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Article

Investigation of Solanum carolinense Dominance and Phytotoxic Effect in Festuca arundinacea with Special Reference to Allelochemical Identification, Analysis of Phytohormones and Antioxidant Mechanisms

by
Lee-Rang Kim
1,
Arjun Adhikari
2,
Yosep Kang
2,
Ho-Jun Gam
2,
Sang-Mo Kang
2,
Ki-Yong Kim
3 and
In-Jung Lee
1,2,*
1
Division of Plant Biosciences, Kyungpook National University, Daegu 41566, Korea
2
Department of Applied Biosciences, Kyungpook National University, Daegu 41566, Korea
3
National Institute of Animal Science, Rural Development Administration (RDA), Cheonan 31000, Korea
*
Author to whom correspondence should be addressed.
Agronomy 2022, 12(8), 1954; https://doi.org/10.3390/agronomy12081954
Submission received: 1 July 2022 / Revised: 12 August 2022 / Accepted: 15 August 2022 / Published: 19 August 2022
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Abstract

:
Exposure to invasive weeds in pasturelands may result in significant losses and toxicity in forage crops. These species may also contain a compound that may be toxic as well as beneficial depending upon the effect induced. The Ministry of Environment of the Republic of Korea has now recognized Solanum carolinense (Horsenettle)—an invasive weed species—as a potential threat to forage crops in pasturelands and to the entire agro-ecosystem. As a forage crop, Festuca arundinacea (Tall fescue) is one of the major economical crops and diets of livestock; in this study, the competition patterns of Solanum carolinense and Festuca arundinacea were examined with respect to their seeding ratios and growth periods. In addition, an extract from the root of Solanum carolinense (SCE) was prepared and treated at 2500 ppm and 5000 ppm in a Festuca arundinacea plant to observe its effect. The experimental results showed that as the growth period of the Horsenettle and the SCE treatment increased, the germination rate, plant height, root length, fresh weight, and dry weight of the tall fescue were significantly decreased. Moreover, the SCE treatment significantly increased the quantities of reactive oxygen species (O2− and H2O2), antioxidants (Catalase and Peroxidase), and endogenous phytohormones (Abscisic acid and Salicylic acid), and simultaneously decreased the superoxide dismutase content in the tall fescue shoots. Furthermore, we identified several glycoalkaloids from the SCE extract, among which Solanidan-3-ol, (3β,5α)’ possessed a higher number (52%). Based on these results, we predicted that the Solanidan-3-ol, (3β,5α)’ present in horsenettle has a major role in imposing phytotoxicity on agricultural crops. The glycoalkaloids in the Solanum species have been reported to possess both phytotoxic and therapeutic uses. Based on this concept, we believe that the compound available in Solanum carolinense could be used in developing crop protection or medicinal products through broader research. Conversely, our findings also showed the probable risk of horsenettle to the agro-ecosystem, especially in terms of forage production.

1. Introduction

Forage crops are one of the major diets of livestock and occupy vast areas used for commercial land cultivation [1]. They are considered the backbone of sustainable agriculture and the world economy [2]. Tall fescue is one of the most important forage plants due to its tolerance to drought, salinity, heavy metals, and excessive grazing, as well as its ability to minimize soil erosion. It is also widely cultivated as a forage base for beef, dairy, and wool production; thus, it can be a significant choice for large-scale cultivation [2,3]. This grass is often cultivated for slope stabilization in the Republic of Korea [4]. However, the potential threat of invasion in forage croplands posed by invasive species may result in detrimental effects on forage production [5]. Solanum carolinense has been recognized as a significant threat to agricultural land and the ecosystem according to the report by the Ministry of the Environment of the Republic of Korea in 2021 (Appendix A). Solanum carolinense has a high capacity for spatial dispersal by natural means and different human-mediated pathways. As a result, the plant is likely to spread its range and infest cultivated land [6]. Solanum carolinense is expected to take over a wide range of locations in a short amount of time whenever it emerges due to its unpleasant qualities, e.g., herbivores find it unappealing to eat.
The glycoalkaloids present in Solanum sp. may result in both beneficial and detrimental effects, such as Solanum chacoense and Solanum maglia extracts, whose application has a strong inhibitory effect on mustard growth; however, the bioactive glycoalkaloids solasodine, solasonine, and solamargine isolated from Solanum melongena have medicinal properties [7,8]. A wide range of glycoalkaloids has been detected in Solanum plants [9]. Solanum species have also been reported to possess a strong allelopathic potential through varieties of allelochemical production [10]. In addition, Solanum carolinense has been reported to induce autoallelopathy in a few reports [11]. Exotic plants are characterized by having rapid fecundity and containing several allelochemicals that may also induce positive or negative allelopathy in the host plants [12,13]. The bioavailability and phytotoxicity of allelochemicals are determined by the outcome of the species interactions [14,15]. Moreover, allelochemicals are a novel class of herbicides that may be particularly useful in crop management [16]. Plants and other organisms interact through the release of allelochemicals and signaling chemicals into the environment [17,18]. As a result, allelochemicals help plants defend themselves against microbial attacks, herbivore predation, and/or competition with other plants, which prevents competing plants from adaptation [19,20]. The effect of allelochemicals in other species—especially on agricultural land—is important for optimum management and productivity [21,22]. Since Solanum carolinense has been previously reported on account of its detrimental effect as an invading species, identifying its allelochemicals and its effect on forage crops such as tall fescue are significant for sustainable agricultural practices.
Allelochemicals may induce secondary oxidative stress, thereby encouraging excessive reactive oxygen species in plants [23]. Conversely, some allelochemicals, such as those in garlic could improve the growth of plants by inducing a defense response system through regulating antioxidants and phytohormones [24]. Hence, understanding the underlying physiology, such as the reactive oxygen species, signaling through endogenous phytohormones, and the antioxidant system, helps to understand the defense mechanisms of plants [25,26]. Furthermore, the measurement of the invading tendencies of invasive species is crucial to assessing their impacts on pasture plants. The study of exotic weeds has led to the discovery of allelochemicals that can be used for a variety of agricultural applications [27,28]. However, little information is available about Solanum carolinense’s effects on agriculture. In this experiment, we will elucidate how we identified the allelochemical derivatives from Solanum carolinense and elaborate on its phytotoxic effect in Festuca arundinacea.

2. Materials and Methods

2.1. Plant Materials

The Solanum carolinense plants used in this experiment were collected from Daegu (35°53′43.5″ N 128°36′47.7″ E) in January 2020. The seeds of Festuca arundinacea were purchased from Da-nong Inc (Kentucky 31 tall fescue, Da-nong Inc., Namyangju, Korea). The Solanum carolinense used for extraction was freeze-dried using a freeze dryer (PVTFD20R, Ilshin Inc., Seoul, Korea).

2.2. Investigation of Competition Patterns between Festuca arundinacea and Solanum carolinense

2.2.1. Investigation of Competition Patterns according to the Seeding Ratio of Festuca arundinacea and Solanum carolinense

The total number of Solanum carolinens:Festuca arundinaceae seeds were sown, at a ratio of (So:Fe; 20:10, 10:10, and 10:20), into a pot (140 mm × 90 mm × 50 mm). The experiment was conducted in a greenhouse with temperature of 27 ± 4 °C and relative humidity 60~70%. Four weeks after sowing, a growth survey was conducted on plant height, root length, and fresh weight, and the sample was stored in an oven at 70 °C for 48 h to measure dry weight.

2.2.2. Investigation of Growth Patterns of Festuca arundinacea according to the Growth Period of Solanum carolinense

Solanum carolinense was transplanted into a pot 20, 40, and 60 days after sowing. One week after transplantation, 20 Festuca arundinacea seeds were sown into the pot containing 20-, 40-, and 60-day-old Solanum carolinense plants. After four weeks, the plants were harvested and plant height, root length, and fresh weight were measured, and the sample was stored in an oven at 70 °C for 48 h to measure dry weight.

2.3. Investigation of Phytotoxicity of SCE on Festuca arundinacea

2.3.1. Preparation of Crude Extract

A 350 g sample of lyophilized Solanum carolinense was suspended in 1150 mL of MeOH and kept in a shaker for 72 h. Afterward, it was filtered using filter paper (Advantec no. 2, Toyo Roshi Kaisha Ltd., Tokyo, Japan), and then concentrated in a round flask using a rotary vacuum evaporator (Eyela Rotary Vacuum Evaporator NN series, Eyela, Tokyo, Japan). The concentrated round flask was suspended using dH2O and then freeze-dried using a freeze-dryer.

2.3.2. Treatment of Crude Extract in Festuca arundinacea

Fifteen grains of Festuca arundinacea seeds were sown in a pot (100 mm × 90 mm) and allowed to grow for four-weeks. A 10,000-ppm stock solution was prepared using crude extract and dH2O. Accordingly, 2500 ppm and 5000 ppm of treatment solvent were prepared. A 5 mL pot−1 of each concentration was applied once a week for three weeks. After one week following harvesting of the last treatment sample, morphological parameters were measured and stored for biochemical analysis. Chlorophyll content was measured using portable CCM-300 Chlorophyll Contents Meter (ADC Bioscientific Ltd., Herts, UK).

2.4. Determination of Reactive Oxygen Species (ROS)

Reactive oxygen species are the result of stress suspected by the plant. These oxygen radicals alter the overall metabolism of the crops. Herein, to understand these complexities, we determine superoxide anion radical and Hydrogen peroxide measurements.
  • Superoxide anion radical (O2) measurement
The content of O2− was measured using the method of Navari-Izzo et al. [29]. In brief, the grounded sample was extracted using 10 mM potassium phosphate buffer (pH 7.8), 0.05% nitro blue tetrazolium (NBT), and 10 mM NaN3. The mixture was suspended at 85 °C for 15 min using a water bath, immediately cooled, filtered, and measured at 580 nm using a spectrophotometer (Multiskan GO UV/Vis Microplate Spectrophotometer, Thermo-Fisher Scientific, Waltham, MA, USA).
  • Hydrogen peroxide (H2O2) measurement
The content of H2O2 was measured using the protocol described by Jana and Choudhuri [30]. In brief, the sampled plant was harvested and immediately dipped in liquid N2, grounded, and extracted with phosphate buffer (pH 7.5), and was then centrifuged at 8160× g for 20 min at 4 °C. The extract was suspended with 20% H2SO4 and dissolved in 0.5% of TiCl4. The supernatant was collected through centrifugation at 8160× g for 20 min and measured at 410 nm using a spectrophotometer. The H2O2 content was calculated with a molar extinction coefficient of 0.28 mmol−1 cm−1.
  • Visualization of ROS (H2O2)
H2O2 visual evaluation was performed according to the method described by Thordal-Christensenet et al. [31], namely, a DAB (3,3-diaminobenzidine) staining method using the shoot of the Festuca arundinacea. In brief, the sample was kept in the dark at room temperature while immersed in DAB solution (1 mg/mL; pH 3.8) for 12 h, and then the stained sample was heated using ethanol in a water bath at 90 °C for 10 min. After that, the sample was stored in 60% glycol for 1 to 2 min and evaluated visually.

2.5. Determination of Antioxidant Enzyme

  • Superoxide dismutase (SOD) measurement
The SOD was measured by the methods described by Marklund and Marklund [32]. MeOH was added to the freeze-dried sample and extracted to prepare a sample solution. Tris-HCl buffer solution (50 mM Tris, pH 8.5) and 7.2 mM pyrogallol were added to dH2O (AC) or each sample solution (AS) to react at room temperature for 10 min. Thereafter, 1 N HCl was added to measure absorbance at 420 nm using a spectrophotometer. The SOD-like activity was calculated by the following equation.
SOD-like activity (%) = [1 − (AC/AS)] × 100
  • Catalase (CAT) measurement
CAT activity was measured by the method described by Aebi [33]. Frozen samples were extracted with a solution (50 mM Tris HCl, pH 7.0 3 mM MgCl2, 1 mM EDTA, and 1% PVP), and supernatant was separated and mixed with the solution (0.1 M Phosphate buffer pH 7.0, 0.2 M H2O2). The degree of decomposition of H2O2 was measured at 240 nm using a spectrophotometer.
  • Peroxidase (POD) measurement
The method described by Pütter [34] was used to confirm the activity of POD. The fresh sample was extracted using 0.1 M phosphate buffer (pH 6.8) and centrifuged at 19,386× g at 4 °C for 15 min. The supernatant was mixed with 0.1 M phosphate buffer, 50 μM pyrogallol, and 50 μM H2O2 and kept at room temperature for 5 min. Then, 5% of H2SO4 was mixed and measured at 420 nm using a spectrophotometer.

2.6. Quantification of Endogenous Phytohormones

  • Abscisic acid (ABA) measurement
The extraction and quantification of ABA in plants were performed according to the method described by Kang, et al. [35]. In brief, a lyophilized sample was extracted using an extraction solvent of 95% isopropanol and 5% acetic acid and stirred at 1.15× g for 30 min. The extract was filtered and standard [(±-3,5,5,7,7,7-d6]-ABA 100 ng was added. The extract was concentrated using rotary vacuum evaporator, extracted with 1N Sodium hydroxide (NaOH), and then adjusted to pH 12 to 13 using a pH meter. Chlorophyll was removed using Dichloromethane (CH2Cl2) and the pH of the supernatant was adjusted to 2.5 to 3.5, followed by the addition of Ethyl acetate (EtOAc), and then the supernatant was collected. The extract was concentrated, extracted by phosphate buffer (pH 8.0) in polyvinylpolypyrrolidone (PVPP), and stirred for 1 h. The solution was filtered, and pH was adjusted to 2.5 to 3.5. EtOAc was added to collect the supernatant, concentrated in a vial with nitrogen gas, and methylation was performed with diazomethane and anhydrous CH2Cl2. The obtained solution was injected into GC-MS (6890N Network GC System and 5973 Network Mass Selective Detector: Agilent Technologies, Santa Clara, CA, USA) equipped with a 30 m × 0.25 mm (i.d.) HP-1 capillary column, and quantitative calculations were performed by comparison to the standard curve derived from ABA-internal standard mentioned above.
  • Salicylic acid (SA) measurement
Extraction and quantification of endogenous SA were performed by the method described by Seskar et al. [36]. A freeze-dried sample was extracted for 20 min by adding 90% MeOH. The extract was centrifuged at 9660× g and 4 °C for 15 min, and then the supernatant was collected. Then, 100% MeOH was added to the remaining pellet portion and extracted again using a centrifuge. After collecting the supernatant, it was concentrated using speedvac (SPD2030, Thermo Fisher Scientific, Waltham, MA, USA), 5% trichloroacetic acid was added, separation was performed in a centrifuge at 9660× g and 4 °C for 10 min, and the supernatant was collected. An extraction solution mixed at a ratio of 49.5%, cyclopentane and 1% iso-propanol was added to the supernatant; then, the supernatant was recovered and dried with nitrogen gas. The dried sample was dissolved with 1 mL of MeOH and 20 µL was injected into HPLC to perform quantitative analysis. HPLC conditions were used for the analysis and quantification of SA.

2.7. Identification of Allelochemical in Solanum carolinense

2.7.1. Herbicidal Activity Assay

A 10,000-ppm Solanum carolinense extract was prepared using dH2O. Fifteen grains of Festuca arundinacea seeds were sowed on petri-dish (60 mm × 15 mm) layered with filter paper. After that, 2 mL of extract solution was inoculated and kept in an incubator at 30 °C for 7 days, and the germination rate and growth were investigated.

2.7.2. Isolation, Purification, and Identification of Allelochemicals

The Solanum carolinense root sample was ground and extracted with absolute methanol, concentrated using rotary vacuum evaporator, freeze-dried, and extracted using dH2O. Solvent fractionation was performed with 100 mL of Hexane, Chloroform (CHCl3), EtOAc, n-Butanol (BuOH), and dH2O per 10 g of crude extract according to the polarity of the solvent. Each fractional layer was compared by performing a herbicidal activity assay by the method described above. Allelochemical separation and purification were performed on the CHCl3 fraction, which had the highest growth inhibition rate among the solvent fractions. TLC (thin layer chromatography) was performed to set the appropriate mobile phase solvent for column chromatography. Column chromatography was carried out using silica gel (60, 0.040–0.063 nm, Merck Millipore, Darmstadt, Germany), and separation was carried out using a solvent in which MeOH, CHCl3, and dH2O were mixed at a ratio of 7:14:1. Consequently, three fractions—A, B, and C—were obtained. Each fraction was concentrated, and a germination inhibition assay was performed by the method described above; among them, column chromatography was performed on the B fraction, which had the highest growth inhibition rate with a solvent in which MeOH, CHCl3, and dH2O were mixed at a ratio of 6:14:1. Six fractions of BA, BB, BC, BD, BE, and BF were obtained and a herbicidal activity assay was performed. The BD fraction showed the highest activity to inhibit growth and was finally analyzed using GC-MS (Figure 1).

2.8. Statistical Analysis

All experiments were performed in three repetitions. Statistical significance analysis was expressed as mean and standard deviation using the Statistics Analysis System (SAS Software, Version 9.4, SAS Institute Inc., CARY, NC, USA) program. The difference between each processing sequence was tested at p < 0.05 through Duncan’s Multiple Range Test (DMRT). Chemsketch version 12 was used to construct the molecular structure of the compound.

3. Results

3.1. Investigation of Competition Patterns

3.1.1. Evaluation of Competition Patterns according to the Seeding Ratio

The Festuca arundinacea:Solanum carolinense growth rates were tested at ratios of 2:1, 1:1, and 1:2 (Figure 2, Table 1). The results showed that the germination rate, plant height, root length, fresh weight, and dry weight of Festuca arundinacea were significantly decreased when compared to the untreated group. This showed that Solanum carolinense has a significant dominance over the growth of Festuca arundinacea.

3.1.2. Competition Patterns according to the Growth Period

The Solanum carolinense was grown for 20, 40, and 60 days and Festuca arundinacea was incorporated to observe the growth pattern. The germination rate, plant height, root length, fresh weight, and dry weight of Festuca arundinacea were significantly decreased in all treatment groups compared to the control. (Figure 3 and Table 2). According to this evidence, regardless of the growth phase, if Solanum carolinense dominates first, it has a significant inhibitory effect on Festuca arundinacea.

3.2. Investigation of Phytotoxicity of SCE on Festuca arundinacea

3.2.1. Effect on Morphological Characteristics and Chlorophyll Content

The results of the foliar treatment of SCE at 2500 and 5000 ppm concentrations showed a decrease in Festuca arundinacea height by 24.9% and 43.4%, fresh weight by 20% and 40%, and dry weight by 14.2% and 42.8%, respectively, when compared to the untreated plant (Figure 4, Table 3). The chlorophyll content decreased by 7.5% and 9.3% after treatment with the extract at 2500 ppm and 5000 ppm concentrations, respectively (Figure 5). Based on these results, it was predicted that SCE contains an allelochemical that inhibits the growth of Festuca arundinacea.

3.2.2. Determination of Reactive Oxygen Species (ROS)

ROS act as signaling molecules regulating plant responses to biotic and abiotic stresses [37,38]. In our study, the crude extract treatments at 2500 and 5000 ppm significantly increased the Superoxide anion radical (O2−) content by 7.8% and 33.4%, respectively (Figure 6); similarly, the H2O2 content significantly increased to 33.3% and 85.8% (Figure 7). Moreover, the visual evaluation of H2O2 was observed after processing 5000 ppm of SCE in Festuca arundinacea using the DAB staining method. It was visually confirmed that the H2O2 content of the Festuca arundinacea leaves treated with the SCE was increased (Figure 8). The ROS radicals generate lipid peroxide, affect membrane permeability, and degrade DNA and proteins. Allelochemicals also depolarize the cell membrane, causing cellular disruption and cell death. Although all organisms require an appropriate level of ROS concentration, an excessive accumulation of ROS in plants can destroy chlorophyll and affect root development [39,40]. Based on these results, we can conclude that allelochemicals in the SCE induce detrimental effects in Festuca arundinacea.

3.2.3. Determination of Antioxidant Enzyme

Antioxidants play a key role in conferring tolerance in plants under stress [41]. Here, as the SCE treatment increased in Festuca arundinacea from 2500 ppm to 5000 ppm, the SOD decreased by 38.3% and 80.5%, respectively; the CAT content increased by 34.1% and 64.5%, respectively; and the POD content increased by 6.5% and 12.7%, respectively (Figure 9A–C).

3.2.4. Abscisic Acid (ABA) and Salicylic Acid (SA) Quantification

Allelochemicals affect plant growth and development by regulating phytohormones such as ABA and SA [42,43]. In this study, as the concentration of the extract increased to 2500 and 5000 ppm, the ABA content in Festuca arundinacea increased by 35.5 % and 49.7 % (Figure 10A); likewise, the SA content increased by 12.8% and 26.3%, respectively (Figure 10B), compared to the untreated group.

3.3. Identification of Allelochemical in Solanum carolinense

As a result of performing the GC-MS analysis on the BD fraction, Solanidan-3-ol, (3β,5α) showed the highest concentration (51.96%). Several other glycoalkaloids such as 1H, 7H-[1,3]Benzodioxino[6,5-g][1,3]Benzodioxolo[5,6-a]quinolizine,9,10,15b,16-tetrahydro-5,15-dimethoxy-, (S) (11.5%), 5,5-Dimethylimidazolidin-2,4-dione (5.65%), solanidan-3-one (5.64%), and D-Allose (4.02%) were identified as major components (Figure 11 and Table 4)

4. Discussion

Invasive plant species harm agriculture around the world, reducing crop productivity and quality [44]. However, the allelochemicals available in these species may be of significant use for defensive actions, such as herbicidal and insecticidal usages [19,45]. Since Solanum carolinense has been reported as a threat to agriculture and the eco-system, the current study demonstrates the growth pattern of Solanum carolinense and evaluates its toxic effect in the tall fescue type of forage grass. In addition, several allelochemicals were identified from Solanum carolinense, which might have induced a detrimental effect on tall fescue.
The current study demonstrated that the growth of tall fescue was significantly dominated by Solanum carolinense in all the seeding ratios as well as the increasing number of days after sowing. These enhanced the competition of the forage crops in response to S. carolinense. Our results are in line with Beeler et al. [46] who reported the adverse effect of S. carolinense on tall fescue’s quality and yield. Moreover, the dominance of S. carolinense was reported in several other crops such as cereals especially wheat and maize, followed by soybean, potatoes and lucerne [6]. In general, one Solanum carolinense entity may produce 100 or more fruits, where each fruit may contain 40 to 170 seeds, and its roots are deeply lowered with a high starch content, making it difficult to achieve mechanical control [47]. In addition, chemical control is arduous due to its deeper root system [48]. Invading populations may remain undetected for years, and an invasion is only recognized once it has reached an unstable stage. Unfortunately, at this point, eradication is no longer an option, and slowing expansion rates are prohibitively expensive [49].
In addition to the high susceptibility of tall fescue to horsenettle invasions, our study also showed that when the tall fescue seedlings were treated with SCE, the treatment resulted in detrimental effects in plant growth and development. As a result, a further investigation was performed to identify the possible inhibitory compound in SCE. Following our investigation, we discovered numerous substances, the most prominent of which were the glycoalkaloids (Solanidan-3-ol, (3β,5α)) in SCE. In general, glycoalkaloids inhibit acetylcholinesterase (AChE) in living organisms and destroy biological membranes, and are toxic to pathogens, insects, and humans [50,51]. This compound might have induced stress in the tall fescue plants, resulting in a significant drop in their growth and development. Similar results were shown by Fukuhara et al. [52], who reported that the steroidal glycoalkaloid arudonine inhibited the growth of Lactuca Sativa. Similarly, Sun et al. [9] reported that the glycoalkaloids solamargine/solasonine and chaconine/solanine retarded cucumber root growth. Moreover, our results are in line with Sołtys-Kalina et al. [53], who demonstrated the phytotoxicity induced by wild potatoes (Solanum sp.) against mustard.
Allelochemicals may be directly involved in the production of vulnerable ROS that stimulate oxidizing enzymes and increase free radicals [54,55]. In other cases, the allelochemicals might directly inhibit oxidizing enzymes in some way, leaving the plant vulnerable to oxidative damage [56]. Hence, the interplay of metabolomic aspects such as endogenous phytohormones (ABA and SA), antioxidants (CAT, POD, and SOD), and ROS (O2 and H2O2) is crucial for understanding the resistance patterns of plants as they are directly involved in the cross signaling of plants [57,58,59]. The current study showed that the H2O2 and O2 content was significantly elevated in tall fescue plants with the treatment of SCE. These results are supported by several authors; for instance, allelochemicals have induced ROS in various crops, from donor tobacco to acceptor lettuce [60,61], fescue to tomato [62], Chinese licorice to lettuce, and aromatic plants to wheat, wild oats, walnuts, and maize [26].
The plant activates an antioxidant defense system to assist in ROS detoxification under various abiotic stresses [63]. A variety of antioxidant systems counteract ROS accumulation in stress-induced cells, which include SOD, APX, GPX, GST, and CAT [64]. Our study showed that antioxidants such as CAT and POD were considerably elevated with the SCE treatment, while simultaneously dropping SOD levels. In general, O2 is converted to H2O2 by superoxide dismutase; catalases then induce detoxification by converting 2H2O2 to O2 + 2H2O [65]. These phenomena were triggered by the influence of endogenous phytohormones such as ABA and SA [66].
The phytohormone ABA is involved in cross-signaling and SA in inducing systemic resistance in plants under stress [35,67]. The mechanism is involved in regulating antioxidants, modulating enzymes, coding amino acids, and triggering stress-responsive genes [68]. Our study showed that the SCE treatment elevated the ABA and SA levels of tall fescue. To a large extent, the higher ABA and SA levels signify the plant’s ability to defend itself against the stress. Our results are in line with Han et al. [69], who showed that elevated ABA levels led to a higher accumulation of H2O2 in tall fescue under cadmium stress. However, the higher elevation of ABA and SA for defense against stress may cost significant losses in plant growth. Hence, the exogenous application of ABA and SA are generally preferred to ease the tall fescue defense mechanism, which has been reported by several authors on account of mitigating drought stress [70]; conferring heat tolerance [71]; improving phytoremediation [72]; strengthening the antioxidant system and photosynthesis [73]; enhancing shelf life, photochemical efficiency, and the transplant success rate [74]; and increasing gene coding and the production of enzymes [75].

5. Conclusions

Overall, our results demonstrated that Solanum carolinense has a high potential to cause agricultural crop invasions, resulting in adverse effects on the ecosystem. Moreover, the glycoalkaloid compounds in SCE induced phytotoxicity through increasing the number of ROS and activating defense-responsive mechanisms such as phytohormone signaling and the antioxidant system. This evidence may provide significant insights into developing strategies for the management of invasive species and forage crop production. Moreover, from the perspective of the beneficial and detrimental effects of Solanum sp. glycoalkaloids, the compound that we have discovered from Solanum carolinense extract may be valuable for future research to ease the scientific burden involving the identification of the plants.

Author Contributions

Conceptualization and investigation, L.-R.K.; biochemical analysis, Y.K. and H.-J.G., methodology and writing—original draft preparation, A.A.; resources management, K.-Y.K.; supervision, project administration, funding acquisition, S.-M.K. and I.-J.L. All authors have read and agreed to the published version of the manuscript.

Funding

This study was supported by the Agenda Program (Project No. PJ015026022022) Rural Development Administration, Republic of Korea.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results.

Appendix A

Information regarding different exotic species as reported in the database of the Ministry of Environment, South Korea, is available through the following link: (law.go.kr) (accessed on 5 July 2021).

References

  1. Barnes, R.F. Importance and problems of tall fescue. In Biotechnology in Tall Fescue Improvement; CRC Press: Boca Raton, FL, USA, 2018; pp. 1–12. [Google Scholar]
  2. Chen, L.; Auh, C.K.; Dowling, P.; Bell, J.; Chen, F.; Hopkins, A.; Dixon, R.A.; Wang, Z.Y. Improved forage digestibility of tall fescue (Festuca arundinacea) by transgenic down-regulation of cinnamyl alcohol dehydrogenase. Plant Biotechnol. J. 2003, 1, 437–449. [Google Scholar] [CrossRef] [PubMed]
  3. Shahabzadeh, Z.; Mohammadi, R.; Darvishzadeh, R.; Jafari, M.; Breeding, F.P.; Research, G. Investigation of genetic diversity of forage yield and morphological traits in tall fescue (Festuca arundinacea Schreb.) populations. Mol. Biol. Rep. 2020, 28, 17–36. [Google Scholar] [CrossRef]
  4. Park, S.; Kim, J.H.; Lee, E.J. Resistance of plant communities to invasion by tall fescue. An experimental study combining species diversity, functional traits and nutrient levels. Basic Appl. Ecol. 2022, 58, 39–49. [Google Scholar] [CrossRef]
  5. Tanveer, A.; Khaliq, A.; Ali, H.H.; Mahajan, G.; Chauhan, B.S. Interference and management of parthenium: The world’s most important invasive weed. Crop Prot. 2015, 68, 49–59. [Google Scholar] [CrossRef]
  6. Follak, S.; Strauss, G. Potential distribution and management of the invasive weed Solanum carolinense in Central Europe. Weed Res. 2010, 50, 544–552. [Google Scholar] [CrossRef]
  7. Fekry, M.I.; Ezzat, S.M.; Salama, M.M.; Alshehri, O.Y.; Al-Abd, A.M. Bioactive glycoalkaloides isolated from Solanum melongena fruit peels with potential anticancer properties against hepatocellular carcinoma cells. Sci. Rep. 2019, 9, 1746. [Google Scholar] [CrossRef]
  8. Altesor, P.; García, Á.; Font, E.; Rodríguez-Haralambides, A.; Vilaró, F.; Oesterheld, M.; Soler, R.; González, A. Glycoalkaloids of Wild and Cultivated Solanum: Effects on Specialist and Generalist Insect Herbivores. J. Chem. Ecol. 2014, 40, 599–608. [Google Scholar] [CrossRef]
  9. Sun, F.; Li, S.; He, D.; Cao, G.; Ni, X.; Tai, G.; Zhou, Y.; Wang, D. Effects of glycoalkaloids from Solanum plants on cucumber root growth. Phytochemistry 2010, 71, 1534–1538. [Google Scholar] [CrossRef]
  10. Waseem, M.; Badruzzaman, S.M. Allelopathy in Solanaceae plants. J. Plant Prot. Res. 2018, 58, 1–7. [Google Scholar] [CrossRef]
  11. Solomon, B.P. Autoallelopathy in Solanum carolinense: Reversible delayed germination. Am. Midl. Nat. 1983, 110, 412–418. [Google Scholar] [CrossRef]
  12. Bais, H.P.; Vepachedu, R.; Gilroy, S.; Callaway, R.M.; Vivanco, J.M. Allelopathy and Exotic Plant Invasion: From Molecules and Genes to Species Interactions. Science 2003, 301, 1377–1380. [Google Scholar] [CrossRef] [PubMed]
  13. Hierro, J.L.; Maron, J.L.; Callaway, R.M. A biogeographical approach to plant invasions: The importance of studying exotics in their introduced and native range. J. Ecol. 2005, 93, 5–15. [Google Scholar] [CrossRef]
  14. Scavo, A.; Abbate, C.; Mauromicale, G. Plant allelochemicals: Agronomic, nutritional and ecological relevance in the soil system. Plant Soil 2019, 442, 23–48. [Google Scholar] [CrossRef]
  15. Schandry, N.; Becker, C. Allelopathic plants: Models for studying plant–interkingdom interactions. Trends Plant Sci. 2020, 25, 176–185. [Google Scholar] [CrossRef] [PubMed]
  16. Soltys, D.; Krasuska, U.; Bogatek, R.; Gniazdowska, A. Allelochemicals as Bioherbicides—Present and Perspectives. In Herbicides—Current Research and Case Studies in Use; IntechOpen: Dallas, TX, USA, 2013. [Google Scholar] [CrossRef]
  17. Cheng, F.; Cheng, Z. Research progress on the use of plant allelopathy in agriculture and the physiological and ecological mechanisms of allelopathy. Front. Plant Sci. 2015, 6, 1020. [Google Scholar] [CrossRef] [PubMed]
  18. Macias, F.A.; Molinillo, J.M.; Varela, R.M.; Galindo, J.C. Allelopathy—A natural alternative for weed control. Pest Manag. Sci. 2007, 63, 327–348. [Google Scholar] [CrossRef]
  19. Tlak Gajger, I.; Dar, S.A. Plant allelochemicals as sources of insecticides. Insects 2021, 12, 189. [Google Scholar] [CrossRef]
  20. Saraf, M.; Pandya, U.; Thakkar, A. Role of allelochemicals in plant growth promoting rhizobacteria for biocontrol of phytopathogens. Microbiol. Res. 2014, 169, 18–29. [Google Scholar] [CrossRef]
  21. Vyvyan, J.R. Allelochemicals as leads for new herbicides and agrochemicals. Tetrahedron 2002, 58, 1631–1646. [Google Scholar] [CrossRef]
  22. Dayan, F.E.; Duke, S.O. Natural compounds as next-generation herbicides. J. Plant Physiol. 2014, 166, 1090–1105. [Google Scholar] [CrossRef]
  23. Bogatek, R.; Gniazdowska, A. ROS and phytohormons in plant-plant allelopathic interaction. Plant Signal. Behav. 2007, 2, 317–318. [Google Scholar] [CrossRef]
  24. Ali, M.; Ahmad, H.; Hayat, S.; Ghani, M.I.; Amin, B.; Atif, M.J.; Wali, K.; Cheng, Z. Application of garlic allelochemicals improves growth and induces defense responses in eggplant (Solanum melongena) against Verticillium Dahliae. Ecotoxicol. Environ. Saf. 2021, 215, 112132. [Google Scholar] [CrossRef] [PubMed]
  25. Nadarajah, K.K. ROS homeostasis in abiotic stress tolerance in plants. Int. J. Mol. Sci. 2020, 21, 5208. [Google Scholar] [CrossRef] [PubMed]
  26. Staszek, P.; Krasuska, U.; Ciacka, K.; Gniazdowska, A. ROS Metabolism Perturbation as an Element of Mode of Action of Allelochemicals. Antioxidants 2021, 10, 1648. [Google Scholar] [CrossRef] [PubMed]
  27. Das, C.; Dey, A.; Bandyopadhyay, A. Allelochemicals: An emerging tool for weed management. In Evidence Based Validation of Traditional Medicines; Springer: Singapore, 2021; pp. 249–259. [Google Scholar] [CrossRef]
  28. Kong, C.-H.; Xuan, T.D.; Khanh, T.D.; Tran, H.-D.; Trung, N.T. Allelochemicals and Signaling Chemicals in Plants. Molecules 2019, 24, 2737. [Google Scholar] [CrossRef] [PubMed]
  29. Navari-Izzo, F.; Pinzino, C.; Quartacci, M.F.; Sgherri, C.L. Superoxide and hydroxyl radicai generation, and superoxide dismutase in PII membrane fragments from wheat. Free Radic. Res. 1999, 31, 3–9. [Google Scholar] [CrossRef]
  30. Jana, S.; Choudhuri, M.A. Glycolate metabolism of three submersed aquatic angiosperms during ageing. Aquat. Bot. 1982, 12, 345–354. [Google Scholar] [CrossRef]
  31. Thordal-Christensen, H.; Zhang, Z.; Wei, Y.; Collinge, D.B.J. Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley—Powdery mildew interaction. Plant J. 1997, 11, 1187–1194. [Google Scholar] [CrossRef]
  32. Marklund, S.; Marklund, G. Involvement of the superoxide anion radical in the autoxidation of pyrogallol and a convenient assay for superoxide dismutase. Eur. J. Biochem. 1974, 47, 469–474. [Google Scholar] [CrossRef]
  33. Aebi, H. Catalase. In Methods of Enzymatic Analysis; Elsevier: Amsterdam, The Netherlands, 1974; pp. 673–684. [Google Scholar]
  34. Pütter, J. Peroxidases. In Methods of Enzymatic Analysis; Elsevier: Amsterdam, The Netherlands, 1974; pp. 685–690. [Google Scholar]
  35. Kang, S.-M.; Adhikari, A.; Lee, K.-E.; Khan, M.A.; Shahzad, R.; Dhungana, S.K.; Lee, I.-J. Inoculation with Indole-3-acetic acid-producing rhizospheric Rhodobacter sphaeroides KE149 augments growth of adzuki bean plants under water stress. J. Microbiol. Biotechnol. 2020, 30, 717–725. [Google Scholar] [CrossRef]
  36. Seskar, M.; Shulaev, V.; Raskin, I. Endogenous methyl salicylate in pathogen-inoculated tobacco plants. Plant Physiol. 1998, 116, 387–392. [Google Scholar] [CrossRef]
  37. Foyer, C.H.; Noctor, G. Redox homeostasis and antioxidant signaling: A metabolic interface between stress perception and physiological responses. Plant Cell 2005, 17, 1866–1875. [Google Scholar] [CrossRef] [PubMed]
  38. Kwak, J.M.; Nguyen, V.; Schroeder, J.I. The role of reactive oxygen species in hormonal responses. Plant Physiol. 2006, 141, 323–329. [Google Scholar] [CrossRef] [PubMed]
  39. Zafra, A.; Rodríguez-García, M.I.; Alché, J.d.D. Cellular localization of ROS and NO in olive reproductive tissues during flower development. BMC Plant Biol. 2010, 10, 36. [Google Scholar] [CrossRef]
  40. Foreman, J.; Demidchik, V.; Bothwell, J.H.; Mylona, P.; Miedema, H.; Torres, M.A.; Linstead, P.; Costa, S.; Brownlee, C.; Jones, J.D.; et al. Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 2003, 422, 442–446. [Google Scholar] [CrossRef]
  41. Kusvuran, S.; Kiran, S.; Ellialtioglu, S.S. Antioxidant enzyme activities and abiotic stress tolerance relationship in vegetable crops. In Abiotic and Biotic Stress in Plants—Recent Advances and Future Perspectives; Intech: Dallas, TX, USA, 2016; pp. 481–506. [Google Scholar] [CrossRef]
  42. Cheng, F.; Cheng, Z.-H.; Meng, H.-W. Transcriptomic insights into the allelopathic effects of the garlic allelochemical diallyl disulfide on tomato roots. Sci. Rep. 2016, 6, 38902. [Google Scholar] [CrossRef]
  43. Escobar-Bravo, R.; Ruijgrok, J.; Kim, H.K.; Grosser, K.; Van Dam, N.M.; Klinkhamer, P.G.; Leiss, K.A. Light intensity-mediated induction of trichome-associated allelochemicals increases resistance against thrips in tomato. Plant Cell Physiol. 2018, 59, 2462–2475. [Google Scholar] [CrossRef]
  44. Pimentel, D.; Lach, L.; Zuniga, R.; Morrison, D. Environmental and economic costs of nonindigenous species in the United States. Biosci. J. 2000, 50, 53–65. [Google Scholar] [CrossRef]
  45. Berry, J.P.; Gantar, M.; Perez, M.H.; Berry, G.; Noriega, F.G. Cyanobacterial toxins as allelochemicals with potential applications as algaecides, herbicides and insecticides. Mar. Drugs 2008, 6, 117–146. [Google Scholar] [CrossRef]
  46. Beeler, J.E.; Rhodes, G.N.; Bates, G.E.; Main, C.L.; Mueller, T.C. Horsenettle (Solanum carolinense) control in tall fescue (Festuca arundinacea) and clover (Trifolium sp.) pastures with mixtures of 2,4-D and picloram. Camb. Core Weed Technol. 2004, 18, 1091–1095. [Google Scholar] [CrossRef]
  47. Gorrell, R.M.; Bingham, S.W.; Foy, C.L. Control of Horsenettle (Solarium carolinense) Fleshy Roots in Pastures. Camb. Core Weed Sci. 1981, 29, 586–589. [Google Scholar] [CrossRef]
  48. Nichols, R.L.; Cardina, J.; Lynch, R.L.; Minton, N.A.; Wells, H.D. Insects, Nematodes, and Pathogens Associated by Horsenettle (Solanum carolinense) in Bermudagrass (Cynodon dactylon) Pastures. Camb. Core Weed Sci. 1992, 40, 320–325. [Google Scholar] [CrossRef]
  49. Davies, K.W.; Sheley, R.L. A conceptual framework for preventing the spatial dispersal of invasive plants. Camb. Core Weed Sci. 2007, 55, 178–184. [Google Scholar] [CrossRef]
  50. Milner, S.E.; Brunton, N.P.; Jones, P.W.; O’Brien, N.M.; Collins, S.G.; Maguire, A.R. Bioactivities of glycoalkaloids and their aglycones from Solanum species. J. Agric. Food. Chem. 2011, 59, 3454–3484. [Google Scholar] [CrossRef]
  51. Yencho, G.C.; Kowalski, S.P.; Kennedy, G.G.; Sanford, L.L. Segregation of leptine glycoalkaloids and resistance to Colorado potato beetle (Leptinotarsa decemlineata (Say)) in F2 Solanum tuberosum (4x) × S. chacoense (4x) potato progenies. Am. J. Potato Res. 2000, 77, 167–178. [Google Scholar] [CrossRef]
  52. Fukuhara, K.; Shimizu, K.; Kubo, I. Arudonine, an allelopathic steroidal glycoalkaloid from the root bark of Solanum arundo Mattei. Phytochemistry 2004, 65, 1283–1286. [Google Scholar] [CrossRef]
  53. Sołtys-Kalina, D.; Murawska, Z.; Strzelczyk-Żyta, D.; Wasilewicz-Flis, I.; Marczewski, W. Phytotoxic potential of cultivated and wild potato species (Solanum sp.): Role of glycoalkaloids, phenolics and flavonoids in phytotoxicity against mustard (Sinapis alba L.). Acta Physiol. Plant. 2019, 41, 55. [Google Scholar] [CrossRef]
  54. Rudrappa, T.; Bonsall, J.; Gallagher, J.L.; Seliskar, D.M.; Bais, H.P. Root-secreted allelochemical in the noxious weed Phragmites australis deploys a reactive oxygen species response and microtubule assembly disruption to execute rhizotoxicity. J. Chem. Ecol. 2007, 33, 1898–1918. [Google Scholar] [CrossRef]
  55. Coelho, É.M.P.; Barbosa, M.C.; Mito, M.S.; Mantovanelli, G.C.; Oliveira, R.S.; Ishii-Iwamoto, E.L. The activity of the antioxidant defense system of the weed species Senna obtusifolia L. and its resistance to allelochemical stress. J. Chem. Ecol. 2017, 43, 725–738. [Google Scholar] [CrossRef]
  56. Weir, T.L.; Park, S.-W.; Vivanco, J.M. Biochemical and physiological mechanisms mediated by allelochemicals. Curr. Opin. Plant Biol. 2004, 7, 472–479. [Google Scholar] [CrossRef]
  57. Nabi, R.B.S.; Tayade, R.; Hussain, A.; Adhikari, A.; Lee, I.-J.; Loake, G.J.; Yun, B.-W. A Novel DUF569 Gene Is a Positive Regulator of the Drought Stress Response in Arabidopsis. Int. J. Mol. Sci. 2021, 22, 5316. [Google Scholar] [CrossRef] [PubMed]
  58. Bhusal, N.; Lee, M.; Lee, H.; Adhikari, A.; Han, A.R.; Han, A.; Kim, H.S. Evaluation of morphological, physiological, and biochemical traits for assessing drought resistance in eleven tree species. Sci. Total Environ. 2021, 779, 146466. [Google Scholar] [CrossRef] [PubMed]
  59. Kazerooni, E.A.; Maharachchikumbura, S.S.; Adhikari, A.; Al-Sadi, A.M.; Kang, S.-M.; Kim, L.-R.; Lee, I.-J. Rhizospheric Bacillus amyloliquefaciens protects Capsicum annuum cv. Geumsugangsan from multiple abiotic stresses via multifarious plant growth-promoting attributes. Front. Plant Sci. 2021, 12, 821. [Google Scholar] [CrossRef] [PubMed]
  60. Zhang, S.; Sun, S.-W.; Shi, H.-L.; Zhao, K.; Wang, J.; Liu, Y.; Liu, X.-H.; Wang, W.J.P. Physiological and biochemical mechanisms mediated by allelochemical isoliquiritigenin on the growth of lettuce seedlings. Plants 2020, 9, 245. [Google Scholar] [CrossRef]
  61. Ren, X.; Yan, Z.-q.; He, X.-f.; Li, X.-z.; Qin, B. Allelopathic effect of β-cembrenediol and its mode of action: Induced oxidative stress in lettuce seedlings. Emir. J. Food Agric. 2017, 6, 441–449. [Google Scholar] [CrossRef]
  62. Krasuska, U.; Andrzejczak, O.; Staszek, P.; Borucki, W.; Gniazdowska, A. meta-Tyrosine induces modification of reactive nitrogen species level, protein nitration and nitrosoglutathione reductase in tomato roots. Nitric Oxide 2017, 68, 56–67. [Google Scholar] [CrossRef] [PubMed]
  63. Hasanuzzaman, M.; Bhuyan, M.H.M.B.; Zulfiqar, F.; Raza, A.; Mohsin, S.M.; Mahmud, J.A.; Fujita, M.; Fotopoulos, V. Reactive Oxygen Species and Antioxidant Defense in Plants under Abiotic Stress: Revisiting the Crucial Role of a Universal Defense Regulator. Antioxidants 2020, 9, 681. [Google Scholar] [CrossRef]
  64. Gill, S.S.; Tuteja, N. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol. Biochem. 2010, 48, 909–930. [Google Scholar] [CrossRef]
  65. You, J.; Chan, Z. ROS regulation during abiotic stress responses in crop plants. Front. Plant Sci. 2015, 6, 1092. [Google Scholar] [CrossRef]
  66. Ahmad, P.; Umar, S.; Sharma, S. Mechanism of free radical scavenging and role of phytohormones in plants under abiotic stresses. In Plant Adaptation and Phytoremediation; Springer: Dordrecht, The Netherlands, 2010; pp. 99–118. [Google Scholar] [CrossRef]
  67. Adhikari, A.; Khan, M.A.; Imran, M.; Lee, K.-E.; Kang, S.-M.; Shin, J.Y.; Joo, G.-J.; Khan, M.; Yun, B.-W.; Lee, I.-J. The Combined Inoculation of Curvularia lunata AR11 and Biochar Stimulates Synthetic Silicon and Potassium Phosphate Use Efficiency, and Mitigates Salt and Drought Stresses in Rice. Front. Plant Sci. 2022, 13, 816858. [Google Scholar] [CrossRef]
  68. Adhikari, A.; Khan, M.A.; Lee, K.-E.; Kang, S.-M.; Dhungana, S.K.; Bhusal, N.; Lee, I.-J. The Halotolerant Rhizobacterium—Pseudomonas koreensis MU2 Enhances Inorganic Silicon and Phosphorus Use Efficiency and Augments Salt Stress Tolerance in Soybean (Glycine max L.). Microoganisms 2020, 8, 1256. [Google Scholar] [CrossRef] [PubMed]
  69. Han, M.; Wang, B.; Song, G.; Shi, S. Comparative study of alleviation effects of DMTU and PCIB on root growth inhibition in two tall fescue varieties under cadmium stress. Ecotoxicol. Environ. Saf. 2020, 196, 110528. [Google Scholar] [CrossRef]
  70. Pirnajmedin, F.; Majidi, M.M.; Taleb, H.; Saeidi, G.; Shojaiefar, S. Genotypic-specific response to exogenous applied salicylic acid in tall fescue under different irrigation conditions. Crop Sci. 2020, 60, 1123–1130. [Google Scholar] [CrossRef]
  71. Zhang, X.; Wang, X.; Zhuang, L.; Gao, Y.; Huang, B. Abscisic acid mediation of drought priming-enhanced heat tolerance in tall fescue (Festuca arundinacea) and Arabidopsis. Physiol. Plant. 2019, 167, 488–501. [Google Scholar] [CrossRef] [PubMed]
  72. Rostami, M.; Rostami, S. Effect of salicylic acid and mycorrhizal symbiosis on improvement of fluoranthene phytoremediation using tall fescue (Festuca arundinacea Schreb). Chemosphere 2019, 232, 70–75. [Google Scholar] [CrossRef]
  73. Chen, Z.; Wang, Z.; Yang, Y.; Li, M.; Xu, B. Abscisic acid and brassinolide combined application synergistically enhances drought tolerance and photosynthesis of tall fescue under water stress. Sci. Hortic. 2018, 228, 1–9. [Google Scholar] [CrossRef]
  74. Ervin, E.; Zhang, X.; Schmidt, R. Exogenous Salicylic Acid Enhances Post-Transplant Success of Heated Kentucky Bluegrass and Tall Fescue Sod. Crop Sci. 2005, 45, 240–244. [Google Scholar] [CrossRef]
  75. Zhang, X.; Liu, Y.; Liu, Q.; Zong, B.; Yuan, X.; Sun, H.; Wang, J.; Zang, L.; Ma, Z.; Liu, H.; et al. Nitric oxide is involved in abscisic acid-induced photosynthesis and antioxidant system of tall fescue seedlings response to low-light stress. Environ. Exp. Bot. 2018, 155, 226–238. [Google Scholar] [CrossRef]
Agronomy 12 01954 g001 550
Figure 1. The process of separating and purifying allelochemical of Solanum carolinense.
Figure 1. The process of separating and purifying allelochemical of Solanum carolinense.
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Figure 2. Effect of seeding ratio of Solanum carolinense on the growth of Festuca arundinacea.
Figure 2. Effect of seeding ratio of Solanum carolinense on the growth of Festuca arundinacea.
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Figure 3. The effect of dominance of Solanum carolinense on the growth of Festuca arundinace.
Figure 3. The effect of dominance of Solanum carolinense on the growth of Festuca arundinace.
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Figure 4. Effect of SCE treatment on the growth of Festuca arundinacea.
Figure 4. Effect of SCE treatment on the growth of Festuca arundinacea.
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Figure 5. Effect of SCE treatment on chlorophyll content of Festuca arundinacea. Error bars represent standard deviations. Each data point represents the mean of at least six replications. Bars with different letters are significantly different from each other at p ≤ 0.05.
Figure 5. Effect of SCE treatment on chlorophyll content of Festuca arundinacea. Error bars represent standard deviations. Each data point represents the mean of at least six replications. Bars with different letters are significantly different from each other at p ≤ 0.05.
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Figure 6. Effect of SCE treatment on the O2− content of Festuca arundinacea. Error bars represent standard deviations. Each data point represents the mean of at least eight replications. Bars with different letters are significantly different from each other at p ≤ 0.05.
Figure 6. Effect of SCE treatment on the O2− content of Festuca arundinacea. Error bars represent standard deviations. Each data point represents the mean of at least eight replications. Bars with different letters are significantly different from each other at p ≤ 0.05.
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Figure 7. Effect of SCE treatment on H2O2 content of Festuca arundinacea. Error bars represent standard deviations. Each data point represents the mean of at least six replications. Bars with different letters are significantly different from each other at p ≤ 0.05.
Figure 7. Effect of SCE treatment on H2O2 content of Festuca arundinacea. Error bars represent standard deviations. Each data point represents the mean of at least six replications. Bars with different letters are significantly different from each other at p ≤ 0.05.
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Figure 8. Visual evaluation of the adverse effect of SCE treatment on H2O2 content of Festuca arundinacea.
Figure 8. Visual evaluation of the adverse effect of SCE treatment on H2O2 content of Festuca arundinacea.
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Figure 9. Effect of SCE treatment on the antioxidant content of Festuca arundinacea (A) SOD, (B) CAT, and (C) POD. Error bars represent standard deviations. Each data point represents the mean of at least six replications. Bars with different letters are significantly different from each other at p ≤ 0.05.
Figure 9. Effect of SCE treatment on the antioxidant content of Festuca arundinacea (A) SOD, (B) CAT, and (C) POD. Error bars represent standard deviations. Each data point represents the mean of at least six replications. Bars with different letters are significantly different from each other at p ≤ 0.05.
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Figure 10. Effect of SCE treatment on abscisic acid (ABA) and salicylic acid (SA) content of Festuca arundinacea. Error bars represent standard deviations. Each data point represents the mean of at least three replications. Bars with different letters are significantly different from each other at p ≤ 0.05.
Figure 10. Effect of SCE treatment on abscisic acid (ABA) and salicylic acid (SA) content of Festuca arundinacea. Error bars represent standard deviations. Each data point represents the mean of at least three replications. Bars with different letters are significantly different from each other at p ≤ 0.05.
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Figure 11. Molecular structure of Solanidan-3-ol, (3β,5α).
Figure 11. Molecular structure of Solanidan-3-ol, (3β,5α).
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Table
Table 1. Effect of seeding ratio of Solanum carolinense: Festuca arundinacea on plant growth-promoting traits of Festuca arundinacea.
Table 1. Effect of seeding ratio of Solanum carolinense: Festuca arundinacea on plant growth-promoting traits of Festuca arundinacea.
Control2:11:11:2
Germination rate (%)81.7 ± 1.67 a65 ± 0 b56.7 ± 3.33 c50 ± 2.89 c
Plant height (cm)27.2 ± 0.92 a18 ± 1.01 b16.4 ± 0.79 b15.6 ± 0.91 b
Root length (cm)15.3 ± 0.88 a8.6 ± 0.84 b8.3 ± 0.58 b10.2 ± 1.05 b
Fresh weight (mg)1236 ± 174 a110 ± 19.5 b84 ± 13.3 b57 ± 9.9 b
Dry weight (mg)120 ± 17.51 a14.8 ± 2.4 b9.5 ± 1.79 b9.1 ± 1.58 b
Each value represents the mean ± SD. Each data point represents the mean of at least six replicates. Different letters in the column after mean values represent the least significant differences at p ≤ 0.05. The ratio is indicated as Solanum Carolinense: Festuca arundinacea.
Table
Table 2. Effect of Solanum carolinense dominance on the growth of Festuca arundinacea at different time intervals.
Table 2. Effect of Solanum carolinense dominance on the growth of Festuca arundinacea at different time intervals.
Control20 DAS40 DAS60 DAS
Germination rate (%)80 ± 0 a61.7 ± 4.41 b60 ± 2.89 b60 ± 2.89 b
Plant height (cm)22.9 ± 0.88 a11.3 ± 0.48 b9.8 ± 0.53 b8.2 ± 0.39 b
Root length (cm)12.8 ± 0.54 a4.1 ± 0.34 b3.9 ± 0.37 b3.5 ± 0.44 b
Fresh weight (mg)586.2 ± 58.7 a55.1 ± 6.47 b39.8 ± 13.74 b17.9 ± 2.61 b
Dry weight (mg)77.2 ± 11.4 a5 ± 0.7 b4.3 ± 1.59 b2.8 ± 0.37 b
Each value represents the mean ± SD. Each data point represents the mean of at least six replicates. Different letters in the row after mean values represent the least significant differences at p ≤ 0.05.
Table
Table 3. Effect of SCE treatment on the growth of Festuca arundinacea.
Table 3. Effect of SCE treatment on the growth of Festuca arundinacea.
Concentration (ppm)Control25005000
Plant height (cm)32.8 ± 1.21 a24.7 ± 1.54 b18.6 ± 2.42 c
Fresh weight (g)1.5 ± 0.06 a1.2 ± 0.05 b0.9 ± 0.04 c
Dry weight (g)0.21 ± 0.005 a0.18 ± 0.006 b0.12 ± 0.005 c
Each value represents the mean ± SD. Each data point represents the mean of at least six replicates. Different letters in the row after mean values represent the least significant differences at p ≤ 0.05.
Table
Table 4. Main compounds of SCEs analyzed by GC/MS.
Table 4. Main compounds of SCEs analyzed by GC/MS.
NoName of the CompoundPeak Area (%)
1Solanidan-3-ol, (3β,5α)51.96
21H,7H-[1,3]Benzodioxino[6,5-g]
[1,3]benzodioxolo[5,6-a]quinolizine,
9,10,15b,16-tetrahydro-5,15-dimethoxy-, (S)		11.59
35,5-Dimethylimidazolidin-2,4-dione5.65
4solanidan-3-one5.64
5D-Allose4.02
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Kim, L.-R.; Adhikari, A.; Kang, Y.; Gam, H.-J.; Kang, S.-M.; Kim, K.-Y.; Lee, I.-J. Investigation of Solanum carolinense Dominance and Phytotoxic Effect in Festuca arundinacea with Special Reference to Allelochemical Identification, Analysis of Phytohormones and Antioxidant Mechanisms. Agronomy 2022, 12, 1954. https://doi.org/10.3390/agronomy12081954

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Kim L-R, Adhikari A, Kang Y, Gam H-J, Kang S-M, Kim K-Y, Lee I-J. Investigation of Solanum carolinense Dominance and Phytotoxic Effect in Festuca arundinacea with Special Reference to Allelochemical Identification, Analysis of Phytohormones and Antioxidant Mechanisms. Agronomy. 2022; 12(8):1954. https://doi.org/10.3390/agronomy12081954

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Kim, Lee-Rang, Arjun Adhikari, Yosep Kang, Ho-Jun Gam, Sang-Mo Kang, Ki-Yong Kim, and In-Jung Lee. 2022. "Investigation of Solanum carolinense Dominance and Phytotoxic Effect in Festuca arundinacea with Special Reference to Allelochemical Identification, Analysis of Phytohormones and Antioxidant Mechanisms" Agronomy 12, no. 8: 1954. https://doi.org/10.3390/agronomy12081954

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