To identify the tolerance mechanisms of wetland plants exposed to heavy metal, a hydroponic experiment was used to investigate variations in photosynthetically physiological parameters and antioxidant enzyme activities in leaves of Monochoria korsakowii exposed to 0.05, 0.15, 0.30, and 0.45 mM Cd2+ for 7 d. The Cd2+ concentrations in the plant roots, stems, and leaves were also investigated. Cd2+ exposure significantly decreased the total chlorophyll content, net photosynthetic rate, intercellular carbon dioxide concentration, and stomatal conductance, while stomatal limitation value had the opposite trend (P < 0.05). During Cd2+ stress, ascorbate peroxidase activity significantly increased (P < 0.05). The translocation factor for Cd2+ was significantly lower than that of the control, and both were less than 1 (P < 0.05). Cd2+ stress damaged the photosynthetic apparatus in the leaves. During Cd2+ stress, M. korsakowii alleviated oxidative stress by increasing the activities of antioxidant enzymes, such as APX. Under 0.45 mM Cd2+ stress, increased heat dissipation was responsible for alleviating the photooxidative damage to photosynthetic organs in the leaves. Meanwhile, the majority of Cd2+ was immobilized in the roots, thus alleviating excessive Cd2+ phytotoxicity in the aboveground parts. Generally, M. korsakowii has potential application in the phytoremediation of low-cadmium-polluted water.

  • Ascorbate peroxidase plays a significant role in alleviating oxidative stress in the leaves.

  • Cadmium immobilized in roots accounted for the plant tolerance to cadmium exposure.

  • M. korsakowii has potential application in phytopremediation of low-cadmium polluted water.

Graphical Abstract

Graphical Abstract
Graphical Abstract

Cadmium (Cd) is listed as the fourth most toxic heavy metal element causing phytotoxicity, with a long decomposition cycle, strong mobility, high toxicity, difficult degradation, and easy absorption by plants, posing a serious threat to environmental quality, food safety, and human health (Haider et al. 2021). Cd2+ first destroys the balance of the redox system in plant cells, inducing the accumulation of reactive oxygen species (ROS), such as the superoxide anion radical (O2−·), hydroxyl radical (·OH), nitric oxide radical (NO·), hydroperoxyl radical (HOO·), alkoxy radical (RO·), and alkane peroxide (ROO·), which denature biological macromolecules, such as proteins and nucleic acids (Yang et al. 2019). Thus, plants are poisoned. Studies have shown that excessive Cd2+ in the environment aggravates the peroxidation of plant cell membranes, disrupts the metabolism of minerals, such as nitrogen and sulfur, reduces the content of chlorophyll, destroys the ultrastructure of chloroplasts, decreases the activity of key enzymes in the photosynthetic reaction and the water potential and turgor pressure of mesophyll cells, and interferes with the primary light energy capture ability and electron transport ability of photosystem II, thereby hindering photosynthesis and transpiration and adversely affecting plant seedling development and root elongation growth (Ying et al. 2010; Gill et al. 2013; Cocozza et al. 2015).

Plants have evolved various mechanisms to cope with Cd stress, such as efflux, cell wall immobilization, chelation, induction of antioxidant enzymes and proteins, vacuolar compartments, and signaling pathways (El Rasafi et al. 2022). AtIRT1, a transporter of the Zrt- and Irt-protein-like families in plant roots, is involved in Cd uptake (Uraguchi & Fujiwara 2012). Cd transport in cells is mediated by natural resistance-associated macrophage protein (NRAMP) family transporters (Pottier et al. 2015). The xylem mediates Cd transport to the aboveground fraction (Fontanili et al. 2016). Plant chelation is an important detoxification method under Cd stress. It binds Cd through specific low-molecular-weight chelators, such as glutathione (GSH), phytocomplexin (PC), and metallothionein (MT). Multidrug resistance-related proteins (MRPs) mediate the translocation of Cd-phytocomplexin through the vacuolar membrane into the vacuole (Shri et al. 2014), the cation exchanger (CAX) located on the vacuolar membrane also plays an important role in the absorption and chelation of Cd (Sharma et al. 2016). Cd can ameliorate Cd stress by stimulating various hormone signaling pathways and regulating many physiological processes in plants (Khanna et al. 2022). Indole-3-acetic acid (IAA) plays an important role in signal transduction pathways and regulates plant growth and development during Cd stress (Ostrowski et al. 2016). Oxidative bursts in plants during Cd stress indicate that calmodulin-/calmodulin-dependent proteins mediate the involvement of the Ca/calmodulin pathway (Virdi et al. 2015). Meanwhile, during Cd stress, plants activate antioxidant systems that remove ROS. These include antioxidant enzymes (superoxide dismutase (SOD), peroxidase (POD), catalase (CAT), ascorbate peroxidase (APX), glutathione reductase (GR), and glutathione peroxidase (GPX)) and non-enzymatic antioxidants (glutathione (GSH), ascorbic acid (ASA), carotenoids, etc.) (Shanthala et al. 2006). By acting as reducing agents, these free radical scavengers ultimately convert ROS into harmless products, H2O and O2, becoming an essential defense system for plants against Cd toxicity. In addition, the activation of antioxidant enzymes has been reported to be caused by changes in gene regulation and an increase in their substrate content under Cd stress (Anjum et al. 2012).

Monochoria korsakowii is an aquatic herb. It often grows in waterbodies, such as ponds, lakes, and marshes, and has stout rhizomes, terminal racemes, and small blue flowers with high ornamental garden value, and it is widely used in urban landscape water. Previous studies have shown that this plant could effectively remove total nitrogen and phosphorus in eutrophic water, and meanwhile maintain a good physiological condition (Fu et al. 2013; Li et al. 2016). Meanwhile, M. korsakowii could immobilize most lead in the root system, and enhance the tolerance of leaf cells to lead stress by improving SOD, CAT, and total antioxidant activity (Kim et al. 2009). To clarify the tolerance and related resistance mechanism of M. korsakowii photosynthesis under heavy metal stress and explore its application potential in heavy-metal contaminated water phytoremediation, a hydroponic experiment was used to investigate variations in photosynthetic physiological parameters, chlorophyll fluorescence characteristics, and antioxidant enzyme activities in leaves of M. korsakowii exposed to 0.05, 0.10, 0.15, 0.30, and 0.45 mM Cd2+ concentration for 7 d. The distribution characteristics of Cd2+ in the roots, stems, and leaves of M. korsakowii were also investigated.

Test materials and Cd treatment

This experiment was conducted in the greenhouse at the National Landscape Architecture Experimental Teaching Demonstration Center, Nanjing Forestry University. Monochoria korsakowii was purchased from the Shengyue Flower and Seedling Garden of Shuyang County. In August 2021, the plants were cultured in pond water. When the height of the plants was 40–50 cm, plants with the same growth trend and good growth status were selected and placed in half-strength Hoagland's solution for adaptive cultivation for 7 d.

After the adaptive culture, M. korsakowii was treated with Cd2+ stress. The hydroponic experiment was prepared using CdCl2·2.5H2O and half-strength Hoagland's solution. A single-factor experimental randomized block design was used in the experiment. Four Cd2+ concentration gradients were set: 0.05, 0.15, 0.30, and 0.45 mM (560, 1,680, 3,360, and 5,040 times water class V in the GB3838-2002 Surface Water Environmental Quality Standard, respectively). The control was half-strength Hoagland's solution. Each treatment was repeated three times with 12 plants. During the experiment, ultrapure water was regularly used to replenish the evaporated water in the incubator to maintain a stable water level. After 7 d of treatment, the leaves were collected for the determination of physiological indexes.

Measurement indexes and methods

Photosynthetic pigment content

Following Li (2000), fresh leaves were immersed in 20 mL of 95% ethanol in the dark for photosynthetic pigment extraction. Chlorophyll a (Chl a), chlorophyll b (Chl b), and total chlorophyll (Chl T) content were determined using ultraviolet visible spectrophotometer Lambda 25 (Perkin-Elmer, Waltham, MA, USA). Absorbance was determined at 665, 649, and 470 nm.

Photosynthetic gas exchange parameters

The photosynthetic rate (Pn), transpiration rate (E), stomatal conductance (Gs), intercellular CO2 concentration (Ci), and leaf saturated vapor pressure deficit (VPD) in the leaves were determined at 9:00–11:00 on a sunny day using a portable photosynthetic system, CIRAS-3 (PP System, Norfolk, UK). Stomatal limitation value (Ls), water utilization efficiency (WUE), and CO2 utilization efficiency (CUE) were calculated according to Wu et al. (2002), Zhang & Shan (1997), and He & Ma (2000), respectively.

Chlorophyll a fluorescence parameter

A Handy PEA Plant Efficiency Analyzer (Hansatech Instruments Limited, Norfolk, UK) was used to measure chlorophyll a fluorescence parameters (Appendix A). After the leaves were fully dark adapted for 30 min, the analysis probe was placed on the dark adaptation clip, which was then drawn out, and the leaves were exposed to saturated pulsed light (3,000 mmol⋅m−2⋅s−1) for 1 s. The measured data were derived using the corresponding software.

Antioxidant enzyme activity

Fresh leaves (0.3 g) were homogenized with 5 mL 50 mmol·L−1 PBS (pH 7.8, containing 1% PVP). The suspension was centrifuged at 12,000 g for 20 min at 4 °C. The activities of SOD, POD, CAT, GR, and APX were measured with an ultraviolet visible spectrophotometer.

SOD activity was the amount of this enzyme needed for 50% NBT reduction (Dhindsa et al. 1981). One unit of POD activity was defined as H2O2 decomposition per minute. Increases in absorbance because of guaiacol were assayed at 470 nm (Sancho et al. 1996). CAT activity was determined following Li (2000), and the amount of enzyme that reduced OD240 by 0.1 within 1 min was defined as one enzyme active unit (U). GR activity was determined according to Halliwell & Foyer (1978), and one unit of GR activity was defined as a reduction of 0.1 absorbance units per min at 340 nm. APX activity was determined following Nakano & Asada (1981), and reductions in absorbance due to a reduction in ascorbic acid were recorded at 290 nm.

Cd2+ concentrations in roots, stems, and leaves

Root samples were immersed in EDTA-Na2 for 30 min, rinsed in distilled water, desorbed, and blotted for Cd2+ determination. The root, stem, and leaf samples were then dried for 48 h at 80 °C, weighed, ground to fine powder, and digested with concentrated HNO3 and HClO4 (4:1, v/v). The Cd2+ concentration was determined with an atomic absorption spectrophotometer (Chary et al. 2008).

Statistical analysis

The data were analyzed by one-way analysis of variance (ANOVA) using SPSS 26.0 software, and Duncan's multiple range test was used to assess the differences among the treatments. Graphs were prepared using Microsoft Excel.

Variations in Chl a, Chl b, and Car content and Chl a/b values

As shown in Table 1, compared with the control, 0.05 mM Cd2+ treatment for 7 d had no significant effect on Chl a content in M. korsakowii leaves (P > 0.05). After 0.15–0.45 mM Cd2+ treatment for 7 d, the Chl a content in leaves significantly decreased by 33.33–50% (P < 0.05). After 7 d of treatment, 0.05–0.45 mM Cd2+ exposure significantly decreased Chl b content by 28.57–51.79% compared with that in the control, and a similar tendency was also observed in Chl T content (P < 0.05). In comparison with the control, no significant variations in the Car content were observed after 0.05 and 0.15 mM Cd2+ exposure for 7 d (P > 0.05). However, the Car content decreased by 34.62 and 26.92% after 0.30 and 0.45 mM exposure, respectively, after 7 d (P < 0.05).

Table 1

Variations in contents of Chl a, Chl b, and Car, and values of Chl a/b in leaves of M. korsakowii exposed to different Cd2+ concentrations for 7 d

Cd2+/mMChl a/mg·g−1Chl b/mg·g−1Chl a/bChl T/mg·g−1Car/mg·g−1
1.44 ± 0.03a 0.56 ± 0.02a 0.13 ± 0.00a 2.01 ± 0.05a 0.26 ± 0.00a 
0.05 1.08 ± 0.16ab 0.40 ± 0.06b 0.13 ± 0.00a 1.48 ± 0.23b 0.23 ± 0.03ab 
0.15 0.96 ± 0.03b 0.36 ± 0.01b 0.13 ± 0.00a 1.32 ± 0.04b 0.22 ± 0.01abc 
0.30 0.72 ± 0.12b 0.27 ± 0.04b 0.13 ± 0.00a 0.98 ± 0.16b 0.17 ± 0.02c 
0.45 0.82 ± 0.16b 0.30 ± 0.06b 0.14 ± 0.00a 1.11 ± 0.22b 0.19 ± 0.02bc 
Cd2+/mMChl a/mg·g−1Chl b/mg·g−1Chl a/bChl T/mg·g−1Car/mg·g−1
1.44 ± 0.03a 0.56 ± 0.02a 0.13 ± 0.00a 2.01 ± 0.05a 0.26 ± 0.00a 
0.05 1.08 ± 0.16ab 0.40 ± 0.06b 0.13 ± 0.00a 1.48 ± 0.23b 0.23 ± 0.03ab 
0.15 0.96 ± 0.03b 0.36 ± 0.01b 0.13 ± 0.00a 1.32 ± 0.04b 0.22 ± 0.01abc 
0.30 0.72 ± 0.12b 0.27 ± 0.04b 0.13 ± 0.00a 0.98 ± 0.16b 0.17 ± 0.02c 
0.45 0.82 ± 0.16b 0.30 ± 0.06b 0.14 ± 0.00a 1.11 ± 0.22b 0.19 ± 0.02bc 

Data is mean value ± SE of three independent experiments. Different small letters in the same column indicate significant differences at P < 0.05. The same below.

Variations in photosynthetic gas exchange parameters

As shown in Table 2, compared with the control, 0.05–0.45 mM Cd2+ exposure for 7 d markedly declined Pn by 68.8–83.72%, and a similar tendency was also observed in E (68.91–78.11%), Ci (10.78–17.11%), Gs (94.58–96.68%), and CUE (60–80%) (P < 0.05). In contrast, VPD and Ls increased by 208.26–240.37% and 58.33–116.67% (P < 0.05), respectively. However, WUE significantly decreased by 34.53% with the plant cultivated with 0.45 mM Cd2+ for 7 d in comparison with the control (P < 0.05).

Table 2

Photosynthetic gas exchange parameters of M. korsakowii exposed to different Cd2+ concentrations for 7 d

Cd2+/mMPn/μmol·m−2·s−1E/mmol·m−2·s−1Ci/μmol·mol−1Gs/mmol·m−2·s−1VPD/kPaLsWUE/μmol·mmol−1CUE/mol·m−2·s−1
17.63 ± 2.16a 12.61 ± 0.64a 374.00 ± 3.06a 2,196.67 ± 552.36a 1.09 ± 0.10b 0.12 ± 0.01c 1.39 ± 0.13a 0.05 ± 0.01a 
0.05 5.50 ± 1.25b 3.78 ± 0.64b 310.00 ± 9.81c 115.00 ± 24.95b 3.37 ± 0.17a 0.26 ± 0.02a 1.45 ± 0.22a 0.02 ± 0.01b 
0.15 4.77 ± 0.50b 3.92 ± 0.39b 320.33 ± 1.86b 119.00 ± 16.50b 3.36 ± 0.12a 0.23 ± 0.00ab 1.21 ± 0.23ab 0.01 ± 0.00b 
0.30 3.33 ± 0.12b 2.76 ± 0.10b 312.67 ± 0.67bc 73.00 ± 3.46b 3.71 ± 0.32a 0.24 ± 0.00ab 1.21 ± 0.01ab 0.01 ± 0.00b 
0.45 2.87 ± 0.24b 3.32 ± 0.43b 333.67 ± 11.26b 95.00 ± 16.52b 3.52 ± 0.12a 0.19 ± 0.03b 0.91 ± 0.17b 0.01 ± 0.00b 
Cd2+/mMPn/μmol·m−2·s−1E/mmol·m−2·s−1Ci/μmol·mol−1Gs/mmol·m−2·s−1VPD/kPaLsWUE/μmol·mmol−1CUE/mol·m−2·s−1
17.63 ± 2.16a 12.61 ± 0.64a 374.00 ± 3.06a 2,196.67 ± 552.36a 1.09 ± 0.10b 0.12 ± 0.01c 1.39 ± 0.13a 0.05 ± 0.01a 
0.05 5.50 ± 1.25b 3.78 ± 0.64b 310.00 ± 9.81c 115.00 ± 24.95b 3.37 ± 0.17a 0.26 ± 0.02a 1.45 ± 0.22a 0.02 ± 0.01b 
0.15 4.77 ± 0.50b 3.92 ± 0.39b 320.33 ± 1.86b 119.00 ± 16.50b 3.36 ± 0.12a 0.23 ± 0.00ab 1.21 ± 0.23ab 0.01 ± 0.00b 
0.30 3.33 ± 0.12b 2.76 ± 0.10b 312.67 ± 0.67bc 73.00 ± 3.46b 3.71 ± 0.32a 0.24 ± 0.00ab 1.21 ± 0.01ab 0.01 ± 0.00b 
0.45 2.87 ± 0.24b 3.32 ± 0.43b 333.67 ± 11.26b 95.00 ± 16.52b 3.52 ± 0.12a 0.19 ± 0.03b 0.91 ± 0.17b 0.01 ± 0.00b 

Variations in Fm, Fv, Fo/Fm, Fv/Fm, Fv/Fo, Vj, Vi, dVG/dto, and dV/dto

As shown in Table 3, in comparison with the control, no significant variations in Fo were observed after 0.05–0.30 mM Cd2+ exposure for 7 d (P > 0.05). However, Fo increased by 8.69% after 0.45 mM exposure for 7 d (P < 0.05), and a similar tendency was also observed in Vj (26.53%) and dV/dto (44.25%)(P < 0.05). Compared with the control, 0.05–0.45 mM Cd2+ treatment for 7 d had no significant effect on Fm,Fv, Fm/Fo, Fv/Fm, Fv/Fo, Vi, and dVG/dto (P > 0.05).

Table 3

Variations in Fm, Fv, Fo/Fm, Fv/Fm, Fv/Fo, Vj, Vi, dVG/dto and dV/dto of M. korsakowii exposed to different Cd2+ concentrations for 7 d

Cd2+/mMFoFmFvFm/FoFv/FmFv/FoVjVidVG/dtodV/dto
468.00 ± 15.62b 3,012.33 ± 116.03a 2,544.33 ± 128.67a 0.16 ± 0.01a 0.84 ± 0.01a 5.46 ± 0.43a 0.49 ± 0.10b 0.89 ± 0.01a 0.70 ± 0.05a 1.13 ± 0.01b 
0.05 487.33 ± 2.96ab 3,020.33 ± 91.10a 2,533.00 ± 93.86a 0.16 ± 0.01a 0.84 ± 0.01a 5.20 ± 0.22a 0.58 ± 0.03ab 0.90 ± 0.01a 0.98 ± 0.20a 1.42 ± 0.16ab 
0.15 497.67 ± 11.10ab 2,869.00 ± 197.87a 2,371.33 ± 188.27a 0.17 ± 0.01a 0.83 ± 0.01a 4.76 ± 0.30a 0.57 ± 0.02ab 0.87 ± 0.01a 1.06 ± 0.25a 1.44 ± 0.14ab 
0.30 502.33 ± 6.84ab 2,909.00 ± 164.59a 2,406.67 ± 161.22a 0.17 ± 0.01a 0.83 ± 0.01a 4.79 ± 0.30a 0.56 ± 0.02ab 0.86 ± 0.02a 1.09 ± 0.19a 1.47 ± 0.12ab 
0.45 508.67 ± 14.77a 2,866.00 ± 111.27a 2,357.33 ± 125.48a 0.18 ± 0.01a 0.82 ± 0.01a 4.66 ± 0.37a 0.62 ± 0.05a 0.88 ± 0.01a 1.22 ± 0.20a 1.63 ± 0.17a 
Cd2+/mMFoFmFvFm/FoFv/FmFv/FoVjVidVG/dtodV/dto
468.00 ± 15.62b 3,012.33 ± 116.03a 2,544.33 ± 128.67a 0.16 ± 0.01a 0.84 ± 0.01a 5.46 ± 0.43a 0.49 ± 0.10b 0.89 ± 0.01a 0.70 ± 0.05a 1.13 ± 0.01b 
0.05 487.33 ± 2.96ab 3,020.33 ± 91.10a 2,533.00 ± 93.86a 0.16 ± 0.01a 0.84 ± 0.01a 5.20 ± 0.22a 0.58 ± 0.03ab 0.90 ± 0.01a 0.98 ± 0.20a 1.42 ± 0.16ab 
0.15 497.67 ± 11.10ab 2,869.00 ± 197.87a 2,371.33 ± 188.27a 0.17 ± 0.01a 0.83 ± 0.01a 4.76 ± 0.30a 0.57 ± 0.02ab 0.87 ± 0.01a 1.06 ± 0.25a 1.44 ± 0.14ab 
0.30 502.33 ± 6.84ab 2,909.00 ± 164.59a 2,406.67 ± 161.22a 0.17 ± 0.01a 0.83 ± 0.01a 4.79 ± 0.30a 0.56 ± 0.02ab 0.86 ± 0.02a 1.09 ± 0.19a 1.47 ± 0.12ab 
0.45 508.67 ± 14.77a 2,866.00 ± 111.27a 2,357.33 ± 125.48a 0.18 ± 0.01a 0.82 ± 0.01a 4.66 ± 0.37a 0.62 ± 0.05a 0.88 ± 0.01a 1.22 ± 0.20a 1.63 ± 0.17a 

Variations in specific activity parameters (activity per unit PSII reaction center when QA is the reduced state)

As shown in Table 4, compared with the control, ABS/RC, DIo/RC, TRo/RC, and ETo/RC had no significant changes after 0.05–0.45 mM Cd2+ treatment for 7 d (P > 0.05). Compared with the control, REo/RC significantly increased by 44% after treatment with 0.30 mM Cd2+ for 7 d (P < 0.05). These results indicated that Cd2+ treatment may not have a significant inhibitory effect on electron transport efficiency in the photosynthetic apparatus.

Table 4

Variations in specific activity parameters of M. korsakowii exposed to different Cd2+ concentrations for 7 d (activity of the unit PSII reaction centre when QA is in the reduced state)

Cd2+/mMABS/RCDIo/RCTRo/RCETo/RCREo/RC
2.73 ± 0.10a 0.43 ± 0.05a 2.31 ± 0.06a 1.17 ± 0.05a 0.25 ± 0.02b 
0.05 2.91 ± 0.19a 0.47 ± 0.05a 2.44 ± 0.14a 1.03 ± 0.02a 0.25 ± 0.00b 
0.15 3.04 ± 0.23a 0.54 ± 0.07a 2.51 ± 0.16a 1.07 ± 0.03a 0.33 ± 0.03ab 
0.30 3.19 ± 0.20a 0.56 ± 0.07a 2.63 ± 0.13a 1.16 ± 0.01a 0.36 ± 0.03a 
0.45 3.19 ± 0.14a 0.57 ± .06a 2.62 ± 0.10a 0.98 ± 0.11a 0.32 ± 0.02ab 
Cd2+/mMABS/RCDIo/RCTRo/RCETo/RCREo/RC
2.73 ± 0.10a 0.43 ± 0.05a 2.31 ± 0.06a 1.17 ± 0.05a 0.25 ± 0.02b 
0.05 2.91 ± 0.19a 0.47 ± 0.05a 2.44 ± 0.14a 1.03 ± 0.02a 0.25 ± 0.00b 
0.15 3.04 ± 0.23a 0.54 ± 0.07a 2.51 ± 0.16a 1.07 ± 0.03a 0.33 ± 0.03ab 
0.30 3.19 ± 0.20a 0.56 ± 0.07a 2.63 ± 0.13a 1.16 ± 0.01a 0.36 ± 0.03a 
0.45 3.19 ± 0.14a 0.57 ± .06a 2.62 ± 0.10a 0.98 ± 0.11a 0.32 ± 0.02ab 

Variations in specific activity parameters (activity per unit cross-sectional area of light receiving leaves, t = 0)

As shown in Table 5, compared with the control, when treated with 0.45 mM Cd2+ for 7 d, ABS/CSo and DIo/CSo increased significantly by 8.69 and 28.66%, respectively (P < 0.05). In contrast, ETo/CSo decreased by 21.59% (P < 0.05). Compared with the control, when treated with 0.05–0.45 mM Cd2+ for 7 d, there was no significant change in TRo/CSo and REo/CSo (P > 0.05).

Table 5

Variations in specific activity parameters of M. korsakowii exposed to different Cd2+ concentrations for 7 d (activity per unit cross-sectional area of lighted leaves, t = 0)

Cd2+/mMABS/CSoDIo/CSoTRo/CSoETo/CSoREo/CSo
468.00 ± 15.62b 73.41 ± 7.54b 394.59 ± 8.61a 200.75 ± 6.53a 43.29 ± 4.23a 
0.05 487.33 ± 2.96ab 78.83 ± 3.27ab 408.50 ± 0.80a 173.18 ± 13.57ab 42.61 ± 2.63a 
0.15 497.67 ± 11.10ab 86.80 ± 3.28ab 410.87 ± 13.01a 176.56 ± 12.83ab 53.39 ± 4.28a 
0.30 502.33 ± 6.84ab 87.22 ± 4.38ab 415.11 ± 8.41a 184.26 ± 9.60ab 56.80 ± 7.60a 
0.45 508.67 ± 14.77a 94.45 ± 9.00a 417.55 ± 5.86a 157.40 ± 17.39b 51.68 ± 2.34a 
Cd2+/mMABS/CSoDIo/CSoTRo/CSoETo/CSoREo/CSo
468.00 ± 15.62b 73.41 ± 7.54b 394.59 ± 8.61a 200.75 ± 6.53a 43.29 ± 4.23a 
0.05 487.33 ± 2.96ab 78.83 ± 3.27ab 408.50 ± 0.80a 173.18 ± 13.57ab 42.61 ± 2.63a 
0.15 497.67 ± 11.10ab 86.80 ± 3.28ab 410.87 ± 13.01a 176.56 ± 12.83ab 53.39 ± 4.28a 
0.30 502.33 ± 6.84ab 87.22 ± 4.38ab 415.11 ± 8.41a 184.26 ± 9.60ab 56.80 ± 7.60a 
0.45 508.67 ± 14.77a 94.45 ± 9.00a 417.55 ± 5.86a 157.40 ± 17.39b 51.68 ± 2.34a 

Variations in specific activity parameters (activity per unit cross-sectional area of light receiving leaves, t = tFM)

As shown in Table 6, compared with the control, DIo/CSm significantly increased by 8.69% after treatment with 0.45 mM Cd2+ for 7 d (P < 0.05). Compared with the control, 0.05–0.45 mM Cd2+ treatment for 7 d had no significant effect on ABS/CSm, and a similar tendency was also observed in TRo/CSm, ETo/CSm, and REo/CSm (P > 0.05).

Table 6

Specific activity parameters of M. korsakowii exposed to different Cd2+ concentrations for 7 d (activity per unit cross-sectional area of lighted leaves, at t = tFM) (7 d)

Cd2+/mMABS/CSmDIo/CSmTRo/CSmETo/CSmREo/CSm
3,012.33 ± 116.03a 468.00 ± 15.62b 2,544.33 ± 128.67a 1,292.00 ± 46.60a 282.67 ± 41.82a 
0.05 3,020.33 ± 91.10a 487.33 ± 2.96ab 2,533.00 ± 93.86a 1,079.67 ± 122.11a 265.33 ± 26.03a 
0.15 2,869.00 ± 197.87a 497.67 ± 11.10ab 2,371.33 ± 188.27a 1,023.67 ± 123.54a 307.67 ± 30.94a 
0.30 2,909.00 ± 164.60a 502.33 ± 6.84ab 2,406.67 ± 161.23a 1,072.33 ± 108.82a 332.33 ± 59.12a 
0.45 2,866.00 ± 111.27a 508.67 ± 14.77a 2,357.33 ± 125.48a 903.00 ± 151.74a 293.33 ± 29.61a 
Cd2+/mMABS/CSmDIo/CSmTRo/CSmETo/CSmREo/CSm
3,012.33 ± 116.03a 468.00 ± 15.62b 2,544.33 ± 128.67a 1,292.00 ± 46.60a 282.67 ± 41.82a 
0.05 3,020.33 ± 91.10a 487.33 ± 2.96ab 2,533.00 ± 93.86a 1,079.67 ± 122.11a 265.33 ± 26.03a 
0.15 2,869.00 ± 197.87a 497.67 ± 11.10ab 2,371.33 ± 188.27a 1,023.67 ± 123.54a 307.67 ± 30.94a 
0.30 2,909.00 ± 164.60a 502.33 ± 6.84ab 2,406.67 ± 161.23a 1,072.33 ± 108.82a 332.33 ± 59.12a 
0.45 2,866.00 ± 111.27a 508.67 ± 14.77a 2,357.33 ± 125.48a 903.00 ± 151.74a 293.33 ± 29.61a 

Variations in performance index

The photosynthetic performance index can accurately reflect the changes in photosynthetic reaction center activity in plant leaves under adversity. PIabs is a performance index that mainly absorbs light energy and can reflect the overall status of the function and structure of PSII in plant leaves. As shown in Table 7, compared with the control, 0.05 mM Cd2+ treatment for 7 d had no significant effect on PIInst and PIabs (P > 0.05). After 0.15–0.45 mM Cd2+ treatment for 7 d, PIInst and PIabs significantly decreased by 41.04–53.76% and 40.86–53.85%, respectively (P < 0.05). Compared with the control, 0.05–0.45 mM Cd2+ treatment for 7 d had no significant effect on PItotal (P > 0.05).

Table 7

Variations in performance index of M. korsakowii exposed to different Cd2+ concentrations for 7 d

Cd2+/mMPIInstPIabsPItotal
1.73 ± 0.16a 2.08 ± 0.19a 0.59 ± 0.12a 
0.05 1.16 ± 0.27ab 1.39 ± 0.32ab 0.45 ± 0.10a 
0.15 1.02 ± 0.20b 1.23 ± 0.24b 0.52 ± 0.08a 
0.30 1.03 ± 0.20b 1.24 ± 0.23b 0.58 ± 0.18a 
0.45 0.80 ± 0.21b 0.96 ± 0.25b 0.45 ± 0.08a 
Cd2+/mMPIInstPIabsPItotal
1.73 ± 0.16a 2.08 ± 0.19a 0.59 ± 0.12a 
0.05 1.16 ± 0.27ab 1.39 ± 0.32ab 0.45 ± 0.10a 
0.15 1.02 ± 0.20b 1.23 ± 0.24b 0.52 ± 0.08a 
0.30 1.03 ± 0.20b 1.24 ± 0.23b 0.58 ± 0.18a 
0.45 0.80 ± 0.21b 0.96 ± 0.25b 0.45 ± 0.08a 

Variations in the kinetics curve of chlorophyll fluorescence induction

The chlorophyll fluorescence induction kinetic curve usually reflects the growth status and stress tolerance of plants. As shown in Figure 1, after 0.05–0.45 mM Cd2+ treatment for 7 d, the variation trend of the OJIP curve of the long-flowering leaves was basically the same. Compared with the control, after 0.05–0.45 mM Cd2+ treatment for 7 d, the curves rose sharply at the O, K, and J points, which were highest in the 0.45 mM Cd2+ treatment. From point I, the rise rate of the curves decreased under 0.05–0.45 mM Cd2+ treatment for 7 d, and the values of I and P points were the highest under 0.05 mM Cd2+ treatment.
Figure 1

The chlorophyll fluorescence induction kinetic curve of M. korsakowii exposed to different Cd2+ concentrations for 7 d.

Figure 1

The chlorophyll fluorescence induction kinetic curve of M. korsakowii exposed to different Cd2+ concentrations for 7 d.

Close modal

Variations in SOD, POD, CAT, GR, and APX activities

Figure 2 shows the activities of antioxidant enzymes in the leaves of M. korsakowii under different Cd2+ concentrations. Compared with the control, 0.15–0.30 mM Cd2+ treatment for 7 d decreased SOD activity by 47.66–59.89% (P < 0.05), and SOD activity reached the lowest value in the 0.30 mM Cd2+ treatment. Compared with the control, 0.05–0.30 mM Cd2+ treatment for 7 d had no significant effect on POD activity (P > 0.05), while 0.45 mM Cd2+ treatment for 7 d increased POD activity by 25.44% (P < 0.05). Compared with the control, CAT activity significantly increased by 16.97% after treatment with 0.30 mM Cd2+ for 7 d (P < 0.05). Compared with the control, 0.05–0.45 mM Cd2+ treatment for 7 d had no significant effect on GR activity (P > 0.05). Compared with the control, 0.05–0.45 mM Cd2+ treatment for 7 d markedly increased APX activity by 208.53–391.51% (P < 0.05).
Figure 2

Variations in SOD (a), POD (b), CAT (c), GR (d), and APX (e) activities in leaves of M. korsakowii exposed to different Cd2+ concentrations for 7 d. Different lowercase letters indicate significant differences (P < 0.05).

Figure 2

Variations in SOD (a), POD (b), CAT (c), GR (d), and APX (e) activities in leaves of M. korsakowii exposed to different Cd2+ concentrations for 7 d. Different lowercase letters indicate significant differences (P < 0.05).

Close modal

Cd2+ concentrations in roots, stems, and leaves

As shown in Table 8, compared with the control, 0.05–0.45 mM Cd2+ treatment for 7 d markedly increased the root Cd2+ content of M. korsakowii from 10.43 to 57.86 times (P < 0.05). Compared to the control, after 0.15–0.45 mM Cd2+ treatment for 7 d, the Cd2+ content in the aboveground parts significantly increased from 6.33 to 18.67 times (P < 0.05), and the change trend of Cd2+ in the stem was the same as that in the aboveground parts, with a significant increase from 39 to 109 times (P < 0.05). Compared to the control, 0.05–0.45 mM Cd2+ treatment for 7 d had no significant change on leaf Cd2+ content (P > 0.05). Compared to the control, the transport factor (TF) was significantly decreased by 64.63–73.17% after treatment with 0.05–0.45 mM Cd2+ for 7 d (P < 0.05). These results indicate that the root is an important organ for the enrichment of Cd2+ in M. korsakowii, which can reduce the Cd2+ content in shoots to a certain extent.

Table 8

Variations in Cd2+ concentrations accumulated in roots, stems, and leaves of M. korsakowii exposed to different Cd2+ concentrations for 7 d

Cd2+/mMCd2+ concentration (g/kg, dry weight)
TF
RootAboveground partStemLeaf
0.07 ± 0.01e 0.06 ± 0.01d 0.01 ± 0.00d 0.04 ± 0.01a 0.82 ± 0.07a 
0.05 0.80 ± 0.07d 0.17 ± 0.02d 0.10 ± 0.02d 0.08 ± 0.01a 0.22 ± 0.01b 
0.15 1.71 ± 0.12c 0.44 ± 0.09c 0.40 ± 0.08c 0.03 ± 0.01a 0.27 ± 0.07b 
0.30 3.06 ± 0.05b 0.76 ± 0.05b 0.72 ± 0.05b 0.03 ± 0.01a 0.25 ± 0.03b 
0.45 4.12 ± 0.13a 1.18 ± 0.05a 1.10 ± 0.03a 0.07 ± 0.02a 0.29 ± 0.02b 
Cd2+/mMCd2+ concentration (g/kg, dry weight)
TF
RootAboveground partStemLeaf
0.07 ± 0.01e 0.06 ± 0.01d 0.01 ± 0.00d 0.04 ± 0.01a 0.82 ± 0.07a 
0.05 0.80 ± 0.07d 0.17 ± 0.02d 0.10 ± 0.02d 0.08 ± 0.01a 0.22 ± 0.01b 
0.15 1.71 ± 0.12c 0.44 ± 0.09c 0.40 ± 0.08c 0.03 ± 0.01a 0.27 ± 0.07b 
0.30 3.06 ± 0.05b 0.76 ± 0.05b 0.72 ± 0.05b 0.03 ± 0.01a 0.25 ± 0.03b 
0.45 4.12 ± 0.13a 1.18 ± 0.05a 1.10 ± 0.03a 0.07 ± 0.02a 0.29 ± 0.02b 

Data is mean value ± SE of three independent experiments. Different small letters in the same column indicate significant differences at P < 0.05.

Chlorophyll is the material basis for photosynthesis in plants. In our present study, in the 0.05 mM Cd2+ treatment the plant showed a normal growth, while the 0.15 mM Cd2+ treatment induced chlorosis in M. korsakowii leaves. Under a higher Cd2+ concentration (0.30–0.45 mM), most leaves showed obvious chlorosis and drying, which was probably related to the large decrease in chlorophyll contents (Table 1). This may be because Cd2+ (i) directly interferes with chlorophyll biosynthesis (Nanda & Agrawal 2016); (ii) binds to sulfhydryl (-SH) groups of various enzymes in chloroplasts, resulting in disruption of the chloroplast structure and function (Sakuraba et al. 2013); and (iii) inhibits Mg2+ chelation with protoporphyrin IX, thus hindering chlorophyll biosynthesis (Xin et al. 2020). In this experiment, the carotenoid content decreased less than the chlorophyll content, which is consistent with Singh & Tewari (2003) conclusion that heavy metals generally have a greater effect on chlorophyll than carotenoids. Bayat et al. (2022) found that carotenoids of Heliantus annus increased under heavy metal stress, and played an important role in scavenging reactive oxygen species and reducing photochemical damage. However, at high Cd2+ concentration (0.30–0.45 mM), carotenoid content of M. korsakowii decreased significantly, indicating that the degree of Cd2+ stress exceeded its antioxidant capacity at this time.

Pn, Gs, E, and VPD are important indicators of photosynthesis, and their changes can directly reflect the photosynthetic capacity of plants (Tartachnyk & Blanke 2004). We found that with the increase of Cd2+ concentration, Pn, Gs, and Ci decreased, while Ls increased (Table 2). Berry & Downton (1982) found that the reasons for the decrease of Pn in plant leaves caused by stress include stomatal and non-stomatal factors. If Gs decreased and Ci increased, the decrease in the photosynthetic rate was mainly caused by non-stomatal factors. If Gs and Ci decreased at the same time, the decrease in photosynthetic rate was mainly caused by stomatal factors (Shi et al. 2009). Therefore, stomatal closure is likely the main factor in the decrease of Pn under Cd2+ stress. Additionally, we found that Cd2+ stress induced a significant decrease in CUE, which may be due to the reduction of CO2 absorption capacity because of stomatal closure, which hinders plant biomass accumulation. In addition, there is a significant negative correlation between VPD and Gs (y = −860.6x + 3,110.1, r2 = 0.9875), and E decreases significantly under Cd2+ stress, indicating that the increase in VPD caused by Cd2+ treatment leads to a decrease in stomatal conductance and thus hinders transpiration, which destroys the water metabolism balance in leaves. Similar results have also been found in Pontederia cordata under heavy metal stress (Ma et al. 2020).

Chlorophyll a fluorescence is an important tool for detecting and analyzing photosynthetic functions in plants, providing a wealth of information for studying the photosystem and its electron transfer processes, and is an ideal probe for studying the photosynthetic physiological status of plants and the relationship between plants and adversity stress (Lin 1992). The light energy (ABS/CSo and ABS/RC) absorbed per unit PSII reaction center in plant leaves is mainly used for the distribution of electron transport (ETo/CSo and ETo/RC) and energy dissipation (DIo/CSo and DIo/RC) (Meng et al. 2014). In this study, under the stress of 0.45 mM Cd2+ concentration, the absorbed light energy (ABS/CSo) per unit cross-sectional area of the leaves increased significantly, while the energy captured per unit reaction center for QA reduction (TRo/CSo and TRo/RC) did not change significantly. Moreover, the energy used for electron transport per unit cross-section area (ETo/CSo) decreased significantly (Tables 4 and 5), which may be due to the high concentration of Cd2+ causing stress. This led to the absorption and capture of light energy in the reaction center of the leaves, most of which dissipated in the form of heat, as demonstrated by the significant increase in DIo/CSo (Table 5). This will help maintain a balance between light absorption and utilization, thereby alleviating photooxidative damage to photosynthetic organs (Perron et al. 2012). Singh et al. (2022) found that PIabs continuously increased with increasing concentration of Cu up to 30 μM, and this indicates PSII reaction center of L. minor were still working well. However, under 0.45 mM Cd2+ concentration stress, the variable fluorescence Vj of M. korsakowii significantly increased (Table 3), while the leaf performance indexes PIInst and PIabs decreased (0.15–0.45 mM Cd2+) (Table 7), indicating that the activity of the PSII reaction center in leaves decreased under a higher Cd2+ concentration. This reduced the utilization and conversion efficiency of light energy in PSII reaction center.

OJIP fluorescence kinetics is sensitive to environmental stress and can reveal changes in photosynthetic mechanism efficiency in plant leaves under stress. It has become one of the most popular tools in photosynthesis research (Zhang & Liu 2016). The PSII reaction center is reduced to QA- after photoexcitation, and QB cannot accept electrons from QA- in time to oxidize it, resulting in a large accumulation of QA- and thus the appearance of the J phase (Luka & Aegerter 1993). In this study, the 0.45 mM Cd2+ treatment had a higher Vj, indicating that the transfer of electrons from QA- to QB was blocked, leading to a large accumulation of QA- and an increase in the fluorescence value, indicating that M. korsakowii was subjected to significant Cd2+ stress. Other studies have shown that when the donor side of photosynthetic plant PSII is damaged, its water lysis system is inhibited and the oxygen release complex (OEC) is damaged, so that the characteristic site (before point J of the OJIP curve) will appear about 300 μs after the plant is exposed to light. At this time, the chlorophyll fluorescence yield will rise rapidly, and point K will appear. The polyphase fluorescence O-J changes to O-K-J (Li et al. 2005). This was also demonstrated in this study (Figure 1), indicating that Cd2+ destroys the PSII oxygen-evolving complex in leaves.

Antioxidant enzymes play a very important role in plants’ responses to heavy metal stress and can indicate the degree of pollution of heavy metals through the degree of oxidation (Seth et al. 2007). SOD can disproportionate superoxide anions into hydrogen peroxide (H2O2) and alleviate the oxidative damage induced by superoxide anions (Khan et al. 2016). When Cd2+ concentration was 0.15–0.30 mM, SOD activity in the leaves significantly decreased. Similar result was also demonstrated in Miscanthus sacchariflorus (Zhang et al. 2021) under heavy metal stress. This may be because Cd2+ binds to the SOD enzyme protein-SH, causing damage to its catalytic center or enzyme structure (Li & Mei 1989). POD, CAT, and APX are responsible for the decomposition of H2O2 into H2O and O2 (Bowler et al. 1992). POD has a dual role. On the one hand, POD can remove H2O2 in the early stage of adversity or aging, showing a protective effect; on the other hand, POD participates in the production of reactive oxygen species and chlorophyll degradation and can trigger membrane lipid peroxidation, which is manifested as a harmful effect. It is generally believed that its main role lies in the latter (Zhang & Kirkham 1993). In this study, the POD activity of leaves under high concentrations of Cd treatment increased significantly, indicating that Cd2+ may stimulate the process of phenolic biosynthesis, thereby inducing an increase in POD enzyme activity (Zhu et al. 2021). CAT activity changes significantly only when the concentration of Cd2+ is 0.30 mM, which may be because CAT shows a low affinity for H2O2 in plant cells and cannot effectively scavenge H2O2 itself (Iqbal et al. 2010). In this study, Cd2+ stress induced a significant increase in APX activity in leaves. This is conducive to improving the ability of leaf cells to scavenge H2O2 and alleviating membrane peroxidation, which may be a physiological mechanism by which M. korsakowii copes with Cd2+ stress (Younis et al. 2018). However, under the treatment of different concentrations of Cd2+, the GR activity in leaves did not significantly change. This may be because Cd2+ stress interfered with the electron transfer in the photosynthetic electron transport chain and destroyed the dynamic balance of NADPH/NADP+, resulting in a lack of reducing power in plant cells (Zhang & Kirkham 1996).

In this study, the Cd2+ content in the shoot of M. korsakowii reached 100 mg·kg−1, and the bioconcentration factor (BCF) of Cd2+ was greater than 1, while the transport factor (TF) was less than 1 (Table 8), indicating that M. korsakowii was efficient in enriching Cd2+, and mainly immobilized Cd2+ in the roots and inhibited its transportation to the shoot. This may be related to the accumulation of stable macromolecular complexes or insoluble organic macromolecules after Cd2+ enters root cortex cells with proteins, polysaccharides, ribose, and nucleic acids, among others, thus alleviating the toxic effect of excessive Cd2+ on the aboveground parts (Zhang & Huang 2000). In the process of enrichment and translocation of Cd2+, M. korsakowii can still maintain normal growth and ornamental garden value when the plant was exposed to 0.05 mM Cd2+. Meanwhile, with characteristics of large biomass and easy harvesting, M. korsakowii has great utilization value in the phytoremediation of low-cadmium-polluted water. Similar results have been found in many wetland plants such as Typha domingensis (Akhter et al. 2022).

In order to evaluate the phytoremediation potential of Monochoria korsakowii in heavy metal contaminated water, we in the present study investigated variations in photosynthesis, chlorophyll contents, antioxidant enzyme activities in leaves, and Cd2+ translocation and accumulation in the plant with various Cd2+ concentration exposure. Cd2+ disturbed the plant photosynthesis in terms of declined chlorophyll content and the disturbed gas exchange parameters. With the plant exposed to Cd2+, the reduced photosynthetic efficiency was related to electron transport chain activity inhibition and oxygen-evolving complex destruction. The increased APX activity in leaves accounted for the plant tolerance, and increased heat dissipation in photosynthetic apparatus in the plant leaves could alleviate the photooxidative damage induced by the highest Cd2+ concentration exposure. In addition, majority of Cd2+ immobilized in the plant roots declined Cd2+ translocation from roots to shoots, thus alleviating the toxic effect of excessive Cd2+ on the aboveground parts. In conclusion, M. korsakowii can be a potential candidate in phytoremediation of low-cadmium-polluted water.

We are grateful for the support provided by the Advanced Analysis and Testing Center (AATC) of Nanjing Forestry University. We also thank LetPub (www.letpub.com) for its linguistic assistance during the preparation of this manuscript.

Wei Zhou: Conceptualization, methodology, software, data curation, writing – original draft, visualization, investigation, and validation. Jianpan Xin: Conceptualization, supervision, writing – review and editing. Runan Tian: Conceptualization, methodology, supervision, writing – review and editing, project administration, and funding acquisition.

The present investigation was funded by the National Natural Science Foundation of China (No. 30972408) and the Priority Academic Program Development of Jiangsu Higher Education Institutions.

Data cannot be made publicly available; readers should contact the corresponding author for details.

The authors declare there is no conflict.

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Author notes

The authors contributed equally to this work.

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