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Article

Glycine Betaine Induces Tolerance to Oxidative Stress in Cherry Radishes under High-Temperature Conditions

by
Zexi Zhang
,
Chunhua Jia
*,
Yuezhuo Zhuang
,
Min Zhang
and
Baocheng Chen
College of Resources and Environment, Shandong Agricultural University, Tai’an 271018, China
*
Author to whom correspondence should be addressed.
Agronomy 2024, 14(6), 1294; https://doi.org/10.3390/agronomy14061294
Submission received: 11 May 2024 / Revised: 8 June 2024 / Accepted: 13 June 2024 / Published: 14 June 2024
(This article belongs to the Section Horticultural and Floricultural Crops)
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Abstract

:
Cool-season plant growth and development are impacted by high temperatures. As a biostimulant, glycine betaine is responsible for inducing tolerance to both biotic and abiotic stressors. However, the mechanism by which glycine betaine protects cool-season crops against high-temperature stress is not clear. In the present study, under the conditions of high temperatures (35 °C/30 °C day/night), cherry radishes (Raphanus sativus var. radicula Pers.) (Brassicaceae) were cultured for 9, 18, and 27 days, and different concentrations (0, 0.067, 8.79, 11.72, 14.65, and 17.58 mg L−1) of glycine betaine were applied to investigate the influence of glycine betaine on cherry radish biomass, quality, net photosynthetic rate, chlorophyll content, antioxidant enzyme activity, and endogenous hormone content under high-temperature stress. The results showed that, under high-temperature conditions, cherry radishes grew best with the 17.58 mg L−1 glycine betaine treatment. At day 27, comparing the 17.58 mg L−1 glycine betaine treatment with 0 mg L−1 glycine betaine under high-temperature stress, the cherry radish biomass increased by 44.7%, while the soluble protein and vitamin C content increased by 14.4% and 21.6%, respectively, the net photosynthetic rate and chlorophyll a content increased by 7.8% and 44.1%, respectively, and the peroxidase and catalase levels increased by 81.0% and 146.3%, respectively. On day 9, the auxin, abscisic acid, and glycine betaine contents significantly increased by 67.4%, 6.8%, and 32.9%, respectively, in comparing the 17.58 mg L−1 glycine betaine treatment with 0 mg L−1 glycine betaine under high-temperature stress. Therefore, the application of 17.58 mg L−1 betaine to cherry radishes grown under high-temperature stress had positive effects. The appropriate concentration of glycine betaine can improve the resistance of cherry radish to high temperatures and maintain yield.

1. Introduction

Plants are very sensitive to temperature changes, and temperature plays a crucial role in plant growth and development. Due to global warming, extreme climates, high temperatures, and droughts are increasing [1]. High-temperature stress affects the growth and development of plants and impairs the integrity of the cell membrane. Under these conditions, plants produce a large amount of superoxide anions and reactive oxygen species (ROS) [2]. When the ROS content is too high, they destroy the macromolecular structure of cells, causing membrane lipid peroxidation [3,4] and leading to metabolic disorders and weakened photosynthesis, which greatly reduce crop yield and quality [5]. Studies carried out by Wang et al. [6] showed that high-temperature stress induces programmed cell death in maize seedling leaves. González-Schain et al. [7] showed that high-temperature stress affects transcriptome changes during flowering in rice. Dutta et al. [8] also showed that high-temperature stress leads to impairment of chlorophyll biosynthesis in plastids, thus reducing the rate of photosynthesis. A study by Zhao et al. [9] showed that the superoxide dismutase activity of pineapples decreased significantly under short-term high-temperature stress. High-temperature stress, due to the physiological damage it causes to plants, has emerged as a major challenge to global crop yields.
Glycine betaine (GB) is a quaternary amine-type water-soluble alkaloid. GB plays a key role in regulating plant responses to environmental stresses such as heat and drought [10,11,12], cold [13], salt stress, and strong light [14,15]. Most plants accumulate a large amount of GB under stress, since it not only maintains cell swelling pressure as a non-toxic osmotic regulator, but also stabilizes enzymes and the cell membrane structure and scavenges free radicals [16]. In addition, it can maintain a higher photosynthesis rate. Numerous studies have shown that under stress conditions, spraying GB on leaves, applying GB to roots, or soaking seeds with a GB solution can increase the resistance of plants to stress. A study by Yang et al. [17] indicated that exogenous GB can alleviate the damage to tobacco grown under high-temperature stress. It may enhance heat resistance by inhibiting the accumulation of ROS or by enhancing the repair of Photosystem II (PSII), which is inactivated by light stress. A study by Wang et al. [18] showed that the accumulation of GB increased the high-temperature tolerance and drought resistance of chloroplasts in wheat leaves. Moreover, Park et al. [19] indicated that the chilling tolerance of tomatoes could be increased via the exogenous application of GB.
The cherry radish (Raphanus sativus var. radicula Pers.) (Brassicaceae) is an annual cold-season vegetable with a rapid germination period and a growth cycle spanning 25 to 40 days. Notably, the cherry radish boasts a rich nutritional profile, economic benefits, and ease of cultivation [20]. These attributes have contributed to its widespread cultivation in northern China, where it serves as a significant cash crop for greenhouse farming. High temperatures can reduce the activity of antioxidant enzymes and the chlorophyll content of cherry radishes [21], resulting in decreased production in large-area planting. Existing studies have focused on the effects of GB on salt tolerance [22], drought resistance [23], and cold resistance [13] in chenopodium and gramineae. A study by Oukarroum et al. indicated that the exogenous application of proline and glycine betaine increased the connectivity between the antennae of Photosystem II by playing a protective role against the oxygen evolving complex, and the exogenous application of proline and glycine betaine improved the tolerance of barley leaves to 45 °C heat stress [24]. Sorwong et al. indicated that the application of GB at 0.5 mM and 1 mM to all marigold cultivars effectively increased gs and ROS scavenging and protected the photosynthetic machinery, thus alleviating the negative effects of heat stress [25]. However, there are few studies on GB improving the heat resistance of crops, especially cherry radishes, under the conditions of greenhouse planting with poor ventilation and large diurnal temperature variations. In this study, we investigated the appropriate concentration and mechanism of GB to improve the high-temperature tolerance of cherry radishes. The effects of different concentrations of exogenous GB on the antioxidant enzyme activity, photosynthetic system, and endogenous hormone levels of cherry radishes under intermittent high-temperature stress were studied to analyze the optimum concentration of GB and explore the physiological and biochemical mechanisms of GB related to improving the tolerance of cherry radishes to high temperatures. When planting cherry radishes in greenhouses, applying the proper concentration of glycine betaine could effectively improve the resistance of the cherry radishes, alleviate the influence of high-temperature stress, and ensure the yield and quality of the cherry radish crop.

2. Materials and Methods

2.1. Experimental Design

GB was supplied by Sunwin Biotech Shandong Co., Ltd. (Weifang, China). Cherry radish seeds were obtained from BEJO China (Shanghai, China), after being produced in 2023 with a 1000-grain weight of 1.2 g. We sowed three seeds at 0.3 cm depth in each nursery box (10 cm length, 8 cm width, and 7 cm height). The three seeds in the same box corresponded to the three different sampling times for the same treatment. A total of 63 seeds were planted. After about 5 days, the seeds germinated. The nursery boxes were placed in an artificial climate incubator (50–60% relative humidity, 25 °C/20 °C day/night temperature), with a 16/8 h photoperiod and light intensity of 15,000 lx [26]. During the 27-day growth period [20], the seedlings were subjected to six GB concentrations: 0 (GB0.00), 0.067 (GB0.07), 8.79 (GB8.79), 11.72 (GB11.7), 14.65 (GB14.7), and 17.58 mg L−1 (GB17.6) and 35 °C/30 °C (day/night) as a high-temperature stress environment [18]. For the control group (CK), the plants were grown at a normal temperature (25 °C/20 °C). Each treatment was repeated three times. The GB solution (10 mL) diluted with 40 mL Hoagland’s solution (Shanghai Xinfan Biotechnology Co., Ltd., Shanghai, China) per pot was applied as substrate irrigation at 7, 16, and 25 days after germination [26]. Hoagland’s solution was applied to the roots of the plants to promote plant growth and enhance the diffusion of GB through the roots. After each sample was treated, the samples were exposed to high-temperature stress. Tissue samples were collected at 9, 18, and 27 days (2 days after the application of GB). On day 9, the antioxidant enzyme activity, malondialdehyde (MDA) content, endogenous hormone levels, GB content, and proline content were measured. On day 18, the net photosynthetic rate, chlorophyll content, biomass, fruit quality, antioxidant enzyme activity, MDA content, endogenous hormone level, GB content, and proline content were measured. On day 27, the net photosynthetic rate, chlorophyll content, biomass, fruit quality, antioxidant enzyme activity, MDA content, endogenous hormone levels, GB content, and proline content were measured, and ultra-structures of the chloroplasts and thylakoids of the cherry radishes treated with different treatments were prepared.

2.2. Assay of the Photosystem and Chlorophyll Content of Leaves

The net photosynthetic rate (Pn) was measured with a LI-COR 6400 portable photosynthetic analyzer (LI-COR Inc., Lincoln, LI-6400, NE, USA), following the user manual instructions. The photosynthetically active radiation (PAR) intensity was set to 1000 μmol·m−2·s−1, and the reference CO2 concentration was 350 μmol·mol−1 [27]. The chlorophyll level was measured using Knudson methods [28]. Fresh leaf tissue (0.5 g) was extracted in the dark with 2 mL of 95% (v/v) ethanol for 24 h, and the concentrations of chlorophyll a, b, and carotenoid in the extract were determined using a spectrophotometer (SHIMADZU UV-2450, Kyoto, Japan). The absorbance was measured at 665, 649, and 470 nm [21]. The preparation and observation of the chloroplast ultra-structure were carried out according to Xu et al. [29]. The ultra-structure of the chloroplasts was observed by cutting 1 mm2 patches near the main vein at the halfway position between the leaf base and the leaf tip. In preparation for transmission electron microscopy, the leaves were impregnated in 0.1 M phosphate buffer (pH 7.4) for 2 h, and then impregnated with 1% citric acid in the same buffer for 5 h. The ultrathin sections were cut and continuously stained with uranyl acetate in pure ethanol and citrate for 15 min. The sections were observed under a HITACHI transmission electron microscope (Carl Zeiss, Gottingen, Germany) at an accelerating voltage of 80 kV [26].

2.3. Measurement of Oxidative Stress Indicators: Antioxidant Enzyme Activities and Malondialdehyde Content

The MDA content was assessed by grinding fresh leaf tissue in 0.1% trichloroacetic acid (TCA) and then centrifuging the homogenate at 10,000× g for 5 min. The resulting supernatant (1 mL) was combined with 4 mL of thiobarbituric acid (5% TBA prepared in 20% TCA) and heated to boiling point at 100 °C for 30 min. After cooling, the samples were centrifuged at 10,000× g for 10 min, and the resulting supernatant was measured at wavelengths of 532 nm and 600 nm using a Beckman spectrophotometer (model: 640 D, Beckman Coulter, Inc., Indianapolis, IN, USA), as described by Madhava Rao and Sresty in 2000 [30]. An extinction coefficient of 155 mM−1 cm−1 was used for calculations.
To extract the enzyme, 0.5 g of fresh leaf tissue was mixed with ice-cold potassium phosphate buffer (100 mM, pH 7.0) containing PVP (1%) using a pre-chilled mortar and pestle. After centrifugation at 12,000× g for 15 min at 4 °C, the resulting supernatant was used as the enzyme source in the assays described below [31].
The activity of superoxide dismutase (SOD, EC1.15.1.1) was assessed by measuring the enzyme extract’s ability to inhibit the photochemical reduction of nitroblue tetrazolium (NBT). A mixture containing 100 mM phosphate buffer (pH 7.4), 10 mM methionine, 1.0 mM EDTA, 50 μM riboflavin, 75 μM NBT, and 100 μL of enzyme extract was incubated for 15 min under fluorescent lights. The optical density was measured at a wavelength of 560 nm using a Beckman 640 D spectrophotometer (Beckman Coulter, Inc., Indianapolis, IN, USA), and the activity was reported as U mg−1 protein [32].
The activity of catalase (CAT, EC1.11.1.6) was measured by observing the breakdown of hydrogen peroxide (H2O2) at a wavelength of 240 nm using a Beckman 640 D spectrophotometer from the USA for a duration of 2 min. The reaction mixture consisted of 50 mM phosphate buffer (pH 6.0), 0.1 mM EDTA, 20 mM H2O2, and 100 μL of enzyme extract in a final volume of 2 mL. The CAT activity was quantified as U mg−1 protein [33].

2.4. Endogenous Hormone, Glycine Betaine, and Proline Content Determination

To assess the fruit quality, ascorbate peroxidase (APX) activity, glutathione reductase (GR) activity, auxin (IAA) content, abscisic acid (ABA) content, GB content, and proline (Pro) content, 1 g of plant leaf samples was ground in liquid nitrogen and then transferred to 5 mL of extraction mixture (acetone:methanol:water = 89:10:1). The mixture was extensively homogenized on ice, and the homogenate was centrifuged at 4500× g for 5 min at 4 °C. Then, the supernatant was transferred to a new centrifuge tube containing 0.5 mL of 1% trichloric acid for protein precipitation. After centrifugation at 12,000× g for 10 min at 4 °C, the ELISA kit from Shanghai HengYuan Biological Technology Co., Ltd. (Shanghai, China) was used for measurement, as described by Shi et al. [34,35].

2.5. Statistical Analyses

The test data were analyzed using IBM SPSS Statistics 19 (Armonk, NY, USA), utilizing variance (ANOVAs) and Duncan’s test (p < 0.05). We used Microsoft Excel 2016 for data processing operations and Microsoft Excel 2016 (Redmond, WA, USA) and SigmaPlot 12.5 (San Jose, CA, USA) to draw the figures. The statistical analysis was based on a 95% confidence interval.

3. Results

3.1. The Impact of Glycine Betaine on the Net Photosynthetic Rate and Chlorophyll Content of Cherry Radishes

Under high-temperature stress, the Pn of the cherry radishes was greatly affected in the early growth stage, and the addition of different concentrations of GB alleviated this effect. At 27 days, the GB11.7 increased the Pn of the cherry radishes compared with GB0.00, and the GB17.6 treatment significantly increased the concentration by 7.8% (Figure 1a).
The addition of a high concentration of GB increased the contents of chlorophyll a, chlorophyll b, and carotenoid, as compared with GB0.00. At 27 days, the above indicators of the GB17.6 treatment were significantly increased compared with GB0.00 by 44.1%, 34.5%, and 38.6% (Figure 1b), respectively. The chlorophyll a, chlorophyll b, and carotenoid contents under the high-GB-concentration treatment significantly improved compared with that under the normal-temperature condition without stress.
Chloroplasts are an electron-specific organelle and a major source of ROS, and they are especially susceptible to oxidative stress [36]. Under high-temperature stress, the cell membrane is degraded, chloroplasts swell, and osmiophilic bodies accumulate (Figure 2B,E). Under high concentrations of GB, the chloroplast granum lamellae were blurred and the osmiophilic bodies were reduced (Figure 2C,F).

3.2. The Impact of Glycine Betaine on Cherry Radish Biomass and Fruit Quality

By comparing the experimental group with the control group (CK), the analysis showed that the growth of cherry radish plants was seriously affected by high-temperature stress. However, compared with GB0.00, the growth inhibition induced by high-temperature stress was mitigated by the 17.58 mg L−1 GB treatment on day 27. Compared with the GB0.00 treatment, the biomass (fresh weight of the whole radish) increased by 44.7% under the GB17.6 treatment (Figure 3).
At day 27, by comparing the results of the GB17.6 treatment with those of GB0.00 (Table 1), we found that the soluble protein and vitamin C (Vc) contents of the GB17.6 treatment were significantly higher by 14.4% and 21.6%, respectively. Compared with the control group (CK), both indexes in the GB17.6 treatment were significantly improved. The results showed that GB improved the plant growth and the quality of cherry radishes. There appears to be an optimal concentration range for GB.

3.3. The Impact of Glycine Betaine on Cherry Radish Antioxidant Activity

Oxidative stress in cherry radishes is caused by high-temperature stress. We examined the activity and action of antioxidant enzymes in cherry radishes. The results show that on the 27th day, under the influence of high-temperature stress, the activities of SOD, POD, and CAT of the cherry radishes significantly decreased (Table 2) [26]. However, the activities of these enzymes could be significantly improved by applying an appropriate concentration of GB in a high-temperature growing environment. Compared with GB0.00, the SOD, POD, and CAT activities of cherry radish leaves increased by 32.1%, 81.0%, and 146.3%, respectively, after 27 days of high-temperature exposure. Under high-temperature stress, the application of GB17.6 was able to reduce MDA accumulation in the leaves during plant growth (Table 2). On day 9, the APX and GR activities of the cherry radish leaves were affected by high-temperature stress. The activity levels were significantly reduced; however, this inhibition was alleviated by an appropriate concentration of GB (Table 2). For example, when treated with GB17.6, as compared to GB0.00, the activities of APX and GR increased by 17.8% and 55.6%, respectively.

3.4. The Impact of Glycine Betaine on Cherry Radish Endogenous Hormones, Glycine Betaine, and the Proline Content

High-temperature stress has a significant impact on cherry radish seedling growth. After 9 days, the IAA content was significantly decreased under high-temperature stress, which inhibited crop growth. Compared with GB0.00 after 9 days, GB17.6 significantly increased the IAA content, ABA content, and GB content of the cherry radish seedlings by 67.4%, 6.8%, and 32.9% (Figure 4a–c), respectively. The results show that a high concentration of GB could alleviate the effect of high-temperature stress on the seedlings. After 9 days, GB17.6 also enhanced the proline content, which was significantly higher than the GB0.00 proline content by 12.2% (Figure 4d).

4. Discussion

The cherry radish is a cold-season crop that is sensitive to temperature, especially high-temperature stress. GB is an N,N,N-trimethylglycine quaternary ammonium compound that is naturally produced in numerous living organisms, including plants [37]. In the present study, we showed that GB, as an organic solute commonly referred to as an osmotic protectant, had positive impacts on the response of cherry radishes to high-temperature stress, such that the effects of high-temperature stress on the plants were reduced. The application of appropriate concentrations of GB before the onset of high-temperature stress can increase the activity of antioxidant enzymes (Table 2), the net photosynthetic rate (Figure 1a), the chlorophyll content (Figure 1b), and the endogenous hormone content (Figure 4a–c), thereby increasing biomass accumulation (Figure 3). Khalid et al. found similar results [38]. Therefore, by controlling the different stress resistance indicators of each system, the osmotic adjustment process was improved, enabling the maintenance of normal or superior growth in high-temperature environments.
Cherry radishes can reduce the effects of high-temperature stress by increasing the activity of antioxidant enzymes, chlorophyll, or endogenous hormones, thereby increasing their biomass [26]. Li et al. [39] indicated that adding GB could increase the fresh weight and plant height of tomatoes grown under high-temperature stress, and they confirmed that GB can improve plant heat tolerance. In this study, high-temperature stress significantly inhibited the growth of cherry radishes. The tolerance of the cherry radishes to high-temperature stress could be improved by adding an appropriate concentration of GB, and its growth-promoting effect on the cherry radishes showed a gradual upward trend. Malekzadeh also showed the same trend in a study on GB’s ability to alleviate salt stress in soybeans [40]. The optimum concentration of GB is different for different crops; the growth promotion and stress resistance of GB depend largely on its concentration. In this study, with an increasing concentration of GB, the growth and stress resistance of cherry radishes exhibited a notable improvement. However, whether the highest GB concentration in this experiment is the most suitable concentration for cherry radishes under high-temperature stress needs to be further verified.
Higher plants usually have reduced photosynthetic activity when subjected to abiotic stress [41,42], which may be due to or lead to photoinhibition. The application of GB was observed to reduce the damage to PSII in flag leaves of wheat under high-temperature stress [43]. Our results showed that the net photosynthetic rate in cherry radish leaves at 18 days was significantly decreased by the influence of high-temperature stress (Figure 1a). The Pn increased with increasing GB at the seedling stage and later growth stage of cherry radishes, and a high concentration of GB increased the Pn more significantly at the later growth stage.
The chlorophyll content of plants decreases under high-temperature stress. In this study, the content of chlorophyll decreased or no significant change was observed under a low concentration of exogenous GB, while the contents of chlorophyll a, b, and carotenoid were significantly promoted by adding a high concentration of GB (17.58 mg L−1), which indicated that a suitable concentration for growth promotion and stress resistance should be selected for different crops. A high concentration of GB can result in a blurred appearance of the chloroplast granum lamella and reduce the osmotropic bodies (Figure 2C,F). These results indicate that the addition of high concentrations of GB could alleviate the damage to chloroplasts and thylakoids caused by high-temperature stress to some extent. In this study, a high concentration of GB significantly increased the chlorophyll content under high-temperature stress (Figure 1b) by reducing the damage caused by high-temperature stress at the cellular level.
Suboptimal temperatures can cause plants to produce excessive amounts of reactive oxygen species, which can lead to oxidative damage. Plants have evolved many mechanisms to avoid reactive oxygen species reaching toxic levels [44]. Enhanced antioxidant metabolism benefits plants exposed to acute oxidative stress [45]. Higher plants have antioxidant enzymes, including SOD, POD, CAT, and APX, which can clear ROS. Chen et al. indicated that the exogenous application of GB and enhanced accumulation of GB through transgenic methods can enhance ROS clearance [46]. Since GB does not directly remove ROS, it must regulate the process by activating or stabilizing ROS-scavenging enzymes or inhibiting ROS production through an unknown mechanism [14]. In this study, the SOD, POD, and CAT activities of plants treated with 17.58 g/L−1 glycine betaine increased compared with those of plants subjected to GB0.00 (Table 2). This led to increased biomass (Figure 3) due to improved high-temperature stress tolerance in the cherry radishes. Hence, the decrease in oxidants and the elevation of antioxidant enzyme production in GB-pretreated seedlings were involved in the increase in plant high-temperature tolerance. This finding is consistent with the results of Yang et al. [17].
With the growth of the crop, the crop itself will produce a certain degree of resistance, and no more GR will be required. Therefore, the GR content is relatively high in the early growth stage of cherry radishes and shows a decreasing trend in the middle and late growth stages [26]. Adding the proper concentration of GB at the seedling stage can promote GR production and improve seedling resistance to high-temperature stress. At high concentrations of GB, APX was significantly higher than that in GB0.00 for cherry radishes in the early seedlings stage and in the later stage, but lower than that in GB0.00 in the middle stage. A possible reason was that the stress resistance at the seedling stage was weak and more APX was needed to resist high-temperature stress, while APX was produced less in the middle growth stage with the improvement in the plant’s stress resistance. At the later stage, the fruit formation of the cherry radishes and the increase in APX promoted an increase in the ascorbic acid content and improved the quality of the fruit. MDA is a key index to determine the level of membrane lipid peroxidation, which indicates that the addition of an appropriate concentration of GB can enhance the antioxidant system of plants, thereby supporting them to resist high-temperature stress by clearing reactive oxygen species.
Phytohormones play an important role in regulating plant growth under biological and abiotic stress [47]. Studies have shown that the tolerance of IAA [48] and ABA [49] to stress is related to morphological adaptation, which is significantly regulated by specific hormones. In addition, it has been reported that osmoprotectants such as GB [50] and proline increase in response to thermal stress [51]. These molecules are widely believed to have a variety of roles, such as stress signaling, protecting enzymes from denaturation, membrane stabilization, and maintaining osmotic homeostasis to keep stressed cells from expanding. In this study, due to the influence of high-temperature stress, the content of IAA in cherry radish seedlings was inhibited, resulting in abnormal plant growth. Adding an appropriate concentration of GB could significantly promote IAA synthesis and plant growth at the seedling stage. High-temperature stress can lead to increased ABA production in crops. The addition of a suitable concentration of exogenous GB can increase the ABA content in the seedling stage and, consequently, increase resistance to high-temperature injury. Plants exhibit strong stress resistance in later growth stages, and a reduction in the ABA content could prevent a premature decline in crops. As osmotic regulators, GB and proline can regulate the osmotic pressure to maintain cell homeostasis in crop cells. The resistance of cherry radishes in the seedling stage is weak. Adding an appropriate concentration of exogenous GB can promote the accumulation of endogenous GB and improve the stress resistance of crops during the seedling stage. Furthermore, cherry radishes produce more proline to resist high-temperature stress, and the addition of exogenous GB could promote the production of proline, especially at the seedling stage. Gupta et al. obtained similar findings in wheat [52]. The above results indicate that GB can improve the stress resistance of cherry radishes as a result of the interaction of various endogenous hormones.

5. Conclusions

This study showed that an ambient temperature of 35 °C/30 °C (day/night) impacted the growth of cherry radishes due to high-temperature stress, but adding an appropriate concentration of GB improved the heat resistance of the cherry radishes. The optimal concentration in this study was found to be 17.58 mg L−1. Comparing a concentration of 17.58 mg L−1 with GB0.00 at 27 days, the biomass was significantly increased by 44.7%; the soluble protein and vitamin C contents increased by 14.4% and 21.6%, respectively; and the net photosynthetic rate and chlorophyll a content increased by 7.8% and 44.1%, respectively. The antioxidant enzyme activity was enhanced and lipid peroxidation was reduced: POD and CAT increased by 81.0% and 146.3%, respectively. Moreover, at 9 days the IAA, ABA, and GB contents significantly increased by 67.4%, 6.8%, and 32.9%, respectively, compared with those under GB0.00. Therefore, utilizing an appropriate concentration of GB can bolster the heat tolerance of cherry radishes, which has the potential of enhancing their biomass and quality under high-temperature stress conditions. This study provides a theoretical basis for the research and development of GB in functional agricultural inputs for growth promotion and stress resistance and for efficient GB applications to greenhouse cash crops. This study was based on indoor simulation experiments; the compound effects of betaine and nutrient elements, as well their practical applications in greenhouses, should be investigated in the future.

Author Contributions

Conceptualization, Z.Z. and C.J.; data curation, Z.Z. and C.J.; formal analysis, Z.Z. and Y.Z.; funding acquisition, B.C.; project administration, B.C.; supervision, B.C.; validation, Y.Z. and M.Z.; writing—original draft, Z.Z. and M.Z.; writing—review and editing, C.J. and B.C. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Shandong Key Research and Development Program (2022SFGC0301).

Data Availability Statement

The original contributions presented in the study are included in the article, further inquiries can be directed to the corresponding author.

Conflicts of Interest

The authors declare no conflict of interest.

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Agronomy 14 01294 g001
Figure 1. Net photosynthetic rates (a) and chlorophyll (27 days) contents (b) of cherry radishes under different treatments (n = 3). Bar heights represent means and error bars represent ± SE. Within each graph, means followed by the same letter are not significantly different based on one-way ANOVA followed by Duncan’s multiple-range test (p < 0.05).
Figure 1. Net photosynthetic rates (a) and chlorophyll (27 days) contents (b) of cherry radishes under different treatments (n = 3). Bar heights represent means and error bars represent ± SE. Within each graph, means followed by the same letter are not significantly different based on one-way ANOVA followed by Duncan’s multiple-range test (p < 0.05).
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Agronomy 14 01294 g002
Figure 2. Ultra-structures of chloroplasts (A–C) and thylakoids (D–F) at 27 days in cherry radishes grown under different treatments. (A,D) CK (25 °C/20 °C day/night temperature treatment without GB); (B,E) GB0.00 (35 °C/30 °C day/night temperature treatment without GB); (C,F) GB17.6 (35 °C/30 °C day/night temperature treatment with 17.58 mg L−1 GB). The chloroplast outer membrane is marked by arrow a, the granum lamellae are marked by arrow b, and the osmiophilic globules are marked by arrow c. The scale bars for chloroplasts and thylakoids are 2 µm and 1 µm, respectively.
Figure 2. Ultra-structures of chloroplasts (A–C) and thylakoids (D–F) at 27 days in cherry radishes grown under different treatments. (A,D) CK (25 °C/20 °C day/night temperature treatment without GB); (B,E) GB0.00 (35 °C/30 °C day/night temperature treatment without GB); (C,F) GB17.6 (35 °C/30 °C day/night temperature treatment with 17.58 mg L−1 GB). The chloroplast outer membrane is marked by arrow a, the granum lamellae are marked by arrow b, and the osmiophilic globules are marked by arrow c. The scale bars for chloroplasts and thylakoids are 2 µm and 1 µm, respectively.
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Agronomy 14 01294 g003
Figure 3. Biomasses of cherry radishes under different treatments (n = 3). Bar heights represent means and error bars represent ± SE. Within each graph, means followed by the same letter are not significantly different based on one-way ANOVA followed by Duncan’s multiple-range test (p < 0.05).
Figure 3. Biomasses of cherry radishes under different treatments (n = 3). Bar heights represent means and error bars represent ± SE. Within each graph, means followed by the same letter are not significantly different based on one-way ANOVA followed by Duncan’s multiple-range test (p < 0.05).
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Agronomy 14 01294 g004
Figure 4. IAA (a), ABA (b), glycine betaine (c), and Pro contents (d) of cherry radishes under different treatments (n = 3). Bar heights represent means and error bars represent ± SE. Within each graph, means followed by the same letter are not significantly different based on one-way ANOVAs followed by Duncan’s multiple-range tests (p < 0.05).
Figure 4. IAA (a), ABA (b), glycine betaine (c), and Pro contents (d) of cherry radishes under different treatments (n = 3). Bar heights represent means and error bars represent ± SE. Within each graph, means followed by the same letter are not significantly different based on one-way ANOVAs followed by Duncan’s multiple-range tests (p < 0.05).
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Table 1. Fruit quality of cherry radishes under different treatments.
Table 1. Fruit quality of cherry radishes under different treatments.
TreatmentSoluble Protein (mg g−1)Vc Content (mg g−1)Soluble Solids (%)Nitrate Content (mg kg−1)
CK32.55 ± 0.30 f1.88 ± 0.02 g4.09 ± 0.02 abc145.64 ± 3.72 bc
GB0.0043.06 ± 0.12 e2.13 ± 0.01 e3.93 ± 0.04 c133.43 ± 5.17 c
GB0.0729.81 ± 0.41 g2.66 ± 0.02 a4.27 ± 0.10 a159.03 ± 11.23 ab
GB8.7947.45 ± 0.38 b2.20 ± 0. 02 d3.87 ± 0.16 c153.02 ± 8.27 bc
GB11.744.15 ± 0.32 d2.27 ± 0.01 c3.92 ± 0.06 c144.93 ± 5.39 bc
GB14.746.21 ± 0.31 c2.01 ± 0.01 f4.22 ± 0.04 ab177.43 ± 8.66 a
GB17.649.27 ± 0.21 a2.59 ± 0.02 b4.01 ± 0.02 bc131.14 ± 5.50 c
Note: Means within each column followed by the same letters were not significantly different based on one-way ANOVAs followed by Duncan’s multiple-range tests (p < 0.05).
Table 2. Antioxidant enzyme activities and MDA content of cherry radishes.
Table 2. Antioxidant enzyme activities and MDA content of cherry radishes.
TreatmentSOD Activity (U g−1 FW)POD Activity (U g−1 min−1 FW)
9 days18 days27 days9 days18 days27 days
CK821.83 ± 20.15 a801.68 ± 4.61 a643.57 ± 14.96 c13.80 ± 0.46 d7.20 ± 0.60 e6.50 ± 0.26 d
GB0.00593.79 ± 14.28 d743.34 ± 22.15 b509.96 ± 15.73 d3.59 ± 0.10 e6.60 d ± 0.92 e5.78 ± 0.17 e
GB0.07683.28 ± 7.45 b722.75 ± 18.72 b866.94 ± 13.05 a32.28 ± 1.03 a22.95 ± 1.30 b6.13 ± 0.09 de
GB8.79564.65 ± 4.60 d126.30 ± 3.56 d724.59 ± 10.85 b12.07 ± 0.84 d12.13 ± 0.35 d10.64 ± 0.10 a
GB11.7640.29 ± 13.06 c115.18 ± 3.76 d655.08 ± 11.24 c23.47 ± 1.12 c13.84 ± 0.35 d8.60 ± 0.26 c
GB14.7-148.26 ± 9.64 d709.76 ± 6.31 b-18.36 ± 1.21 c9.20 ± 0.16 b
GB17.6645.76 ± 6.42 bc189.44 ± 12.93 c673.85 ± 4.14 c29.04 ± 1.22 b29.80 ± 1.64 a10.46 ± 0.10 a
TreatmentCAT activity [U g−1 min−1 FW]MDA content (μmol g−1 FW)
9 days18 days27 days9 days18 days27 days
CK23.90 ± 0.52 ab18.83 ± 1.21 a11.32 ± 0.12 a3.54 ± 0.16 a3.98 ± 0.19 d9.28 ± 0.16 a
GB0.0022.20 ± 2.50 b14.39 ± 2.00 bc4.69 ± 0.19 e2.67 ± 0.12 b7.90 ± 0.29 a6.13 ± 0.05 bc
GB0.0728.20 ± 1.20 a12.72 ± 0.21 cd8.09 ± 0.15 c2.39 ± 0.20 b4.46 ± 0.21 d5.88 ± 0.10 cd
GB8.7924.20 ± 0.35 ab10.58 ± 0.23 de6.83 ± 0.11 d0.84 ± 0.02 c6.95 ± 0.32 b5.90 ± 0.07 cd
GB11.721.60 ± 1.85 b9.55 ± 0.13 e11.69 ± 0.14 a0.88 ± 0.02 c5.21 ± 0.07 c6.54 ± 0.17 b
GB14.7-7.85 ± 0.74 e9.74 ± 0.18 b-4.13 ± 0.09 d5.26 ± 0.23 e
GB17.622.39 ± 0.62 b16.48 ± 0.45 b11.55 ± 0.16 a0.91 ± 0.01 c3.95 ± 0.17 d5.65 ± 0.14 de
TreatmentAPX activity (mIU L−1)GR activity (IU L−1)
9 days18 days27 days9 days18 days27 days
CK98.24 ± 0.58 c95.07 ± 0.48 b55.45 ± 1.28 g374.83 ± 5.43 d357.15 ± 3.16 e279.19 ± 5.84 f
GB0.0086.06 ± 1.38 d117.57 ± 0.93 a79.24 ± 0.83 d309.32 ± 5.79 e514.69 ± 5.12 b601.22 ± 5.15 a
GB0.07110.56 ± 1.13 a62.90 ± 0.70 d123.70 ± 1.19 a421.10 ± 1.38 c470.49 ± 2.70 c532.24 ± 5.24 b
GB8.7972.03 ± 0.66 e75.48 ± 0.93 c73.85 ± 0.67 e295.80 ± 3.60 f543.28 ± 1.38 a430.84 ± 0.48 cd
GB11.785.14 ± 0.81 d60.25 ± 0.40 de118.13 ± 0.48 b428.38 ± 1.80 c549.35 ± 0.46 a438.58 ± 3.28 c
GB14.752.57 ± 0.48 f52.55 ± 1.47 f65.86 ± 0.64 f566.16 ± 5.50 a298.10 ± 2.16 f422.37 ± 1.95 b
GB17.6101.42 ± 0.35 b58.72 ± 0.79 e85.12 ± 0.57 c481.41 ± 1.80 b368.34 ± 4.68 d320.79 ± 5.15 e
Note: On the 9th day shown in the table, the relevant indicators could not be determined in the GB14.7 treatment due to an insufficient sampling weight at seedling stage. Means within each column followed by the same letter are not significantly different based on one-way ANOVAs followed by Duncan’s multiple-range tests (p < 0.05).
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Zhang, Z.; Jia, C.; Zhuang, Y.; Zhang, M.; Chen, B. Glycine Betaine Induces Tolerance to Oxidative Stress in Cherry Radishes under High-Temperature Conditions. Agronomy 2024, 14, 1294. https://doi.org/10.3390/agronomy14061294

AMA Style

Zhang Z, Jia C, Zhuang Y, Zhang M, Chen B. Glycine Betaine Induces Tolerance to Oxidative Stress in Cherry Radishes under High-Temperature Conditions. Agronomy. 2024; 14(6):1294. https://doi.org/10.3390/agronomy14061294

Chicago/Turabian Style

Zhang, Zexi, Chunhua Jia, Yuezhuo Zhuang, Min Zhang, and Baocheng Chen. 2024. "Glycine Betaine Induces Tolerance to Oxidative Stress in Cherry Radishes under High-Temperature Conditions" Agronomy 14, no. 6: 1294. https://doi.org/10.3390/agronomy14061294

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