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Article

Photosynthetic Performance and Phytoremediation Potential of Narrow Crown Black-Cathay Poplar Under Combined Cadmium and Phenol Pollution

by
Huimei Tian
1,2,
Kaixin Zheng
1,2,
Qiyun Lu
1,2,
Siyuan Sun
1,2,
Chuanrong Li
1,2,* and
Huicheng Xie
1,2,*
1
Research Center for Forest Carbon Neutrality Engineering of Shandong Higher Education Institutions, Taian 271018, China
2
College of Forestry, Shandong Agricultural University, Taian 271018, China
*
Authors to whom correspondence should be addressed.
Forests 2025, 16(10), 1531; https://doi.org/10.3390/f16101531
Submission received: 4 September 2025 / Revised: 25 September 2025 / Accepted: 29 September 2025 / Published: 30 September 2025
(This article belongs to the Special Issue Physiological Mechanisms of Plant Responses to Environmental Stress)
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Abstract

Heavy metal pollutants and organic contaminants often co-exist in the environment, posing significant ecological risks due to their combined toxicity. Phytoremediation, a plant-based biotechnology, offers a promising solution for pollutant removal. This study investigated the potential cadmium (Cd) removal capacity of Narrow Crown Black-Cathay poplar (Populus × canadensis Moench × Populus simonii Carr. f. fastigiata Schneid.) under combined Cd-phenol stress. The results showed that the combined stress synergistically inhibited the photosynthetic physiological characteristics, with an inhibition rate up to 54.0%, significantly higher than that under single stress (p < 0.05). Cd accumulation varied markedly among plant organs, following the order: root (ranging from 4000.2 to 9277.0 mg/kg) > stems (ranging from 96.0 to 383.6 mg/kg) > leaf (ranging from 10.3 to 40.1 mg/kg). Phenol enhanced Cd absorption and enrichment in the roots by up to 1.8 times but reduced its translocation to aboveground parts by 37.8–40.0%. Notably, at low Cd concentrations, the Cd removal efficiency under combined stress (26.0%) was substantially higher than under single Cd stress (6.6%). In contrast, biomass, tolerance index, and root–shoot ratio were slightly affected in all treatments (p > 0.05). These findings demonstrate that Narrow Crown Black-Cathay poplar is a suitable candidate for the short-term remediation of Cd in environments co-contaminated with cadmium and phenol.

1. Introduction

The pollution arising from industrial and agricultural activities is inherently complex, characterized by the frequent co-occurrence of heavy metals and organic compounds in environmental matrices such as soil, water, and sediments [1,2,3,4,5,6,7,8]. Compared with single contamination, this coexistence often gives rise to multifaceted interactions—comprising synergistic, antagonistic, or additive effects—that significantly change environmental behavior, bioavailability, and toxicological impacts of pollutants [9,10,11,12,13]. For instance, recent studies have confirmed that combined pollution can induce synergistic cytotoxic effects, leading to a significantly greater inhibition of plant growth and physiological damage than the sum of individual pollutants [13]. Furthermore, the biodegradation of organic contaminants was found to be significantly minimized in soil in the presence of trace metals [14,15]. Consequently, these dynamic interactions complicate pollution management, as traditional risk assessments based on single pollutants often fail to capture the actual ecological risks posed by such complex contaminant mixtures.
Among the various combinations of co-pollutants, cadmium (Cd) and phenol have been identified as prevalent and hazardous in ecosystems. Cd is a persistent, non-degradable heavy metal that accumulates in soils and bio-magnifies through trophic levels. It disrupts cellular functions by replacing essential elements in enzymes and inducing oxidative stress in both plants and animals [16,17,18,19,20,21,22]. As a water-soluble organic pollutant, phenol contaminates aquatic and terrestrial systems due to its low biodegradability, impairing photosynthesis in plants, triggering reactive oxygen species (ROS) mediated oxidative damage, causing protein denaturation and organ toxicity, and exacerbating heavy metal toxicity through ligand-promoted uptake [23,24,25,26]. Critically, their coexistence results in complex interactions that pose risks to both flora and fauna, affecting physiological processes and ecosystem stability. For instance, phenol has been shown to enhance the bioavailability of Cd through the formation of soluble complexes, while Cd, in turn, can inhibit the microbial degradation of phenol, thereby prolonging its environmental persistence.
Conventional physiochemical methods have been widely applied to remediate single cadmium or phenol combined pollution [17,27]. However, these techniques are often hampered by high operational costs, substantial energy consumption, and the potential for secondary contamination (e.g., leaching of stabilized pollutants or chemical additives), constraining their large-scale and long-term applicability [6]. In contrast, solar-driven phytoremediation is an eco-sustainable alternative with minimal secondary impact [13,28,29,30]; woody plants, with greater biomass, extensive root systems, and longer lifespans, outperform herbaceous species in heavy metal remediation [31,32,33]. For example, poplars and willows in Central European polluted sites accumulate high heavy metal concentrations in above- and below-ground tissues [34], and Populus/Salix species rely on robust antioxidant systems and intracellular metal sequestration for tolerance [35]. This approach also preserves soil structure and fertility for ecological restoration. Its utility is particularly promising for combined pollution scenarios, as selected plant species have been observed to concurrently uptake metals and metabolize organic compounds through enzymatic degradation, sophisticated internal defense mechanisms, and rhizospheric interactions [13,36,37,38,39,40,41]. For instance, Medicago sativa L. (alfalfa) has demonstrated significant potential for remediating soil co-contaminated with Cd and pyrene, achieving high removal efficiency while activating complex antioxidant defense mechanisms [13]. Similarly, Eichhornia crassipes (water hyacinth) exhibited enhanced Cr(VI) uptake in the presence of phenol due to ligand-induced metal mobilization [42], and Lemna minuta Kunth has been proven to be capable of efficiently removing both Cr(VI) and phenol from aqueous solutions [5].
The efficacy of phytoremediation is governed by both the bioavailability of the pollutants and key functional traits of the plant species employed. Ideal candidates possess high photosynthetic potential, high biomass, an extended root system, high and stable water use efficiency (WUE), and the ability to translocate metals to the aerial parts [34,43,44,45,46]. In this context, tree species within the genus Populus have emerged as highly promising candidates and are characterized by rapid growth, deep root systems, high biomass production, and a well-documented capacity for metal accumulation and translocation [47,48,49,50]. Hydroponic studies have underscored their remarkable tolerance to heavy metal stress and their effectiveness in decontaminating polluted waters, with removal rates reaching approximately 50% for metals like copper [47]. However, while the phytoremediation potential of poplars for single or mixed heavy metal pollution is well-established, their response to the more complex and environmentally relevant scenario of combined heavy metal and organic pollutant stress—particularly phenol—remains poorly understood. This constitutes a critical knowledge gap, given that antagonistic or synergistic pollutant interactions can drastically alter their bioavailability, toxicity, and ultimate fate within the plant system.
To address this, the present study investigated the performance of a salt-tolerant poplar clone, Narrow Crown Black-Cathay poplar (Populus × canadensis Moench × Populus simonii Carr. f. fastigiata Schneid.) that is known for its columnar architecture and general resilience to abiotic stresses. We specifically aimed to: (i) quantify the physiological impact of Cd-phenol co-stress on photosynthesis and growth, testing the hypothesis of a synergistic toxic effect; (ii) elucidate the patterns of Cd uptake, partitioning, and translocation across different plant organs (roots, stems, leaves) under the influence of phenol; and (iii) evaluate the overall Cd removal efficiency and tolerance capacity of this clone in both single and combined pollution settings. It is anticipated that the findings of this study will provide a scientific basis for the practical application of poplar trees in the short-term remediation of sites co-contaminated with heavy metals and phenolic compounds.

2. Materials and Methods

2.1. Plant Materials

In early March, healthy branches of Narrow Crown Black-Cathay poplar were cut from the primary lateral branches of a 3-year-old mother tree at a height of 3 to 4 m on the main trunk at the Forestry Experimental Station in South Campus of Shandong Agricultural University (36°06′ N,116°08′ E). These branches were cut into 20 cm long sections and were planted in plastic pots filled with non-polluted fine river sand (6 kg per pot, with pots of height 17 cm and diameter 23 cm). These pots were placed on an open-air balcony and watered with 1 L of tap water every two days to maintain an air relative humidity of approximately 80%. In mid-April, when these cuttings grew into healthy seedlings, they were transplanted into a 250 mL conical flask filled with 200 mL half strength modified Hoagland nutrient solution for further culture under the photoperiod (14 h light/10 h dark) at a temperature of 25 °C during the daytime and 20 °C during the night in a light incubator. The light intensity of the incubator was 200 μmol·m−2·s−1. The flasks were wrapped in a black plastic bag to inhibit algae growth and sealed with a rubber stopper to reduce the evaporation. One liter modified Hoagland nutrient solution contained 4 mL solution A (101 g KNO3, 136 g KH2PO4, 242.25 g MgSO4·7H2O per one liter solution), 5 mL solution B (236 g Ca (NO3)2·4H2O per one liter solution), 4 mL solution C (0.72 g H3BO3, 0.45 g MnCl2·4H2O, 0.055 g ZnSO4·7H2O, 0.02 g CuSO4·5H2O, 0.023 g H2MoO4·H2O per one liter solution), and 4 mL solution D (1.4 g FeSO4·7H2O, 1.9 g EDTA-Na2 per one liter solution).

2.2. Experiment Design

In this experiment, 50% Hoagland nutrient solution containing Cd and phenol was used to treat Narrow Crown Black-Cathay poplar (80 days old) with similar growing conditions, and the stress test was carried out on 30 June. Cd was set at 4 levels: 0, 10, 20 and 40 mg·L−1, respectively, and phenol was selected at 0 and 100 mg·L−1; respectively, eight treatments were conducted in triplicate, as listed in Table 1. All phenol concentrations reported in this study were nominal, as phenol is prone to volatilization. To minimize phenol volatilization as much as possible, the mouths of all conical flasks were sealed by wrapping them with aluminum foil. Furthermore, the hydroponic system utilized a half-strength Hoagland nutrient solution and was maintained in a dark environment (by wrapping the flasks in black plastic bags). During the pollutants’ treatment process, the corresponsive solutions were replaced every 3 days, and 2 rounds was conducted. Photosynthetic indices were measured on the fifth day. After the end of the experiment on the sixth day, the plant biomass and Cd content in various organs were measured. The total experimental duration (6 days) was designed to assess acute stress responses and the initial removal capacity rather than the long-term phytoremediation potential.

2.3. Measurement of Photosynthetic Physiological Parameters

Photosynthetic physiological parameters were determined using the CIRAS-2 photosynthesis system (PP Systems, Hoddesdon, Hertfordshire, UK). Photosynthetic physiological parameters, including net photosynthetic rate (Pn), transpiration rate (Tr), stomatal conductance (GS), intercellular CO2 concentration (Ci), photosynthetically active radiation (PAR), WUE, and light use efficiency (LUE), were measured in the morning on a sunny day (8:30–11:30), where WUE = Pn/Tr and LUE = Pn/PAR. The CO2 concentration, air temperature, relative humidity, and photosynthetic effective radiation were (400 ± 10) μmol·mol−1, 25 °C, 40–45%, and (300 ± 10) μmol·m−2·s−1, respectively.

2.4. Determination of Residual Cd Content in Culture Medium

On the third day, deionized water was added to the Erlenmeyer flask to supplement water evapotranspiration, shaken evenly, and 20 mL aliquot of solution was taken to determine the Cd concentration. The solution samples were centrifuged at 10,000× g for 15 min, and the supernatants were obtained. Cd content in the supernatants was determined by an atomic absorption spectrophotometer. Then, the residual Cd content of each treatment was calculated. For the plants of each treatment, these were placed in new nutrient solutions under the second round treatment. On the sixth day, the residual concentration of Cd in the treatment solution was measured again. Cd removal efficiency (%) = ((initial Cd concentration − final Cd concentration)/initial Cd concentration) × 100%.

2.5. Determination of Plant Biomass and Cd Content in Various Organs

At the end of the experiment, plant samples were collected from the roots, stems, and leaves, respectively. For the cadmium analysis, the entire root system, the entire stem, and all leaves of each plant were harvested. The plant samples were washed and cut into pieces and then were dried at 105 °C for 30 min and kept at 80 °C until reaching a constant weight. The dried tissues from each organ were then ground into a fine powder and thoroughly mixed to ensure homogeneity. The Cd in each plant sample was extracted by HNO3-HClO4 (4:1, v/v) digestion of a 0.25 mg aliquot of the homogenized powder and the concentration of Cd was measured by flame atomic absorption spectrometry (Hitachi Z-6100; Hitachi High-Tech Corporation, Tokyo, Japan). Each sample were measured in triplicate.

2.6. Data Processing and Analysis

In this study, the translocation factor (Tf) was calculated by the ratio of Cd content in the aerial part (mg/kg) to that in the underground part (mg/kg), which was used to evaluate the ability of Cd absorbed by the underground part of Narrow Crown Black-Cathay poplar to accumulate in the aerial part [43]. The tolerance index (Ti) was calculated by the ratio of total biomass between the treatment group and the control group [51]. Data were processed and graphed by IBM SPSS Statistics 20.0 (IBM Corporation, Armonk, NY, USA) and Origin 2019 (OriginLab Corporation, Northampton, MA, USA). The differences between treatments were analyzed by one-way analysis of variance (ANOVA) and Duncan, p < 0.05. Prior to one-way analysis of variance (ANOVA), data normality was assessed using the Shapiro–Wilk test, and variance homogeneity was confirmed via Levene’s test. All treatments included three biological replicates (n = 3), where each replicate represented an independent seedling grown in a separate conical flask. Statistical significance was determined at p < 0.05 using Duncan’s multiple range test.

3. Results

3.1. Photosynthetic Physiological Characteristics of Narrow Crown Black-Cathay Poplar

In our study, the photosynthetic performance of Narrow Crown Black-Cathay poplar was evaluated by measuring a suite of key physiological parameters including the net photosynthetic rate (Pn), transpiration rate (Tr), stomatal conductance (Gs), intercellular CO2 concentration (Ci), water use efficiency (WUE), and light use efficiency (LUE). These parameters of the poplar clone were significantly influenced by Cd and phenol stress across all treatments (Figure 1). Single cadmium stress reduced Pn, Tr, Gs, Ci, LUE, and WUE to different degrees up to 100.0%, and the inhibition rates increased with the concentration increasing except for LUE (Table 1). The effects of the Cd concentration gradient on Pn, Tr, Gs, Ci, and WUE were increased by 45.6%, 56.9%, 68.0%, 14.4%, 44.9%, respectively. Photosynthesis, water use capacity, and light use capacity were sensitive to the addition of single Cd as Pn, WUE, and LUE were significantly decreased by 17.6%, 18.2%, and 15.5% (p < 0.05) at a low concentration (10 mg·L−1). In terms of Tr and Gs, when the concentration of single Cd reached 20 mg·L−1, they were notable decreases of about 57.9% and 69.9%, respectively. The influence of Cd on the Ci was different with the other characteristics, which first decreased and then increased (Figure 1d). Compared with TP0, Pn, Tr, Gs, Ci, WUE, and LUE of the examined poplar clone were decreased by single phenol stress (35.6%, 10.3%, 24.1%, 11.2%, 35.5%, and 27.2%, respectively). Treated with the binary stress of Cd and phenol, all photosynthetic parameters in the leaves of the examined poplar clone were lower than that of single stress, and the inhibition rates were higher, up to 54.0% (the examined poplar clone died under the TP7 condition). Considering the inhibition abilities of phenol under binary stresses, they seemed to be more powerful in the low concentration of Cd (10 mg·L−1) than that of the moderate concentration (20 mg·L−1). The discrepancy was more obvious on Gs (48.3%), Tr (22.1%), Pn (20.7%), and WUE (19.9%). The utilization rate of light energy, comprehensive restriction of growth, and distribution of aboveground parts of plants were determined by LUE. Here, both single Cd and single phenol reduced the LUE and then affected the normal growth of the examined poplar clone leaves.
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Figure 1. Photosynthetic physiological parameters of Narrow Crown Black-Cathay poplar to the concentration of single Cd, single phenol, and Cd-phenol compound stress. (a) Pn: net photosynthetic rate; (b) Tr: transpiration rate; (c) GS: stomatal conductance; (d) Ci: intercellular CO2 concentration; (e) LUE: light use efficiency, LUE = Pn/PAR, PAR: photosynthetically active radiation; (f) WUE: water use efficiency, WUE = Pn/Tr. Data are the means ± standard deviation. Bars followed by different letters show significant differences between treatments (p < 0.05, ANOVA followed by Duncan’s test).
Figure 1. Photosynthetic physiological parameters of Narrow Crown Black-Cathay poplar to the concentration of single Cd, single phenol, and Cd-phenol compound stress. (a) Pn: net photosynthetic rate; (b) Tr: transpiration rate; (c) GS: stomatal conductance; (d) Ci: intercellular CO2 concentration; (e) LUE: light use efficiency, LUE = Pn/PAR, PAR: photosynthetically active radiation; (f) WUE: water use efficiency, WUE = Pn/Tr. Data are the means ± standard deviation. Bars followed by different letters show significant differences between treatments (p < 0.05, ANOVA followed by Duncan’s test).
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Here, a mathematical model was constructed to intuitively display the effect of combined stress (Figure 2). The simulation curve and regression equation were established by taking the Pn of Narrow Crown Black-Cathay poplar to leaves as a dependent variable and Cd concentration as an independent variable. The single Cd stress was closely consonant with the quadratic curve equations Y = 0.0014X2 − 0.2859X + 9.0245 (R2 = 0.973), while Cd-phenol combined stress accorded with Y = 0.0064X2 − 0.4698X + 8.57 (R2 = 0.9951). From the simulation curve, we found that the inhibition effect on photosynthesis of the examined poplar clone was enhanced by Cd-phenol combined stress than single Cd stress (Figure 2). The inhibition abilities on the photosynthetic physiological characteristics of the examined poplar clone leaves by Cd-phenol stress were higher than that of single Cd or phenol pollution, but lower than the additive effects of Cd and phenol single stress, especially at the moderate and high concentrations (Table 1). Based on the models, when Pn decreased by 50% compared with the control group, the Cd concentrations were calculated to be 17.92 and 10.48 mg·L−1 for single and combined stress, respectively (Figure 2). Thus, when the examined poplar clone was used to remediate single Cd or Cd-phenol combined pollution in practical application, the concentration of Cd was suggested to be lower than 17.92 and 10.48 mg·L−1, respectively, avoiding inhibiting the normal growth of plants and reducing the remediation efficiency.

3.2. Biomass and Tolerance Index (Ti) of Narrow Crown Black-Cathay Poplar

Biomass production and tolerance indices are summarized in Table 2. For single Cd stress (TP1-3), both the underground and aboveground biomass showed minimal changes that were not statistically significant, with increases of 2.0% and 0.7% observed under the 10 mg·L−1 Cd treatment, respectively. Under the combined stress of Cd-phenol (TP5-7), slight increases in the underground part, aboveground part, and total biomass of Narrow Crown Black-Cathay poplar were noted at 10 mg·L−1 Cd, while slight decreases were observed at higher concentrations (20 and 40 mg·L−1). It is important to emphasize that with the exception of the lethal TP7 treatment, none of these variations in biomass reached statistical significance, and the observed changes were biologically minimal.
The tolerance of plants to heavy metals can be measured by the tolerance index (Ti), which was based on plant biomass. Here, the Ti of Narrow Crown Black-Cathay poplar decreased gradually with increasing Cd concentration, from 100.0% to 91.8%, with a significant reduction only under TP7 (p < 0.05) (Figure 3). Compared with the single Cd stress treatments, Ti increased by 1.11% and 0.16% for the Cd-phenol combined stress treatment when the concentration of Cd was 10 and 20 mg·L−1, respectively. Researchers have classified the tolerance of plants into three types: sensitivity (Ti < 0.35), moderate tolerance (0.35 < Ti < 0.60), and high tolerance (Ti > 0.60) [52]. In this study, under the single phenol, Cd, and binary stress, the Ti of the examined poplar clone was about 0.99, 0.98, and 0.92, respectively, which illustrated that the examined poplar clone had a high tolerance to Cd. In terms of the root–shoot (R/S) ratios of the examined poplar clone, an important index for assessing plant health, particularly under adverse environmental conditions, they tended to increase under higher Cd concentrations, particularly in combined stress treatments.

3.3. Cd Content and Translocation Factor (Tf) in Different Organs

The concentration of Cd in different organs of Narrow Crown Black-Cathay poplar including the roots, stems, and leaves were detected to analyze its absorption and accumulation characteristics. As illustrated in Figure 4a, the concentration of Cd in the organs increased significantly with the concentration of Cd and phenol (p < 0.05), and the highest content was in the roots (ranging from 4000.2 to 9277.0 mg/kg), which was about 190 to 584 times higher than that in the leaves (ranging from 10.3 to 40.1 mg/kg). Compared with the single Cd stress treatments, it was found that phenol promoted the absorption of Cd by the roots of Narrow Crown Black-Cathay poplar with a maximum of 1.8 times (TP5/TP1), but had no notable influence on the absorption of stems and leaves. Notably, the higher the concentration of Cd, the greater the translocation factor (Tf) of the Cd of roots transferred to the aboveground parts, especially when the concentration of Cd was 40 mg·L−1 (Figure 4b). However, the Tf of Narrow Crown Black-Cathay poplar for Cd was only 0.021~0.06, indicating that it had a weak ability to transfer Cd. Compared with single cadmium stress, the Tf of organs of plant under Cd-phenol combined stress decreased nearly 40%, suggesting that phenol could evidently inhibit the transfer ability of Cd from the roots to the aerial part of plant and affect the distribution of Cd in different organs of Narrow Crown Black-Cathay poplar.

3.4. Removal Efficiency of Cd

Residues of pollutants in water bodies reflect the removal capacity of plants. The residual Cd concentration in the culture medium on the third and sixth days was used to represent the removal ability of Cd in the first and second round. The removal efficiencies of Cd by Narrow Crown Black-Cathay poplar under different treatments were calculated as shown in Figure 5 (plants died under TP7 treatment). In the first round, the removal efficiency under single Cd stress increased with Cd concentration, peaking at 15.8% (TP3). Under combined stress (TP5), removal efficiency reached 26.0%—approximately four times higher than in the corresponding single Cd treatment (TP1, 6.6%). However, this promotive effect was concentration-dependent and transient. When the cadmium concentration increased to 20 mg/L, the removal efficiency under combined stress declined relative to lower concentrations, but remained significantly higher—by 6 percentage points—than under single cadmium stress. Notably, the promoting effect was no longer observed in the second experimental round. In this round, the highest removal efficiency occurred on TP2, and the Cd removal efficiencies decreased by 40.6% to 77.6% compared with the first round. Moreover, phenol no longer exerted a significant promotive effect on the Cd removal efficiency (p > 0.05).

4. Discussion

The coexistence of heavy metals and organic pollutants presents a complex challenge for ecosystem health and phytoremediation applications [11,53,54,55]. The combined toxicity often differs from single pollutants, leading to unpredictable effects on plant physiology and remediation efficiency [9,10,11,12,13]. Against this backdrop, the present study elucidated the physiological and adaptive responses of Narrow Crown Black-Cathay poplar to the single and combined stress of Cd and phenol, offering critical insights into its potential use in co-contaminated environments.
We found that Cd and phenol, particularly when combined, significantly inhibited the photosynthetic apparatus of Narrow Crown Black-Cathay poplar. This observation is consistent with previous reports on plant responses to combined heavy metal and organic pollutant stress, such as Cd and polycyclic aromatic hydrocarbon (PAH) co-pollution, which also considerably impedes plant growth [56]. The greater photosynthetic inhibition under combined stress may be attributed to exacerbated oxidative damage and impaired stomatal function. The concurrent decline in net photosynthetic rate (Pn), stomatal conductance (Gs), and transpiration rate (Tr) strongly suggests that stomatal limitation is the primary factor initially restricting photosynthesis under stress conditions [57]. This pattern aligns with earlier findings in tobacco, where Cd was shown to inhibit chlorophyll synthesis enzymes such as CHLH and POR [58], suggesting a common mechanistic pathway across species. Furthermore, disrupted nutrient and water uptake, transport, and utilization, along with impaired metabolic processes including respiration, likely contribute to the photosynthetic decline [59,60,61].
To quantitatively assess the interaction between the pollutants, we developed a mathematical model that effectively captured the synergistic effect of combined stress. The model revealed that phenol markedly lowered the Cd concentration threshold required to cause a 50% reduction in photosynthesis (Figure 2), demonstrating a clear “synergistic effect” of phenol on Cd toxicity that was more pronounced than previously reported for single-stress scenarios. While research into the effects of phenol on the photosynthesis of woody plants is limited, studies on algae have shown that phenol and its derivatives can inhibit important photosynthetic processes [62,63,64]. For example, Duan et al. (2017) [63] showed that phenol induces ROS accumulation and disrupts thylakoid membrane integrity in algae, a mechanism that may similarly operate in poplar and explain the enhanced sensitivity to Cd under combined stress. Based on this evidence, we propose that phenol initially compromises the photosynthetic apparatus in poplar, likely through membrane disruption and enzymatic inhibition, thereby increasing its susceptibility to Cd. Cadmium may then further aggravate toxicity by inducing oxidative stress and impairing the electron transport chain and carbon fixation, resulting in a synergistic breakdown of photosynthesis under combined stress. This mechanistic interpretation bridges the gap between model-derived parameters and physiological toxicity, moving beyond a purely mathematical analysis.
Further supporting the notion of a dynamic photosynthetic limitations, the pattern of intercellular CO2 concentration (Ci)—initially decreasing, then rising under higher Cd stress—indicates a shift from stomatal to non-stomatal limitations at elevated concentrations. This transition is consistent with previous studies under heavy metal stress, where non-stomatal factors such as damage to chlorophyll structure and Calvin cycle enzymes become dominant at higher concentrations [58,61,65,66]. It is well-established that the primary constraints on photosynthesis can transition between stomatal and non-stomatal factors in response to environmental stress [67]. Under low Cd concentration exposure (10 mg∙L−1), stomatal limitation predominates, with Gs decreasing by 68.0% and Ci declining accordingly, indicating that CO2 diffusion into the leaf is restricted. In terms of energy use efficiency, both Cd and phenol alone reduced LUE, a response that mirrors findings in other species where plants sacrifice LUE to improve WUE under stress [68]. The decrease in WUE may be due to reduced Tr, which helps to avoid water loss and inhibits water uptake and transport in vivo—a strategy for maintaining water balance that is possibly mediated by stomatal closure induced by elevated ABA content [69].
A central finding of this study was that Narrow Crown Black-Cathay poplar maintained a high biomass accumulation—reflected by a high tolerance index (Ti)—under combined Cd-phenol stress, despite the significant inhibition of key photosynthetic parameters such as the net photosynthetic rate (Pn). This apparent dissociation between photosynthetic decline and biomass stability suggests a decoupling effect under combined pollution stress, a phenomenon also observed in other tolerant woody species such as Populus and Salix clones [43,52]. For example, hydroponic studies of Populus and Salix clones have shown that certain cultivars (e.g., Populus × canadensis) can maintain total biomass (Ti > 0.8) even when photosynthesis declines by 30–40% through a strategy that combines enhanced root cadmium sequestration with increased belowground biomass allocation [43]. Similarly, Lux et al. [52] demonstrated that Cd-tolerant Salix clones mitigated biomass loss despite a 25% reduction in Rubisco activity through structural adaptations such as root vessel thickening and cortical lignification, which improve metal immobilization. In contrast, Cd-sensitive clones exhibited a significant biomass reduction under similar photosynthetic inhibition. These collective findings support the notion that tolerant woody species can preserve growth stability under metal stress through integrated physiological strategies that involve resource reallocation and enhanced root metal retention. In our study, the consistently high Ti values (>0.9) across treatments confirm the strong innate Cd tolerance of Narrow Crown Black-Cathay poplar, underscoring its potential for phytoremediation applications. This trait is further reinforced by its pronounced root Cd accumulation and low translocation factor, consistent with the exclusion mechanism documented in other metal-tolerant poplars [48,50]. Such characteristics are particularly advantageous for phytostabilization, where the root confinement of metals is critical, even if they may limit the phytoextraction efficiency. Recent studies attribute such resilience in poplars under combined pollution to efficient antioxidant defenses and vacuolar metal compartmentalization [22,41], mechanisms that may also underpin the performance observed here.
Furthermore, applying the “stress threshold early warning model” proposed by Wang et al. (2024) [54], the Cd concentration thresholds for a 50% decline in Pn—calculated through regression equation inversion in this study as 17.92 mg·L−1 for single Cd and 10.48 mg·L−1 for combined stress—provide quantitative indicators for balancing plant growth and remediation efficiency. These thresholds are lower than those reported for some herbaceous species under single Cd stress, highlighting the heightened sensitivity of poplar under combined pollution and underscoring the need for species-specific threshold assessments in phytoremediation planning. However, remediation efficiency was not static but exhibited a dynamic decline in the second exposure round, with the promotive effect of phenol disappearing, indicating physiological fatigue and the saturation of detoxification and sequestration capacities. This temporal pattern aligns with previous reports on limited detoxification capacity upon re-exposure in other plant systems, suggesting that practical phytoremediation designs should incorporate rotation or microbial augmentation to sustain long-term efficacy.
It should be noted that this study focused on acute plant responses under controlled laboratory conditions. The nominal phenol concentrations applied may not accurately reflect the actual exposure levels due to potential volatilization and biodegradation. Future research should utilize closed systems with the real-time monitoring of pollutant concentrations to better simulate field scenarios and evaluate long-term phytoremediation efficacy. Additionally, incorporating analyses of pigment content (e.g., chlorophyll) and relevant biochemical markers in subsequent studies would help elucidate the response mechanisms of the photosynthetic apparatus under combined Cd-phenol stress.

5. Conclusions

Here, through a series of controlled laboratory experiments, we investigated the tolerance and cadmium accumulation behavior of Narrow Crown Black-Cathay poplar under combined cadmium-phenol pollution. The results showed that this poplar exhibits remarkable resilience to combined stress, employing an integrated adaptive strategy that includes the modulation of photosynthetic activity, strategic reallocation of biomass, and efficient root-based sequestration of cadmium. While all treatments inhibited photosynthetic function, the presence of phenol exacerbated this effect by up to 54.0%, highlighting its synergistic toxicity with cadmium. Tissue-specific analysis revealed a distinct pattern of cadmium accumulation: root > stem > leaf, with the root Cd concentrations increasing by up to 1.8-fold under elevated pollutant levels. Interestingly, during the initial exposure phase, phenol initially enhanced the Cd removal efficiency at low Cd concentrations, though this effect was concentration-dependent and not sustained upon re-exposure. Phenol plays a dual role in this system, intensifying phytotoxicity while concurrently promoting a shift toward phytostabilization—a safer remediation mechanism. Based on these findings, we propose a conceptual framework in which the physiological response is shaped by dose-dependent interactions between stressors, ultimately governing the efficiency and strategy of remediation. These results reflect acute stress responses and short-term removal capacity, and longer-term studies are needed to assess field applicability.

Author Contributions

Conceptualization, H.X. and C.L.; Methodology, H.T. and Q.L.; Formal analysis and investigation, H.T., K.Z. and S.S.; Writing—original draft preparation, H.T. and K.Z.; Writing—review and editing: H.X.; Supervision, C.L. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Data Availability Statement

The data presented in this study are available on request from the corresponding author.

Acknowledgments

We thank DeepSeek-V3 for the English-language polishing of an earlier draft. The final wording and content were revised and approved by the authors, who take full responsibility for any errors or omissions.

Conflicts of Interest

The authors have no relevant financial or non-financial interests to disclose; all authors declare that there are no competing interests in this research manuscript.

References

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Forests 16 01531 g002
Figure 2. Simulation curve of single Cd and Cd-phenol combined stress on Pn of Narrow Crown Black-Cathay poplar. Pn: net photosynthetic rate.
Figure 2. Simulation curve of single Cd and Cd-phenol combined stress on Pn of Narrow Crown Black-Cathay poplar. Pn: net photosynthetic rate.
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Figure 3. Effects of single Cd, single phenol, and Cd-phenol combined stress on the tolerance index (Ti) and the root shoot ratio of Narrow Crown Black-Cathay poplar. Data are the means ± standard deviation. Bars followed by different letters show significant differences between treatments (p < 0.05, ANOVA followed by Duncan’s test).
Figure 3. Effects of single Cd, single phenol, and Cd-phenol combined stress on the tolerance index (Ti) and the root shoot ratio of Narrow Crown Black-Cathay poplar. Data are the means ± standard deviation. Bars followed by different letters show significant differences between treatments (p < 0.05, ANOVA followed by Duncan’s test).
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Figure 4. Content of Cd ion (a) and its translocation factor (b) in different organs of Narrow Crown Black-Cathay poplar under different treatments. Data are the means ± standard deviation. Bars followed by different letters show significant differences between treatments (p < 0.05, ANOVA followed by Duncan’s test).
Figure 4. Content of Cd ion (a) and its translocation factor (b) in different organs of Narrow Crown Black-Cathay poplar under different treatments. Data are the means ± standard deviation. Bars followed by different letters show significant differences between treatments (p < 0.05, ANOVA followed by Duncan’s test).
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Figure 5. Removal efficiency of Cd by Narrow Crown Black-Cathay poplar in different time periods under different treatments. Data are the means ± standard deviation. Bars followed by different letters show significant differences between treatments (p < 0.05, ANOVA followed by Duncan’s test).
Figure 5. Removal efficiency of Cd by Narrow Crown Black-Cathay poplar in different time periods under different treatments. Data are the means ± standard deviation. Bars followed by different letters show significant differences between treatments (p < 0.05, ANOVA followed by Duncan’s test).
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Table 1. Average inhibition rates on the photosynthesis physiological characteristics of Narrow Crown Black-Cathay poplar under different treatments.
Table 1. Average inhibition rates on the photosynthesis physiological characteristics of Narrow Crown Black-Cathay poplar under different treatments.
TreatmentCompositionAverage Inhibition Rate (%)
Cd (mg·L−1)Phenol (mg·L−1)PnTrGSCiWUELUE
TP000------
TP110017.61.11.90.218.215.5
TP220063.257.969.914.663.213.3
TP3400100.036.186.90.0100.0100.0
TP4010035.610.324.111.235.527.2
TP51010052.131.255.915.152.128.8
TP62010077.066.075.618.177.133.1
TP740100ndndndndndnd
Pn: net photosynthetic rate; Tr: transpiration rate; GS: stomatal conductance; Ci: intercellular CO2 concentration; WUE: water use efficiency, WUE = Pn/Tr; PAR: photosynthetically active radiation; LUE: light use efficiency, WUE = Pn/PAR; nd means not detected as plants of TP7 died. Inhibition rates were calculated from the mean values of the original data. Statistical significance should be inferred from the analysis of the original parameters presented in Figure 1.
Table 2. Biomass of different parts of Narrow Crown Black-Cathay poplar under different treatments.
Table 2. Biomass of different parts of Narrow Crown Black-Cathay poplar under different treatments.
TreatmentAboveground Parts Biomass (mg)Underground Part Biomass (mg)Total Biomass (mg)
StemLeafRoot
TP0299.20 ± 0.59 a297.33 ± 8.29 a302.17 ± 1.73 bc898.70 ± 8.93 a
TP1298.47 ± 1.32 a300.85 ± 1.24 a299.37 ± 0.43 cd898.68 ± 2.98 a
TP2300.53 ± 0.56 a296.80 ± 2.90 a297.40 ± 0.69 d894.73 ± 3.30 a
TP3300.53 ± 0.18 a284.00 ± 4.04 a297.03 ± 0.58 d881.57 ± 4.08 a
TP4299.87 ± 1.48 a304.90 ± 2.83 a292.70 ± 1.67 e897.47 ± 2.69 a
TP5301.13 ± 0.39 a299.40 ± 2.55 a308.23 ± 1.65 a908.77 ± 0.99 a
TP6301.13 ± 1.39 a290.95 ± 0.38 a304.07 ± 1.24 b896.15 ± 1.65 a
TP7285.43 ± 0.37 b254.78 ± 5.73 b285.43 ± 0.32 f825.65 ± 7.49 b
Data are shown as the mean ± standard deviation (SD) (n = 3). Different letters in the same column represent statistically significant differences between treatments (p < 0.05, ANOVA followed by Duncan’s test).
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Tian, H.; Zheng, K.; Lu, Q.; Sun, S.; Li, C.; Xie, H. Photosynthetic Performance and Phytoremediation Potential of Narrow Crown Black-Cathay Poplar Under Combined Cadmium and Phenol Pollution. Forests 2025, 16, 1531. https://doi.org/10.3390/f16101531

AMA Style

Tian H, Zheng K, Lu Q, Sun S, Li C, Xie H. Photosynthetic Performance and Phytoremediation Potential of Narrow Crown Black-Cathay Poplar Under Combined Cadmium and Phenol Pollution. Forests. 2025; 16(10):1531. https://doi.org/10.3390/f16101531

Chicago/Turabian Style

Tian, Huimei, Kaixin Zheng, Qiyun Lu, Siyuan Sun, Chuanrong Li, and Huicheng Xie. 2025. "Photosynthetic Performance and Phytoremediation Potential of Narrow Crown Black-Cathay Poplar Under Combined Cadmium and Phenol Pollution" Forests 16, no. 10: 1531. https://doi.org/10.3390/f16101531

APA Style

Tian, H., Zheng, K., Lu, Q., Sun, S., Li, C., & Xie, H. (2025). Photosynthetic Performance and Phytoremediation Potential of Narrow Crown Black-Cathay Poplar Under Combined Cadmium and Phenol Pollution. Forests, 16(10), 1531. https://doi.org/10.3390/f16101531

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