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Article

The Physiological Mechanism of Low-Temperature Tolerance Following the UV-B Radiation of Eucommia ulmoides Oliver

by
Ying Zhang
1,2,3,†,
Xuchen Tian
1,2,3,†,
Wenling Zhou
4,†,
Zhonghua Tang
1,2,3,
Jing Yang
1,2,3,
Ye Zhang
1,2,3,
Xiaoqing Tang
1,2,3,
Dewen Li
1,2,3,* and
Ying Liu
1,2,3,*
1
College of Chemistry, Chemical Engineering and Resource Utilization, Northeast Forestry University, Harbin 150040, China
2
Key Laboratory of Forest Plant Ecology, Ministry of Education, Northeast Forestry University, Harbin 150040, China
3
Heilongjiang Provincial Key Laboratory of Ecological Utilization of Forestry-Based Active Substances, Northeast Forestry University, Harbin 150040, China
4
Guizhou Province LongLi County XiMa Town Agriculture, Forestry and Water Service Center, Longli 551202, China
*
Authors to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Agriculture 2024, 14(6), 878; https://doi.org/10.3390/agriculture14060878
Submission received: 9 April 2024 / Revised: 25 May 2024 / Accepted: 26 May 2024 / Published: 31 May 2024
(This article belongs to the Section Crop Production)
Browse Figures
Versions Notes

Abstract

:
Eucommia ulmoides Oliver with rich active components, such as flavonoids, lignans, polysaccharides, is used as a medicinal plant. Unfortunately, its popularization and cultivation are limited due to its low-temperature sensitivity. In this study, we aimed to explore the effect of different doses of ultraviolet-B (UV-B) radiation (UV-1, UV-2, and UV-3) and low-temperature (LT) stress, both applied individually and in combination, on the photosynthetic properties, biochemical parameters, and the contents of salicylic acid in E. ulmoides plants. The results showed that UV-B radiation alone significantly reduced photosynthetic performance and soluble total sugar content, as well as causing increases in soluble protein, proline, and superoxide anion content and antioxidant activity including SOD, POD, CAT, total phenol, and total flavonoid content. The leaf thickness and photosynthetic parameters significantly increased, as well as a significant decrease in SOD activity and soluble sugar, proline, and superoxide anion content after 14 days of none-UV-B radiation exposure. UV-B combined with LT significantly improved photosynthetic properties, Chl content, and soluble sugar content but significantly decreased proline content. Principal component analysis showed that salicylic acid was the key factor in improving LT tolerance, and UV-2 radiation showed the best LT resistance. We aim to provide new ideas and a theoretical basis for the directional cultivation and LT stress tolerance research of E. ulmoides. Our findings demonstrate that the combined effect was more positively helpful in improving the ability to resist LT tolerance via the improvement of photosynthetic ability and the increase in soluble sugar and salicylic acid content in E. ulmoides.

1. Introduction

Plant growth and development are affected by a great number of factors such as extreme temperature, radiation, salinity, drought, and so on [1]. Both UV-B radiation and low temperature (LT) have adverse and profound influences on plants [2]. Subjecting plants to UV-B radiation and cold stress leads to the generation of reactive oxygen species (ROS) that damage normal cell metabolism and cause oxidative damage [3]. However, LT is the major aspect that limits the productivity and geographical distribution of crops [4]. Eucommia ulmoides Oliver (E. ulmoides) is the sole species of the genus Eucommia [5], which is a kind of perennial herb that has great medicinal and economic value [6]. It mainly grows in the temperate regions of China, but due to its sensitivity to LT stress, it is difficult to introduce into new regions, such as the northeastern area [7].
The antioxidant defense systems of plants such as SOD, CAT, and POD [8] and proline [9] have been found to resist oxidative stress through rapid ROS removal, resulting in improved tolerance to cold stress. The synthesis of secondary metabolites, such as phenolic acids and flavonoids, is one defense mechanism used by plants to resist the stress induced by LT [10] and UV-B radiation [11]. Flavonoids are mainly involved in defense against UV-B radiation, and they also have the capacity to reduce ROS generation [12]. Therefore, controlling the accumulation of ROS is an effective way to reduce damage [13]. Salicylic acid (SA) is an important phenolic plant hormone that acts as a regulatory signal and is involved in the regulation of plant defense responses such as those against UV-B radiation and low temperature [14].
Interestingly, interactive effects between UV-B radiation and LT have been progressively studied in plants, demonstrating that UV-B radiation and LT can exhibit a coordinated effect on the response to stress [15]. Dhanya et al. reported that UV-B priming can induce cross-tolerance, thereby promoting the ability to cope with subsequent stress [16]. UV-B radiation enhanced the ability of freezing tolerance in winter wheat seedlings via antioxidant defense systems and the ascorbate–glutathione cycle [17]. Additionally, pre-UV-B radiation reduced H2O2 and O2 levels and protection from membrane oxidative damage to cope with cold stress [18]. Although most studies have concentrated on the responses of plants to UV-B or LT, the effect of interaction between UV-B and LT on E. ulmoides has received little attention and there is scarce information about its effects. We hypothesized that the interactions between UV-B and LT would show a greater ability to resist stress than those exposed to E. ulmoides individually. Therefore, the objective of this study was to evaluate the impact of UV-B treatment and the combined effect of LT and UV-B radiation on some aspects of physiology, such as photosynthetic performance, phenol and flavonoid content as well as salicylic acid content in E. ulmoides.

2. Materials and Methods

2.1. Plant Materials and Experimental Design

E. ulmoides plants were cultivated at a temperature of 25 °C in the artificial growth room and artificial climate box of the Key Laboratory of Forest Plant Ecology of the Ministry of Education of Northeast Forestry University (N 45.75°, E 126.63°). Three-year-old potted E. ulmoides seedlings with consistent growth were randomly divided into different groups: the CK groups (no UV-B and low temperature), three treatment groups (low-temperature stress was carried out after receiving UV–B radiation at 1.40 (UV-1), 2.80 (UV-2) and 4.20 (UV-3) kJ·m−2·d−1, and CK* (only low temperature). They were irradiated for 3 days and with 7 h UV-B exposure (9:00–16:00) per day (Figure 1), and three replicate samples were collected. The ultraviolet light emitted by the lamp was filtered by 0.08 mm cellulose acetate to eliminate the influence of UV-C. The lamps were turned on 30 min before the start of experiment to ensure stability and kept in the dark for the duration of the experiment. UV–B was delivered via fluorescent UV lamps (The Q-Panel Company, Cleveland, OH, USA) with a spectral peak at 308 nm, and the UV-B intensity being measured by AvaSpec 2048-2 (Avantes BV, Apeldoorn, The Netherlands). The E. ulmoides plants were located approximately 40 cm below the lamps and were consistently irradiated at well-distributed distances from the lamps. Halfway through the treatment period, the E. ulmoides plants were rotated by 180 degrees.
Subsequently, the E. ulmoides plants went through a 14-day UV-B radiation recovery (UV-B~R14D) stage. This was followed by exposure to low-temperature stress (UV-B + LT) for 3 days, and then, they went through a 14-day UV-B radiation recovery (UV-B + LT~R14D) stage (Figure 1). Each treatment was repeated three times.

2.2. Measurement of Photosynthetic Parameters

Photosynthetic rate (Pn) and stomatal conductance (Gs) of the first completely expanded leaf were selected for measurement using an Li-6400 (LICOR 6400, Lincoln, NE, USA), and each leaf was measured three times. The measurements were taken at 25 ± 3 °C with 400 μmol/mol CO2 and 60% relative humidity.

2.3. Determination of Pigment Content

The contents of total chlorophyll, carotenoids, and chlorophyll a and b in the leaves were determined using a spectrophotometer (UV-754, Shanghai Meipda Instrument Co., Ltd., Shanghai, China). E. ulmoides fresh leaves (0.1 g) were extracted in 95% (v/v) ethanol. The absorbance values were measured at 470, 649, and 665 nm after the leaves were placed in a dark box for 24 h.

2.4. Measurement of Antioxidant Enzyme Activities

The activity of SOD was determined using the NBT photochemical reduction method [19]. The measurement of POD activity was based on the guaiacol method [20]. The method of Aebi was used for the determination of CAT activity [21]. We used the UV absorption method for the determination of APX activity [22].

2.5. Measurement of Soluble Sugar, Soluble Protein, Proline, Malondialdehyde, and Superoxide Anion Contents

E. ulmoides leaves were collected for the determination of the content of soluble sugar, soluble protein, malondialdehyde (MDA), and free proline. The soluble sugar content was determined via the anthrone sulfuric acid method using glucose as a standard [23]. The Coomassie brilliant blue G-250 staining method was used to detect soluble protein content [24]. The free proline content in fresh 0.5 g E. ulmoides leaf samples was measured using the acid ninhydrin colorimetry method [25]. MDA was determined using the thiobarbituric acid method [26]. The content of superoxide anion was determined using the hydroxylamine reaction method [27].

2.6. Measurement of Total Phenol and Total Flavonoid Content

The total phenol content was determined using the Folin–Ciocalteu method [28]. A fresh sample (0.2 g) was placed into a 10 mL centrifuge tube, and 5 mL of preheated 70% methanol was added. The sample was extracted for 10 min at 70 °C water bath, and then t centrifuged at 10,000 r·min−1 for 10 min. Then, the supernatant was diluted with methanol (70%) to 1000 mL. We took 10 mL of solution and added 5 mL of Folin–Ciocalteu solution. Adding 4 mL anhydrous carbonic acid (7.5%), the absorbance was read at 765 nm after 7 min. The total flavonoid content was determined using the aluminum chloride colorimetric method by Luximon-Ramma et al. [29].

2.7. Measurement of Salicylic Content

The leaves were weighed, flash-frozen, and immediately ground into a fine powder. We added 20 mL 90% methanol and then carried out centrifugation at 10,000 r·min−1 at low temperature for 30 min. We repeated this step twice, and the obtained supernatants were pooled and concentrated in a rotary evaporator. Then, we added 15 mL of 5% trichloroacetic acid and performed extraction twice using 40 mL of ethyl acetate and cyclohexane (1:1, v/v). Next, 15 mL of 8 mol·L−1 HCl was added and then incubated at 80 °C in a water bath for 60 min. The organic phases were combined after two extractions and then evaporated to dryness. The samples were resolved with 30 mL of 80% methanol (chromatography grade) and then, we determined the volume with sodium acetate buffer (0.2 M, pH 5.5). The C18 column (150 mm × 4.6 mm, 5 μm; Agilent, Santa Clara, CA, USA) was selected. The mobile phases were composed of sodium acetate (0.2 m, pH 5.5) and methanol with a ratio of 4/6. The sample volume injected was 10 μL and the flow rate was 5 mL·min−1.

2.8. Statistical Analysis

Excel 2021, SPSS 22.0, and Origin 2021 software were used for the correlation analysis and principal component analysis. Differences between factors and treatments were determined via one-way ANOVA using Duncan’s multiple-range test at p < 0.05.

3. Results

3.1. Photosynthetic Parameters under Different UV-B Doses of Radiation in Different Stages of E. ulmoides

After different doses of UV-B radiation (UV-1, UV-2, and UV-3) treatment, the net photosynthetic rate (Pn) (Figure 2A), transpiration rate (Tr) (Figure 2C), intercellular carbon dioxide concentration (Ci) (Figure 2D), and stomatal conductance (Gs) (Figure 2B) were significantly lower (p < 0.05) than CK. After a recovery period of 14 days without UV-B radiation (UV-B~R14D), the photosynthetic performance showed a slight improvement. The performances of Pn, Tr, Ci, and Gs were higher under UV-B + LT than under LT, but the and water use efficiency (WUE) (Figure 2E) and leaf efficiency (Ec) (Figure 2F) trends were simply the opposite. It was obvious that the abilities of Pn, Gs, Ci, and Tr were higher after a recovery period of 14 days without LT stress (UV-B + LT~R14D) than after UV-B~R14D; Ec and WUE also demonstrated the opposite trend.

3.2. Leaf Pigment Content under Different UV-B Doses of Radiation in Different Stages of E. ulmoides

The Chl content (Figure 3C) was significantly lower (p < 0.05) after UV-1, UV-2, and UV-3 radiation than after UV-B + LT. Chl b (Figure 3B) and total Chl demonstrated the highest (p < 0.05) content compared with the other treatments after UV-2 treatment. After UV-B~R14D, Chl content was also found to be higher than after UV-B + LT~R14D.

3.3. Antioxidant System Analysis under Different UV-B Doses of Radiation in Different Stages of E. ulmoides

The activities of SOD (Figure 4A), CAT (Figure 4B), POD (Figure 4C), and APX (Figure 4D) all reached a maximum value in the UV-2 treatment, increasing by 15.5%, 63.7%, 22.6%, and 71.3% compared with CK (p < 0.05). After the UV-B + LT stage, POD activities gradually increased with the increase in the UV-B radiation dose and reached a maximum value in UV-3 treatment (Figure 4C). The activities of SOD and CAT were higher after UV-B radiation and UV-B~R14D than after UV-B + LT and UV-B + LT~R14D, but POD and APX showed an opposite trend.

3.4. Osmoregulatory Substance, MDA, and Superoxide Anion Contents under Different UV-B Doses of Radiation in Different Stages of E. ulmoides

With the increase in UV-B radiation dose, the soluble sugar content and soluble protein content decreased and increased, respectively (Figure 5A,B). The proline and superoxide anion contents were higher after UV-B radiation and UV-B~R14D than after UV-B + LT and UV-B + LT~R14D (Figure 5C,E), but malonaldehyde (MDA) content was lower after UV-B radiation and UV-B~R14D than after UV-B + LT and UV-B + LT~R14D (Figure 5D).

3.5. Total Phenol and Total Flavonoid Contents under Different UV-B Doses of Radiation in Different Stages of E. ulmoides

The total phenol contents after different UV-B treatments was significantly higher (p < 0.05) than CK (Figure 6A). With the increase in UV-B radiation dose, total flavonoid content gradually increased in four stages (Figure 6B). The total phenols and total flavonoid contents were higher after UV-B radiation and UV-B~R14D than after UV-B + LT and UV-B + LT~R14D.

3.6. Salicylic Acid Content under Different UV-B Treatments in Different Stages of E. ulmoides

The salicylic acid content was lower after UV-B radiation and UV-B~R14D than after UV-B + LT and UV-B + LT~R14D) and reached a maximum value under UV-2 radiation and increased 70.5% compared with LT stress.

3.7. Evaluation Model of the Low-Temperature Tolerance of E. ulmoides

In order to optimize and screen which UV-B irradiation treatment can effectively improve the low-temperature resistance of E. ulmoides, we selected five treatments after UV-B + LT treatment including CK* (LT), UV-1~UV-3 (UV-B + LT), and CK (no UV-B and LT). Nine indexes, including SOD and POD activities, salicylic acid (SA), plant height, soluble protein (sp), soluble sugar (ss), proline (pro), MDA, and Pn, were processed using the Z-score (Table 1). Whether they were suitable for factor analysis was judged using the KMO test and Bartlett sphericity test. And the Bartlett sphericity test significance was 0.000, which demonstrated that our data could be used for factor analysis.
Principal component analysis (PCA) results showed that the first, second, and third principal components (PC1, PC2, and PC3) represented 45.701%, 39.732%, and 13.064% of the variance in the data, respectively (Table 2). The cumulative contribution rate of PC1, PC2, and PC3 was 98.497% and sufficient to explain the nine indexes. PC1 mainly included plant height and salicylic acid (SA) content. PC2 was positively correlated with proline (pro) content, POD activity, and MDA content. PC3 was mainly correlated with soluble sugar (SS) content and SOD activity (Table 2).
The composite scores of CK*~UV-3 were as follows: −2.048, 0.090, 0.259, 1.031, and 0,668. The order of LT resistance was as follows: UV-2 > UV-3 > UV-1 > CK > CK*. Therefore, UV-2 radiation resulted in the best LT resistance (Table 3).

4. Discussion

We investigated the effect of different doses of UV-B radiation (UV-1, UV-2, and UV-3) applied individually and combined with low temperature (LT) on some growth and physiological characteristics of E. ulmoides. It is known that chlorophyll concentration is positively correlated with photosynthesis [30]. In this work, E. ulmoides leaves had a higher concentration of Chl b under UV-B radiation (Figure 3B). The Chl a content was higher in E. ulmoides leaves exposed to UV-B + LT than those under LT stress (Figure 3A), showing a positive correlation between UV-B radiation and LT. The increase in Chl content (Figure 3C) under UV-B was in agreement with the results of earlier studies on canola [31] and soybean [32], with both studies finding that UV-B increased Chl content.
High-dose UV-B radiation has negative impacts on plants, a stress factor causing photochemical damage to cellular DNA, but low-dose UV-B radiation is able to positively regulate plant growth and development [33]. UV-B radiation had been shown to have an adverse influence on many aspects of plant photosynthesis [34]. In this study, it was obvious that the photosynthetic performance of E. ulmoides leaves tended to decrease as the UV-B radiation doses increased (Figure 2). Photosynthesis was negatively affected by cold stress, which damaged the chloroplast and inhibited the growth and photosynthesis of the plants [35]. It was found that the photosynthetic performance of E. ulmoides leaves tended to increase as UV-B radiation exposure increased under LT stress (Figure 2). In particular, the Pn of E. ulmoides leaves was highest after UV-2 treatment with a given intensity (2.8 kJ·m−2·d−1) under cold stress. At UV-3 treatment, however, Pn decreased significantly (p < 0.05) (Figure 2A). This suggested that a moderate dose of UV-B treatment might improve the photosynthetic performance in E. ulmoides, having positive effect on subsequent activities, whereas excessive UV-B treatment might have negative effects on E. ulmoides. Additionally, it was obvious that the abilities of Pn, Gs, Ci, and Tr were higher after UV-B + LT~R14D than after UV-B~R14D. This indirectly showed that UV-B radiation was of great significance for E.ulmoides to cope with LT stress.
Antioxidant enzymes are able to protect plants from oxidative damage via ROS accumulation [36]. Many antioxidant enzymes are important for reducing ROS that stabilize the membranes [37]. For example, in response to oxidative stress, POD alleviated or regulated ROS to enhance antioxidant capacity under cold stress [38]. In this study, we found that the application of UV-B radiation increased the content of superoxide anion (O2−) in E. ulmoides (Figure 5E). In order to resist the imbalance in the defense system and the harm of membrane lipid peroxidation caused by the increase in superoxide anion content, four antioxidant enzymes, SOD, POD, CAT, and APX, were further activated and had a better effect after UV-2 radiation (Figure 3). In addition, the total phenol and flavonoid contents accumulated and remained at a high level after UV-B radiation but decreased under UV-B + LT (Figure 6A,B). This suggested that UV-B radiation influenced the accumulation of antioxidant substances and enhanced antioxidant abilities, so as to cope well with the damage caused by LT stress. Therefore, we speculate that the increase in antioxidant abilities against oxidative damage can induce greater LT tolerance.
Proline plays a key role in balancing osmoregulation and protecting the cell from damage [39]. Malondialdehyde (MDA) is the final decomposition product of membrane lipid peroxidation, and its content can reflect the degree of damage to a plant cell membrane [40]. In this study, the soluble sugar content gradually decreased with the increase in UV-B radiation dose, but this was not the case for soluble protein content (Figure 5A,B). The proline content was higher after UV-B radiation and UV-B~R14D than after UV-B + LT and UV-B + LT~R14D (Figure 5C). It demonstrated that UV-B radiation promoted the accumulation of proline to maintain the normal metabolism of cells [41]. But MDA content was lower after UV-B radiation and UV-B~R14D than after UV-B + LT and UV-B + LT~R14D (Figure 5D), which showed that LT stress mainly caused lipid peroxidation, generating membrane damage [42]. It is generally known that a high concentration of superoxide anion induces severe damage in plant cells [43]. In our study, the O2− content under UV-B + LT was lower than that under UV-B radiation (Figure 5E), implying that UV-B + LT was beneficial in improving the LT resistance of plants. Salicylic acid is involved in stress resistance and mediates abiotic stress responses in plants [44]. In our study, salicylic acid content was even higher under UV-B + LT than under UV-B radiation and LT stress (Figure 7). Therefore, the increase in salicylic acid content under UV-B + LT can be considered a stress response to protect E. ulmoides from LT. Based on these results, it can be concluded that UV-B + LT show a greater ability to resist LT stress than those exposed to E. ulmoides individually.
Principal component analysis (PCA) aims to use the method of dimensionality reduction to transform multiple indicators into a few important components so that they reflect the main characteristics of the object [45]. In this study, nine physiological indexes of E. ulmoides were analyzed using PCA to search for the anti-adversity factor. It showed that salicylic acid was the key factor in improving LT tolerance, and UV-2 radiation showed the best LT resistance. In conclusion, the results of this study show that UV-B radiation and LT had adverse effects on the performance of three-year-old E. ulmoides seedlings, but these effects were partially ameliorated by cooperation. This validates our original hypotheses. In the future, plants can be engineered to upregulate the salicylic acid gene, so as to improve the endogenous level and produce Eucommia ulmoides Oliv., which can positively cope with climate change.

5. Conclusions

Some specific details, such as the decrease in photosynthetic capacity and the increase in superoxide anion content, indicated that the E. ulmoides leaves were damaged to some extent after UV-B radiation. However, after 7 days of recovery, the plants can cope well with the damage caused by low-temperature (LT) stress. For example, the improvement in photosynthetic performance, the reduction in superoxide anion content, and the high amount of salicylic acid accumulation. Principal component analysis further showed that E. ulmoides irradiated by 2.8 kJ·m−2·d−1 UV-B radiation had a greater LT tolerance ability than those that had not been exposed to UV-B radiation. The results of this study parse the mechanism of improving LT tolerance via UV-B radiation from a physiological perspective and lay the foundation for improving the LT tolerance of E. ulmoides.

Author Contributions

D.L. and Y.L. conceived the project and critically edited the manuscript; Y.Z. (Ying Zhang) conducted the experiments and wrote the manuscript; X.T. (Xuchen Tian) and W.Z. analyzed the data; J.Y., Y.Z. (Ye Zhang) and X.T. (Xiaoqing Tang) assisted with the experiments; Z.T. provided guidance on the experimental methods. All authors have read and agreed to the published version of the manuscript.

Funding

This work was funded by the Heilong Jiang Province Natural Science Fund Project (No. LH2021C014), the Heilong Jiang Province Seed Industry Innovation Project (ZQTYB231700002), the Construction of Key Chinese Herbal Medicine Resource Gardens such as Acanthopanax Senticosus and Schisandra chinensis, and the development and demonstration of its industrialized breeding technology, the National Forestry and Grassland Science and Technology Achievement Promotion Project (No. 2023133125), Project 111 of Heilongjiang Goose Innovation Team (No. B20088), and the Horizontal Project (No. 2021).

Institutional Review Board Statement

Not applicable.

Data Availability Statement

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

Conflicts of Interest

The authors declare no conflicts of interest.

References

  1. Poongodi, S.; Rajesh Babu, M. Analysis of crop suitability using clustering technique in Coimbatore region of Tamil Nadu. Concurr. Comput. Pract. Exp. 2019, 31, e5294. [Google Scholar] [CrossRef]
  2. Kakani, V.G.; Reddy, K.R.; Zhao, D.; Sailaja, K. Field crop responses to ultraviolet-B radiation: A review. Agric. For. Meteorol. 2003, 120, 191–218. [Google Scholar] [CrossRef]
  3. Lee, J.; Kwon, M.C.; Jung, E.S.; Lee, C.H.; Oh, M. Physiological and metabolomic responses of kale to combined chilling and UV-A treatment. Int. J. Mol. Sci. 2019, 20, 4950. [Google Scholar] [CrossRef] [PubMed]
  4. Hussain, S.; Khan, F.; Hussain, H.A.; Nie, L. Physiological and biochemical mechanisms of seed priming-induced chilling tolerance in rice cultivars. Front. Plant Sci. 2016, 7, 178194. [Google Scholar] [CrossRef]
  5. Liu, H.; Fu, J.; Du, H.; Hu, J.; Wuyun, T. De novo sequencing of Eucommia ulmoides flower bud transcriptomes for identification of genes related to floral development. Genom. Data 2016, 9, 105–110. [Google Scholar] [CrossRef] [PubMed]
  6. Li, L.; Liu, M.; Shi, K.; Yu, Z.; Zhou, Y.; Fan, R.; Shi, Q. Dynamic changes in metabolite accumulation and the transcriptome during leaf growth and development in Eucommia ulmoides. Int. J. Mol. Sci. 2019, 20, 4030. [Google Scholar] [CrossRef] [PubMed]
  7. Wu, X.; Zhao, D. Cloning, characterization, and functional analysis of EuTIL1, a gene-encoding temperature-induced lipocalin in Eucommia ulmoides Oliv. Horticulturae 2023, 9, 950. [Google Scholar] [CrossRef]
  8. Ghorbani, B.; Pakkish, Z.; Khezri, M. Nitric oxide increases antioxidant enzyme activity and reduces chilling injury in orange fruit during storage. N. Z. J. Crop Hortic. Sci. 2018, 46, 101–116. [Google Scholar] [CrossRef]
  9. Peppino Margutti, M.; Reyna, M.; Meringer, M.V.; Racagni, G.E.; Villasuso, A.L. Lipid signalling mediated by PLD/PA modulates proline and H2O2 levels in barley seedlings exposed to short- and long-term chilling stress. Plant Physiol. Biochem. 2017, 113, 149–160. [Google Scholar] [CrossRef]
  10. Theocharis, A.; Clément, C.; Barka, E.A. Physiological and molecular changes in plants grown at low temperatures. Planta 2012, 235, 1091–1105. [Google Scholar] [CrossRef]
  11. Neugart, S.; Majer, P.; Schreiner, M.; Hideg, É. Blue light treatment but not green light treatment after pre-exposure to UV-B stabilizes flavonoid glycoside changes and corresponding biological effects in three different Brassicaceae sprouts. Front. Plant Sci. 2021, 11, 611247. [Google Scholar] [CrossRef] [PubMed]
  12. He, Y.; Pan, L.; Yang, T.; Wang, W.; Li, C.; Chen, B.; Shen, Y. Metabolomic and confocal laser scanning microscopy (CLSM) analyses reveal the important function of flavonoids in Amygdalus pedunculata pall leaves with temporal changes. Front. Plant Sci. 2021, 12, 648277. [Google Scholar] [CrossRef] [PubMed]
  13. Subramanian, P.; Kim, K.; Krishnamoorthy, R.; Mageswari, A.; Selvakumar, G.; Sa, T. Cold stress tolerance in Psychrotolerant soil bacteria and their conferred chilling resistance in tomato (Solanum lycopersicum Mill.) Under low temperatures. PLoS ONE 2016, 11, e161592. [Google Scholar] [CrossRef] [PubMed]
  14. Martel, A.B.; Qaderi, M.M. Does salicylic acid mitigate the adverse effects of temperature and ultraviolet-B radiation on pea (Pisum sativum) plants? Environ. Exp. Bot. 2016, 122, 39–48. [Google Scholar] [CrossRef]
  15. León-Chan, R.G.; López-Meyer, M.; Osuna-Enciso, T.; Sañudo-Barajas, J.A.; Heredia, J.B.; León-Félix, J. Low temperature and ultraviolet-B radiation affect chlorophyll content and induce the accumulation of UV-B-absorbing and antioxidant compounds in bell pepper (Capsicum annuum) plants. Environ. Exp. Bot. 2017, 139, 143–151. [Google Scholar] [CrossRef]
  16. Dhanya, T.T.; Dinakar, C.; Puthur, J.T. Effect of UV-B priming on the abiotic stress tolerance of stress-sensitive rice seedlings: Priming imprints and cross-tolerance. Plant Physiol. Biochem. 2020, 147, 21–30. [Google Scholar] [CrossRef] [PubMed]
  17. Yang, S.; Wang, L.; Li, S. Ultraviolet-B irradiation-induced freezing tolerance in relation to antioxidant system in winter wheat (Triticum aestivum L.) Leaves. Environ. Exp. Bot. 2007, 60, 300–307. [Google Scholar] [CrossRef]
  18. Jiang, Z.; Xu, M.; Dong, J.; Zhu, Y.; Lou, P.; Han, Y.; Hao, J.; Yang, Y.; Ni, J.; Xu, M. UV-B pre-irradiation induces cold tolerance in tomato fruit by SIUVR8-mediated upregulation of superoxide dismutase and catalase. Postharvest Biol. Technol. 2022, 185, 111777. [Google Scholar] [CrossRef]
  19. Beyer, W.F., Jr.; Fridovich, I. Assaying for superoxide dismutase activity: Some large consequences of minor changes in conditions. Anal. Biochem. 1987, 161, 559–566. [Google Scholar] [CrossRef]
  20. Zheng, X.; Tian, S.; Meng, X.; Li, B. Physiological and biochemical responses in peach fruit to oxalic acid treatment during storage at room temperature. Food Chem. 2007, 104, 156–162. [Google Scholar] [CrossRef]
  21. Hugo, A. [13] Catalase in vitro. Methods Enzymol. 1984, 105, 121–126. [Google Scholar]
  22. Nakano, Y.K.U.U.; Asada, K. Purification of ascorbate peroxidase in Spinach chloroplasts; Its inactivation in ascorbate-depleted medium and reactivation by monodehydroascorbate radical. Plant Cell Physiol. 1987, 28, 131–140. [Google Scholar]
  23. Li, X.; Hao, C.; Zhong, J.; Liu, F.; Cai, J.; Wang, X.; Zhou, Q.; Dai, T.; Cao, W.; Jiang, D. Mechano-stimulated modifications in the chloroplast antioxidant system and proteome changes are associated with cold response in wheat. BMC Plant Biol. 2015, 15, 1–13. [Google Scholar] [CrossRef] [PubMed]
  24. Zhou, Y.; Wang, W.; Wei, R.; Jiang, G.; Li, F.; Chen, X.; Wang, X.; Long, S.; Ma, D.; Xi, L. Serum bradykinin levels as a diagnostic marker in cervical cancer with a potential mechanism to promote VEGF expression via BDKRB2. Int. J. Oncol. 2019, 55, 131–141. [Google Scholar] [CrossRef] [PubMed]
  25. Bates, L.S.; Waldren, R.P.; Teare, I.D. Rapid determination of free proline for water-stress studies. Plant Soil 1973, 39, 205–207. [Google Scholar] [CrossRef]
  26. Du, Z.; Bramlage, W.J. Modified thiobarbituric acid assay for measuring lipid oxidation in sugar-rich plant tissue extracts. J. Agric. Food Chem. 1992, 40, 1566–1570. [Google Scholar] [CrossRef]
  27. Wu, Y.X.; von Tiedemann, A. Impact of fungicides on active oxygen species and antioxidant enzymes in spring barley (Hordeum vulgare L.) exposed to ozone. Environ. Pollut. 2002, 116, 37–47. [Google Scholar] [CrossRef]
  28. Pang, L.; Adeel, M.; Shakoor, N.; Guo, K.; Ma, D.; Ahmad, M.A.; Lu, G.; Zhao, M.; Li, S.; Rui, Y. Engineered nanomaterials suppress the soft rot disease (Rhizopus stolonifer) and slow down the loss of nutrient in sweet potato. Nanomaterials 2021, 11, 2572. [Google Scholar] [CrossRef]
  29. Luximon-Ramma, A.; Bahorun, T.; Soobrattee, M.A.; Aruoma, O.I. Antioxidant activities of phenolic, proanthocyanidin, and flavonoid components in extracts of Cassia fistula. J. Agric. Food. Chem. 2002, 50, 5042–5047. [Google Scholar] [CrossRef]
  30. Chen, J.; Wu, F.; Shang, Y.; Wang, W.; Hu, W.; Simon, M.; Liu, X.; Shangguan, Z.; Zheng, H. Hydrogen sulphide improves adaptation of Zea mays seedlings to iron deficiency. J. Exp. Bot. 2015, 66, 6605–6622. [Google Scholar] [CrossRef]
  31. Sangtarash, M.H.; Qaderi, M.M.; Chinnappa, C.C.; Reid, D.M. Differential responses of two Stellaria longipes ecotypes to ultraviolet-b radiation and drought stress. Flora Morphol. Distrib. Funct. Ecol. Plants 2009, 204, 593–603. [Google Scholar] [CrossRef]
  32. Koti, S.; Reddy, K.R.; Kakani, V.G.; Zhao, D.; Gao, W. Effects of carbon dioxide, temperature and ultraviolet-B radiation and their interactions on soybean (Glycine max L.) Growth and development. Environ. Exp. Bot. 2007, 60, 1–10. [Google Scholar] [CrossRef]
  33. Yadav, A.; Singh, D.; Lingwan, M.; Yadukrishnan, P.; Masakapalli, S.K.; Datta, S. Light signaling and UV-B-mediated plant growth regulation. J. Integr. Plant Bio. 2020, 62, 1270–1292. [Google Scholar] [CrossRef]
  34. Ri, I.; Pak, S.; Pak, U.; Yun, C.; Tang, Z. How does UV-B radiation influence the photosynthesis and secondary metabolism of Schisandra chinensis leaves? Ind. Crop Prod. 2024, 208, 117832. [Google Scholar] [CrossRef]
  35. Deng, S.; Ma, J.; Zhang, L.; Chen, F.; Sang, Z.; Jia, Z.; Ma, L. De novo transcriptome sequencing and gene expression profiling of Magnolia wufengensis in response to cold stress. BMC Plant Biol. 2019, 19, 1–23. [Google Scholar]
  36. Zafari, S.; Vanlerberghe, G.C.; Igamberdiev, A.U. The Role of Alternative Oxidase in the Interplay between Nitric Oxide, Reactive Oxygen Species, and Ethylene in Tobacco (Nicotiana tabacum L.) Plants Incubated under Normoxic and Hypoxic Conditions. Int. J. Mol. Sci. 2022, 23, 7153. [Google Scholar] [CrossRef] [PubMed]
  37. Kumar, M.; Yusuf, M.A.; Yadav, P.; Narayan, S.; Kumar, M. Overexpression of chickpea defensin gene confers tolerance to water-deficit stress in Arabidopsis thaliana. Front. Plant Sci. 2019, 10, 290. [Google Scholar] [CrossRef] [PubMed]
  38. Zhang, J.; An, H.; Zhang, X.; Xu, F.; Zhou, B. Transcriptomic analysis reveals potential gene regulatory networks under cold stress of loquat (Eriobotrya japonica Lindl.). Front. Plant Sci. 2022, 13, 944269. [Google Scholar] [CrossRef]
  39. Vuković, R.; Amagajevac, I.Š; Vuković, A.; Aunić, K.; Begović, L.; Mlinarić, S.; Sekulić, R.; Sabo, N.; Apanić, V. Physiological, biochemical and molecular response of different winter wheat varieties under drought stress at germination and seedling growth stage. Antioxidants 2022, 11, 693. [Google Scholar] [CrossRef]
  40. Rao, Y.; Jiao, R.; Wang, S.; Wu, X.; Ye, H.; Pan, C.; Li, S.; Xin, D.; Zhou, W.; Dai, G.; et al. SPL36 encodes a receptor-like protein kinase that regulates programmed cell death and defense responses in rice. Rice 2021, 14, 34. [Google Scholar]
  41. Liu, S.; Fang, S.; Liu, C.; Zhao, L.; Cong, B.; Zhang, Z. Transcriptomics integrated with metabolomics reveal the effects of ultraviolet-b radiation on flavonoid biosynthesis in antarctic moss. Front. Plant Sci. 2021, 12, 788377. [Google Scholar] [CrossRef] [PubMed]
  42. Amin, B.; Atif, M.J.; Meng, H.; Ali, M.; Li, S.; Alharby, H.F.; Majrashi, A.; Hakeem, K.R.; Cheng, Z. Melatonin rescues photosynthesis and triggers antioxidant defense response in Cucumis sativus plants challenged by low temperature and high humidity. Front. Plant Sci. 2022, 13, 855900. [Google Scholar] [CrossRef] [PubMed]
  43. Neira, G.; Vergara, E.; Cortez, D.; Holmes, D.S. A large-scale multiple genome comparison of acidophilic archaea (pH ≤ 5.0) extends our understanding of oxidative stress responses in polyextreme environments. Antioxidants 2022, 11, 59. [Google Scholar] [CrossRef] [PubMed]
  44. Zhou, Z.; Guo, K.; Elbaz, A.; Yang, Z. Salicylic acid alleviates mercury toxicity by preventing oxidative stress in roots of Medicago sativa. Environ. Exp. Bot. 2009, 65, 27–34. [Google Scholar] [CrossRef]
  45. Shao, L.; Cao, Y.; Jones, T.; Santosh, M.; Silva, L.F.O.; Ge, S.; Da Boit, K.; Feng, X.; Zhang, M.; Bérubé, K. COVID-19 mortality and exposure to airborne PM2.5: A lag time correlation. Sci. Total Environ. 2022, 806, 151286. [Google Scholar] [CrossRef]
Agriculture 14 00878 g001
Figure 1. Schematic diagram of the experimental treatment.
Figure 1. Schematic diagram of the experimental treatment.
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Figure 2. Changes in photosynthetic parameters in E. ulmoides leaves. (A) photosynthetic rate (Pn); (B) stomatal conductance (Gs); (C) transpiration rate (Tr); (D) internal CO2 concentration (Ci); (E) water use efficiency (WUE); (F) carboxylation efficiency (Ec) at different stages in E. ulmoides leaves. UV-B radiation stage (UV-1, UV-2, and UV-3); recovered for 14 days after ultraviolet radiation (UV-B~R14D); low-temperature stress after pre-UV-B treatment stage (UV-B + LT); recovered for 14 days after double treatments (UV-B + LT~R14D). Data are the means ± SD (n = 3). Different letters indicate significant differences between samples at the same time point.
Figure 2. Changes in photosynthetic parameters in E. ulmoides leaves. (A) photosynthetic rate (Pn); (B) stomatal conductance (Gs); (C) transpiration rate (Tr); (D) internal CO2 concentration (Ci); (E) water use efficiency (WUE); (F) carboxylation efficiency (Ec) at different stages in E. ulmoides leaves. UV-B radiation stage (UV-1, UV-2, and UV-3); recovered for 14 days after ultraviolet radiation (UV-B~R14D); low-temperature stress after pre-UV-B treatment stage (UV-B + LT); recovered for 14 days after double treatments (UV-B + LT~R14D). Data are the means ± SD (n = 3). Different letters indicate significant differences between samples at the same time point.
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Figure 3. Changes in photosynthetic pigment content at different stages in E. ulmoides leaves. UV-B radiation stage (UV-1, UV-2, and UV-3); recovered for 14 days after ultraviolet radiation (UV-B~R14D); low-temperature stress after pre-UV-B treatment stage (UV-B + LT); recovered for 14 days after double treatments (UV-B + LT~R14D). (A) Chl a, chlorophyll a; (B) Chl b, chlorophyll b; (C) total Chl (total chlorophyll); (D) Chl a/Chl b, the ratio of chlorophyll content to chlorophyll b content. Data are the means ± SD (n = 3). Different letters indicate significant differences between samples at the same time point.
Figure 3. Changes in photosynthetic pigment content at different stages in E. ulmoides leaves. UV-B radiation stage (UV-1, UV-2, and UV-3); recovered for 14 days after ultraviolet radiation (UV-B~R14D); low-temperature stress after pre-UV-B treatment stage (UV-B + LT); recovered for 14 days after double treatments (UV-B + LT~R14D). (A) Chl a, chlorophyll a; (B) Chl b, chlorophyll b; (C) total Chl (total chlorophyll); (D) Chl a/Chl b, the ratio of chlorophyll content to chlorophyll b content. Data are the means ± SD (n = 3). Different letters indicate significant differences between samples at the same time point.
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Figure 4. Changes in antioxidant enzyme activities at different stages in E. ulmoides leaves. UV-B radiation stage (UV-1, UV-2, and UV-3); recovered for 14 days after ultraviolet radiation (UV-B~R14D); low-temperature stress after pre-UV-B treatment stage (UV-B + LT); recovered for 14 days after double treatments (UV-B + LT~R14D). (A) SOD activity; (B) CAT activity; (C) POD activity; (D) APX activity. Data are the means ± SD (n = 3). Different letters indicate significant differences between samples at the same time point.
Figure 4. Changes in antioxidant enzyme activities at different stages in E. ulmoides leaves. UV-B radiation stage (UV-1, UV-2, and UV-3); recovered for 14 days after ultraviolet radiation (UV-B~R14D); low-temperature stress after pre-UV-B treatment stage (UV-B + LT); recovered for 14 days after double treatments (UV-B + LT~R14D). (A) SOD activity; (B) CAT activity; (C) POD activity; (D) APX activity. Data are the means ± SD (n = 3). Different letters indicate significant differences between samples at the same time point.
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Figure 5. Changes in osmoregulatory substance, MDA, and superoxide anion content at different stages in E. ulmoides leaves. UV-B radiation stage (UV-1, UV-2, and UV-3); recovered for 14 days after ultraviolet radiation (UV-B~R14D); low-temperature stress after pre-UV-B treatment stage (UV-B + LT); recovered for 14 days after double treatments (UV-B + LT~R14D). (A) Soluble sugar content; (B) Soluble protein content; (C) Proline content; (D) MDA content; (E) Superoxide anion content. Data are the means ± SD (n = 3). Different letters indicate significant differences between samples at the same time point.
Figure 5. Changes in osmoregulatory substance, MDA, and superoxide anion content at different stages in E. ulmoides leaves. UV-B radiation stage (UV-1, UV-2, and UV-3); recovered for 14 days after ultraviolet radiation (UV-B~R14D); low-temperature stress after pre-UV-B treatment stage (UV-B + LT); recovered for 14 days after double treatments (UV-B + LT~R14D). (A) Soluble sugar content; (B) Soluble protein content; (C) Proline content; (D) MDA content; (E) Superoxide anion content. Data are the means ± SD (n = 3). Different letters indicate significant differences between samples at the same time point.
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Figure 6. Changes in total phenol and total flavonoid contents at different stages in E. ulmoides leaves. UV-B radiation stage (UV-1, UV-2, and UV-3); recovered for 14 days after ultraviolet radiation (UV-B~R14D); low-temperature stress after pre-UV-B treatment stage (UV-B + LT); recovered for 14 days after double treatments (UV-B + LT~R14D). (A) Total phenols content; (B) Total flavonoid content. Data are the means ± SD (n = 3). Different letters indicate significant differences between samples at the same time point.
Figure 6. Changes in total phenol and total flavonoid contents at different stages in E. ulmoides leaves. UV-B radiation stage (UV-1, UV-2, and UV-3); recovered for 14 days after ultraviolet radiation (UV-B~R14D); low-temperature stress after pre-UV-B treatment stage (UV-B + LT); recovered for 14 days after double treatments (UV-B + LT~R14D). (A) Total phenols content; (B) Total flavonoid content. Data are the means ± SD (n = 3). Different letters indicate significant differences between samples at the same time point.
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Figure 7. Changes in salicylic acid content at different stages in E. ulmoides leaves. UV-B radiation stage (UV-1, UV-2, and UV-3); recovered for 14 days after ultra-violet radiation (UV-B~R14D); low-temperature stress after pre-UV-B treatment stage (UV-B + LT); recovered for 14 days after double treatments (UV-B + LT~R14D). Different letters indicate significant differences between samples at the same time point.
Figure 7. Changes in salicylic acid content at different stages in E. ulmoides leaves. UV-B radiation stage (UV-1, UV-2, and UV-3); recovered for 14 days after ultra-violet radiation (UV-B~R14D); low-temperature stress after pre-UV-B treatment stage (UV-B + LT); recovered for 14 days after double treatments (UV-B + LT~R14D). Different letters indicate significant differences between samples at the same time point.
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Table 1. The following nine indexes were processed using the Z-score.
Table 1. The following nine indexes were processed using the Z-score.
TreatmentPlant HeightPnSS ContentSP
Content		Pro ContentSOD ActivityPOD ActivityMDA ContentSA Content
CK−0.5671.789−0.3410.103−1.7341.167−1.434−0.685−1.109
CK*−0.921−0.461−1.4271.2750.725−0.4311.1091.131−0.754
UV-1−0.610−0.4700.8030.5930.6160.8490.1940.891−0.211
UV-20.692−0.4291.089−0.8020.275−0.3050.643−0.1391.080
UV-31.407−0.429−0.124−1.1700.118−1.280−0.513−1.1990.995
CK* stands for E. ulmoides only under low temperature stress.
Table 2. Principal component extraction and analysis.
Table 2. Principal component extraction and analysis.
Component 1Component 2Component 3
Feature VectorLoad ValueFeature VectorLoad ValueFeature VectorLoad Value
Plant height0.4680.949−0.156−0.295−0.098−0.106
Pn−0.280−0.568−0.427−0.807−0.036−0.039
SS content0.2340.474−0.076−0.1430.8020.869
SP content−0.415−0.8420.2820.534−0.054−0.059
Pro content0.1800.3650.4850.9170.0460.050
SOD activity−0.376−0.763−0.154−0.2920.5320.577
POD activity0.0720.1460.5020.9490.0230.025
MDA content−0.246−0.4990.4330.8380.2010.218
SA content0.4860.9850.0330.0630.1350.146
eigenvalues4.1133.5761.176
Contribution rate (%)45.701%39.732%13.064%
Cumulative contribution rate (%)45.701%85.433%98.497%
Table 3. Principal component and comprehensive evaluation value under LT stress.
Table 3. Principal component and comprehensive evaluation value under LT stress.
TreatmentPrincipal Component ValueComposite ScoresOrder
123
CK*−2.114−2.701−0.067−2.0485
CK−1.4372.259−1.1520.0904
UV-1−0.7291.0551.3240.2593
UV-21.8010.2440.8471.0311
UV-32.479−0.858−0.9520.6682
CK* stands for E. ulmoides only under low temperature stress.
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MDPI and ACS Style

Zhang, Y.; Tian, X.; Zhou, W.; Tang, Z.; Yang, J.; Zhang, Y.; Tang, X.; Li, D.; Liu, Y. The Physiological Mechanism of Low-Temperature Tolerance Following the UV-B Radiation of Eucommia ulmoides Oliver. Agriculture 2024, 14, 878. https://doi.org/10.3390/agriculture14060878

AMA Style

Zhang Y, Tian X, Zhou W, Tang Z, Yang J, Zhang Y, Tang X, Li D, Liu Y. The Physiological Mechanism of Low-Temperature Tolerance Following the UV-B Radiation of Eucommia ulmoides Oliver. Agriculture. 2024; 14(6):878. https://doi.org/10.3390/agriculture14060878

Chicago/Turabian Style

Zhang, Ying, Xuchen Tian, Wenling Zhou, Zhonghua Tang, Jing Yang, Ye Zhang, Xiaoqing Tang, Dewen Li, and Ying Liu. 2024. "The Physiological Mechanism of Low-Temperature Tolerance Following the UV-B Radiation of Eucommia ulmoides Oliver" Agriculture 14, no. 6: 878. https://doi.org/10.3390/agriculture14060878

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