Integrative study of subcellular distribution, chemical forms, and physiological responses for understanding cadmium tolerance in two garden shrubs

doi:10.21203/rs.3.rs-5311541/v1

Background and aims Urban ornamental shrubs have significant potential for restoring cadmium (Cd)-contaminated soil. Simulated pot pollution was applied to Buxus sinica and Ligustrum × vicaryi to study their Cd enrichment characteristics and tolerance mechanisms.

Methods Cd content and accumulation were analyzed in different plant organs, subcellular distribution and chemical forms of Cd in the roots, and the effects of Cd on the ultrastructure of root cells under various Cd concentrations (0, 25, 50, 100, and 200 mg·kg⁻¹).

Results (1) With increasing Cd treatment levels, the total biomass of B. sinica gradually decreased, while L. ×vicaryi exhibited a stimulation effect at low Cd concentrations and inhibition at high Cd concentrations. (2) The Cd content in different organs of both shrubs increased with rising Cd levels, with L. × vicaryi showing a significantly higher increase than B. sinica, indicating a stronger Cd accumulation capability in L. × vicaryi. (3) Cd in the root of both shrubs was primarily present in NaCl-extractable forms, and was majorly bound to the cell wall. (4) Excessive Cd caused damage to the cellular structure of B. sinica leaves, while the cells of L. × vicaryileaves maintained normal morphology. (5) In both shrubs, Cd primarily binds to the cell wall through hydroxyl, amino functional groups, and soluble sugars.

Conclusion Converting Cd to less active forms, immobilizing Cd in the cell wall, and providing binding sites through functional groups may be crucial resistance mechanisms for both shrubs in response to Cd stress.

Cadium

Buxus sinica

Ligustrum × vicaryi

Physiological changes

Subcellular distribution

Chemical form

Industrial activities, transportation emissions, and substantial construction waste associated with urban development have significantly increased the heavy metal content of soils in urban areas, leading to environmental pollution (Capuana 2020). Cadmium (Cd) is one of the most widely distributed heavy metals and is known for its high toxicity and mobility (Ali et al. 2014; Kong et al. 2020). Research on heavy metal pollution in urban soils in China indicates that Cd contamination levels exceed the background values for urban soils, making it a heavy metal pollutant that requires focused management (He et al. 2023; Pan et al. 2018; Tong et al. 2020). Cd is a typical non-essential mineral element that can harm photosynthesis and metabolic activities in plants when it accumulates excessively. Furthermore, Cd can easily enter animals and humans through the food chain, posing a significant risk to human health (Guo et al. 2015; Zhao et al. 2019). Therefore, it is crucial to implement active remediation measures for Cd-contaminated soil to maintain a stable ecosystem.

Physical and chemical methods for remediating heavy metal-contaminated soil have limitations, such as high costs and the potential for secondary pollution. Phytoremediation technology is a green, in-situ remediation approach that utilizes plants to extract or stabilize heavy metals in the soil, offering favorable economic and ecological benefits along with promising application prospects (Ali et al. 2013; Zeng et al. 2018). Currently, research on the phytoremediation of Cd primarily focuses on herbs such as Sedum alfredii (Li et al. 2015), Thlaspi caerulescens (Zhao et al. 2003), and Solanum nigrum (Wei et al. 2005). However, herbs face challenges for large-scale engineering applications due to low biomass production and prolonged remediation times. In contrast, woody plants possess larger biomass and well-developed root systems, enhancing the exchange of heavy metal ions between soil and roots, thereby effectively absorbing heavy metal pollutants. Consequently, woody plants have become a research hotspot in phytoremediation in recent years (Capuana 2011). Based on the distribution and accumulation characteristics of Cd in woody plants, these species serve different phytoremediation purposes. For example, Salix spp. (Yang et al. 2020), Morus alba (Zeng et al. 2020), Koelreuteria bipinnata (Luo et al. 2015), and Lonicera japonica (Liu et al. 2009) primarily assimilate Cd in their roots, making them ideal tree species for Cd phytostabilization. Populus spp. (He et al. 2013), Koelreuteria paniculata (Yang et al. 2018) and Eucalyptus spp. (Iori et al. 2017) exhibit strong adaptability to Cd stress, showcasing great potential for restoring Cd-contaminated soil. Existing studies primarily conduct pot or hydroponic experiments with saplings, while there is a lack of research focusing on commonly used urban ornamental shrubs that have high aesthetic value and broad applicability.

B. sinica and L. × vicaryi are common shrubs found in urban green spaces, characterized by their strong stress resistance, wide adaptability, and ease of transplantation and survival. Studies have shown that both shrubs can accumulate Cd in urban environments and have potential for remediating Cd-contaminated soil (Chen et al. 2022; Zeng et al. 2018; Zhang et al. 2022). However, research on the mechanisms of Cd accumulation and tolerance in these two shrubs still needs to be conducted. Therefore, this experiment selected B. sinica and L. × vicaryi as subjects for pot pollution simulation experiments. It investigated their physiological indices, Cd content, and accumulation characteristics in different plant organs, as well as the subcellular distribution, chemical form, ultrastructure, and cell wall functional groups of Cd in the roots under various Cd treatments. The aim is to analyze the enrichment characteristics and tolerance mechanisms of both shrubs under Cd stress, providing a theoretical basis for their effective application in remediating Cd-contaminated soil.

Plant material

The 4-year-old saplings of B. sinica and L. × vicaryi used in the experiment were purchased from a nursery stock base in Shunyi District, Beijing, China. The experimental soil was a mixture of peat soil and perlite (v/v, 8:2), with its basic physicochemical properties and background values of heavy metals shown in Table 1. Based on the Cd content of soil in Beijing (Jia et al. 2023) and the range of content adapted by plants in preliminary tests, this experiment established five levels of Cd contamination treatments: 0 (CK), 25 (T₁), 50 (T₂), 100 (T₃), and 200 mg·kg^− 1 (T₄).

Table 1

Basic physical and chemical properties and heavy metal background value of soil
pH	Organic matter/ g·kg^− 1	Total N/ g·kg^− 1	Alkali-hydrolyzable N/ g·kg^− 1	Total P/ mg·kg^− 1	Available P/ mg·kg^− 1	Total K/ mg·kg^− 1	Olsen-K/ mg·kg^− 1	Cd mg·kg^− 1
7.55	329.2	11.28	1.75	556	4.93	3274	57.32	0.21

Experimental design

In early March, 5 kg of mixed soil was added to each 3-gallon plastic pot (24 cm in diameter, 26.5 cm deep), with trays placed underneath the pots to prevent heavy metal loss and environmental pollution. According to the predetermined gradients, analytical-grade CdCl₂·2.5H₂O powder was weighed and dissolved in deionized water. Subsequently, an aerosol sprayer was used to ensure that the heavy metal solution uniformly penetrated the soil, guaranteeing an even mixture of the drug and soil. After that, the contaminated soil was placed in a cool location to equilibrate for one month, and three parallel groups were processed for each Cd concentration treatment. In early April, saplings with similar height, crown width, and root length were selected for transplantation into the pots, with one plant per pot. Deionized water was regularly sprayed in consistent amounts during subsequent growth to maintain the soil moisture content at 60–70% of field holding capacity. In early September, samples were collected using the complete harvest method.

Measurement Methods

The harvested plants were thoroughly rinsed with tap water three times. Subsequently, the plant roots were dipped in 20 mmol·L^− 1 Na₂-EDTA for 20 minutes to eliminate surface-absorbed cadmium (Cd). Afterward, the plants were rinsed three times with deionized water, dried, and then divided into leaf, stem, and root tissues, which were later used for the determination of various studied parameters. Some plant samples were dried in an oven at 105°C for 30 minutes, followed by further drying at 70°C until a constant dry weight was achieved, allowing for the determination of plant dry weight and Cd content. The final samples were stored after being finely ground using a pulverizer. Other plant samples were preserved in a − 80°C refrigerator (Meng et al. 2024).

After grinding, 1 g of each root, branch, and leaf sample was digested using the HNO₃-H₂O₂ method. Following complete digestion, the samples were filtered and brought to a constant volume of 50 mL. The Cd content in the plant tissues was measured using inductively coupled plasma emission spectrometry (ICP-OES, Agilent 5110) (Konieczynski et al. 2020). Additionally, 0.5 g of fresh leaf samples was soaked in 10 mL of 96% ethanol in the dark for 24 hours to measure chlorophyll a, b, and carotenoid contents, as described by Chen et al. (2022) Cell membrane permeability was assessed using the electrical conductivity method, following Kaya et al. (2009). Different chemical forms of Cd in the plants were sequentially extracted using differential centrifugation and chemical reagents, according to the method of Zou et al. (2023). Differential centrifugation was employed to separate the subcellular distribution of Cd, as outlined by Wang et al. (2012). The ultrastructure of plant cells was observed using transmission electron microscopy, following the method of Jiang et al. (2007). The plant cell walls of the roots were extracted using the method described by Riaz et al. (2018), elucidating the information on chemical functional groups in the plant cell walls under Cd stress through Fourier transform infrared spectroscopy measurements.

Statistical analysis

All data obtained were statistically analyzed using Excel 2010 and presented as mean ± standard deviation (S.D.). One-way analysis of variance (ANOVA) was performed on the data using SPSS 26.0, followed by Duncan's test at p < 0.05. Graphical representations were created using Origin 2021.

The bioconcentration factor (BCF) in the plant was calculated as BF = Cd content in plant tissues (mg·kg^− 1)/Cd content in the soil (mg·kg^− 1). This factor reflects the ability of the plant to assimilate and transfer Cd from the soil to its tissues (Uddin et al. 2020).

The translocation factor (TF) of Cd in the plant was calculated as TF = Cd content in shoots (mg·kg^− 1)/Cd content in roots (mg·kg^− 1), which is used to evaluate the plant's capability to transport Cd from the roots to the shoots (Zakaria et al. 2021).

Plant growth

To study the effect of exogenously applied Cd on plant growth, the biomass of B. sinica and L. × vicaryi was analyzed. Results indicated that the total biomass of B. sinica gradually decreased as the Cd treatment gradient increased, while that of L. × vicaryi showed a pattern of promotion at low Cd concentrations and inhibition at high Cd concentrations. Under different Cd treatment gradients, the leaf biomass of B. sinica was not affected compared to the control. However, the biomass of the branches and roots of B. sinica decreased gradually with increasing Cd treatment gradients, with minimum values of 26.80 g and 29.46 g, respectively, representing reductions of 31.89% and 62.69% under T2 and T4 treatments compared with the control (P < 0.05). Likewise, the biomass of leaves and branches in L. × vicaryi showed no notable change under Cd stress, whereas root biomass exhibited an initial increase followed by a decrease as Cd concentrations increased. As shown in Table 1, the reduction in root biomass was smallest (32.71 g) at T3 treatment, significantly reduced by 27.05% compared to the control (P < 0.05; Table 1).

Table 1 Biomass of two shrubs treated with different Cd treatments (g)

Shrub	Treatment	Leaf	Branch	Root	Total
Buxus sinica	CK	44.87±8.92a	39.35±7.01a	78.97±8.56a	163.19±21.48a
	T₁	49.50±4.67a	38.11±4.91a	68.07±12.23ab	155.67±16.32ab
	T₂	38.18±8.27a	26.80±5.43b	54.20±9.11b	119.18±19.75c
	T₃	38.65±2.55a	32.09±4.49ab	54.81±11.48b	125.54±16.58bc
	T₄	39.84±7.33a	28.04±2.72b	29.46±6.97c	102.09±19.00c
Ligustrum×vicaryi	CK	40.90±2.78a	42.51±4.36a	44.84±4.52ab	128.26±9.48ab
	T₁	42.11±4.73a	43.77±4.01a	46.63±4.38a	132.50±9.59a
	T₂	41.87±5.46a	42.92±4.13a	53.17±10.60a	137.96±11.76a
	T₃	39.35±3.84a	42.40±1.45a	32.71±1.32c	114.46±1.09b
	T₄	36.67±3.82a	41.48±2.24a	35.44±3.79bc	113.58±9.26b

Note: Values are presented as mean ± S.D. Values with different letters within the same column indicate significant differences at the P < 0.05 level between concentrations according to Duncan test.

Leaf pigment content

With the increase of the Cd treatment gradient, the chlorophyll a and carotenoid contents in the leaves of B. sinica displayed a decreasing trend, peaking at T4 treatment (0.58 mg·g⁻¹) and reaching the lowest at T3 treatment (0.16 mg·g⁻¹), both of which were significantly different from the control (P < 0.05). Additionally, the chlorophyll b content of B. sinica initially decreased and then increased with the increasing Cd treatment gradient, reaching its minimum at T1 treatment and maximum at T4 treatment, both noticeably lower compared to the control (P < 0.05). The chlorophyll a content of L. × vicaryi showed a tendency to increase and then decrease with increasing Cd treatment gradients, reaching a maximum value of 0.78 mg·g⁻¹ at T2 treatment, but there was no significant difference compared with the control. Similarly, the chlorophyll b and carotenoid contents were unaffected by Cd exposure compared to the control (P > 0.05; Fig. 1).

Fig. 1 Changes in the leaf pigment content of two shrubs with different Cd treatments. Data points and error bars represent mean and S.D., respectively. Different letters within the same pattern indicate statistically significant differences at P < 0.05 according to Duncan test.

Cell membrane permeability

Low to medium concentrations of cadmium (Cd) had a beneficial effect on the cell membrane permeability of B. sinica branches, which gradually decreased as the Cd concentration increased to high levels. The membrane permeability of B. sinica branches was highest in the T4 treatment, being 1.33-fold greater than that of the control (P<0.05). The root membrane permeability of B. sinica also gradually increased with rising Cd content, peaking in the T4 treatment, with significant differences compared to the control (P<0.05). However, there was no significant difference in the membrane permeability of B. sinica leaves compared to the control under different Cd treatments. In contrast, the membrane permeability of the leaves did not significantly differ from the control across various treatment gradients. The membrane permeability of L. × vicaryi leaves increased with increasing Cd content. In the T1-T4 Cd treatments, it was 1.01- to 1.57-fold higher than that of the control. However, Cd treatment did not significantly impact the cell membrane permeability of L. × vicaryi branches and roots (Fig. 2).

Fig. 2 Changes in cell membrane permeability of two shrubs at different Cd concentrations. Data points and error bars represent mean and S.D., respectively. Different letters within the same pattern indicate statistically significant differences at P < 0.05 according to Duncan test.

Cd content in various tissues

The Cd content in various tissues of B. sinica and L. × vicaryi significantly increased with the Cd treatment gradient, peaking at the T4 treatment with notable differences compared to the control (P<0.05). Generally, the Cd content in the roots of B. sinica and L. × vicaryi was significantly higher than that in the leaves and branches within the same treatment gradient, being 117.68-fold and 38.30-fold higher than that of the leaves, and 133.90-fold and 32.73-fold higher than that of the branches, respectively. Moreover, exogenous Cd application could noticeably further increase the Cd content in various tissues of L. × vicaryi compared to B. sinica as the Cd content increased. As shown in Table 2, the Cd content in the leaves, branches, and roots of L. × vicaryi was 19.01 times, 9.42 times, and 2.01 times higher than that of B. sinica, respectively (Table 2).

Table 2 Cd concentration in tissues of two shrubs at different Cd concentration treatments

Shrub	Treatment	Leaf	Branch	Root
Buxus sinica	CK	0.14±0.04b	0.20±0.04d	0.57±0.13c
	T₁	0.25±0.09b	0.41±0.08cd	16.29±4.57c
	T₂	0.68±0.16a	0.66±0.06b	63.64±12.55b
	T₃	0.70±0.18a	0.50±0.17bc	66.95±12.81b
	T₄	0.82±0.16a	1.71±0.21a	96.50±7.87a
Ligustrum×vicaryi	CK	0.14±0.04d	0.12±0.03d	0.76±0.05e
	T₁	0.94±0.06d	1.10±0.13d	36.00±3.07d
	T₂	2.93±0.19c	5.24±0.76c	74.01±10.70c
	T₃	9.74±0.39b	9.32±0.21b	158.23±21.58b
	T₄	15.59±2.05a	16.11±2.69a	202.73±31.42a

Note: Values are presented as mean ± S.D. Values with different letters within the same column indicate significant differences at P < 0.05 level between concentrations according to Duncan test.

Cd bioconcentration factors and translocation factor

Under Cd treatment, the bioconcentration factor (BCF) of the aerial parts of both shrubs was less than 1, with no significant differences among the various treatment gradients. After the application of exogenous Cd, the BCF values of the roots of both shrubs increased at low Cd levels, gradually decreasing as the Cd concentration rose to high levels, with the lowest BCF values observed in the T4 treatment. Furthermore, the BCF values of the roots of L. × vicaryi were consistently greater than 1, while those of B. sinica exceeded 1.0 only in the T2 treatment. By calculating the translocation factor (TF) of Cd, it was found that the TF values of B. sinica and L. × vicaryi were both significantly less than 1, ranging from 0.01 to 0.32 and 0.03 to 0.17, respectively. Additionally, after increasing exogenous Cd treatment, the TF of L. × vicaryi was higher than that of B. sinica under the same Cd treatment (Table 3).

Table 3 Cd enrichment coefficients in tissues of two shrubs at different Cd concentrations

Shrub	Treatment	BCF			TF
Shrub	Treatment	Leaf	Branch	Root	TF
Buxus sinica	CK	0.67±0.19a	0.95±0.04a	2.70±0.60a	0.32±0.11a
	T₁	0.01±0.00b	0.02±0.27b	0.65±0.18c	0.02±0.04b
	T₂	0.01±0.00b	0.02±0.00b	1.27±0.25b	0.02±0.00b
	T₃	0.01±0.00b	0.01±0.00b	0.67±0.13c	0.01±0.00b
	T₄	0.00±0.00b	0.01±0.00b	0.48±0.04c	0.01±0.00b
Ligustrum×vicaryi	CK	0.68±0.17a	0.59±0.12a	3.63±0.23a	0.17±0.03a
	T₁	0.04±0.00b	0.04±0.01b	1.44±0.12b	0.03±0.00b
	T₂	0.06±0.00b	0.10±0.02b	1.48±0.21b	0.06±0.00b
	T₃	0.10±0.00b	0.09±0.00b	1.58±0.22b	0.06±0.01b
	T₄	0.08±0.01b	0.08±0.01b	1.01±0.16c	0.08±0.23b

Note: Values are presented as mean ± S.D. Values with different letters within the same column indicate significant differences at the P < 0.05 level between concentrations according to Duncan test.

Chemical forms

According to our analyses, the chemical form of Cd extracted by NaCl was dominant in the roots of B. sinica (19.21% to 69.45%) and L. × vicaryi (21.02% to 69.87%). The distribution ratio of NaCl-extractable Cd in the roots of these two shrubs increased with exogenous Cd application and peaked at the T4 treatment (P<0.05). In B. sinica roots, Cd extracted by HAc, which is less mobile and toxic, increased when Cd content was low and then decreased as the exogenous Cd treatment content increased. However, the distribution ratios of the more mobile and toxic Cd_E and Cd_W tended to decrease with enhanced Cd levels. In contrast, the proportions of CdE and Cd_W in L. × vicaryi roots did not change significantly with increasing Cd treatment gradient, while the proportions of other chemical forms of Cd showed a decreasing trend. Overall, the dominant chemical form of Cd in the roots of both shrubs was moderately active (Fig. 3).

Fig. 3 Distribution ratio of Zn chemical forms in roots of two shrubs. Cd_E, nitrate, chloride based inorganic salts and amino acids, etc. Cd_W, water soluble organic acid salts, heavy metal phosphates [M(H₂PO₄)₂], etc.; Cd_NaCl, pectinates, heavy metals in the bound or adsorbed state of proteins, etc.; Cd_HAc, insoluble metallic phosphates; Cd_HCl, oxalic acid salt etc.; Cd_R, residual form.

Subcellular distribution

Under Cd treatment, the proportion of Cd in the roots of B. sinica and L. × vicaryi primarily accumulated in the cellular debris fractions, accounting for 54.95% to 72.95% and 30.50% to 60.70%, respectively. The proportion of Cd in the cellular debris fraction of B. sinica increased with the addition of Cd to the soil and peaked at the T4 treatment (P<0.05). Nevertheless, the percentages of Cd in the organelle component and heat-sensitive protein fractions gradually decreased with increasing Cd concentration in the soil. As the Cd treatment gradient increased, the subcellular distribution of Cd in L. × vicaryi showed a remarkable increase in heat-stabilized proteins, while opposite trends were observed in metal-enriched particles and heat-sensitive protein fractions. Moreover, the proportion of Cd in L. × vicaryi's cellular debris fractions increased when the Cd level was low and gradually reduced as the Cd concentration increased to higher levels (Fig. 4).

Fig. 4 Proportion of Zn in subcellular distribution of roots of two shrubs. F1, Metal-enriched particles; F2, Cellular debris；F3, Organelle components; F4, Heat-sensitive protein; F5, Heat stabilized protein.

Ultrastructure of root cells

In this study, control (CK), low content (T2), and high content (T4) groups were selected to further observe the microscopic changes in root cell morphology and the distribution of Cd in the cells under Cd treatment using transmission electron microscopy (TEM). Fig. 5a,b showed that, under low concentration Cd treatment, there was an increase in the intercellular gap compared with CK in B. sinica, along with obvious black deposits in the cells. When Cd content was high, the cell arrangement in B. sinica was disrupted, cells were significantly deformed, and a large amount of black deposits accumulated on the cell walls and in the vacuoles. Similarly, for L. × vicaryi, there was a substantial aggregation of black deposits within the cells, predominantly near the cell walls, vacuoles, and cell plasmodesmata under low Cd treatment. At high levels of Cd, some Ligustrum vicaryi cells disintegrated, and cell walls ruptured, with black deposits accumulating near the cell walls and cell plasmodesmata.

Fig. 5 Ultrastructure of root cells of two shrubs at different Cd concentration treatments. (a) Buxus sinica. (b) Ligustrum×vicaryi. co, cortex; pe, pericycle; ph, phloem; ca, cambium; xy, xylem; SG, starch grain; CW, Cell wall; CP, cell plasmodesmata; V, vacuole; M, mitochondria; BM, black matter.

Fourier transform infrared spectroscopy of root cell wall

The Fourier transform infrared spectroscopy (FTIR) spectra of B. sinica and L. × vicaryi were analyzed in the control (CK), low concentration (T2), and high concentration (T4) groups to determine the changes in functional groups of the cell wall in plant roots under Cd stress (Fig. 6a,b, Table 5). The ratio A/A₂₉₂₇ represents the absorbance of the characteristic peak of methyl (-CH3) relative to that of the characteristic peak, which can be used for semi-quantitative analysis of the functional groups involved in heavy metal binding based on changes in the ratio. The study showed that the cell walls of B. sinica and L. × vicaryi roots contain abundant functional groups, especially oxygen-containing functional groups. Under Cd treatment, the absorption peaks with the largest shifts in the cell walls of Buxus roots were the stretching vibration peaks of hydroxyl/amino and cellulose carbohydrate rings, which shifted 12 cm to lower frequencies and 8 cm to higher frequencies under low Cd treatment, and 8 cm to lower frequencies and 6 cm to higher frequencies under high Cd treatment, respectively. In the cell walls of L. × vicaryi roots, significant shifts were observed in the stretching vibration peaks of hydroxyl/amino, carboxyl, and cellulose glycan carbohydrate rings under Cd treatment, resulting in shifts of 6, 5, and 4 cm to higher frequencies at T4 treatment, respectively. Additionally, the A/A₂₉₂₇ values of the hydroxyl/amino and cellulose glycan stretching vibration absorption peaks in the cell walls of L. × vicaryi roots decreased with increasing Cd treatment, while the A/A₂₉₂₇ values of the carboxyl characteristic peaks in the treatment groups were higher than those in the control.

Fig. 6 Infrared spectrum characterization of root cell walls of two shrubs with different Cd concentration treatments. (a) Buxus sinica. (b) Ligustrum×vicaryi.

Table 5 Analysis of infrared spectrum characteristic peaks in the root cell walls of two shrubs under different Cd concentration treatments

Species	Number	Function group	Wavenum-ber/cm^-1	CK	Cd-T₂		Cd-T₄
Species	Number	Function group	Wavenum-ber/cm^-1	A/A_29-27	A/A_29-27	Offset/cm^-1 cm^-1	A/A_29--27	Offse-t/cm^-1 cm^-1
Buxus sinica	1	hydroxyl/amino (-OH/-NH)	3400	1.43	1.47	-12	1.37	-8
	2	Methyl (-CH₃)	2927	1.00	1.00	0	1.00	0
	3	Amide(I) (-C=O)	1644	1.13	1.20	1	1.14	2
	4	Amide(Ⅱ) (-N-H)	1515	0.87	0.82	1	0.85	1
	5	Carbon-Hydrogen(C-H)or Carbon-Oxygen (C-O)	1429	0.94	0.91	1	0.93	2
	6	alcoholic hydroxyl C-O	1315	0.86	0.79	0	0.84	0
	7	Sulfate ester (C-O-S) or carboxyl (C-O) or phosphoric acid (C-O-P)	1264	0.92	0.84	-1	0.88	-1
	8	cellulose glycan bending (-C-H) or (-C-C, -C-O)	1042	1.27	1.28	8	1.26	6
Ligustrum×vicaryi Ligustrum×vicaryi Ligustrum×vicaryium×vicaryi	1	hydroxyl/amino (-OH/-NH)	3400	1.71	1.62	4	1.60	6
	2	Methyl (-CH₃)	2927	1.00	1.00	0	1.00	0
	3	Amide(I) (-C=O)	1644	1.11	1.15	-2	1.17	-1
	4	Amide(Ⅱ) (-N-H)	1515	0.74	0.83	1	0.82	0
	5	Carbon-Hydrogen (C-H) or Carbon-Oxygen (C-O)	1429	0.91	0.95	-1	0.94	-3
	6	Carboxyl (-COOH) or Amide(Ⅲ) (-C-N)	1377	0.88	0.93	3	0.92	5
	7	alcoholic hydroxyl (C-O)	1315	0.86	0.91	-2	0.90	0
	8	Sulfate ester (C-O-S) or carboxyl (C-O) or phosphoric acid C-O-P	1264	0.93	0.98	0	0.95	-1
	9	cellulose glycan bending (-C-H) or (-C-C, -C-O)	1042	1.60	1.47	2	1.42	4

Tolerance characteristics of two shrubs under Cd stress

Plant growth characteristics and physiological metabolism are crucial evaluation indicators for assessing plant tolerance to heavy metal toxicity. Cd is a non-essential element for plant growth; however, excessive Cd can inhibit plant development, damage cellular structures, and impair functional activity, leading to irreversible effects on the plant (Wang et al. 2020). In this study, Cd exhibited a strong toxic effect on B. sinica. As the levels of Cd treatment increased, the biomass of B. sinica gradually decreased. Additionally, the results indicated that lower concentrations of Cd (25, 50 mg·kg⁻¹) promoted biomass accumulation in L. × vicaryi, while higher concentrations of Cd (100, 200 mg·kg⁻¹) inhibited plant growth to some extent. This suggests that L. × vicaryi has a stronger tolerance to Cd-contaminated soil compared to B. sinica. Similar responses were observed in other plants under Cd stress. The biomass accumulation of Sphagneticola calendulacea showed no significant effect at lower concentrations of 25 mg·kg⁻¹; however, higher Cd treatment (≥ 100 mg·kg⁻¹) notably inhibited plant growth (Lu et al. 2020). In L. × vicaryi,, biomass production significantly increased when Cd concentrations were low (≤ 100 mg·kg⁻¹), but there was a sharp decline under higher Cd treatment (≥ 25 mg·kg^− 1) (Jia et al. 2015). These studies suggest that different plants have varying adaptation ranges to Cd content, and appropriate levels of Cd can promote plant growth to a certain extent, potentially playing a positive role in Cd accumulation.

Photosynthesis is a crucial process by which plants convert energy from their environment, and the levels of photosynthetic pigments reflect the efficiency of this process. Chlorophyll a, chlorophyll b, and carotenoids are the primary components of photosynthetic pigments. Studies have shown that Cd stress can reduce the activity of chlorophyll synthase and activate enzymes involved in chlorophyll degradation, leading to a decrease in the synthesis and content of photosynthetic pigments, manifesting as leaf yellowing (Zhang et al. 2020). Additionally, since Cd is a non-essential element for plants, it can bind with thiol groups in proteins, damaging the structure and functional activity of chloroplasts (Cherif et al. 2012). In this study, it was observed that the contents of chlorophyll a and carotenoids in B. sinica exhibited an overall declining trend with increasing Cd treatment levels, and similar trends were seen in chlorophyll a, chlorophyll b, and carotenoids of L. × vicaryi. Similarly, Dutta et al. (2024)reported a reduction in chlorophyll a, chlorophyll b, and carotenoid contents in the leaves of Arachis hypogaea with higher exogenous Cd levels. Furthermore, this study revealed that low Cd content initially inhibited chlorophyll b content in B. sinica, but higher levels promoted it. The same trend was observed in Davidia involucrata, where chlorophyll b levels initially decreased under lower Cd treatment but increased with higher Cd concentrations (Yang et al. 2020). This phenomenon suggests that plants may enhance their tolerance to Cd by increasing their chlorophyll content (Dezhban et al. 2015).

The cell membrane is a crucial structure that regulates and controls the transport and exchange of substances across cells. Under normal conditions, the cell membrane exhibits selective permeability. However, when plants are stressed by heavy metals, the permeability of the cell membrane increases, leading to the leakage of intracellular components and the entry of external substances, resulting in physiological dysfunction (Wei et al. 2014). Changes in plasma membrane permeability are assessed by the conductivity of plant cell extracts, which serves as an indicator of plant responses to heavy metal pollution. Under Cd stress, the relative conductivity during the tillering and ripening stages of rice significantly exceeded that of the control, indicating increased plasma membrane permeability and severe membrane damage (Huang et al. 2018). Similarly, in the present study, the relative conductivity of cell plasma membranes in various tissues of B. sinica and the leaves of L. × vicaryi increased with higher Cd content, suggesting that the permeability of cell plasma membranes in both shrubs progressively increased, leading to greater intracellular substance leakage. This phenomenon may be attributed to Cd stress causing alterations in the composition of plasma membrane lipid fatty acids and enhanced oxidative processes, which result in increased permeability and reduced membrane stability (Spiridonova et al. 2019).

Analysis of tolerance characteristics of two shrubs under Cd stress

Root retention or translocation to the aerial parts of plants plays a pivotal role in their tolerance to heavy metals in the soil (Shen et al. 2021). In this study, the Cd content in various tissues of B. sinica and L. × vicaryi significantly increased with higher Cd concentrations. Furthermore, most of the Cd absorbed was retained in the roots, suggesting that both shrubs can limit the translocation of Cd to the aerial parts, consistent with previous studies on species such as Impatiens walleriana (Lai 2015), Morus spp. (Huang et al. 2018), and Boehmeria nivea (Wang et al. 2008), which primarily accumulate Cd in their roots, with accumulation levels increasing alongside Cd concentration. Therefore, the accumulation of heavy metals in the roots is one of the key mechanisms for tolerating heavy metal stress. The excessive accumulation of Cd in the roots may be due to the role of inner cortex cells in the root tissue, which serve as lateral interceptors, limiting the transfer of Cd to the aerial parts and thereby mitigating Cd toxicity and its impacts on physiological metabolism in plants (Akhter et al. 2014).

BCF and TF are two key parameters used to evaluate heavy metal accumulation efficiency in plants (Wu et al. 2011). In this study, the BCF values of the aerial tissues of B. sinica and L. × vicaryi were relatively low. However, the BCF values of the roots of L. × vicaryi were consistently higher than 1 when treated with different concentrations of Cd, while those of the roots of B. sinica exceeded 1 only under T2 treatment. Additionally, BCF values of the roots of both shrubs decreased with increasing Cd concentration. Furthermore, the TF values of both shrubs under Cd treatment were less than 1, which was significantly lower than those in the control group. This phenomenon suggests that Cd stress reduced the ability of the plants to absorb and translocate Cd to the aerial parts. Plants with BCFs and TFs greater than 1 are usually considered suitable for phytoextraction, whereas those with high BCF (> 1) and low TF (< 1) are considered suitable for phytostabilization (Hou et al. 2020). In the present study, the roots of both shrubs exhibited higher BCF and lower TF values, indicating their efficient ability to restrict Cd translocation to the aerial parts, thus positioning them as potential woody plants for stabilizing Cd-contaminated soil. This finding aligns with results from other studies, where the BCF values of Calendula calypso were greater than 1 under each Cd treatment, while TF values were less than 1, making it suitable for the stabilization of Cd-contaminated soil (Farooq et al. 2020). Similarly, the BCF values of the roots and stems of Euryops pectinatus exceeded 1 under Cd stress, while TF values remained lower than 1, reflecting its relatively higher Cd accumulation capacity, thereby protecting the aerial parts from Cd toxicity (Jia et al. 2023).

Analysis of accumulation mechanisms of two shrubs under Cd stress

Heavy metals absorbed and transported by plants in various chemical forms are present in different tissues (Liu et al. 2019). The toxicity and mobility of Cd are closely associated with its chemical forms. Consequently, research has focused on extracting different chemical forms of Cd using various extractants, revealing that the lower the polarity of the chemical forms, the stronger their migration ability and greater their toxicity. The migration ability of Cd in ethanol- and water-extractable fractions is higher than in other forms, and these forms exhibit greater toxicity to organisms (Zheng et al. 2023). In the roots of Landoltia punctata, the NaCl-extracted state, which has moderate toxicity and mobility, was the predominant form of Cd (30.15–88.66%). Additionally, the proportion and concentration of HCl- and HAc-extracted Cd increased with rising Cd concentration (Wang et al. 2021). A similar characteristic has been observed in the roots of oilseed rape (Ru et al. 2006) and Solanum nigrum (Li et al. 2020), where the proportion of NaCl-extractable Cd was the highest. The results of this study align with previous research, indicating that in the roots of B. sinica and L. × vicaryi, most of the Cd was primarily in the NaCl-extractable form, with the proportion of NaCl-extracted Cd notably increasing with higher Cd content. According to Wu et al. (2016), NaCl extraction mainly comprised pectate and protein-integrated Cd, which may form complexes with organic groups on the root cell wall, resulting in reduced toxicity. Furthermore, a larger proportion of Cd in the NaCl-extracted state may alleviate Cd toxicity, allowing it to occupy a relatively high proportion in plants. It was also found that as exogenous Cd content increased, the proportion of chemical forms with high mobility and toxicity decreased in the roots of these two shrubs. These findings are consistent with studies on Agrocybe aegerita, which converted Cd into undissolved pectate and protein-bound forms when subjected to Cd stress to reduce Cd toxicity (Li et al. 2019). Similarly, in the leaves of Salix matsudana, the proportion of HCl- and HAc-extracted Cd in the roots increased with rising Cd concentration ( Zou et al.(2023). Overall, these results suggest that plants may tolerate heavy metals by converting Cd into less toxic chemical forms, with the dominant forms and their proportions varying among different plant species.

The mode of heavy metal subcellular distribution in plants is a crucial factor in determining the extent of metal toxicity and the plant tolerance mechanism. Previous research has shown that plants can regionalize heavy metals in relatively inactive areas, such as cell walls and soluble fractions, to reduce their toxicity (Ma et al. 2023). In this study, Cd in the roots of B. sinica and L. × vicaryi was primarily accumulated in the cell walls (54.95%-72.95% and 30.50%-60.70%, respectively). These findings are consistent with studies on Kandelia obovata (Weng et al. 2012), Salix matsudana (Wu et al. 2017), and Miscanthus sacchariflorus (Xin et al. 2018), which also reported a high proportion of Cd predominantly stored in the cell walls. The cell wall serves as the first barrier for cells to mitigate Cd damage, as its surface can fix heavy metal ions and limit their access to the plasma membrane and cytoplasm, thereby alleviating Cd toxicity (Loix et al. 2017; Yu et al. 2020). Additionally, increasing the thickness of the cell wall to fix heavy metals plays a critical role in Cd retention in woody plants (Li et al. 2023). Furthermore, in the current study, the proportion of heat-sensitive proteins in L. × vicaryi increased with higher Cd content, indicating that these components may also have a mitigating effect under Cd stress. Overall, the subcellular distribution results demonstrate that retaining Cd in the cell walls of roots may play a significant role in the Cd detoxification mechanism of these two shrubs.

To understand the mechanisms of cadmium (Cd) detoxification, it is essential to explore the internal structural changes of cells through ultrastructural observation. In the current study, a significant accumulation of dark deposits was observed on the cell walls of the roots of both shrub species under Cd stress. This finding aligns with previous research, which reported visible Cd deposits in the cell walls of Dittrichia viscosa after 10 days of treatment with 15 mg·kg^− 1 Cd, with a marked increase corresponding to higher Cd concentrations and prolonged exposure (Fernández et al. 2014). Furthermore, electron-dense precipitates were identified in vacuoles and on the cell walls of the roots of cotton and Juncus effusus at high Cd concentrations (1000 µM) (Daud et al. 2013; Najeeb et al. 2011). Cd stress can adversely affect plant cellular structures and impair physiological metabolic functions. For instance, the morphology of root cells in Sesuvium portulacastrum exhibited deformation with increasing Cd treatment concentrations, including cell wall breakdown, cell membrane protrusions, vacuole contraction, mitochondrial and nuclear disassembly, and an increase in the number of starch granules (Uddin et al. 2023). Similar ultrastructural alterations were observed in the root cells of two shrub species under high Cd stress (200 mg·kg^− 1) in this study. The cell structure of B. sinica was severely altered under high Cd stress, with noticeable fracturing in cell arrangement. In contrast, the ultrastructural integrity of L. × vicaryi was less compromised, suggesting a stronger tolerance to Cd-contaminated soil.

The binding and transformation of Cd in plants primarily occur within the cell walls, which are composed mainly of pectin, cellulose, hemicellulose, and proteins. Pectin and hemicellulose provide functional groups such as hydroxyl, carboxyl, amino, and aldehyde groups, which can adsorb and immobilize positively charged heavy metal ions, thereby limiting their entry into the plasma membrane (Lai 2015; Yu et al. 2021). Analysis of the changes in characteristic peaks in FTIR spectra revealed that the cell wall of B. sinica enhanced its adsorption capabilities for Cd ions by regulating the content of hydroxyl and amino functional groups, as well as soluble sugars. Additionally, in L. × vicaryi, the presence of hydroxyl, amino, and carboxyl functional groups, along with soluble sugars in the cell walls, played a pivotal role in mitigating Cd toxicity. This finding corroborates previous studies suggesting that hydroxyl, amino, cyano, and carboxyl functional groups in cell walls can bind to Cd, contributing to tolerance against Cd in castor seedlings (He et al. 2020). Hydroxyl, amino, and carboxyl functional groups have also been shown to be crucial for the tolerance and accumulation of Cd in the cell walls of Solanum nigrum (Jia et al. 2019; Wang et al. 2021). Furthermore, hydroxyl, carboxyl, and amide groups may serve as the primary binding sites for Cd in the cell walls of Conyza canadensis seedlings (Yu et al. 2020). Thus, the ability of B. sinica and L. × vicaryi to accumulate and tolerate Cd may be linked to the compartmentalization of plants, the adjustment of their chemical forms and subcellular distribution under stress, and the immobilization of Cd on the cell wall through functional groups.

From the current study, we concluded that Cd stress inhibited the growth of B. sinica, while it promoted growth at low Cd concentrations and inhibited it at high Cd concentrations in L. × vicaryi. However, neither of the plants died under various Cd treatments. Additionally, considerable dark deposits were observed in the vacuoles as well as attached to the cell walls of the roots of both shrubs following Cd treatment. The cell structure of B. sinica was severely altered under high Cd stress compared to that of L. × vicaryi. Observations of plant biomass and cellular microstructure indicated that L. × vicaryi exhibited stronger resistance to Cd-contaminated soil than B. sinica.

The content of chlorophyll a and carotenoids in the leaves of B. sinica decreased with increasing Cd concentrations, while the content of chlorophyll b initially decreased and then increased as the Cd treatment gradient increased, showing significant differences compared to the control. In contrast, there were no remarkable differences in the chlorophyll a, chlorophyll b, and carotenoid content in the leaves of L. × vicaryi compared with the control. The plasma membrane permeability of various tissues in B. sinica increased with higher Cd treatment gradients, whereas that of L. × vicaryi noticeably increased compared to the control only in the leaves. These results indicated that the photosynthetic pigments and plasma membrane permeability of all tissues in B. sinica are more sensitive to Cd stress.

The Cd content in various organs of both shrubs increased with rising Cd treatment concentrations, with the highest levels found in the roots. In the roots of both shrubs, the NaCl-extracted state, which has moderate toxicity and mobility, was the predominant form of Cd, and the proportion and concentration of less toxic chemical forms increased with rising Cd concentrations. Moreover, both shrubs primarily accumulated Cd in the cell debris fraction of their roots, suggesting that they convert Cd to a less active form and retain it in the cell walls to mitigate its toxicity.

FTIR spectroscopy revealed that certain functional groups, such as hydroxyl and amino groups, were involved in binding with Cd in the cell walls of both shrubs. Additionally, the results suggested that the two shrubs can absorb Cd through various functional groups to alleviate Cd toxicity.

Competing interest

The authors have no relevant fnancial or non-fnancial interests to disclose.

Acknowledgements

This work was supported by the National Natural Science Foundation of China (31600574); Beijing Joint Construction Project; Beijing Forestry University to Build a World-Class Discipline and Guide the Development Special Fund (2019XKJS0322); Scientific Research and Postgraduate Training Joint Research Project of Beijing Education Commission (2019GJ-03). The authors thank all those who provided helpful suggestions and critical comments on this manuscript.

Author Contributions Shiyin Yu, Shan Wang, Min Tang and Meixian Wang designed this research and revised the manuscript critically; Shan Wang, Shuzhen Pan, Min Tang and Meixian Wang conducted feld work and laboratory analysis; Shiyin Yu, Min Tang and Meixian Wang carried out the data analysis and drafted the manuscript. All authors read and approved the final manuscript.

Data Availability

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

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Integrative study of subcellular distribution, chemical forms, and physiological responses for understanding cadmium tolerance in two garden shrubs

Status:

Version 1

Abstract

Figures

Introduction

Materials and methods

Statistical analysis

Results

Discussion

Conclusion

Declarations

Competing interest

Acknowledgements

Data Availability

References

Status:

Version 1