu Province and Determination of Building Outdoor PM2.5 Design Concentration. J. Change Univ. (Nat. Sci. Ed.) 2018, 30, 53–58. [Google Scholar]
  35. Ge, Z.; Ma, Y.; Xing, W.; Wu, Y.; Peng, S.; Mao, L.; Miao, Z. Inorganic Nitrogen-Containing Aerosol Deposition Caused “Excessive Photosynthesis” of Herbs, Resulting in Increased Nitrogen Demand. Plants 2022, 11, 2225. [Google Scholar] [CrossRef]
  36. Giannopolitis, C.N.; Ries, S.K. Superoxide dismutases: I. Occurrence in higher plants. Plant Physiol. 1977, 59, 309–314. [Google Scholar] [PubMed]
  37. Zheng, X.; Van Huystee, R. Peroxidase-regulated elongation of segments from peanut hypocotyls. Plant Sci. 1992, 81, 47–56. [Google Scholar]
  38. Change, B.; Maehly, A. Assay of catalases and peroxidase. Methods Enzym. 1955, 2, 764–775. [Google Scholar]
  39. Mauchly, J.W. Significance Test for Sphericity of a Normal n-Variate Distribution. Ann. Math. Stat. 1940, 11, 204–209. [Google Scholar] [CrossRef]
  40. Nadarajah, K.K. ROS Homeostasis in Abiotic Stress Tolerance in Plants. Int. J. Mol. Sci. 2020, 21, 5208. [Google Scholar] [CrossRef]
  41. Lal, M.K.; Tiwari, R.K.; Altaf, M.A.; Kumar, A.; Kumar, R. Abiotic and biotic stress in horticultural crops: Insight into recent advances in the underlying tolerance mechanism. Front. Plant Sci. 2023, 14, 1212982. [Google Scholar]
  42. He, A.; Dean, J.M.; Lodhi, I.J. Peroxisomes as cellular adaptors to metabolic and environmental stress. Trends Cell Biol. 2021, 31, 656–670. [Google Scholar] [PubMed]
  43. García, G.; Clemente-Moreno, M.J.; Díaz-Vivancos, P.; García, M.; Hernández, J.A. The Apoplastic and Symplastic Antioxidant System in Onion: Response to Long-Term Salt Stress. Antioxidants 2020, 9, 67. [Google Scholar] [CrossRef]
  44. Ramzan, M.; Gillani, M.; Shah, A.A.; Shah, A.N.; Kauser, N.; Jamil, M.; Ahmad, R.T.; Ullah, S. Triticum aestivum: Antioxidant gene profiling and morpho-physiological studies under salt stress. Mol. Biol. Rep. 2023, 50, 2569–2580. [Google Scholar]
  45. Verma, D.; Kaushal, N.; Balhara, R.; Singh, K. Genome-wide analysis of Catalase gene family reveal insights into abiotic stress response mechanism in Brassica juncea and B. rapa. Plant Sci. 2023, 330, 111620. [Google Scholar] [CrossRef]
  46. Trivedi, V.L.; Nautiyal, M.C.; Sati, J.; Attri, D.C. Antioxidant enzyme activities in male and female plants of Hippophae salicifolia D. Don in different pheno-phases. Acta Physiol. Plant. 2020, 42, 64. [Google Scholar]
  47. Yu, L.; Song, M.; Xia, Z.; Korpelainen, H.; Niinemets, Ü.; Li, C. Elevated temperature differently affects growth, photosynthetic capacity, nutrient absorption and leaf ultrastructure of Abies faxoniana and Picea purpurea under intra- and interspecific competition. Tree Physiol. 2019, 39, 1342–1357. [Google Scholar]
  48. Ye, W.; Xiong, D.; Yang, Z.; Zhang, Q.; Liu, X.; Gao, Y.; Xu, C.; Yang, Y. Effects of atmospheric warming on physiological characteristics of leaves and fine roots of Cunninghamia lanceolata saplings. Acta Ecol. Sin. 2020, 40, 7681–7689. [Google Scholar]
  49. Sonmez, M.C.; Ozgur, R.; Uzilday, B.; Turkan, I.; Ganie, S.A. Redox regulation in C3 and C4 plants during climate change and its implications on food security. Food Energy Secur. 2023, 12, e387. [Google Scholar]
  50. Burlacot, A.; Peltier, G. Energy crosstalk between photosynthesis and the algal CO2-concentrating mechanisms. Trends Plant Sci. 2023, 28, 795–807. [Google Scholar]
  51. Epstein, H.E.; Gill, R.A.; Paruelo, J.M.; Lauenroth, W.K.; Jia, G.J.; Burke, I.C. The relative abundance of three plant functional types in temperate grasslands and shrublands of North and South America: Effects of projected climate change. J. Biogeogr. 2002, 29, 875–888. [Google Scholar] [CrossRef]
  52. Nayyar, H.; Gupta, D. Differential sensitivity of C3 and C4 plants to water deficit stress: Association with oxidative stress and antioxidants. Environ. Exp. Bot. 2006, 58, 106–113. [Google Scholar] [CrossRef]
  53. Uzilday, B.; Turkan, I.; Sekmen, A.H.; Ozgur, R.; Karakaya, H.C. Comparison of ROS formation and antioxidant enzymes in (C3) and (C4) under drought stress. Plant Sci. 2012, 182, 59–70. [Google Scholar] [CrossRef]
  54. Gao, P.; Xue, P.; Dong, J.; Zhang, X.; Sun, H.; Geng, L.; Luo, S.; Zhao, J.; Liu, W. Contribution of PM2.5-Pb in atmospheric fallout to Pb accumulation in Chinese cabbage leaves via stomata. J. Hazard. Mater. 2021, 407, 124356. [Google Scholar] [CrossRef]
  55. Zhai, S.; Jacob, D.J.; Wang, X.; Liu, Z.; Wen, T.; Shah, V.; Li, K.; Moch, J.M.; Bates, K.H.; Song, S.; et al. Control of particulate nitrate air pollution in China. Nat. Geosci. 2021, 14, 389–395. [Google Scholar] [CrossRef]
  56. Hu, Y.; Peuke, A.D.; Zhao, X.; Yan, J.; Li, C. Effects of simulated atmospheric nitrogen deposition on foliar chemistry and physiology of hybrid poplar seedlings. Plant Physiol. Biochem. 2019, 143, 94–108. [Google Scholar] [CrossRef] [PubMed]
  57. He, X.; Chi, Q.; Cai, Z.; Cheng, Y.; Zhang, J.; Müller, C. 15N tracing studies including plant N uptake processes provide new insights on gross N transformations in soil-plant systems. Soil Biol. Biochem. 2020, 141, 107666. [Google Scholar] [CrossRef]
  58. Yuan, Z.Y.; Chen, H.Y.H. Negative effects of fertilization on plant nutrient resorption. Ecology 2015, 96, 373–380. [Google Scholar] [CrossRef]
  59. Abid, M.; Tian, Z.; Ata-Ul-Karim, S.T.; Cui, Y.; Liu, Y.; Zahoor, R.; Jiang, D.; Dai, T. Nitrogen Nutrition Improves the Potential of Wheat (Triticum aestivum L.) to Alleviate the Effects of Drought Stress during Vegetative Growth Periods. Front. Plant Sci. 2016, 7, 981. [Google Scholar] [CrossRef]
  60. Wei, S.; Wang, X.; Shi, D.; Li, Y.; Zhang, J.; Liu, P.; Zhao, B.; Dong, S. The mechanisms of low nitrogen induced weakened photosynthesis in summer maize (Zea mays L.) under field conditions. Plant Physiol. Biochem. 2016, 105, 118–128. [Google Scholar] [CrossRef]
  61. Liu, N.; Feng, Y.; Wei, L.; Liu, F. Responses of plant carbon and nitrogen assimilations to nitrogen addition in a subtropical forest: Canopy addition vs. understory addition. Ecotoxicol. Environ. Saf. 2023, 266, 115545. [Google Scholar] [CrossRef]
  62. Li, Y.; Liu, H.; Huang, G. The Effect of Nitrogen Rates on Yields and Nitrogen Use Efficiencies during Four Years of Wheat–Maize Rotation Cropping Seasons. Agron. J. 2016, 108, 2076–2088. [Google Scholar]
  63. Li, Z.; Wen, X.; Hu, C.; Li, X.; Li, S.; Zhang, X.; Hu, B. Regional simulation of nitrate leaching potential from winter wheat-summer maize rotation croplands on the North China Plain using the NLEAP-GIS model. Agric. Ecosyst. Environ. 2020, 294, 106861. [Google Scholar]
  64. Mancuso, G.; Bencresciuto, G.F.; Lavrnić, S.; Toscano, A. Diffuse Water Pollution from Agriculture: A Review of Nature-Based Solutions for Nitrogen Removal and Recovery. Water 2021, 13, 1893. [Google Scholar] [CrossRef]
  65. Su, W.; Kamran, M.; Xie, J.; Meng, X.; Han, Q.; Liu, T.; Han, J. Shoot and root traits of summer maize hybrid varieties with higher grain yields and higher nitrogen use efficiency at low nitrogen application rates. PeerJ 2019, 7, e7294. [Google Scholar] [PubMed]
  66. Green, T.H.; Mitchell, R.J. Effects of nitrogen on the response of loblolly pine to water stress I. Photosynthesis and stomatal conductance. New Phytol. 1992, 122, 627–633. [Google Scholar]
  67. Shen, H.; Dong, S.K.; DiTommaso, A.; Li, S.; Xiao, J.N.; Yang, M.Y.; Zhang, J.; Gao, X.X.; Xu, Y.D.; Zhi, Y.L.; et al. Eco-physiological processes are more sensitive to simulated N deposition in leguminous forbs than non-leguminous forbs in an alpine meadow of the Qinghai-Tibetan Plateau. Sci. Total Environ. 2020, 744, 140612. [Google Scholar] [PubMed]
  68. Ion, A.C.; Vermeylen, R.; Kourtchev, I.; Cafmeyer, J.; Chi, X.; Gelencsér, A.; Maenhaut, W.; Claeys, M. Polar organic compounds in rural PM2.5 aerosols from K-puszta, Hungary, during a 2003 summer field campaign: Sources and diel variations. Atmos. Chem. Phys. 2005, 5, 1805–1814. [Google Scholar]
  69. Lu, J.; Zhong, Y. Effects of Exogenous GA3 and SA on Salt Resistance of Iris germanica. Acta Agric. Jiangxi 2011, 23, 49–56. [Google Scholar]
  70. Reeves, G.; Grangé-Guermente, M.J.; Hibberd, J.M. Regulatory gateways for cell-specific gene expression in C4 leaves with Kranz anatomy. J. Exp. Bot. 2016, 68, 107–116. [Google Scholar]
  71. Majeran, W.; Cai, Y.; Sun, Q.; van Wijk, K.J. Functional Differentiation of Bundle Sheath and Mesophyll Maize Chloroplasts Determined by Comparative Proteomics. Plant Cell 2005, 17, 3111–3140. [Google Scholar] [CrossRef] [PubMed]
  72. Sage, R.F.; Monson, R.K.; Ehleringer, J.R.; Adachi, S.; Pearcy, R.W. Some like it hot: The physiological ecology of C4 plant evolution. Oecologia 2018, 187, 941–966. [Google Scholar] [CrossRef] [PubMed]
  73. Togawa-Urakoshi, Y.; Ueno, O. Photosynthetic nitrogen- and water-use efficiencies in C3 and C4 subtype grasses grown under two nitrogen supply levels. Plant Prod. Sci. 2021, 25, 183–194. [Google Scholar] [CrossRef]
Horticulturae 11 00337 g001
Figure 1. Schematic diagram of the device structure of the experimental device (Patent No: ZL201621111648.7, China) [35]. Note: 1 represents test plant chamber, 2 represents concentration-monitoring port, 3-1 represents vertical fan, 3-2 represents horizontal fan, 4 represents aerosol generator, 5 represents rubber hose, 6 represents PVC tube, and 7 represents alkaline absorber.
Figure 1. Schematic diagram of the device structure of the experimental device (Patent No: ZL201621111648.7, China) [35]. Note: 1 represents test plant chamber, 2 represents concentration-monitoring port, 3-1 represents vertical fan, 3-2 represents horizontal fan, 4 represents aerosol generator, 5 represents rubber hose, 6 represents PVC tube, and 7 represents alkaline absorber.
Horticulturae 11 00337 g001
Horticulturae 11 00337 g002
Figure 2. Effect of fumigation time on superoxide dismutase (SOD) of Iris germanica L. and Portulaca grandiflora Hook. with different growth stages (n = 8). The error bars are standard errors. (a,c) represent April (low-growth season), and (b,d) represent July (high-growth season). Different lowercase letters indicate the significant (p < 0.05) difference in SOD activity of plants at the same fumigation concentration and at different fumigation times.
Figure 2. Effect of fumigation time on superoxide dismutase (SOD) of Iris germanica L. and Portulaca grandiflora Hook. with different growth stages (n = 8). The error bars are standard errors. (a,c) represent April (low-growth season), and (b,d) represent July (high-growth season). Different lowercase letters indicate the significant (p < 0.05) difference in SOD activity of plants at the same fumigation concentration and at different fumigation times.
Horticulturae 11 00337 g002
Horticulturae 11 00337 g003
Figure 3. Effect of fumigation time on peroxidase (POD) of Iris germanica L. and Portulaca grandiflora Hook. with different growth stages (n = 8). The error bars are standard errors. (a,c) represent April (low-growth season), and (b,d) represent July (high-growth season). Different lowercase letters indicate the significant (p < 0.05) difference in POD activity of plants at the same fumigation concentration and at different fumigation times.
Figure 3. Effect of fumigation time on peroxidase (POD) of Iris germanica L. and Portulaca grandiflora Hook. with different growth stages (n = 8). The error bars are standard errors. (a,c) represent April (low-growth season), and (b,d) represent July (high-growth season). Different lowercase letters indicate the significant (p < 0.05) difference in POD activity of plants at the same fumigation concentration and at different fumigation times.
Horticulturae 11 00337 g003
Horticulturae 11 00337 g004
Figure 4. Effect of fumigation time on catalase (CAT) of Iris germanica L. and Portulaca grandiflora Hook. with different growth stages (n = 8). The error bars are standard errors. (a,c) represent April (low-growth season), and (b,d) represent July (high-growth season). Different lowercase letters indicate the significant (p < 0.05) difference in CAT activity of plants at the same fumigation concentration and at different fumigation times.
Figure 4. Effect of fumigation time on catalase (CAT) of Iris germanica L. and Portulaca grandiflora Hook. with different growth stages (n = 8). The error bars are standard errors. (a,c) represent April (low-growth season), and (b,d) represent July (high-growth season). Different lowercase letters indicate the significant (p < 0.05) difference in CAT activity of plants at the same fumigation concentration and at different fumigation times.
Horticulturae 11 00337 g004
Horticulturae 11 00337 g005
Figure 5. Effects of fumigation concentration on SOD, POD, and CAT in Iris germanica L. and Portulaca grandiflora Hook. at different growth stages (Duncan’s test, n = 40, p < 0.05). The error bars are standard errors. (A,C,E) represent April (low-growth season), and (B,D,F) represent July (high-growth season). Different uppercase and lowercase letters indicate the significant (p < 0.05) difference in three antioxidant enzymes activities (SOD, POD, and CAT) in Iris germanica L. and Portulaca grandiflora Hook., respectively, under varying fumigation concentrations.
Figure 5. Effects of fumigation concentration on SOD, POD, and CAT in Iris germanica L. and Portulaca grandiflora Hook. at different growth stages (Duncan’s test, n = 40, p < 0.05). The error bars are standard errors. (A,C,E) represent April (low-growth season), and (B,D,F) represent July (high-growth season). Different uppercase and lowercase letters indicate the significant (p < 0.05) difference in three antioxidant enzymes activities (SOD, POD, and CAT) in Iris germanica L. and Portulaca grandiflora Hook., respectively, under varying fumigation concentrations.
Horticulturae 11 00337 g005
Horticulturae 11 00337 g006
Figure 6. Effects of different growth stages and fumigation concentrations on the weight ratio of N in different organs of Iris germanica L. and Portulaca grandiflora Hook. (Duncan’s test, n = 4). The error bars are standard errors. (A) represents the low-growth season, and (B) represents the high-growth season. In (A,B), different lowercase letters indicate significant (p < 0.05) differences in nitrogen ratios between different concentrations in the same organ of the same plant, and different uppercase letters indicate significant (p < 0.05) differences in nitrogen ratios between different organs at the same concentration.
Figure 6. Effects of different growth stages and fumigation concentrations on the weight ratio of N in different organs of Iris germanica L. and Portulaca grandiflora Hook. (Duncan’s test, n = 4). The error bars are standard errors. (A) represents the low-growth season, and (B) represents the high-growth season. In (A,B), different lowercase letters indicate significant (p < 0.05) differences in nitrogen ratios between different concentrations in the same organ of the same plant, and different uppercase letters indicate significant (p < 0.05) differences in nitrogen ratios between different organs at the same concentration.
Horticulturae 11 00337 g006
Table 1. ANOVA analysis for the effects of growth stage, plant species, fumigation concentration, fumigation time, and their interactions on plant antioxidant enzyme activities.
Table 1. ANOVA analysis for the effects of growth stage, plant species, fumigation concentration, fumigation time, and their interactions on plant antioxidant enzyme activities.
IndexesSODPODCAT
FPFPFP
Stage (S)13.496***389.110***101.999***
Plant (P)9.675**0.343NS3545.908***
Concentration (C)115.293***15.283***26.914***
Time (T)104.232***185.639***442.188***
S × P161.042***221.821***1.303NS
S × C7.706***0.961NS16.166***
S × T41.691***151.212***78.761***
P × C12.998***21.516***45.363***
P × T42.304***59.682***54.925***
C × T5.098***5.749***19.204***
S × P × C0.695NS15.087***31.297***
S × P × T23.368***23.783***14.019***
S × C × T4.969***5.499***15.425***
P × C × T4.846***10.407***32.018***
S × P × C × T2.351**6.046***33.128***
Abbreviations: SOD, POD, CAT for superoxide dismutase, peroxidase, and catalase, respectively. Bold characters indicate significant differences. **, and *** p values are less than 0.01, and 0.001, respectively. NS is not statistically significant.
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Xiao, K.; Wang, Y.; Wang, R.; Hu, Z.; Peng, S.; Miao, Z.; Ge, Z. Physiological and Biochemical Adaptation of Common Garden Plants to Inorganic Nitrogen-Laden Fine Particulate Matter Stress. Horticulturae 2025, 11, 337. https://doi.org/10.3390/horticulturae11030337

AMA Style

Xiao K, Wang Y, Wang R, Hu Z, Peng S, Miao Z, Ge Z. Physiological and Biochemical Adaptation of Common Garden Plants to Inorganic Nitrogen-Laden Fine Particulate Matter Stress. Horticulturae. 2025; 11(3):337. https://doi.org/10.3390/horticulturae11030337

Chicago/Turabian Style

Xiao, Keqin, Yiying Wang, Rongkang Wang, Zhanpeng Hu, Sili Peng, Zimei Miao, and Zhiwei Ge. 2025. "Physiological and Biochemical Adaptation of Common Garden Plants to Inorganic Nitrogen-Laden Fine Particulate Matter Stress" Horticulturae 11, no. 3: 337. https://doi.org/10.3390/horticulturae11030337

APA Style

Xiao, K., Wang, Y., Wang, R., Hu, Z., Peng, S., Miao, Z., & Ge, Z. (2025). Physiological and Biochemical Adaptation of Common Garden Plants to Inorganic Nitrogen-Laden Fine Particulate Matter Stress. Horticulturae, 11(3), 337. https://doi.org/10.3390/horticulturae11030337

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