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Article

Epichloë bromicola Enhances Elymus dahucirus Plant Growth and Antioxidant Capacity under Cadmium Stress

by
Qian Shi
1,
Wayne R. Simpson
2,
Yuling Li
1,3,
Chengti Xu
1,3,
Kejia De
1,3 and
Xiuzhang Li
1,3,*
1
State Key Laboratory of Plateau Ecology and Agriculture, Qinghai University, Xining 810016, China
2
AgResearch Grasslands Research Centre, Tennent Drive, Private Bag 11008, Palmerston North 4442, New Zealand
3
Qinghai Academy of Animal and Veterinary Science, Qinghai University, Xining 810016, China
*
Author to whom correspondence should be addressed.
Agronomy 2024, 14(2), 365; https://doi.org/10.3390/agronomy14020365
Submission received: 26 December 2023 / Revised: 28 January 2024 / Accepted: 2 February 2024 / Published: 12 February 2024
(This article belongs to the Special Issue Advances in Stress Biology of Forage and Turfgrass)
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Versions Notes

Abstract

:
Elymus dahucirus is an essential plant for ecological restoration in fragile ecological areas and mining area restoration. As lawn grass, it can quickly cover soil and prevent soil erosion, so it is commonly used as a pioneer grass for lawn greening and slope protection. In recent years, with the development of mineral resources, Qinghai–Tibet Plateau soil is facing the threat of heavy metal cadmium (Cd) pollution. E. dahuricus can host the filamentous fungus Epichloë bromicola. To make better use of the advantages that Epichloë bring to host plants to alleviate heavy metal pollution in soil, plant growth and antioxidant capacity effects on E. bromicola infected (E+) and uninfected (E−) E. dahuricus were determined under Cd stress. During Cd treatment, plant growth was decreased by Cd stress, while E+ plants exhibited equal or better growth compared to E− plants. Cd treatment induces a proline and antioxidant enzyme burst in infected plants, while malondialdehyde (MDA) increases. E. bromicola improved plant growth and antioxidant capacity. E. dahuricus breeding strategies could use the information here in efforts to improve the performance of E. dahuricus in both environmental protection and agronomic contexts.

1. Introduction

The natural environment has been significantly impacted by technological advancements and societal changes in the modern era. Currently, the degradation of soil by metallic compounds is widely acknowledged as a prominent threat to agro-ecosystems worldwide, with direct implications for food safety [1,2]. Toxic metals, especially cadmium (Cd), are widely distributed in the natural environment. Cd ranks among the most significant heavy metal pollutants in soil [3,4]. Cd is harmful to various biochemical and physiological processes in plants, reducing seed germination, early seedling growth, and plant biomass. It causes changes in photosynthesis, relative water content, transpiration rate, stomatal conductance, and electrolyte leakage. Cd activates reactive oxygen species that induce chromosomal aberrations, gene mutations, and DNA damage affecting the cell cycle and cell division. The accumulation of Cd in crops and its potential entry into the food chain pose serious concerns for public health [5]. Even at very low concentrations in the body, Cd poses a significant health hazard and can lead to DNA mutation and damage, potentially resulting in carcinogenesis. Therefore, it has been classified as a human carcinogen (Group I) by the International Agency for Research on Cancer [6]. The Qinghai–Tibet Plateau is an essential area for biodiversity conservation and is rich in mineral resources, with one of the most valuable nonferrous metal deposits in the region. Presently, oil is facing the threat of heavy metal Cd pollution following the development of mineral resources [7].
About one-third of C3 grass species are capable of being, or becoming, infected with Epichloe [8]. Anamorh-typified Epichloë can develop asymptomatic mutualistic interactions that feature seed transmission of the fungus [9]. The enhanced growth of Epichloë-infected plants can be a feature of mutualistic interaction [10,11], along with increased plant nutrient uptake [12], the inhibition of plant pathogen growth [12], and increased fitness through improved responses to biotic [13,14,15,16] and abiotic influences [12,17,18,19,20,21]. However, some symbionts can produce metabolites that are harmful to grazing animals, an example being ergovaline, produced by Epichloë coenophiala in its host grass, which contributes to the occurrence of “fescue toxicosis’” in grazing animals. theT stock ailment “ryegrass staggers’” can also present due the presence of Epichloë within Lolium perenne. These Epichloë can produce indole diterpenes (IDTs) [22]. In China, E. gansuensis var. inebrians-infected Achnatherum inebrians produces ergot alkaloids and toxicity in domestic animals [23]. There are many studies examining the benefits, including stress resistance, of grasses hosting infections of Epichloë,and the abatement of heavy metal stress features in many of these studies [5]. The Epichloë hosted by tall fescue, perennial ryegrass, and drunken horse grass (Epichloë gansuensis) play a positive role under Cd stress [24,25,26]. toT make better use of the advantages that Epichloë bring to host plants to alleviate heavy metal pollution in soil, the performance of a large number of host plants under Cd stress needs to be studied.
The Elymus dahuricus growing throughout northwest China has excellent genes for disease, pest, and stress resistance and has strong drought and cold resistance, barren resistance, and high nutritional and feeding value [27,28,29]. It makes a key contribution to degraded grassland restoration and the sustainable development of grassland animal husbandry in northwestern China [28,30] and is also an essential plant for ecological restoration in fragile ecological areas and mining area restoration [31]. As a lawn grass, it can quickly cover soil and prevent soil erosion, so it is commonly used as a pioneer grass for lawn greening and slope protection [32]. E. bromicola forms host-specific symbioses with Elymus spp. and E. bromicola is commonly found in Elymus spp. [33,34,35]. Despite the presence of gene coding for ergot alkaloids, cases of livestock toxicosis are not reported [33]. In addition, there have been no studies on the effect of E. bromicola on E. dahuricus under Cd stress in the Qinghai–Tibet Plateau. To address this knowledge gap, E. dahuricus, both infected (E+) and uninfected (E−) with Epichloë, were collected from Qinghai–Tibet Plateau, forming material to study the growth indicators and antioxidant capacity of seedlings to evaluate performance under high Cd levels.

2. Material and Methods

2.1. Plant Material

In September 2020, mature individual plants of E. dahuricus with fully ripened seedheads were collected from 3 sites (Table 1) distributed on wild permanent grassland on the Qinghai–Tibet Plateau. Tillers of 20–-40 plants were collected at each of the 3 sites. Sampling information, including spatial coordinates and elevation, were recorded, and samples were transported to the laboratory for analysis. Culms were examined using aniline blue following the staining method described by Cheplick [36].
Seeds sourced from the 3 sites were planted February 2021, and the emerged seedlings were examined for endophyte presence. Seeds were sown at 1 cm depth, 1600 with seed per site, and germinated in a glasshouse set to maintain 18–24 °C and 10 h light/14 h dark. Epichloë infection status was determined one month after sowing. Plants were separated into two populations, one confirmed Epichloë infected and the other uninfected [36].

2.2. Experiental Design

Infected and uninfected seedlings were potted to 35 cm × 32 cm pots using a 3:1 mix of sterilized soil and vermiculite. Pots were planted with 6 seedlings and received equal initial water treatment. CdCl2 solutions with concentrations of 0, 40, 90, 140, and 190 μmol/L were prepared. CdCl2 treatments were applied as 400 mL of each solution to pots at 3-day intervals, and control pots received 400 mL of distilled water. Treatments were applied over 5 replicates. Temperature was maintained at 25 ± 2 °C, and humidity was maintained at 42 ± 5%.

2.3. Measurements

About 2.0 g of leaf tissue per plant was harvested for malondialdehyde (MDA), proline content antioxidant enzyme analysis following 30 days of MDA CdCl2 treatment. Each treatment measured 5 plants, with each plant serving as one replicate.

2.3.1. MDA Content

MDA was quantified following the protocol established by Esterbauer and Cheeseman [37] to estimate lipid peroxidation. A total of 0.5 g of sample was mixed with trichloroacetic acid solution (5 mL) to produce a 5% solution, which was subjected to centrifugation at a speed of 12,000 r/min for a duration of 25 min. A total of 2 mL of thiobarbituric acid (0.67%) was added to supernatant (2 mL) and maintained at 100 °C for 30 min. The precipitate was separated through centrifugation after the cooling process. Absorbance measurements were made at 450, 535, and 600 nm, and a blank solution was measured as a control. MDA content was determined using the following:
C/μmol/L = 6.45 × (A532 − A600) − 0.56 × A450

2.3.2. Proline Content

The determination of proline content was conducted using a modified method from Li [38]. Leaves were freeze-dried, 0.5 g were finely powdered, and 5 mL of sulphosalicylic acid (3%) was added and maintained at 100 °C for 10 min. A total of 2 mL of supernatant was combined with 2 mL each of glacial acetic acid and acidic ninhydrin solution (2.5% w/v) and heated for 25 min at 100 °C. A total of 4 mL of toluene was added to the cooled mixture, and the absorbance was measured at a wavelength of 520 nm to obtain the μg/g dry matter concentration.

2.3.3. Activity of Antioxidant Enzymes

A total of 0.5 g of leaf tissue was dissolved in a test tube, and 5 mL 50 mmol/Lof sodium phosphate buffer was added into the test tube (pH 7 when catalase (CAT) was measured; superoxide dismutase (SOD), peroxidase (POD), and ascorbate peroxidase (APX) were determined at pH 7.8), along with 1% (w/v) of polyvinylpyrrolidone and 0.1 mmol/L Na2EDTA. The homogenate was filtered with four layers of gauze and then centrifuged at 15,000 r/min for 20 min. The supernatant was absorbed and stored in a refrigerator at 4 °C for the determination of antioxidant enzyme activity. CAT activity was determined using Clairborne’s method [39]. The enzyme solution (0.2 mL), phosphoric acid buffer solution (pH 7.8, 1.5 mL), and distilled water (1 mL) were added to the test tube. After preheating at 25 °C, hydrogen peroxide (0.3 mL of 0.1 mol/L) was added and quickly poured into a quartz colorimetric cup. Absorbance was measured at 240 nm. SOD activity was determined using a spectrophotometer, with reference to Beryer and Fridovich’s’ method [40]. The inhibition of SOD on the photochemical reduction of nitrogen blue tetrazole (NBT) was determined at 560 nm. One unit of SOD activity is defined as the amount of enzyme required to inhibit 50% of the photochemical reduction of NBT. POD activity was determined using guaiacol as an electron donor. According to Chance and Maehly et al. (1955) [41], 2.5 mL of 0.1 mol/L guaiacol solution and 1 mL of enzyme solution were added into the test tube. After 10 min, 0.5 mL of 1 mol/L hydrogen peroxide solution was quickly added, and the solution was put into the water bath to keep the temperature at about 30 °C for a reaction time of 15 min. The test tube was then removed, and after adding 2.5 mL of distilled water, it was shaken well before measuring the absorbance at 470 nm. APX was determined using a spectrophotometer and the method by Gupta et al. (1993) [42]. A total of 2.6 mL of reaction buffer (containing 0.1 mmol/L EDTA and 0.5 mmol/L ascorbic acid) and 0.1 mL of enzyme extract were added to a test tube, followed by the addition of 0.3 mL of 2 mmol/L H2O2 to initiate the enzymatic reaction. The mixture was immediately mixed, and the timing was started. The absorbance at 290 nm of the reaction system was recorded starting from 15 s after initiation.

2.3.4. Plant Growth

After 30 days of growth, plant height and tiller number were recorded. Whole plants were then carefully removed from pots, washed with distilled water, and dried on filter paper. Dry weight was obtained following oven-drying the tissue at 60 °C until a constant weight was reached. The dry aboveground and underground parts from each treatment were weighed separately to determine the total dry matter per plant.

2.4. Statistical Analyses

Data analyses were performed using SPSS (Version 24.0, Chicago, IL, USA) for Windows. One-way analysis of variance (ANOVA) was employed to analyze the effect of endophyte infection on all parameters measured. The interactions among Cd and the sampling site and endophyte infection on growth parameters, membrane lipid peroxidation, and activity of antioxidant enzymes were determined using three-way ANOVA. Statistical significance was defined at the 95% confidence level. PCA (Principal Component pcanalysis) was conducted using Canoco (ter Braak and Šmilauer 2002) to analyze the relationship among plant growth, antioxidant capacity, Cd concentration, E. bromicola, and sites. Means are reported with their standard errors.

3. Results

3.1. E. dahuricus Growth Parameters

Growth parameters are a direct reflection of plant response to stress [43]. Cd negatively affected plant growth parameters. The growth of was the plants gradually weakening after the start of the Cd treatment (Figure 1, Figure 2, Figure 3 and Figure 4). Therefore, Cd stress decreased plant height (Figure 1), tiller number (Figure 2), aboveground biomass (Figure 3), and underground biomass (Figure 4). In contrast, untreated control plants showed the best growth (Figure 1, Figure 2, Figure 3 and Figure 4). E+ plants generally grew equal to, or better than, E− plants in the Cd treatment (Figure 1, Figure 2, Figure 3 and Figure 4 and Table 2). With an increase in Cd concentration, E+ plant height, aboveground biomass, and belowground biomass were significantly higher than those of E− plants (p < 0.05) (Figure 1, Figure 3 and Figure 4 and Table 2). The site had no significant effect on the aboveground biomass but had a significant effect on the other three growth parameters (p < 0.05). There was also a significant interaction between the site and Cd concentration (p < 0.05), and the interaction between Cd concentration and endophytic fungi was weaker than that between Cd concentration and sampling site (Table 2).

3.2. E. dahuricus Membrane Lipid Peroxidation

The level of membrane lipid peroxidation indicates the extent of Cd stress in plants [5]. Cd positively affected the MDA and proline contents of the plant. The contents of MDA and proline gradually increased after the start of the Cd treatment. When the concentration of Cd was 140 μmol/L and 190 μmol/L, the difference of MDA and proline between E+ and E− plants was significant (Figure 5 and Figure 6). Cd concentration, sampling sites, endophytic fungi and their interactions had significant effects on membrane lipid peroxidation (Table 3).

3.3. E. dahuricus Activity of Antioxidant Enzymes

protectiveP enzymes can protect plants against Cd stress damage [5]. The effect of Cd on antioxidase activity was consistent with the effect of Cd on proline and MDA contents. With an increase in Cd concentration, the activity of antioxidant enzymes generally showed a tendency that E+ was higher than E−, and the difference was significant under the Cd concentration of 140 μmol/L and 190 μmol/L (Figure 7, Figure 8, Figure 9 and Figure 10). Cd concentration, sampling points, endophytic fungi, and their interactions had significant effects on SOD, POD, and CAT activity. The interaction between endophytic fungi and sampling site had no significant effect on APX activity, but other factors and interactions had significant effect on APX activity (Table 4).

3.4. Relationship among Cd Concentration, E. bromicola, Site, Plant Growth, and Antioxidant Capacity

Generally, attention should be paid to the effects of Cd, E. bromicola, and sites on the growth and antioxidant capacity of E. dahuricus. The first and second axes are 97.4% and 2.1%, respectively (Figure 11). Cd stress had the strongest effect on E. dahuricus growth and antioxidant capacity. It was negatively associated with plant growth and positively associated with antioxidant capacity. E. bromicola mainly promoted plant growth and antioxidant capacity by enhancing plant aboveground biomass, plant height, and the activity of SOD and POD. Generally, the influence of sample sites on antioxidant enzyme activity was stronger (negative effect) than plant growth.

4. Discussion

Under Cd stress, plant growth and development are affected by the adaptability and response to this stress [5]. Our experimental results show that E. bromicola can improve the resistance of host plants to Cd stress, E+ plants have higher plant height and biomass, especially under high Cd concentration. Similarly, Ren et al. (2006) found that endophyte infection enhanced L. perenne tillering ability under conditions of Cd stress [25].
When Bacon et al. (1977) found that alkaloids produced by fungal endophytes in tall fescue can lead to livestock toxin [44], defensive mutualism had been the predominant framework for studies on endophyte–grass symbiosis [45,46,47,48,49,50]. Defensive mutualism involves intricate signaling and chemical communication between endophyte and host cells, such as reactive oxygen species and antioxidants, as well as between plants, herbivores, and their natural enemies through volatile organic compounds, salicylic acid, and jasmonic acid pathways. This reveals a significantly more complex network. The significance of reactive oxygen species (ROS) antioxidants in endophyte–grass symbiosis was emphasized by Hamilton et al. (2012) [51]. Lipid peroxidation is a marker of oxidative stress [52], and the MDA content in plants increases in the presence of Cd stress, indicating oxidative stress [53,54]. Cd treatment leads to an increase in MDA content in various plant species. Cd-induced lipid peroxidation impairs membrane structures, which play a crucial role in maintaining plant metabolism. [5]. Proline is a nonessential amino acid [55] that is biosynthesized in chloroplasts and plant cell cytoplasm [5,56]. Plants may synthetize proline in either the absence or presence of abiotic stress (e.g., metal exposure) [57]. It has been reported that in Cd exposure, proline content increases in different plant species. Proline is an important metabolite for plant adaptation, protection, and tolerance to Cd stress. The accumulation of proline in plants is recognized as a strategy counteracting Cd stress by adjusting osmotic potential, the stabilization of membrane structures [5,58,59], and the reduction of oxidative stress [60]. Cd stress in plants also results in drastic changes in enzyme activity [61] due to oxidative stress in the plant cells [62]. Antioxidant enzymes can remove intracellular reactive oxygen species to reduce the damage of Cd to plants [63]. Our results support these conclusions and suggest that pronounced Cd treatment induces a burst of proline and antioxidant enzyme activity in E+ plants, as well as significant increases in MDA levels in E− plants. These findings also indicate that endophyte infection affects the lipid peroxidation and oxidative balance of the host plant Consistent with our results, Song et al. (2015) found that waterlogging induced an increase in proline production and antioxidant enzyme activity, particularly in E+ plants, and had lower MDA content [18]. In Zhang et al. (2010) study, the proline content of Achnatherum inebrians seedlings increased, while the MDAcontent decreased with increasing Cd concentration [14]. The oxidative balance is likely to play a pivotal role in conferring the resistance of the endophyte–plant symbiont against a wide array of environmental stresses [51,63]. Additionally, there is a negative correlation between biomass and MDA and proline, as well as antioxidant enzyme activity. These results indicated that an increase in MDA and proline content and the enhancement of antioxidant enzyme activity were not conducive to the growth of the plant. However, an increase in MDA and proline content occurred with an increase in the Cd concentration. This result also supported the conclusion that an increase in Cd concentration is not conducive to the growth of calcareous grass. The results in Figure 11 further showed that E. bromicola can promote the growth of and increase the antioxidant capacity of the E. dahuricus.
Previous research has shown that the direction and strength of endophyte–host plant interactions depend on plant and endophyte genotype, as well as environmental conditions [64]. In this study, the results showed that, in addition to E. bromicola and Cd concentration, the sites were also an important factor in E. dahuricus growth and antioxidant enzyme activity under Cd stress. The effect of the sites on antioxidant capacity aspects was stronger. This may be due to host genotype variation because the wild E. dahuricus used in this study were collected from wild grasslands on the Qinghai–Tibet Plateau. Tian et al. (2018) [65] reported that natural and wild forage species have great genetic diversity and have not undergone domestication, and this diversity of host plants may have induced different physiological and biochemical response. Our results support this view. The Qinghai–Tibet Plateau climate is harsh, extreme, and changeable [66]. Different geographical coordinates determine the climate of plant growth areas. The adaptation mechanism and survival strategy of plants in this area are the comprehensive effects of reactive oxygen species scavenging, osmosis regulation, and photosynthetic capacity [67]. Therefore, in our study, prevailing climatic factors at different sampling sites may explain the effects of the site on plant antioxidant capacity and growth.
A great deal of research has been conducted examining the effects of Epichloë endophyte infection on host abiotic stress responses. Over 40 years of study on the benefits of symbiotic Epichloë fungal endophytes for host grasses, investigations have focused on the major agricultural species, tall fescue and perennial ryegrass [68]. However, many other grass species remain to be evaluated for the effects of Epichloë endophytes aboticon abiotic stress. In our study, it was confirmed that E. bromicola has an important ecological function for improving E. dahuricus seedling resistance to Cd stress. Before this, Zhang et al. (2012) [30], confirmed that the Epichloë endophyte can improve the E. dahuricus seed germination rate under Cd stress. Therefore, we propose that the higher tolerance of E+ host plants to Cd stresses due to the presence of Epichloë endophytes should be acknowledged in E. dahuricus breeding strategies on the Qinghai–Tibet Plateau.

5. Conclusions

This is the first study on how E. bromicola enhances E. dahuricus resistance to Cd stress on the Qinghai–Tibet Plateau. This provides basic data for reducing the threat of Cd on the Qinghai–Tibet Plateau through grass endophytic fungi restoration. In the future, we believe that a combination of different techniques will help elucidate the phenomenona and mechanisms of Epichloë-induced resistance to Cd stress in host grass. Microbiome, metabolomics, soil science methods, and especially, molecular biology will be used to clarify how Epichloë can improve the biochemistry mechanisms of the host for Cd resistance, which will provide the basis for improving land use efficiency and possibly working toward ensuring food safety.

Author Contributions

Conceptualization, Q.S. and X.L.; methodology, Y.L. and C.X.; software, Q.S. and X.L.; validation, Y.L. and K.D.; formal analysis, X.L.; investigation, Q.S. and Y.L.; data curation, Q.S. and Y.L.; writing—original draft preparation, Q.S.; writing—review and editing, W.R.S. and Q.S.; visualization, W.R.S. and Q.S.; supervision, X.L. and Y.L.; project administration, X.L., Y.L. and Q.S.; funding acquisition, Q.S. and X.L. All authors have read and agreed to the published version of the manuscript.

Funding

This research was supported by The Open Project of the State Key Laboratory of Plateau Ecology and Agriculture, Qinghai University (2022-ZZ-12), and the National Natural Science Foundation of China (32360349).

Data Availability Statement

The datasets presented in this article are not readily available because the data are part of an ongoing study.

Conflicts of Interest

The authors declare no conflicts of interest.

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Figure 1. Plant height of E. dahuricus infected with E. bromicola grown under different CdCl2 treatments. Seeds were collected from Qinghai Tongren (Site 1), Qinghai Zeku (Site 2), and Qinghai Gonghe (Site 3). * indicated significant difference between E+ and E− at 0.05 level.
Figure 1. Plant height of E. dahuricus infected with E. bromicola grown under different CdCl2 treatments. Seeds were collected from Qinghai Tongren (Site 1), Qinghai Zeku (Site 2), and Qinghai Gonghe (Site 3). * indicated significant difference between E+ and E− at 0.05 level.
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Figure 2. Tiller number of E. dahuricus infected with E. bromicola grown under different CdCl2 treatments. Seeds were collected from Qinghai Tongren (Site 1), Qinghai Zeku (Site 2), and Qinghai Gonghe.
Figure 2. Tiller number of E. dahuricus infected with E. bromicola grown under different CdCl2 treatments. Seeds were collected from Qinghai Tongren (Site 1), Qinghai Zeku (Site 2), and Qinghai Gonghe.
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Figure 3. Biomass above ground of E. dahuricus infected with E. bromicola grown under different CdCl2 treatments. Seeds were collected from Qinghai Tongren (Site 1), Qinghai Zeku (Site 2), and Qinghai Gonghe. * indicated significant difference between E+ and E− at 0.05 level.
Figure 3. Biomass above ground of E. dahuricus infected with E. bromicola grown under different CdCl2 treatments. Seeds were collected from Qinghai Tongren (Site 1), Qinghai Zeku (Site 2), and Qinghai Gonghe. * indicated significant difference between E+ and E− at 0.05 level.
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Figure 4. Biomass below ground of E. dahuricus infected with E. bromicola grown under different CdCl2 treatments. Seeds were collected from Qinghai Tongren (Site 1), Qinghai Zeku (Site 2), and Qinghai Gonghe. * indicated significant difference between E+ and E− at 0.05 level.
Figure 4. Biomass below ground of E. dahuricus infected with E. bromicola grown under different CdCl2 treatments. Seeds were collected from Qinghai Tongren (Site 1), Qinghai Zeku (Site 2), and Qinghai Gonghe. * indicated significant difference between E+ and E− at 0.05 level.
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Figure 5. MDA content of E. dahuricus infected with E. bromicola grown under different CdCl2 treatments. Seeds were collected from Qinghai Tongren (Site 1), Qinghai Zeku (Site 2), and Qinghai Gonghe. * indicated significant difference between E+ and E− at 0.05 level.
Figure 5. MDA content of E. dahuricus infected with E. bromicola grown under different CdCl2 treatments. Seeds were collected from Qinghai Tongren (Site 1), Qinghai Zeku (Site 2), and Qinghai Gonghe. * indicated significant difference between E+ and E− at 0.05 level.
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Figure 6. Proline content of E. dahuricus infected with E. bromicola grown under different CdCl2 treatments. Seeds were collected from Qinghai Tongren (Site 1), Qinghai Zeku (Site 2), and Qinghai Gonghe. * indicated significant difference between E+ and E− at 0.05 level.
Figure 6. Proline content of E. dahuricus infected with E. bromicola grown under different CdCl2 treatments. Seeds were collected from Qinghai Tongren (Site 1), Qinghai Zeku (Site 2), and Qinghai Gonghe. * indicated significant difference between E+ and E− at 0.05 level.
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Figure 7. SOD activity of E. dahuricus infected with E. bromicola grown under different CdCl2 treatments. Seeds were collected from Qinghai Tongren (Site 1), Qinghai Zeku (Site 2), and Qinghai Gonghe. * indicated significant difference between E+ and E− at the 0.05 level.
Figure 7. SOD activity of E. dahuricus infected with E. bromicola grown under different CdCl2 treatments. Seeds were collected from Qinghai Tongren (Site 1), Qinghai Zeku (Site 2), and Qinghai Gonghe. * indicated significant difference between E+ and E− at the 0.05 level.
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Figure 8. POD activity of E. dahuricus infected with E. bromicola grown under different CdCl2 treatments. Seeds were collected from Qinghai Tongren (Site 1), Qinghai Zeku (Site 2), and Qinghai Gonghe. * indicated significant difference between E+ and E− at 0.05 level.
Figure 8. POD activity of E. dahuricus infected with E. bromicola grown under different CdCl2 treatments. Seeds were collected from Qinghai Tongren (Site 1), Qinghai Zeku (Site 2), and Qinghai Gonghe. * indicated significant difference between E+ and E− at 0.05 level.
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Figure 9. CAT activity of E. dahuricus infected with E. bromicola grown under different CdCl2 treatments. Seeds were collected from Qinghai Tongren (Site 1), Qinghai Zeku (Site 2), and Qinghai Gonghe. * indicated significant difference between E+ and E− at 0.05 level.
Figure 9. CAT activity of E. dahuricus infected with E. bromicola grown under different CdCl2 treatments. Seeds were collected from Qinghai Tongren (Site 1), Qinghai Zeku (Site 2), and Qinghai Gonghe. * indicated significant difference between E+ and E− at 0.05 level.
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Figure 10. APX activity of E. dahuricus infected with E. bromicola grown under different CdCl2 treatments. Seeds were collected from Qinghai Tongren (Site 1), Qinghai Zeku (Site 2), and Qinghai Gonghe. * indicated significant difference between E+ and E− at 0.05 level.
Figure 10. APX activity of E. dahuricus infected with E. bromicola grown under different CdCl2 treatments. Seeds were collected from Qinghai Tongren (Site 1), Qinghai Zeku (Site 2), and Qinghai Gonghe. * indicated significant difference between E+ and E− at 0.05 level.
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Figure 11. The result of PCA analysis among Cd concentration, Epichloë, site, plant growth, and antioxidant capacity. Note: AGB indicated aboveground biomass; PH indicated plant height; TN indicated tiller number; BGB indicated belowground biomass; S indicated site; E indicated Epichloë bromicola; C indicated Cd concentration; Pro indicated proline.
Figure 11. The result of PCA analysis among Cd concentration, Epichloë, site, plant growth, and antioxidant capacity. Note: AGB indicated aboveground biomass; PH indicated plant height; TN indicated tiller number; BGB indicated belowground biomass; S indicated site; E indicated Epichloë bromicola; C indicated Cd concentration; Pro indicated proline.
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Table 1. E. dahuricus collection data and infection rate.
Table 1. E. dahuricus collection data and infection rate.
SiteLocationElevation (m)LongitudeLatitudeEndophyte Infection Rate (%)
1Qinghai Tongren2438102°05′07″35°57′58″50.0%
2Qinghai Zeku2876101°56′23″35°33′24″33.3%
3Qinghai Gonghe3230100°52′18″36°20′17″25.0%
Table 2. Results of multivariate variance analysis of Cd concentration (C), endophyte (E), and site (S) on E. dahuricus biomass. The significant level was 0.05. Data with significant differences are marked in bold.
Table 2. Results of multivariate variance analysis of Cd concentration (C), endophyte (E), and site (S) on E. dahuricus biomass. The significant level was 0.05. Data with significant differences are marked in bold.
Plant HeightTiller NumberBiomass above GroundBiomass below
Ground
dfF-ValuePF-ValuePF-ValuePF-ValueP
C4610.320.000370.610.000574.580.000359.800.000
E138.540.0003.570.06112.850.00022.550.000
S235.000.00010.940.0002.660.07428.850.000
C × E41.800.1341.030.3972.540.0433.050.020
C × S83.130.0033.290.0022.630.0113.980.000
E × S20.010.9990.080.9260.650.5220.100.904
C × E × S80.400.9180.320.9560.330.9530.570.799
Table 3. Results of multivariate variance analysis of Cd concentration (C), endophyte (E), and site (S) on MDA and proline content. The significant level was 0.05. Data with significant differences are marked in bold.
Table 3. Results of multivariate variance analysis of Cd concentration (C), endophyte (E), and site (S) on MDA and proline content. The significant level was 0.05. Data with significant differences are marked in bold.
MDAProline
dfF-ValuePF-ValueP
C41235.720.00030159.360.000
E1110.530.0003072.030.000
S2170.570.00024.430.000
C × E46.460.0001100.540.000
C × S824.580.0009.630.000
E × S24.160.01829.470.000
C × E × S84.090.0009.220.000
Table 4. Results of multivariate variance analysis of Cd concentration (C), endophyte (E), and site (S) on antioxidant enzyme activity. The significant level was 0.05. Data with significant differences are marked in bold.
Table 4. Results of multivariate variance analysis of Cd concentration (C), endophyte (E), and site (S) on antioxidant enzyme activity. The significant level was 0.05. Data with significant differences are marked in bold.
SODPODCATAPX
dfF-ValuePF-ValuePF-ValuePF-ValueP
C44058.840.0001256.790.0005341.590.0002404.360.000
E1924.710.00051.190.000167.260.000121.470.000
S2117.610.00021.120.00064.680.0006.820.002
C × E4141.480.0009.890.00039.800.00022.830.000
C × S839.560.0003.260.00237.580.00021.210.000
E × S25.160.0075.980.00313.470.0000.210.811
C × E × S89.850.0002.730.0093.560.0017.200.000
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Shi, Q.; Simpson, W.R.; Li, Y.; Xu, C.; De, K.; Li, X. Epichloë bromicola Enhances Elymus dahucirus Plant Growth and Antioxidant Capacity under Cadmium Stress. Agronomy 2024, 14, 365. https://doi.org/10.3390/agronomy14020365

AMA Style

Shi Q, Simpson WR, Li Y, Xu C, De K, Li X. Epichloë bromicola Enhances Elymus dahucirus Plant Growth and Antioxidant Capacity under Cadmium Stress. Agronomy. 2024; 14(2):365. https://doi.org/10.3390/agronomy14020365

Chicago/Turabian Style

Shi, Qian, Wayne R. Simpson, Yuling Li, Chengti Xu, Kejia De, and Xiuzhang Li. 2024. "Epichloë bromicola Enhances Elymus dahucirus Plant Growth and Antioxidant Capacity under Cadmium Stress" Agronomy 14, no. 2: 365. https://doi.org/10.3390/agronomy14020365

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