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7 October 2022 Increasing bioactive compound levels in Agastache rugosa by hydrogen peroxide soaking in a hydroponic culture system
Vu Phong Lam, Vu Ky Anh, Dao Nhan Loi, Jong Seok Park
Author Affiliations +
Abstract

Hydrogen peroxide (H2O2) is a reactive oxygen species that can damage a variety of cellular structures. Recent studies have shown that H2O2 can mediate multiple physiological and biochemical processes by acting as a signaling molecule. This study was performed to explore the optimum H2O2 treatments for increasing the bioactive compounds in Agastache rugosa Fisch. & C.A. May plants with roots temporarily immersed in H2O2 concentrations of 0 (control), 4, 8, 16, 32, 64, and 128mmolL−1 in a hydroponic culture system. All cultivated plants were subjected to root soaking with diniconazole (120µmolL−1) at 7days after transplanting to restrict plant height. H2O2 concentrations of 4, 16, and 64mmolL−1 significantly reduced root length compared with no H2O2 treatment. Root fresh weight was significantly lower in response to exposure to 128mmolL−1 H2O2 compared with control plants. Although shoot and root dry weights were lower in plants exposed to 128mmolL−1 H2O2 compared with control plants, no significant differences were detected among treatments. Soaking roots in 16mmolL−1 H2O2 induced the highest rosmarinic acid (RA) content, and 16, 32, and 64mmolL−1 H2O2 significantly increased tilianin content in the whole plant compared with the control. The highest acacetin content was detected under 32mmolL−1 H2O2. In addition, root extract of A. rugosa had the highest RA concentration, and the tilianin concentration was the highest in flowers. Collectively, these results show that soaking roots in 16 and 32mmolL−1 H2O2 at 3.5weeks after transplanting promotes secondary metabolites of hydroponically grown A. rugosa.

1. Introduction

Korean mint (Agastache rugosa Fisch. & C.A. May), a medicinal herb belonging to the Lamiaceae family, is found in China, Vietnam, Korea, Japan, and Thailand (Zielinska and Matkowski 2014). Some studies have examined the importance of this plant for its antioxidative (Desta et al. 2016), antiallergic, anticancer (Zheng et al. 2013), anti-inflammatory (Lee et al. 2020), and antibacterial activities (Gong et al. 2017). Currently, the pharmaceutical industry uses plant-based sources to produce secondary metabolites or bioactive compounds (Atanasov et al. 2021). Agastache rugosa plants contain numerous bioactive compounds, including carotenoids, flavonoids, and triterpenes, as well as three crucial secondary metabolites, containing rosmarinic acid, tilianin, and acacetin (Tuan et al. 2012; Park et al. 2021). Agastache rugosa plants have a range of medicinal properties and are used as a traditional medication to cure different diseases, including nausea, anxiety, and bacterial infections (Park et al. 2016). Owing to the beneficial effects of diverse polyphenols on human health, the accumulation of polyphenols in A. rugosa through cultivation is of significant interest.

Hydrogen peroxide (H2O2) is created from molecular oxygen with a long half-life and high stability (Bienert et al. 2006). The control of the cellular production of H2O2 is physiologically essential because high cellular levels of H2O2 can induce cell damage and cell death (Park 2012). H2O2 is created in plants in response to both abiotic and biotic stresses and plays an important role in O2-derived cell toxicity. H2O2 acts as an adaptive signaling molecule, stimulating tolerance against different abiotic stresses (Cakmak and Marschner 1993; Almeida et al. 2005). Normally, abiotic stresses, including heat, salt, drought, and cold, increase the accumulation of reactive oxygen species (ROS) in the plant (You and Chan 2015). Lower concentrations of H2O2 (16 and 30mmolL−1) promote plant growth, mineral accumulation, and bioactive compound accumulation in Ficus deltoidea Jack plants (Nurnaeimah et al. 2020). The growth, quality, and yield of apple fruits were increased by treatment with 5 and 20mmolL−1 H2O2 (Khandaker et al. 2012).

Accumulation of bioactive compounds in plants by H2O2 has also been reported in amaranth leaves and seeds (Espinosa-Villarreal et al. 2017) and Vigna unguiculata L. (Walp) (Olowolaju 2019). The influence of H2O2 root soaking on plant growth and secondary metabolites in A. rugosa plants has not been explored previously. Therefore, H2O2 can be used to increase the bioactive compounds of A. rugosa plants. The objective of this study was to find the optimum H2O2 treatments to enhance the accumulation of bioactive compounds of A. rugosa.

2. Materials and methods

2.1. Seedling conditions

Seeds of A. rugosa were germinated and grown on rockwool cubes for four weeks in a controlled environment with the following growth conditions: average air temperature, 22±2°C; light intensity, 180µmolm−2s−1; average relative humidity, 65%±10%; and a 16h photoperiod using white fluorescent lamps (TL5 14 W/865 Philips, Amsterdam, Netherlands). Hoagland solution (pH 6.0 and EC 1.2 dSm−1) was supplied from 2weeks after sowing.

2.2. Treatments

Twenty-eight days after sowing, A. rugosa seedlings were individually transplanted and grown on a deep flow technique system (1.2×0.11×0.7m; L×H×W) in a plant factory. Plants were grown for 39days at an average temperature of 22.5°C, relative humidity of 60%±10%, and photosynthetic photo flux density (PPFD) of 220±10µmolm−2s−1 with a photoperiod of 14h. Each replicate had 18 plants. The plants were subjected to root soaking with diniconazole (120µmolL−1) at 7days after transplanting to induce dwarfing. Six H2O2 concentrations of 4, 8, 16, 32, 64, and 128mmolL−1 (control treatment without H2O2) were applied by soaking roots for 10min at 25days after transplantation.

2.3. Measurement of plant growth parameters

Thirty-nine days after transplantation, leaf width, leaf length, leaf number, fresh weights of roots and shoots, leaf area, dry weights (DWs) of roots and shoots, and the lengths of stem and root were quantified. Leaf length and width and the lengths of stem and root were quantified using a ruler. Fresh weight was quantified using an electronic scale (Si-234; Denver Instrument, Bohemia, NY, USA), and samples were then dried in an oven (HB-502 M, Hanback Sci, Suwon, Korea) at 70°C for 7days prior to measurement of DWs. Leaf area was measured using a leaf area meter (LI-3100 A; Li-Cor, Lincoln, NE, USA).

2.4. Relative chlorophyll value and chlorophyll fluorescence (Fv/Fm) value measurements

The relative chlorophyll value was expressed as the soil plant analysis development (SPAD) value and measured at 39days after transplantation by using a portable chlorophyll meter (502, Minolta Camera Co., Ltd., Japan). The measurement of variable-to-maximum fluorescence (Fv/Fm) was performed by a portable fluorometer (Fluorpen Pen FP 100, Photon System Instruments Ltd., Drasov, Czech Republic).

2.5. Leaf gas exchange parameters

Leaf gas exchange parameters, including net photosynthetic rate (Pn), transpiration rate (Tr), intercellular CO2 concentration (Ci), and stomatal conductance (gs), were determined at 39days after transplanting using a portable photosynthesis system (LICOR 6400, Licor. Inc. Nebraska, NE, USA). The measurement parameters were set as follows: 60% relative humidity, 1500µmolm−2s−1 PPFD, 500cm3s−1 air flow rate, 400µmolL−1 ambient CO2 concentration, and 25°C leaf temperature.

2.6. Acacetin, tilianin, and rosmarinic acid content and concentration

A total of 0.1g of powder of each plant organ (leaves, flowers, roots, and stems) was individually mixed with 1.5mL of 80% (v/v) MeOH to determine tilianin, rosmarinic acid (RA), and acacetin concentrations. The supernatant was collected by passing it through a 0.45µm filter followed by high-performance liquid chromatography analysis at 30°C using a C18 column (250×4.6mm, 5µm; RS tech, Daejeon, Korea). The entire process for extracting samples and analyzing these compounds in A. rugosa has been described in our previous study (Lam et al. 2020a, 2020b). Tilianin, RA, and acacetin (bioactive compounds) concentrations in each plant organ (root, flower, stem, and leaf) were expressed as the amount of bioactive compound per unit DW (mgg−1 DW). Total RA, acacetin, and tilianin concentrations in the entire plant (mgg−1 DW) were calculated as the sum of all plant organs. The RA, acacetin, and tilianin contents (mg/plant organs' DW) in each plant organ were calculated as the RA, acacetin, and tilianin concentrations in the stems, leaves, roots, and flowers (mgg−1 DW) multiplied by plant organs' DW (g). The RA, acacetin, and tilianin contents in the entire plant (mg/plant DW) were calculated by RA, acacetin, and tilianin concentrations (mgg−1 plant DW) multiplied by whole plant DW (g) (Liu et al. 2018; Lam et al. 2020b; El Mazlouzi et al. 2022).

2.7. Statistical analysis

Growth parameters and SPAD values were based on five plants (n=5) per replication, whereas three samples (n=3) per replication were used to determine the Fv/Fm value, leaf gas exchange parameters, and bioactive compounds. This experiment was performed in duplicate using a completely randomized design. All data were analyzed using SPSS software (version 20.0; IBM Corp., Armonk, NY, USA). The results of the experiment were subjected to a one-way analysis of variance (ANOVA) and Tukey's multiple range test. Mean values of H2O2-treated groups were compared by Tukey's multiple range test at a significance level ofp≤0.05.

3. Results

3.1. Plant growth parameters and chlorophyll content

Leaf width was not affected by H2O2, but leaf length was reduced in 8, 16, and 32mmolL−1 H2O2 treatments compared with those in the control group. Treatment with H2O2 did not significantly affect stem length. There was no significant difference in the number of leaves, leaf area, and shoot fresh weight among H2O2 treatments and the control, except in 64mmolL−1 H2O2 treatment, which induced the highest number of leaves, leaf area, and shoot fresh weight. There was no significant difference in root fresh weight among the H2O2 treatments and the control except in the 128mmolL−1 treatment, where root fresh weight was significantly lower for control plants. No significant differences in shoot and root DWs were observed between plants treated with H2O2 and control plants; however, concentrations at 128mmolL−1 H2O2 reduced shoot and root DWs compared with the control plants. Lower root lengths were recorded for plants treated with 4, 16, and 64mmolL−1 H2O2 compared with other treatments and the control (Fig.1; Table1). No significant differences in Fv/Fm and SPAD values between the H2O2 treatment groups and the control were detected (Fig. 2).

Fig. 1.

Images of A. rugosa plants grown at different hydrogen peroxide treatments (0, 4, 8, 16, 32, 64, and 128mmolL−1), subjected to root soaking.

cjps-2022-0088_f1.jpg

Fig. 2:

The SPAD value (A) and Fv/Fm value (B) of A. rugosa at different hydrogen peroxide treatments (0, 4, 8, 16, 32, 64, and 128mmolL−1), subjected to soaked root. The vertical bars show standard errors, SPAD value (n=5), and Fv/Fm value (n=3).

cjps-2022-0088_f2.jpg

Table 1.

The growth characteristics of A. rugosa at different hydrogen peroxide treatments (0, 4, 8, 16, 32, 64, and 128mmolL−1), subjected to soaked root, after 5.5weeks from transplanting.

cjps-2022-0088_tab1.gif

3.2. Leaf gas exchange parameters

There were no significant differences in the net photosynthesis rates and intercellular CO2 concentration among all treatments. However, the stomatal conductance of plants treated with 64 and 128mmolL−1 H2O2 was significantly lower than that for the control. The transpiration rate was significantly decreased as the H2O2 treatment increased at 128mmolL−1 compared with the control plants (Fig.3).

3.3. Acacetin, rosmarinic acid, and tilianin contents and concentrations

H2O2 significantly affected the concentration of RA, acacetin, and tilianin in the flowers, roots, stems, and leaves of A. rugosa (Table2). The RA concentrations in flowers, leaves, and roots were significantly higher in the H2O2-treated group than the control. The applications of 4 and 32mmolL−1 H2O2 significantly increased the RA concentration in stems by 1.13 and 1.09 times, respectively, compared with the control group. Tilianin concentrations in flowers treated with 32mmolL−1 and in stems with 16mmolL−1 were higher (1.52 and 2 times, respectively) than that for the control group. Tilianin concentrations in leaves treated with 64 and 128mmolL−1 H2O2 were approximately 2.94 and 3.32 times higher, respectively, than that in the control treatment, whereas tilianin concentration in the root decreased under all H2O2-treated groups. Within the H2O2-treated groups, acacetin concentration in flowers was the highest for the 32mmolL−1 treatment and was 1.36 times higher than that in the control. Acacetin was not found in the stems, roots, and leaves of A. rugosa plants (Table2).

Fig. 3.

Net photosynthetic rate (Pn) (A), stomatal conductance (gs) (B), intercellular CO2 concentration (Ci) (C), and transpiration rate (Tr) (D) of A. rugosa subjected to different H2O2 treatments (0, 4, 8, 16, 32, 64, and 128mmolL−1), subjected to soaked root. Different lowercase letters indicate significant differences in H2O2 treatments according to Tukey's multiple range test (P≤0.05; n=3).

cjps-2022-0088_f3.jpg

Table 2.

Rosmarinic acid (RA), tilianin, and acacetin concentrations in flowers, stems, leaves, and roots of A. rugosa at different hydrogen peroxide treatments (0, 4, 8, 16, 32, 64, and 128mmolL−1), subjected to soaked root, after 5.5weeks from transplanting.

cjps-2022-0088_tab2.gif

There were no statistically significant differences in RA content in flowers between H2O2-treated groups and the control (except for 128mmolL−1), and the RA content in flowers of the 128mmolL−1 H2O2-treated group was significantly lower than that in the control plants due to lower flower DW. The significantly highest RA content in stems was observed under the 8mmolL−1 treatment. The RA content in leaves of plants treated with H2O2 was significantly higher than that in the control group (except for the 128mmolL−1 H2O2 treatment because of the lower DW of leaves). The RA content in roots was the highest for the plants treated with 16mmolL−1 H2O2, being 1.61 times higher than the control (Table3).

Table 3.

Rosmarinic acid (RA), tilianin, and acacetin contents in flowers, stems, leaves, and roots of A. rugosa at different hydrogen peroxide treatments (0, 4, 8, 16, 32, 64, and 128mmolL−1), subjected to soaked root, after 5.5weeks from transplanting.

cjps-2022-0088_tab3.gif

Tilianin contents were highest in flowers of plants treated with 32mmolL−1 H2O2 and in stems treated with 16mmolL−1 H2O2 and was 1.41 and 2.64 times higher than those in the control, respectively. Tilianin contents in leaves treated with 64 and 128mmolL−1 H2O2 were 2.92 and 3.14 times higher than those of the untreated plant, respectively. However, roots exposed to 64 and 128mmolL−1 H2O2 exhibited significantly lower tilianin contents compared with control plants; however, there were no statistically significant differences between the control and the remaining H2O2-treated groups (4, 8, 16, and 32mmolL−1). Acacetin content in flowers of plants treated with 32mmolL−1 H2O2 was the highest compared with all other treatments and was 1.25 times higher than that of the control (Table3).

Different H2O2 concentration significantly changed the total RA, tilianin, and acacetin concentrations in the whole plant of A. rugosa. The concentrations of RA were significantly increased in all H2O2-treated groups compared with the no H2O2-treated group (Fig.4A). The concentration of tilianin was significantly increased when treated with 16, 32, 64, and 128mmolL−1 H2O2 compared with untreated plants (Fig.4B), while the concentration of acacetin was the highest in the 32mmolL−1 H2O2 treatment (Fig.4C). However, the RA content was higher (1.51 times) in the 16mmolL−1 H2O2 treatment than the control (Fig.4D). Tilianin contents of the plants treated with 16, 32, 64, and 128mmolL−1 H2O2 were significantly higher than the control (Fig.4E). Acacetin content was the highest in the 32mmolL−1 H2O2-treated group among all treatments (Fig.4F).

Fig. 4.

Rosmarinic acid (RA) concentration (A) and content (D), tilianin concentration (B) and content (E), and acacetin concentration (C) and content (F) in the whole plant of A. rugosa at different hydrogen peroxide treatments (0, 4, 8, 16, 32, 64, and 128mmolL−1), subjected to soaked root after 5.5weeks from transplanting. Different lowercase letters indicate significant differences in H2O2 treatments according to Tukey's multiple range test (P≤0.05; n=3).

cjps-2022-0088_f4.jpg

4. Discussion

4.1. Plant growth and chlorophyll content

Some reports have shown that H2O2 is an important signaling molecule involved in plant responses to abiotic stresses, including salinity (Sathiyaraj et al. 2014), drought (Hameed and Iqbal 2014), low temperature (Orabi et al. 2015), and high temperature (Wang et al. 2014). Some studies have indicated that H2O2 levels affect the growth of various crops, including Vigna unguiculata (L.) Walp. (Hasan et al. 2016), canola (Orabi et al. 2018), and F. deltoidea (Nurnaeimah et al. 2020). In contrast, our results demonstrated no significant differences in stem length, number of leaves, leaf area, shoot fresh weight, and leaf width between the H2O2-treated groups and the control. Our results are conflicting with Nurnaeimah et al. (2020), who demonstrated that the height of F. deltoidea significantly increased in response to H2O2 treatment; this may be attributed to the different plant species, treatment times, H2O2 doses, and treatment methods used in these two studies.

We soaked A. rugosa roots in H2O2 solutions at 3.5weeks after transplanting, and the highest H2O2 concentration of 128mmolL−1 limited plant growth by reducing root fresh weight and shoot and root DW. Increasing H2O2 concentration restricts water absorption by roots and causes water stress, which leads to multiple physiological and biological responses (Silva et al. 2015). According to some reports, low H2O2 concentrations can significantly increase plant growth (Hasan et al. 2016; Nurnaeimah et al. 2020). However, high H2O2 concentrations damaged cells and photosynthesis (Park 2012; Nazir et al. 2019, 2021). H2O2 is an important signaling molecule controlling plant growth and development by coordinating Ca2+ and NO signaling pathways (Niu and Liao 2016). In the present study, H2O2 treatment did not have a significant effect on SPAD and Fv/Fm values compared with control plants, probably because H2O2 protects chloroplast ultrastructure to conserve photosynthetic pigments. The effects of H2O2 on chlorophyll were likely due to the interaction among abscisic acid, nitric oxide, and hydrogen peroxide (Neill 2007). We treated the plants with H2O2 at 3.5weeks after transplant and 2.5weeks before harvest, and H2O2 did not affect the chlorophyll content of A. rugosa.

4.2. Leaf gas exchange parameters

No significant differences in net photosynthetic rate were observed between the H2O2-treated groups and the control treatment. In contrast, H2O2 treatment increased the net photosynthetic rate in F. deltoidea (Nurnaeimah et al. 2020; Ralmi et al. 2021) and V. unguiculata (Hasan et al. 2016). Drought tolerance in soybean increased under H2O2 treatment by maintaining the water content of leaves (Guler and Pehlivan 2016). H2O2 is an important regulator of a wide range of biochemical and physiological processes, including plant development and growth, photosynthesis, photorespiration, the cell cycle, stomatal movement, senescence, and stress tolerance (Niu and Liao 2016; Nurnaeimah et al. 2020). In the present study, stomatal conductance, transpiration rate, and intercellular CO2 concentration were decreased by treatment with 128mmolL−1 H2O2 compared with other treatments. Exogenous H2O2 increases the activities of plant cells and antioxidant enzymes. The ROS cause cells to lose their function and harm the cell membrane (Zhang et al. 2011). Therefore, stomatal conductance and transpiration rate were reduced under high H2O2 concentrations.

4.3. Rosmarinic acid, tilianin, acacetin concentrations and contents

Soaking roots in diluted H2O2 solutions significantly increased the RA concentration in A. rugosa compared with the control treatment. Similarly, tilianin concentrations were significantly higher in the high-H2O2-treated groups (16, 32, 64, and 128mmolL−1) than in the control group. The acacetin concentration was highest in the 32mmolL−1 H2O2 treatment (Fig.4). Exposure to H2O2 increases the levels of secondary metabolites in plants, including V. unguiculata (Olowolaju 2019) and F. deltoidea (Nurnaeimah et al. 2020). H2O2 improves antioxidant status by enhancing the expression of specific genes, including those for stilbene synthase, chalcone synthase, and lyase (Nyathi and Baker 2006; Marinho et al. 2014). Stress tolerance was based on H2O2 dose application. Moderate H2O2 doses increased the antioxidant activity and caused increased stress tolerance, while higher H2O2 concentrations induce oxidative stress and hypersensitivity response symptoms (Nurnaeimah et al. 2020). Antioxidant activity increased after treatment with H2O2, probably because H2O2 is a highly reactive molecule, and its degradation can be controlled by the integrated antioxidant system (Veal et al. 2007; Bae et al. 2016). Treatment with H2O2 increases antioxidant activities in cucumber leaves (Zhang et al. 2011). Commonly, excessive H2O2 generation causes cells to lose function and harms the cell membrane; thus, to counter the damaging H2O2 effects, plants create non-enzymatic antioxidants and possess antioxidant enzymes (Das and Roychoudhury 2014). Antioxidant enzyme activities in turfgrass were increased by treatment with H2O2, probably due to H2O2 properties as it can control their degradation and is a highly reactive molecule through the integrated antioxidant system (Bae et al. 2016). H2O2 causes oxidative stress by disrupting cellular ROS homeostasis, which induces an ROS-dependent signaling network and causes the accumulation of latent defense proteins, such as transcription factors and ROS-scavenging enzymes (Hossain et al. 2015). H2O2 is a signal molecule in phenolic synthesis, and plants possess specific antioxidative defense enzymes, including polyphenol oxidase and peroxidase to limit ROS increase under different environmental stress conditions (Niu and Liao 2016; Nazir et al. 2020). Therefore, ROS were accumulated and secondary metabolites were produced under high-H2O2 conditions. Previous studies are consistent with the results of our study, in which tilianin concentrations and contents increased under high-H2O2-treated groups. The RA concentrations significantly increased under all H2O2-treated groups relative to the control and RA content significantly increased in all H2O2-treated groups, with the exception of the 128mmolL−1 treatment, because it depended on plant DWs. The plants treated with 32mmolL−1 H2O2 showed 34.31% higher acacetin content compared with untreated plants. Tilianin and RA differed among the various plant organs, with roots showing the highest accumulation of RA, and flowers exhibited the highest tilianin accumulation. The present study demonstrated that plant organs of A. rugosa contain significant amounts of bioactive compounds and therefore it can be used as a raw material for functional foods and herbal medicines.

5. Conclusion

We demonstrated that root soaking in H2O2 concentrations of 16 and 32mmolL−1 increased bioactive compound contents. The RA, acacetin, and tilianin concentrations in each plant organ (root, flower, stem, and leaf) were determined, which will assist further investigations of the quality of each organ. Future studies are necessary to explore the optimum exposure times for increasing secondary metabolite accumulation in A. rugosa.

Author contributions

Vu Phong Lam: data curation, formal analysis, investigation, methodology, software, writing – original draft, writing – review & editing; Vu Ky Anh: data curation, formal analysis, investigation, methodology, writing – original draft; Dao Nhan Loi: data curation, investigation, methodology, writing – original draft; Jong Seok Park: conceptualization, funding acquisition, methodology, project administration, writing – original draft, writing – review & editing.

Funding information

This work was supported by the Korea Institute of Planning and Evaluation for Technology in Food, Agriculture ,and Forestry (IPET) and the Korea Smart Farm R&D Foundation (KosFarm) through the Smart Farm Innovation Technology Development Program, funded by the Ministry of Agriculture, Food, and Rural Affairs (MAFRA), the Ministry of Science and ICT (MSIT), and the Rural Development Administration (RDA) (421034-04).

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© 2022 The Author(s).
Vu Phong Lam, Vu Ky Anh, Dao Nhan Loi, and Jong Seok Park "Increasing bioactive compound levels in Agastache rugosa by hydrogen peroxide soaking in a hydroponic culture system," Canadian Journal of Plant Science 103(1), 39-47, (7 October 2022). https://doi.org/10.1139/cjps-2022-0088
Received: 28 April 2022; Accepted: 9 September 2022; Published: 7 October 2022
KEYWORDS
diniconazole
hydrogen peroxide
hydroponic
rosmarinic acid
tilianin
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