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. 2024 Oct 23;24:997. doi: 10.1186/s12870-024-05723-z

Exogenous silicon alleviates aluminum stress in Eucalyptus species by enhancing the antioxidant capacity and improving plant growth and tolerance quality

Linjuan Huang 1,2,3,#, Hongying Li 1,2,3,#, Yishan Luo 1,2,3,#, Jingzhong Shi 1,2,3, Le Kong 1,2,3, Weichao Teng 1,2,3,✉
PMCID: PMC11515708  PMID: 39443879

Abstract

Background

As an efficient and high-quality additive in agriculture and forestry production, silicon (Si) plays an important role in alleviating heavy metal stress and improving plant growth. However, the alleviating effect of aluminum (Al) toxicity by Si in Eucalyptus is still incomplete.

Results

Here, a study was conducted using two Al concentrations (0 and 4.5 mM) with four Si concentrations (0, 0.5, 1, and 1.5 mM) to investigate plant growth, tolerance and antioxidant defense system in four Eucalyptus species (Eucalyptus tereticornis, Eucalyptus urophylla, Eucalyptus grandis, and Eucalyptus urophylla × Eucalyptus grandis). The results showed that the stress induced by 4.5 mM Al increased oxidative damage, disturbed the balance of enzymatic and non-enzymatic antioxidant systems, and negatively affected plant growth and tolerance quality in the four Eucalyptus species. However, the addition of 0.5 mM and 1 mM Si alleviated the effects of Al toxicity on plant growth and improved plant growth quality by strengthening stress tolerance. Besides, adding Si significantly facilitated the synergistic action of enzymatic and non-enzymatic antioxidant defenses, increased the removal of reactive oxygen species, reduced lipid peroxidation, and oxidative stress, and promoted the phytoremediation rate of the four Eucalyptus species by 18.7 ~ 34.8% compared to that in the absence of Si.

Conclusions

Silicon can alleviate the effect of Al toxicity by enhancing the antioxidant capacity and improving plant growth and tolerance quality. Hence, the application of Si is an effective method for the phytoremediation of Eucalyptus plantations in southern China.

Supplementary Information

The online version contains supplementary material available at 10.1186/s12870-024-05723-z.

Keywords: Al toxicity, Si alleviation, Enzymatic and non-enzymatic antioxidants, Plant growth quality, Eucalyptus species

Introduction

Soil acidification, indicated by a decrease in soil pH, has become a common challenge for forest management [1]. Acidic soil (pH < 5.5) accounts for nearly 30% of the world's ice-free land area, and about 67% of woodlands and forest ecosystems are found in areas with acidic soils [2]. The sources of soil acidification include mineral weathering, litter decomposition, and anthropogenic activity, and the high rates of anthropogenic inputs (e.g. burning fossil fuels and fertilization) are one of the most important causes of soil acidification [3]. From 1980 to 2019, the soil pH in China’s forest ecosystem decreased from 5.64 to 5.08, severely threatening forestry production, biodiversity, forest quality and ecological environment security [4]. Therefore, it is urgent to carry out the advanced modification of soil acidification to achieve the green and sustainable development of acidic soil.

Aluminum (Al) is the third most abundant element in the Earth’s crust, constituting almost 8% of the lithosphere, and is present primarily in the form of non-toxic aluminosilicates, alumina and sediments in soil [5, 6]. When the soil pH decreases to less than 5.5, Al is solubilized into toxic active aluminum forms, such as Al3+, Al(OH)2+, Al(OH)2+, Al(OH)3-, and Al(OH)4−) [7]. The Al toxicity caused by trivalent aluminum (Al3+) is considered to be an important limiting factor for plant growth and productivity in acidic soil [8]. Aluminum toxicity causes physiological, morphological, and biochemical injuries, such as a decrease in nutrient absorption and photosynthetic capacity, an increase in oxidative stress, inhibition of plant growth, and even damage to the structure and function of plants [9]. Despite the toxicity of Al, the mechanism by which exogenous additives alleviate Al toxicity in acidic soil remains uncertain and incomplete.

Silicon (Si) is the second most abundant element in the Earth’s crust, and its average content in the pedosphere is almost 28% [10]. Numerous studies have reported that Si is an essential and important element for plant growth and development because it regulates plant defense and resistance, especially under biotic and abiotic stress [11, 12]. The bioavailable form of Si is the dissolved monosilicic acid (H4SiO4) or thosilicic acid (Si(OH)4), which is generally absorbed in the range of 0.1–0.6 mM [12, 13]. However, the content of available Si in soil accounts for only 0.02–0.04% of the total Si, and the amount of Si absorbed by terrestrial plants from the soil Si pool greatly exceeds the amount of Si absorbed from rock weathering [14]. As Si is non-toxic, tasteless, non-polluting, and unaffected by runoff, it has been regarded as an efficient and high-quality additive for improving agricultural and forestry productivity and developing a green ecological economy in recent years [15, 16]. Although several researchers have investigated the roles of Si in agricultural and forest production management, it is still necessary to strengthen the basic and in-depth research on the role of Si in stress physiology.

Plant growth is a common index used to measure changes in plant volume, weight, quantity and net productivity, reflecting the physical, chemical and biological characteristics of plants, as well as their response to stressful environments [17]. Plants are exposed to various types of environmental stress along with secondary oxidative stress (e.g. reactive oxygen species (ROS) imbalance) throughout their whole life, and the regulatory mechanism underling growth and defense helps maintain plant normal growth [18]. Numerous studies have proved that the maintenance of normal growth depends on endogenous substances, including enzymatic antioxidants (e.g. superoxide dismutase, SOD; catalase, CAT; peroxidase, POD; ascorbate peroxidase, APX; glutathione reductase, GR) and non-enzymatic antioxidants (e.g. ascorbic acid, ASA; glutathione, GSH; glutathione disulfide content, GSSG) [7, 8]. SOD is the first line of defense against ROS, and CAT, POD and APX are other pivotal enzymes that neutralize or mitigate the harmful effects of oxidative stress [19]. The ASA-GSH cycle is a vital redox mechanism that maintains the balance of antioxidants, such as ASA and GSH, thereby preventing the uncontrolled accumulation of ROS and oxidative damage [17, 20]. Hence, maintenance of inherent redox balance in growth defense is important to counteract oxidative stress and its consequences [20].

Eucalyptus is one of the most widely planted evergreen fast-growing species in southern China. Its plantation area increased from 23 × 104 hm2 in 1976 to 546.7 × 104 hm2 in 2018 [21]. Eucalyptus not only has important economic value in terms of seedling breeding, cultivation, special fertilizer, wood processing and utilization, but also plays a significant role in soil and water conservation, climate regulation, and improvement of the ecological environment [22]. However, Eucalyptus plantations face the problems of low soil pH (< 6.5) and available Si content (79.8 mg/kg), which lead to a decline of plant quality and production [14]. Exogenous Si addition can improve plant stress resistance and tolerance by altering plant morphology, promoting secondary metabolism, and balancing oxidative defense system, but the role of Si in Eucalyptus plantations is not fully recognized [21]. Therefore, four typical Eucalyptus species (e.g. Eucalyptus cirrus, Eucalyptus urophylla, Eucalyptus grandis, and Eucalyptus urophylla × Eucalyptus grandis) were selected to conduct the study, and two levels of Al (0 mM and 4.5 mM Al) and four levels of Si (0 mM, 0.5 mM, 1 mM, and 1.5 mM) at a realistic field level of Eucalyptus artificial forest were used to explore the mitigating effect of Si on Eucalyptus growth under Al stress [12, 23]. In addition, the study aimed to clarify the mechanisms by which Si mitigates Al stress, focusing on oxidative stress, enzymatic and non-enzymatic antioxidant systems, plant growth quality, Al tolerance, and phytoremediation effects. The results of this study may contribute to the practical application of Si to protect plants from damage caused by Al toxicity, improve plant growth quality and phytoremediation, and provide a scientific basis for the rational planting and sustainable development of Eucalyptus artificial forests.

Materials and methods

Soils and plants

Four Eucalyptus species, including E. tereticornis Sm. (ET) and E. urophylla S. T. Blake (EU), E. grandis W. Hill ex Maiden (EG), and E. urophylla × E. grandis (EU × EG), were used in this study. Healthy and uniform seedlings (height: 30–40 cm, base diameter: 2–3 mm) of each species were selected from the Guangxi Dongmen State-owned Forests Farm, which is the largest Eucalyptus gene bank and the largest Eucalyptus propagation research and production base in China [21]. Soils were collected from a hill near Nanning, which is an area with typical acidic soil in southern China. The soils were transported to the experimental site, air-dried at 20–35 ℃ for two months, ground, sieved (1 cm), and fully mixed to ensure uniform physical properties. Previous experiments have shown that 7 kg of dried soil in a 25 cm × 22 cm pot can maintain normal growth for Eucalyptus seedlings with a year [22, 23]. Hence, each seedling was planted in a pot (25 cm high and 22 cm diameter) with 7 kg of dried soil. The chemical properties of the substrates were as follows: pH 5.03, organic matter 17.70 g/kg, total phosphorus 0.49 g/kg, available phosphorus 47.36 mg/kg, total nitrogen 1.54 g/kg, ammonium nitrogen 11.76 mg/kg, nitrate nitrogen 10.77 mg/kg, total potassium 5.62 g/kg, available potassium 27.14 mg/kg, and total aluminum 308.76 mg/kg.

Experimental design

Our pot experiment was carried out at the forestry college of Guangxi University, China (22°50′52.88″N, 108°17′35.11″E). This area belongs to the subtropical monsoon climate, with ample light and rainfall. The average temperature is 21.6 ℃, ranging from 13 ℃ (in January) to 28.9 ℃ (in July). Precipitation amounts to 1290 mm per year, the average humidity is 76%, and the average sunshine hours per year is about 1585 h.

Our pot experiments included eight treatments in each Eucalyptus species (Fig. 1): (1) 0 mM Al + 0 mM Si (Al0Si0, CK), control; (2) 0 mM Al + 0.5 mM Si (Al0Si1), only 0.5 mM Si addition; (3) 0 mM Al + 1.0 mM Si (Al0Si2), only 1.0 mM Si addition; (4) 0 mM Al + 1.5 mM Si (Al0Si3), only 1.5 mM Si addition; (5) 4.5 mM Al + 0 mM Si (Al1Si0), only 4.5 mM Al addition; (6) 4.5 mM Al + 0.5 mM Si (Al1Si1), with 4.5 mM Al and 0.5 mM Si addition; (7) 4.5 mM Al + 1.0 mM Si (Al1Si2), with 4.5 mM Al and 1.0 mM Si addition; and (8) 4.5 mM Al + 1.5 mM Si (Al1Si3), with 4.5 mM Al and 1.5 mM Si addition. The pot experiment was conducted using a completely randomized design (CRD) with eight replicates. After the soils were balanced, each pot was irrigated with 100 mL of water per day to keep a 60–70% of field capacity. Seedlings were transplanted to the pots on 24th March 2023 and left a month for the adaptation of seedling. Thereafter one month of transplantation, Al levels as aluminium chloride (AlCl3·6H2O: 0 mM and 4.5 mM, pH = 5.03) solution and Si levels as sodium silicate (Na2SiO3·9H2O: 0 mM, 0.5 mM, 1 mM, and 1.5 mM, pH = 5.03) solution were applied in pot experiment. The control were added an equal water with same pH. We first added the AlCl3 solution. About one week later, seedlings exhibited a series of Al toxic symptoms (e.g. leaves started withering), and the Na2SiO3 solution was added. Plants were harvested after two months later.

Fig. 1.

Fig. 1

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Design of the pot experiments in this study

Plant measurement

During harvesting, the plants were cut at the stern base and separated into leaves, stems and roots. Roots were extracted carefully with running water to obtain the root system for each plant. The leaf thickness (LT) was measured with the electronic Vernier Caliper (Accuracy: 0.01 mm), while the height (H) was measured with aluminium tape. Leaf area (LA) measure using a scanner and ImageJ Software [25]. Total root length (RL) and root volume (RV) were analyzed with WinRHIZO (Regent Instrument Inc., Canada). Also, plant leaf biomass (LB), stem biomass (SB) and root biomass (RB) samples were dried in the oven at 80–100 ℃ for 48–72 h until the weight was constant, then the biomass was recorded. The below-ground biomass (BGB) is the root biomass, and the above-ground biomass (AGB) is the sum of leaf biomass and stem biomass. Plant leaf tolerance (LTe), plant stem tolerance (STe), and plant root tolerance (RTe) were determined by dividing dry weight at treatments by dry weight at control [26].

About 5 g fresh, healthy and fully expanded leaves were collected for plant oxidative stress (malondialdehyde content, MDA; nicotinamide adenine dinucleotide phosphate oxidase activity, NOX; superoxide anion content, O2·−; hydrogen peroxide content, H2O2), antioxidant enzyme activity (dehydroascorbate reductase activity, DHAR; monodehydroascorbate reductase activity, MDHAR; glutathione reductase activity, GR; catalase activity, CAT; ascorbate peroxidase activity, APX; peroxidase activity, POD; superoxide dismutase activity, SOD), and non-enzymatic antioxidant content (dehydroascorbic acid content, DHA; ascorbate content, ASA; glutathione disulfide content, GSSG; glutathione content, GSH) analysis according to the procedures of Zhao et al. [27], Liang et al. [24], Hasanuzzaman et al. [28], and Duan et al. [29], respectively.

Qualification of plant growth, tolerance, oxidative stress and antioxidant

Plant growth index (PGI) was calculated using an PGI area approach by comparing the area on a radar graph comprising of typical growth parameters [30]. The equations were as follows:

PGI=0.5×∑inSLi2×sin(2π/n) 1
SLi=X/Xmax 2

In this equation, n is the number of parameters using in the PGI area, SLi is the linear score of the factor i varying from 0 to 1, X is the actual measured value, Xmax is the maximum value of the factor i. Based on the formula, seven typical parameters (H, RV, RL, LA, LT, AGB, and BGB) of PGI were selected to represent an improvement in plant growth quality.

Similarly, plant tolerance index (PTI), plant oxidative stress index (POSI), plant enzymatic antioxidant index (PEAI) and non-enzymatic antioxidant index (PNEAI), which are four comprehensive indexes reflecting plant tolerance, oxidative stress, and enzymatic and non-enzymatic antioxidant defense quality, respectively, were determined in a same way with the PGI calculation (Eq. 1–2). Three typical parameters (LTe, STe, and RTe) of PTI, four parameters (H2O2, NOX, O2·−, and H2O2) of POSI, seven parameters (DHAR, MDHAR, GR, CAT, APX, POD, SOD) of PEAI and four parameters (DHA, ASA, GSSG, and GSH) of PNEAI were used to represent an increasing in plant tolerance, oxidative stress, enzymatic and non-enzymatic antioxidants, respectively.

Assessment of the quality of phytoremediation

About 100 g fresh soil in each treatment was collected and mixed during harvesting. After removing plant litters, soil samples were transported to the laboratory, air-dried for a month, and ground to pass through a 0.15 mm sieve for testing soil aluminum concentration. Soils were digested in a mixture of HCl-HNO3-HClO4 to analyze the Al content [31]. Then, the total content of Al was quantified using the inductively coupled plasma-optical emission spectrometer ICP-OES 5000 (Focused Photonics Inc, USA).

The quality of phytoremediation was addressed by the soil Al removal rate [32]. The equation was as follows:

Phyto(%)=(1-GTreatment/GControl)×100 3

In this equation, Phyto is the soil Al removal rate, GTreatment is the content of Al at treatment, and GControl is the content of Al at control. A larger value of Phytoindicates a better phytoremediation effect.

Statistical analysis

All statistical analyses were conducted in R4.3.3 [33]. The values presented in the figures are the means ± standard errors (SE). Data were first tested for normality using the Shapiro–Wilk test (P < 0.05) and homogeneity of variance using the Levene test (P < 0.05). Significant differences in plant growth, tolerance, oxidative stress, enzymatic and non-enzymatic antioxidant, and phytoremediation quality between the Al and Si treatments and their interaction (Al × Si) were analyzed by using a Two-way analysis of variance (ANOVA) along with Fishers’ least significant difference (LSD) test. If Al (Al0, Al1) was significant according to Two-way ANOVA, then One-way ANOVA was performed to show the significant difference between Si treatments at each Al. Radar graphs of the relative responses of plant growth, tolerance, oxidative stress, enzymatic and non-enzymatic antioxidants to Al and Si as well as bar graphs representing the comparative analysis of plant growth, tolerance, oxidative stress, enzymatic and non-enzymatic antioxidant, and phytoremediation indexes were visualized in the R4.3.3 [33]. Under the Al1 treatment, data were first calculated by subtracting the values at control from the values at treatment, then, Pearson correlations between plant growth, tolerance, oxidative stress, enzymatic and non-enzymatic antioxidant, and phytoremediation parameters were analyzed and visualized the “corrplot” package in the R4.3.3 [33].

Results

Plant growth index

Plant growth index (PGI) varied with species, Al and Si levels,. The results of Two-way ANOVA revealed that Al, Si and their interactions significantly changed the PGI in ET and EG (P < 0.05), and the PGI in EU and EU × EG significantly changed by Si and Al × Si interactions, but was not affected by Al (P > 0.05) (Fig. 2). In the same Si0, Si1 and Si2 treatments, compared to no Al addition, the Al1 addition did not affect the PGI in EU (Fig. 2d) and EU × EG (Fig. 2h), whereas the PGI significantly decreased in ET (Fig. 2b) and EG (Fig. 2f). Under Al0 treatment, compared to no Si addition, PGI significantly increased by Si1 (21.6%) and Si2 (37.8%) addition in ET; PGI significantly increased by Si1 (46.0%), Si2 (62.9%) and Si3 (73.4%) addition in EU; PGI significantly increased by Si1 (28.0%) and Si2 (11.1%) addition but decreased by Si3 (25.2%) addition in EG; PGI significantly increased by Si1 (31.6%) and Si2 (22.6%) addition in EU × EG. Under Al1 treatment, compared to no Si addition, PGI significantly increased by Si1 (33.8%) and Si2 (47.5%) addition in ET; PGI significantly increased by Si1 (78.3%), Si2 (89.0%) and Si3(116.0%) addition in EU; PGI significantly increased by Si1 (76.5%), Si2 (95.0%) and Si3(65.6%) addition in EG (Fig. 2f); PGI increased by Si1 (36.2%) and Si2 (39.7%) addition in EU × EG.

Fig. 2.

Fig. 2

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Radar chart of the relative response of plant growth parameters (a, c, e, g) and Two-way ANOVA of plant growth index (PGI) (b, d, f, h) in E. tereticornis (ET) (a, b), E. urophylla (EU) (c, d), E. grandis (EG) (e, f), and E. urophylla × E. grandis (EU × EG) (g, h), respectively. Values are averages ± standard errors (n = 4). The P-values for aluminum (Al), silicon (Si) and their interaction (Al × Si) were based on a Two-way ANOVA. Plant growth parameters included height (H), above-ground biomass (AGB), below-ground biomass (BGB), leaf area (LA), leaf thickness (LT), total root volume (RV), total root length (RL). Lowercase letters indicate that the effect is significantly different on different Si treatments in the same Al treatment, and uppercase letters indicate that the effect is significantly different on different Al treatments in the same Si treatment. Same as follows

Plant tolerance index

Plant tolerance index (PTI) varied with species, Al and Si levels. The results of Two-way ANOVA revealed that Al, Si as well as their interactions significantly changed the PTI in ET, EG and EU × EG, and the PTI in EU significantly changed by Si and Al × Si interaction but was not affected by Al (Fig. 3). In the same Si treatment, compared to no Al addition, the Al1 addition did not affect the PTI in EU (Fig. 3d), whereas PTI significantly decreased in ET (Fig. 3b). In the same Si0 and Si1 treatments, compared to no Al addition, PTI significantly decreased by Al1 addition in EG (Fig. 3f) and EU × EG (Fig. 3h). Under Al0 treatment, compared to no Si addition, PTI significantly increased by Si1 (48.3%), Si2 (89.9%) and Si3 (87.6%) addition in ET; PTIsignificantly increased by Si1 (85.7%), Si2 (118.1%) and Si3(72.3%) addition in EU; PTI significantly increased by Si1 (20.8%) addition but decreased by Si2 (10.6%) and Si3 (42.9%) addition in EG; PTI significantly increased by Si1 (68.3%) and Si2 (42.9%) addition in EU × EG. Under Al1 treatment, compared to Si0 treatment, PTI significantly increased by Si2 (74.5%) in ET; PTI significantly increased by Si1 (121.7%), Si2 (119.7%) and Si3(119.3%) in EU; PTI significantly increased by Si1 (68.3%), Si2 (42.9%) and Si3(19.5%) in EG; PTI significantly increased by Si1 (52.8%), Si2 (88.6%) and Si3(65.7%) in EU × EG.

Fig. 3.

Fig. 3

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Radar chart of the relative response of plant tolerance parameters (a, c, e, g) and Two-way ANOVA of plant tolerance index (PTI) (b, d, f, h) in E.tereticornis (ET) (a, b), E. urophylla (EU) (c, d), E. grandis (EG) (e, f), and E. urophylla × E. grandis (EU × EG) (g, h), respectively. Values are averages ± standard errors (n = 4). The P-values for aluminum (Al), silicon (Si) and their interaction (Al × Si) were based on a Two-way ANOVA. Leaf tolerance, LTe; root tolerance, RTe; stem tolerance, STe. Same as follows

Plant oxidative stress index

Plant oxidative stress index (POSI) varied with species, Al and Si levels., The resulst of Two-way ANOVA revealed that Al, Si as well as their interactions significantly changed the POSI in four Eucalyptus species (Fig. 4). In the same Si0 and Si1 treatment, compared to no Al addition, the POSI significantly increased by Al1addition in ET (Fig. 4b). In the same Si0 treatment, compared to no Al addition, the POSI significantly increased by Al1addition in EU (Fig. 4d), EG (Fig. 4f) and EU × EG (Fig. 4h). Under Al0 and Al0 treatments, compared to no Si addition, POSI significantly decreased by Si1 (33.5 ~ 49.7%), Si2 (48.4 ~ 64.2%) and Si3 (68.6 ~ 74.8%) addition in ET; POSI significantly decreased by Si1 (13.0 ~ 44.3%), Si2 (26.0 ~ 50.2%) and Si3 (46.4 ~ 62.2%) addition in EU; POSI significantly decreased by Si1 (16.6 ~ 22.2%), Si2 (28.6 ~ 34.1%) and Si3 (45.7 ~ 52.5%) addition in EG; POSI significantly decreased by Si1 (21.1 ~ 24.8%), Si2 (26.5 ~ 31.8%) and Si3 (24.6 ~ 50.2%) addition in EU × EG.

Fig. 4.

Fig. 4

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Radar chart of the relative response of plant oxidative stress parameters (a, c, e, g) and two way ANOVA of plant oxidative stress index (POSI) (b, d, f, h) in E. tereticornis (ET) (a, b), E. urophylla (EU) (c, d), E. grandis (EG) (e, f), and E. urophylla × E. grandis (EU × EG) (g, h), respectively. Values are averages ± standard errors (n = 4). The P-values for aluminum (Al), silicon (Si) and their interaction (Al × Si) were based on a Two-way ANOVA. Malondialdehyde content, MDA; nicotinamide adenine dinucleotide phosphate oxidase activity, NOX; O2·− content, O2·−; hydrogen peroxide content, H2O2

Plant enzymatic and non-enzymatic antioxidant defense index

Plant enzymatic antioxidant index (PEAI) varied with species, Al and Si levels. The results of Two-way ANOVA revealed that Al, Si as well as their interactions significantly changed PEAI in four Eucalyptus species (Fig. 5). In the same Si0 and Si1 treatment, compared to no Al addition, the PEAI significantly increased by Al1 addition in ET (Fig. 5b) and EG (Fig. 5f). In the same Si treatment, compared to no Al addition, the PEAI significantly increased by Al1 addition in EU (Fig. 5d). In the same Si0, Si1 and Si2 treatment, compared to no Al addition, the PEAI significantly increased by Al1 addition in EU × EG (Fig. 5h). Under Al0 treatment, compared to no Si addition, the PEAI significantly increased by Si1, Si2 and Si3 in four Eucalyptus species; Under Al1 treatment, compared to no Si addition, the PEAI significantly increased by Si1 and Si2 in four Eucalyptus species, significantly increased by Si3 in EU, but significantly decreased in EG and EU × EG.

Fig. 5.

Fig. 5

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Radar chart of the relative response of plant enzymatic antioxidant defense parameters (a, c, e, g) and two way ANOVA of plant enzymatic antioxidant index (PEAI) (b, d, f, h) in E. tereticornis (ET) (a, b), E. urophylla (EU) (c, d), E. grandis (EG) (e, f), and E. urophylla × E. grandis (EU × EG) (g, h), respectively. Values are averages ± standard errors (n = 4). The P-values for aluminum (Al), silicon (Si) and their interaction (Al × Si) were based on a Two-way ANOVA. Dehydroascorbate reductase activity, DHAR; monodehydroascorbate reductase activity, MDHAR; glutathione reductase activity, GR; catalase activity, CAT; ascorbate peroxidase activity, APX; peroxidase activity, POD; superoxide dismutase activity, SOD; dehydroascorbic acid content, DHA; ascorbate content, ASA; glutathione disulfide content, GSSG; glutathione content, GSH. Same as follows

Plant non-enzymatic antioxidant index (PNEAI) varied with species, Al and Si levels. The results of Two-way ANOVA revealed that Al, Si as well as their interactions significantly changed the PNEAI in ET, EU and EG, the PNEAI in EU × EG significantly changed by Si and Al × Si interaction, but not affected by Al (Fig. 6). In the same Si0, Si1 and Si2 treatment, compared to no Al addition, the PNEAI significantly decreased by Al1 addition in ET (Fig. 6b). In the same Si treatment, compared to no Al addition, Al1 addition did not affect the PNEAI in EU × EG (Fig. 6h), while the PNEAI significantly increased the PNEAI in EU (Fig. 6d). In the same Si0 treatment, compared to no Al addition, the PNEAI significantly decreased by Al1 addition in EG (Fig. 6f). Under Al0 treatment, compared to no Si addition, the PNEAI significantly increased by Si1, Si2 and Si3 addition in ET and EU; the PNEAI significantly increased by Si1 but decreased by Si2 and Si3 addition in EG and EU × EG (Fig. 6). Under Al1 treatment, compared to no Si addition, the PNEAI significantly increased by Si1, Si2 and Si3 addition in ET, EU and EG; PNEAI significantly increased by Si1 addition in EU × EG but decreased by Si2 and Si3 addition.

Fig. 6.

Fig. 6

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Radar chart of the relative response of plant non-enzymatic antioxidant parameters (a, c, e, g) and two way ANOVA of plant non-enzymatic antioxidant index (PNEAI) (b, d, f, h) in E. tereticornis (ET) (a, b), E. urophylla (EU) (c, d), E. grandis (EG) (e, f), and E. urophylla × E. grandis (EU × EG) (g, h), respectively. Values are averages ± standard errors (n = 4). The P-values for aluminum (Al), silicon (Si) and their interaction (Al × Si) were based on a Two-way ANOVA. Dehydroascorbate reductase activity, DHAR; monodehydroascorbate reductase activity, MDHAR; glutathione reductase activity, GR; catalase activity, CAT; ascorbate peroxidase activity, APX; peroxidase activity, POD; superoxide dismutase activity, SOD; dehydroascorbic acid content, DHA; ascorbate content, ASA; glutathione disulfide content, GSSG; glutathione content, GSH. Same as follows

Phytoremediation quality and relationships between plant growth, tolerance, oxidative stress, antioxidant system and phytoremediation

Phytoremediation rate (Phyto) varied with species, and the results of Two-way ANOVA revealed that Al, Si and their interactions significantly changed Phyto in ET (Fig. 7a) and EG (Fig. 7c), whereas the Phyto value in EU (Fig. 7b) and EU × EG (Fig. 7d) significantly changed by Si, but not affected by Al × Si interaction. In the same Si treatment, compared to no Al addition, the Al1 addition non-significantly decreased the Phyto in EU and EU × EG but significantly decreased in ET and EG. Under Al0 treatment, compared to no Si addition, the Phyto was significantly increased by Si1, Si2 and Si3 addition in four Eucalyptus species. Under Al1 treatment, the Phyto values of ET and EG in Si1, Si2 and Si3 addition was higher than those of EU and EU × EG compared to no Si addition.

Fig. 7.

Fig. 7

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Phytoremediation quality (Phyto) in E. tereticornis (ET) (a), E. urophylla (EU) (b), E. grandis (EG) (c) and E. urophylla × E. grandis (EU × EG) (d), respectively, and the Pearson’s correlation between plant growth, tolerance, enzymatic and non-enzymatic antioxidant, oxidative stress and phytoremediation in only the Al1(Si0) treatment (e) and the Al1 + Si(1, 2, 3) interaction treatment (f). The correlations between indexes are shown in bold square. Values are averages ± standard errors (n = 4)

In only Al1 treatment, Phyto was positively correlated with PGI but negatively correlated with POSI and PEAI (P < 0.05), PEAI and POSI were negatively correlated with PGI and PTI, and PGI was positively correlated with PTI (Fig. 7e). In the Al1 + Si(1, 2, 3) treatment, Phyto was positively correlated with PTI, PNEAI and PNEAI, PNEAI was positively correlated with PTI and PEAI, PEAI was negatively correlated with POSI, POSI was negatively correlated with PGI and PTI, and PGI was positively correlated with PTI (Fig. 7f).

Discussion

Si addition improves plant growth and tolerance quality

The quality of plant growth reflects the highly adaptive ability of the environment and the self-regulation ability under environmental pressure, including the overall characteristics of plant morphology, behavior and physiology [17]. We found that 4.5 mM Al (Al1) decreased the PGI and PTI based on a variety of plant growth and tolerance parameters in four Eucalyptus species, which indicated that plant key growth and tolerance indicators, such as ABG, RL, and RV, were negatively affected by the Al1 addition. This finding was in line with the previous studies that 4.5 mM Al has toxic effects on plants growth, limiting root elongation, preventing root, stem and leaf growth, and leading to a reduction in biomass [23]. However, under Al1 stress, we observed that the 0.5 mM (Si1) or 1.0 mM Si (Si2) addition had positive effects on PGI, PTI, plant growth (e.g. BGB, LA, RV, RL) and tolerance (e.g. LTe) indicators compared to no Si addition. These findings reflected that plant key growth and tolerance indicators were positively affected by Si addition, and the addition of Si can mitigate Al toxicity by enhancing plant growth and stress quality. These findings were similar with many studies in which the appropriate addition of Si was found to increase plant stress tolerance by regulating plant key morphology (e.g. root, leaf) and behavior (e.g. root elongation) [12, 15, 16, 27]. Several studies also showed that Si promoted the development of roots (e.g. an increasing in root length), thereby increasing the absorption of nutrients by roots and improving both plant growth and their tolerance to Al stress [19, 34]. However, it is worth noting that the mechanism of Si in alleviation Al toxicity is usually associated with a series of complex responses, involving sensing, oxidative stress, signal transduction, processing and metabolic regulation at both physiological and molecular levels [8, 16, 18]. More studies at metabolic level should be investigated deeper in the next studies.

Si addition enhances plant antioxidant defense capacity

Antioxidant defense system, formed by enzymatic and non-enzymatic antioxidants, such as APX, GR, CAT, as well as ASA and GSH, is a powerful tool for plants to balance ROS at a non-toxic level [20]. We observed that the toxic effect caused by 4.5 mM Al increased NOX activity, reactive oxygen (H2O2, O2·−) content, and the POSI, and disrupted the balance of ROS in four Eucalyptus species. NOX serves as a fuel for the production of O2·−, and the accumulation of ROS in cells may destroy the structure of cell membranes [35]. This was supported in our results that higher NOX activity with higher ROS accumulation and MDA content was observed in the Al1Si0 treatment compared to the control. In general, excessive ROS can be scavenged by an increase in antioxidant enzymatic activities and non-enzymatic antioxidant content [20]. Under Al1 stress, we found a significant increase in the PEAI in four Eucalyptus species, whereas the PNEAI decreased in ET and EG but increased in EU and EU × EG. For example, EU and EU × EG increased antioxidant enzyme activities (e.g. CAT, APX, POD, GR, and MDHAR) and antioxidant contents (e.g. ASA, GSSH, and DHA) to efficiently remove H2O2 and O2·−, whereas a decrease in the antioxidant content in ET and EG weakened the scavenging efficiency of ROS. Besides, the average values for POSI were in the order of ET > EG > EU > EU × EG in the Al1Si0 treatment. These results indicated that there was a difference in plant Al tolerance among the four Eucalyptus species. Compared to the ET and EG, EU originated in Al-rich volcanic soil and developed a relatively higher Al tolerance in genetically during long-term adaptation, and the EU × EG, a hybrid of EU and EG, inherited Al tolerance from EU [36]. Thus, EU and EU × EG are more tolerant of Al than ET and EG. Many studies also noted that antioxidant system was an important tool to block the harmful effects of ROS, those species with a higher antioxidant capacity tended to be more tolerant to stress, whereas those species with a lower antioxidant capacity tended to be more sensitive to stress [19, 37, 38]. Based on these findings, we inferred that ET and EG are Al-sensitive species.

Silicon plays an important role in improving plant growth, promoting antioxidant capacity, and alleviating oxidative stress [14, 27]. Our results also found that exogenous 0.5 mM Si (Si1) addition can alleviate Al stress by enhancing the antioxidant defense capacity in the four Eucalyptus species. This is similar to Pirooz et al. [26], Si can mitigate Al stress not only by strengthening plant physical tolerance and resistance but also by promoting positive regulation of the antioxidant defense system to reduce oxidative stress. SOD is the first line of defense against ROS, clearing excess O2·− in cells and converting O2·− into H2O2 [20]. POD, CAT and APX play important roles in clearing H2O2, and maintaining a nontoxic level of O2·− [19]. Under Al1 treatment, we recorded an increase in SOD, POD, CAT and APX activities and a decrease in O2·− and H2O2 contents in the four Eucalyptus species after Si1 addition compared to no Si addition. The ASA-GSH cycle is a redox cycle that maintains the balance of antioxidant system and prevents oxidative stress [27]. As previously mentioned, ET and EU are sensitive to Al and suffer greater oxidative damage than the two Al-tolerant species (EU and EU × EG). Under Al1 treatment, we observed that the the addition of Si1 can increase the ASA, GSH, DHA, and GSSG contents and decreased the MDA and ROS contents in four Eucalyptus species compared to no Si addition. This reflected that adding Si1 positively affected the plant antioxidant defense system by enhancing the production of ASA-GSH cycle (e.g. increasing the contents of ASA, GSH, DHA, GR, and GSSG) and GR, CAT enzyme activities to remove excessive ROS (e.g. O2·−, H2O2) and reduce lipid peroxidation in Eucalyptus species. Adding Si can effectively compensate for the low Al tolerance caused by the Al-sensitive characteristics. These concerted actions of antioxidant enzymes and antioxidants reflect that the addition of Si plays an important role in mitigating the toxic effects of oxidative stress and keeping a balance of ROS, and plant antioxidant defense capacity can be increased by the synergistic action of antioxidant enzymes and antioxidants. However, the synergistic ROS-scavenging pathway of antioxidant defense system is still efficient, more research is needed to understand how ROS signaling network operates under Al stress [7].

Si addition promotes phytoremediation

Exogenous Si addition as an amendment in acidic soil is a promising method for phytoremediation [39]. Fortunately, we found that even if in an additional 4.5 mM of Al was applied to a typical acidic soil, the addition of 0.5 mM Si could still promote the phytoremediation rate by 18.7 ~ 34.8% in the four Eucalyptus species compared to that with no Si addition. Therefore, we suggested that Eucalyptus artificial forests in acidic soil can supply 0.5 mM Si to promote phytoremediation efficiency in southern China. The positive correlation between the phyto and antioxidant system (also known as PEAI and PNEAI) explained the improving effect of phytoremediation in Al1 + Si(1, 2, 3) interaction treatment (Fig. 7f). This is consistent with several studies that an appropriate amount of Si could reduce Al toxicity, alleviate plant growth limitations and achieve an effective removal of Al in acidic soil [40–42]. It was noticed that the growth, tolerance, enzyme activity and phytoremediation rate of the two Al-sensitive species supplemented with Si3 were significantly lower than those of the species supplemented with Si1 when exposed to 4.5 mM Al stress. This indicated that the concentration of 1.5 mM Si may have adverse effects on plants. This may be related to the fact that the excess Na2SiO3 may lead to a high Na+ accumulation in Eucalyptus species. The double stress caused by excessive Na+ and Al accumulation extremely increased the regulatory pressure of Si on plant defense system, thus decreasing plant growth quality. Therefore, the selection of exogenous additives should be careful to avoid the secondary effects of other exogenous ions on plants. Under Al1 treatment, the 0.5 ~ 1.5 mM Si addition can improve phytoremediation efficiency in four Eucalyptus species compared to no Si addition. Studies have reported that combining exogenous additives with phytoremediation increases efficiency and achieves complete metal removal from soil compared to phytoremediation alone [43, 44]. Additionally, we also noticed that the average Phyto values of two Al-sensitive species with Si addition was higher than those in two Al-tolerant species without Si addition. This difference may be related to the difference of plant Al response strategy. Several studies showed that plants with a high heavy metal tolerance to heavy metals may adopt an avoidance strategy to reduce the absorption of heavy metals, whereas those with a low heavy tolerance to heavy metals must passively accumulate and clean up soil heavy metals in the short-term [12, 18]. Thus, we concluded that Al-sensitive species may be suitable for remediating slightly acidic soils, whereas Al-tolerant species may be suitable for remediating heavily acidic soils.

In only the Al1 treatment, Phyto was positively correlated with PGI but negatively correlated with POSI and PEAI (Fig. 7e). In the Al1 + Si(1, 2, 3) treatment, Phyto was positively correlated with PTI, PEAI and PNEAI (Fig. 7f). As mentioned above, these results indicated that Si application is important for thw detoxification of Al because it improves plant tolerance, enzymatic and non-enzymatic antioxidant defense capacity. And the synergistic Al detoxication pathways involving antioxidant enzymes and antioxidants constitute an important part of the antioxidant system response of Eucalyptus species under Al stress. Other studies have also found similar results [45, 46]. However, the synergistic antioxidant defense interactions under stress are the result of active regulation through a series of complex and elaborate cascades of molecular signals and cross-linked patterns of pathway communication [20, 47, 48]. It is difficult to determine whether synergism is caused by the addition of exogenous Si, as these molecules can also enhance the antioxidant capacity in other ways. Thus, in future studies, researchers should not only pay attention to the changes in plant metabolic pathways and related gene expression regulated by Si under Al stress, but also focus on the process of plant perception and transmission of stress signals during the maintenance of plant antioxidant system balance to further elucidate the mechanism by which Si mitigates Al stress at the molecular level [49, 50].

Conclusion

In this study, 4.5 mM Al limited the quality of plant growth in four Eucalyptus species, resulting in decreased plant tolerance and oxidative damage, as evidenced by an increase in NOX, H2O2, O2·−, MDA, and POSI levels. However, the addition of 0.5 mM and 1 mM Si effectively mitigated these adverse effects of Al toxicity on plant growth and improved in plant growth quality by increasing plant stress tolerance. Moreover, the addition of Si increased the synergistic actions of enzymatic and non-enzymatic antioxidant defense, such as increasing SOD, POD, CAT, APX, MDHAR, DHAR activities, and ASA, GSH, DHA, and GSSG contents to remove over-accumulated ROS and reduce lipid peroxidation. Additionally, under 4.5 mM Al stress, the addition of Si increased the phytoremediation rate of the four Eucalyptus species by 18.7 ~ 34.8% compared to that in the absence of Si treatment. This indicated that the application of Si in acidic soil can be promoted as an effective method for the phytoremediation of Eucalyptus plantations in southern China. This study was carried out in the control conditions, it is suggested that further experiments should be carried out in the natural environmental conditions, and the next study will focus on the changes in plant metabolic pathways and their signal transmission processes regulated by Si under Al stress.

Supplementary Information

Supplementary Material 1. (32.6KB, docx)

Acknowledgements

We are grateful to the Guangxi Dongmen state-owned Forest Farm for providing four Eucalyptus species seedlings.

Abbreviations

Al

Aluminum

Si

Silicon

PGI

Plant growth index

H

Height

LA

Leaf area

RL

Root length

RV

Root volume

BGB

Below-ground biomass

AGB

Above-ground biomass

PTI

Plant tolerance index

LTe

Plant leaf tolerance

STe

Plant stem tolerance

RTe

Plant root tolerance

POSI

Plant oxidative stress index

MDA

Malondialdehyde content

NOX

Nicotinamide adenine dinucleotide phosphate oxidase activity

O2·−

Superoxide anion content

H2O2

Hydrogen peroxide content

PEAI

Plant enzymatic antioxidant index

DHAR

Dehydroascorbate reductase activity

MDHAR

Monodehydroascorbate reductase activity

GR

Glutathione reductase activity

CAT

Catalase activity

APX

Ascorbate peroxidase activity

POD

Peroxidase activity

SOD

Superoxide dismutase activity

PNEAI

Plant non-enzymatic antioxidant index

DHA

Dehydroascorbic acid content

ASA

Ascorbate content

GSSG

Glutathione disulfide content

GSH

Glutathione content

Authors’ contributions

L.J.H., H.Y.L, Y.S.L. and W.C.T. conceived and designed the work, L.J.H., H.Y.L, Y.S.L. and W.C.T. prepared the datasets and discussed the results, J.Z.S. and K.L. contributed materials/analysis tools. L.J.H., H.Y.L. and Y.S.L wrote the manuscript, L.J.H., H.Y.L, Y.S.L. and W.C.T. revised the manuscript. All authors read and approved the final manuscript.

Funding

This work was supported by the Natural Science Foundation of Guangxi Province (2023GXNSFAA026485) and National Natural Science Foundation of China (31800530).

Data availability

No datasets were generated or analysed during the current study.

Declarations

Ethics approval and consent to participate

Not applicable.

Consent for publication

Not applicable.

Competing interests

The authors declare no competing interests.

Footnotes

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Linjuan Huang, Hongying Li and Yishan Luo contributed equally to this work and should be considered co-first authors.

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Supplementary Materials

Supplementary Material 1. (32.6KB, docx)

Data Availability Statement

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