Next Article in Journal
Camellia oleifera CoSWEET10 Is Crucial for Seed Development and Drought Resistance by Mediating Sugar Transport in Transgenic Arabidopsis
Previous Article in Journal
Implications of Below-Ground Allelopathic Interactions of Camelina sativa and Microorganisms for Phosphate Availability and Habitat Maintenance
Previous Article in Special Issue
Improved SVM-Based Soil-Moisture-Content Prediction Model for Tea Plantation
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Plants
Volume 12
Issue 15
10.3390/plants12152817
plants-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Enhancing the Adaptability of Tea Plants (Camellia sinensis L.) to High-Temperature Stress with Small Peptides and Biosurfactants

by
Hao Chen
1,
Yujie Song
1,
He Li
1,
Shah Zaman
2,
Kai Fan
1,
Zhaotang Ding
2,* and
Yu Wang
1,*
1
Tea Research Institute, Qingdao Agricultural University, Qingdao 266000, China
2
Tea Research Institute, Shandong Academy of Agricultural Sciences, Jinan 250100, China
*
Authors to whom correspondence should be addressed.
Plants 2023, 12(15), 2817; https://0-doi-org.brum.beds.ac.uk/10.3390/plants12152817
Submission received: 2 July 2023 / Revised: 21 July 2023 / Accepted: 26 July 2023 / Published: 29 July 2023
(This article belongs to the Special Issue Tea Plants Response to Abiotic Stress)
Browse Figures
Review Reports Versions Notes

Abstract

:
Tea plants are highly susceptible to the adverse effects of a high-temperature climate, which can cause reduced yield and quality and even lead to plant death in severe cases. Therefore, reducing the damage caused by high-temperature stress and maintaining the photosynthetic capacity of tea plants is a critical technical challenge. In this study, we investigated the impact of small oligopeptides (small peptides) and surfactants on the high-temperature-stress tolerance of tea plants. Our findings demonstrated that the use of small peptides and surfactants enhances the antioxidant capacity of tea plants and protects their photosynthetic system. They also induce an increase in gibberellin (GA) content and a decrease in jasmonic acid (JA), strigolactone (SL), auxin (IAA), and cytokinin (CTK) content. At the same time, small peptides regulate the metabolic pathways of diterpenoid biosynthesis. Additionally, small peptides and surfactants induce an increase in L-Carnosine and N-Glycyl-L-Leucine content and a decrease in (5-L-Glutamyl)-L-Amino Acid content, and they also regulate the metabolic pathways of Beta-Alanine metabolism, Thiamine metabolism, and Glutathione metabolism. In summary, small peptides and surfactants enhance the ability of tea plants to resist high-temperature stress.

1. Introduction

With the onset of global warming, the occurrences of extreme high-temperature weather are becoming more frequent. On 13 September 2022, the World Meteorological Organization released a multi-agency report titled “United in Science”, which highlighted that the last seven years (2015–2021) were the warmest recorded and predicted a further rise in global temperatures over the next five years. Extreme high-temperature weather can have a significant impact on plant growth and development, such as reducing plant photosynthesis [1], causing male sterility [2], decreasing yield [3], increasing the likelihood of disease and pests [4], and lowering quality [5]. The tea plant, an evergreen leafy crop, typically tolerates a maximum temperature of around 34–40 °C, with a critical survival temperature of 45 °C. Unfortunately, new shoot growth is stunted when the average daily temperature exceeds 30 °C. Extreme heat waves resulting from global warming could significantly reduce tea production. It is estimated that regions in southeast China, particularly those along the Yangtze River (at approximately 30° north latitude), could experience reductions in tea yields ranging from 14% to 26% due to high-temperature stress [6]. Therefore, it is crucial to enhance the adaptability of tea plants to extreme high-temperature weather to mitigate losses.
Numerous recent studies have demonstrated the widespread involvement of small peptides as signaling molecules in the regulation of plant growth, development, immunity, and environmental adaptation [7]. Specifically, the CLAVATA3/ESR posttranslational modification of small peptides (CLE) hormone, as an extracellular signaling molecule, is widely involved in plant growth and development and responds to environmental stimuli, playing a central role in the regulation of different stem cells’ homeostasis [8]. Additionally, the small peptide hormone CLE42 acts as a negative regulator of leaf senescence. The cle42 mutant exhibits a premature senescence phenotype, while overexpression of CLE42 (CLE42ox) significantly delays the senescence process. Furthermore, exogenous application of the CLE42 mature body peptide (CLE42p) can protect leaves and significantly delay leaf senescence [9]. A signaling pathway composed of small phytocytokines (SCREWs) (small peptides) and their receptor, the kinase plant screw unresponsive receptor (NUT), inhibits the process of abscisic acid (ABA) and microbe-associated-molecular-pattern (MAMP)-induced stomatal closure and can reopen stomata [10]. Small peptides can also sense the signal of water shortage in the root and transport it to the leaves through the vascular bundle for a long distance, regulating the generation of ABA and the closure of stomata in response to drought stress [11,12]. In addition to plant hormones, small peptides can mediate the balance between plant growth and stress response [13]. Some studies have also indicated the potential of small peptides in improving crop agronomic traits, suggesting that the external application of a mixture of several small peptides can enhance crop development and resistance to stress, which is convenient and has important practical applications [14]. Despite these findings, the application of small peptides for tea plant stress resistance has not yet been reported, especially regarding the mechanism of small peptides in tea plant response to high-temperature stress, which remains unclear.
Ensuring adequate wetting of the tea plant surface is critical when applying foliar fertilizer. However, the presence of a wax layer on tea leaves can make it difficult to wet them with water alone. To overcome this challenge, surfactants have become increasingly prevalent in agriculture. These compounds not only enhance the efficiency of fertilizers and pesticides, but also create a protective film on the plant surface. This layer not only helps prevent damage to cellular membranes caused by high-temperature stress, but also improves plants’ antioxidant capacity [15,16,17,18]. Despite these benefits, further research is necessary to determine whether a combination of small peptides and surfactants could more effectively enhance tea plants’ resistance to high-temperature stress.
In the search of environmentally friendly and straightforward protection measures, we combined small peptides with various surfactants, aiming to enhance tea plants’ ability to withstand high-temperature stress. We hypothesized that biosurfactants would be more effective than chemical surfactants. This study not only elucidated the mechanism of small peptides’ response to high-temperature stress in tea plants, but also provides theoretical support for the application of small peptides and surfactants for enhancing tea plants’ resistance to high temperatures.

2. Results

2.1. Effects of Small Peptides and Surfactants on Stress-Resistance-Related Indexes of Tea Leaves under High-Temperature Stress

This study investigated how small peptides and surfactants affected stress-resistance-related indicators in tea leaves under high-temperature stress and temperature recovery across various treatment groups. After subjecting the tea leaves to three days of high-temperature stress, the untreated control group showed yellowing and slight scorching in the second leaf, while the damage observed in each treatment group was relatively minor. The leaves had a glossy appearance with a slightly sticky texture. After six days of high-temperature stress, the chlorosis in the control group was more severe, with some leaves appearing irreversibly scorched. The leaves of each treatment group displayed some degree of damage, with the P0 group being less resilient. However, each treatment group had brighter leaves compared to the control group (Figure 1). Additionally, even after three days of temperature recovery, the color contrast between the control group and each treatment group remained significant, with a decrease in leaf brightness observed in each treatment group. We propose that the tea leaves partially absorbed the small peptides and surfactants. Lastly, the survival rates of each group after the test were as follows: CK 33.33 ± 5.77% b, P0 41.67 ± 2.89% b, PT 53.33 ± 5.77% a, PR 60.00 ± 5.00% a, and PS 61.67 ± 2.89% a. These results suggest that applying small peptides and surfactants can improve the phenotypic resilience of tea leaves under high-temperature stress.
In this study, we aimed to determine how small peptides and surfactants affect stress resistance in tea leaves by measuring the activity of POD, SOD, MDA, and SS content in the leaves before high-temperature stress, three days after high-temperature stress, six days after high-temperature stress, and three days after temperature recovery (Figure 2). Our results showed that, before high-temperature stress, there were no significant differences in POD activity, SOD activity, MDA content, and SS content among the experimental groups. After three days of high-temperature stress, all groups had a significant increase in POD activity, with PT, PR, and PS showing significantly higher values than CK and P0, while P0 had significantly higher activity than CK. Additionally, SOD activity increased in all groups, with P0, PT, PR, and PS exhibiting significantly higher values than CK and PS displaying significantly greater activity than P0. These changes were accompanied by higher MDA content in CK compared to P0 and PT and significantly higher content in PR and PS relative to CK. Similarly, SS content in CK was significantly greater than P0, PT, PR, and PS. After six days of high-temperature stress, POD activity started to decline, with CK having the most-notable decrease, while P0, PT, PR, and PS maintained significantly higher activities than CK. Similarly, SOD activity in PT, PR, and PS remained significantly higher than CK and P0, with P0 having significantly higher values than CK. Concerning MDA content, CK had higher values than each treatment group, with CK being significantly higher than PS. There were no noticeable differences in SS content among the treatment groups. Following three days of temperature recovery, POD activity gradually increased in all groups, with significant differences observed between the groups. Notably, P0, PT, PR, and PS had significantly greater SOD activity than CK, with no significant differences observed in MDA and SS content among the groups, respectively.

2.2. Effects of Small Peptides and Surfactants on Photosynthetic Indexes of Tea Leaves under High-Temperature Stress

To examine the impact of small peptides and surfactants on tea leaf photosynthesis following high-temperature stress, we measured the chlorophyll a (Chl a) content, chlorophyll b (Chl b) content, the chlorophyll a/b (Chl a/b) ratio, carotenoid (Caro) content, and the maximum photochemical efficiency of photosystem II (Fv/Fm) of the leaves before and after high-temperature stress, as well as after a period of temperature recovery (Figure 3). Prior to high-temperature stress, there were no significant differences in Chl a content, Chl b content, the Chl a/b value, Caro content, and the Fv/Fm value among the treatment groups. In fact, after three days of high-temperature stress, there was no significant difference in Chl a content between groups, while CK exhibited a higher Chl b content than P0, though this difference was not significant. CK and P0 had significantly higher Chl b content than PT and PS, with CK showing significantly higher Chl b content than PT, PR, and PS. The Chl a/b value of each treatment group was higher than CK, but the difference was only significant for PT compared to CK. Caro content in each treatment group was significantly higher than CK, and the Fv/Fm value in each treatment group was significantly higher than CK. However, after six days of high-temperature stress, the Chl a content in each treatment group was higher than CK, but only P0 showed a significant increase over CK. The Chl b content in each treatment group was lower than CK, with PR and PS exhibiting significantly lower values than CK and P0. The Chl a/b value in each treatment group was higher than CK, with PS and PR exhibiting significantly higher values than CK. The Caro content in each treatment group was significantly higher than CK, and the Fv/Fm value in each treatment group was significantly higher than CK. Following three days of temperature recovery, the Chl a content in each treatment group was significantly higher than CK, while the Chl b content in each treatment group was significantly lower than CK. The Chl a/b value in each treatment group was significantly higher than CK. Furthermore, the Caro content in each treatment group was higher than CK, but this difference was not significant. The Fv/Fm value in each treatment group was significantly higher than CK. Overall, our findings imply that the use of small peptides and surfactants can slow down the decomposition of photosynthetic pigments in tea leaves under high-temperature stress.

2.3. Effects of Small Peptides and Surfactants on Phytohormones Content in Tea Leaves under High-Temperature Stress

The effect of small peptides and surfactants on the phytohormone content of tea plants under high-temperature stress in different groups after three days was also studied (Table S1). Interestingly, our results demonstrated significant differences in 13 hormone substances between P0 and CK, of which 9 were down-regulated and 4 were up-regulated. The down-regulated hormones were primarily related to IAA, CTK, and JA, whereas the up-regulated hormones were mainly related to GA. Similarly, we observed significant differences in 26 hormone substances between PT and CK, with 21 being down-regulated and 5 being up-regulated. The down-regulated hormones were mainly associated with ABA, IAA, CTK, JA, and SL, while the up-regulated hormones were primarily related to GA. We also noted significant differences in 29 hormone substances between PR and CK, with 20 being down-regulated and 9 being up-regulated. The down-regulated hormones were predominantly related to ABA, IAA, CTK, JA, and SL, while the up-regulated hormones were mainly associated with GA. Finally, we observed significant differences in 28 hormone substances between PS and CK, with 19 being down-regulated and 9 being up-regulated. The down-regulated hormones were largely related to ABA, IAA, CTK, JA, and SL, while the up-regulated hormones were primarily associated with GA.
Following our initial analysis, we conducted KEGG enrichment analysis on various hormones to gain further insight into the underlying metabolic pathways, as shown in Figure 4. Our findings revealed that the differential metabolic pathways between P0 and CK were significantly enriched in diterpenoid biosynthesis (ko00904, p < 0.05). No significantly enriched hormone metabolic pathways were found between the other treatment groups and the control group. We speculated that the use of active agents could affect the absorption and function of small peptides.

2.4. Effects of Small Peptides and Surfactants on Amino Acids in Tea Leaves under High-Temperature Stress

The determination of the amino acid analysis of tea plants in each group after three days of high temperature was also investigated in the present work (Table S1, Figure 5). Our findings revealed significant differences in 9 amino acids between P0 and CK, with 4 increasing and 5 decreasing. The amino acids with increased content were L-Carnosine, N-Glycyl-L-Leucine, L-Trypophyl-L-Glutamic Acid, and Glycylphenylalanine, while the amino acids with decreased content were L-Alanine α-Amino Acid, N-Acetylaspartate, (5-L-Glutamyl)-L-Amino Acid, and N-Acetylaspartate (Figure 5A). Similarly, we observed significant differences in 12 amino acids between PT and CK, with 5 increasing and 7 decreasing. The amino acids with increased content were N-Glycyl-L-L-Leucine, L-Carnosine, L-Cystine, Glycylphenylalanine, and Glycine, while the amino acids with decreased content were L-Asparagine Anhydrous α-Aminoadipic Acid, γ-Aminobutyric Acid, L-Alanine, (5-L-Glutamyl)-L-Amino Acid, N α-Acetyl-L-Arginine, and Beta-Alanine (Figure 5B). Additionally, we found significant differences in 10 amino acids between PR and CK, with 7 increasing and 3 decreasing. The amino acids with increased content were L-Trypophyl-L-Glutamic Acid, N-Glycyl-L-Leucine, Glycylphenylalanine, L-Tyrosine, Glycine, and L-α-Aspartyl-L-Phenylalanine, while the amino acids with decreased content were L-Alanine, (5-L-Glutamyl)-L-Amino Acid, and Beta-Alanine (Figure 5C). Lastly, we observed significant differences in 12 amino acids between PS and CK, with 9 increasing and 3 decreasing. The amino acids with increased content were L-Carnosine, L-Trypophyl-L-Glutamic Acid, N-Glycyl-L-Leucine, L-Methionine, Glycylphenylalanine, L-Cystine, L-Ornithine, L-α-Aspartyl-L-Phenylalanine, and Glycine. The amino acids with decreased content were γ-Aminobutyric Acid, (5-L-Glutamyl)-L-Amino Acid, and α-Aminoadipic Acid (Figure 5D).
Following our initial analysis, we conducted KEGG enrichment analysis on the amino acids to gain further insight into the underlying metabolic pathways, as shown in Figure 6. Our findings revealed that the differential metabolic pathways between PT and CK were significantly enriched in Beta-Alanine metabolism (ko00410, p < 0.05, Figure 7A). Moreover, our observations indicated that the differential metabolic pathways between PR and CK were mainly enriched in Thiamine metabolism (ko00730, p < 0.05, Figure 7B). Lastly, we found that the differential metabolic pathways between PS and CK were mainly enriched in Glutathione metabolism (ko00480, p < 0.05, Figure 7C).

3. Discussion

Under high-temperature stress, the tea plant’s innate active oxygen protection enzyme system plays a critical role in protecting against oxidative damage caused by reactive oxygen species. This enzyme system comprises SOD, POD, and other components that exhibit an initial increase in activity followed by a subsequent decline under high-temperature stress. The active oxygen protection enzyme system plays a vital function in preventing damage to the cellular structure and function by oxygen free radicals, thereby safeguarding cells from oxidative damage [19,20,21]. Our study found that small peptides and surfactants can significantly enhance the resistance of tea plants to high-temperature stress. Each treatment group showed higher SOD and POD activities compared to the control group, indicating that small peptides and surfactants can protect tea plants by improving the high-oxidation-system activity. Under high-temperature stress, the excessive production of reactive oxygen species exceeds the scavenging capacity of the tea plant, leading to the accumulation of reactive oxygen species, membrane lipid peroxidation, elevated MDA content, and ultimately, increased cell plasma membrane permeability [22]. Changes in plasma membrane permeability serve as an indicator of cellular injury and the extent of the damage. Our results showed that the application of small peptides and surfactants reduced the MDA content of leaves under high-temperature stress compared to the control group. Therefore, small peptides and surfactants can enhance tea plant resilience to high-temperature stress and improve survival rates by strengthening the activities of POD and SOD and reducing MDA content. These findings suggest that small peptides and surfactants can be used as effective tools to protect tea plants against high-temperature stress and improve the overall productivity and quality of tea.
High-temperature stress can result in a reduction of chlorophyll content in plant leaves, causing detrimental effects on photosynthesis in tea plants and, in severe cases, causing irreversible damage to photosynthetic protein [23]. High temperature exacerbates the hydrolysis of chlorophyll and impedes its synthesis. Additionally, the destruction of the chloroplast membrane system can lead to a decrease in chlorophyll content. Under high-temperature conditions, the photochemical maximum efficiency of photosystem II significantly decreases, leading to photoinhibition. The actual utilization and transformation ability of photosystem II also decreases, resulting in the reduction of the activity of related enzymes, thereby affecting the photosynthetic rate [24,25,26,27]. Previous studies have indicated that the Chl a/b ratio is associated with a plant’s ability to resist stress. Chl a is blue-green, while Chl b is yellow-green. A higher ratio translates to greener plant leaves and a more-stable photosynthetic system [28,29,30,31]. This study aimed to investigate the impact of exogenous small peptides and surfactants on the photosynthetic system of tea plants. Compared to the control group, small peptides and surfactants increased the content of Chl a, Caro, the value of the Chl a/b ratio, and the Fv/Fm value in tea leaves. Our findings indicated that spraying small peptides and surfactants can mitigate the damage caused to chlorophyll under high-temperature stress and alleviate the impact of high-temperature stress on the photosynthesis of tea plants.
Plants utilize various strategies to survive when faced with high-temperature stress. One such strategy involves modifications to stress phytohormones, such as ABA and SA, as well as growth-promoting phytohormones such as IAA and GA, which can significantly enhance a plant’s ability to withstand high-temperature stress. However, the use of exogenous substances can impact the expression patterns of these plant phytohormones. Thus, it is crucial to consider the potential effects of such substances on plant physiology when attempting to mitigate high-temperature stress [32,33,34,35,36,37]. This study aimed to investigate the impact of exogenous small peptides and surfactants on hormone metabolism in tea plants. GA can enhance the ability of plants to resist abiotic stress by improving the antioxidant system and alleviating the membrane lipid peroxidation process in plants [38,39,40,41,42,43,44]. Moreover, GA can induce an increase in chlorophyll content by improving the morphology of photosynthetic chromatids [45]. In our experiment, the content of GA in the treatment groups was higher than that of the control group, indicating that small peptides and surfactants could up-regulate the expression of GA and enhance the ability of tea plants to resist high-temperature stress. JA functions to inhibit plant growth, promote leaf senescence, promote stomatal closure, inhibit Rubisco biosynthesis, and affect plant absorption of N and P and the transport of organic substances such as glucose [46,47,48,49,50,51,52,53]. In our experiment, the content of JA in the treatment groups was lower than that of the control group, indicating that small peptides and surfactants could down-regulate the expression of JA and delay the senescence of tea plants under high-temperature stress, playing a protective role on tea leaves. SL is also widely involved in plant stress [54,55,56,57,58,59]. Our results showed that small peptides and surfactants down-regulate the expression of SL and enhance the adaptability of tea plants under high-temperature stress.
Under high-temperature stress, plants often turn to differentially expressed amino acids as an essential osmotic regulator to resist stress. Evidence from numerous studies shows that regulating the amino acid metabolism pathway is a successful strategy to enhance plants’ viability in adverse conditions [60,61,62,63,64]. Notably, amino acids in plants enhance their drought resistance by affecting enzyme activity [65], and metabolomics provides evidence that amino acids play a crucial role in salt stress in plants [66]. The present study aimed to investigate the effect of exogenous small peptides and surfactants on amino acid metabolism in tea plants. Our results revealed that amino acids similarly benefit tea plants’ ability to resist high-temperature stress. Specifically, the content of L-Carnosine significantly increased in the treatment groups compared to the control group. This augmentation enhances cell antioxidant capacity, prolongs cell life, and delays aging by maintaining the body’s pH balance. Moreover, Thiamine metabolism with significant differences can help plants respond quickly to external stress by increasing mitochondrial oxidation status [67,68,69]. Glutathione metabolism and Beta-Alanine metabolism can also affect the ability of plants to resist stress by affecting the antioxidant system [70,71,72].

4. Materials and Methods

4.1. Plant Materials and Experimental Treatments

In the present study, the “Longjing 43” approved national tea variety was used. The tea plants were acclimatized with standard nutrition and an appropriate pH level in a growth chamber. Each treatment of 60 tea plants was divided into three groups, each group having 20 plants. The seedling substrate had a bulk density of around 3.5%, a porosity of around 75%, and a total organic matter content of around 60%. The ideal conditions for the tea plants were a 14/10 (day/night) photoperiod, 1000Lux of light, and 70% relative humidity. After 7 days of acclimation to 28 °C/24 °C (day/night), the following parameters were carried out: (i) The tea leaves were treated with water as the control (CK). (ii) The tea leaves were treated with 6 g L−1 small peptides (P0). (iii) The tea leaves were treated with 6 g L−1 small peptides and 0.4% of the chemical surfactant tween-20 (PT). (iv) The tea leaves were treated with 6 g L−1 small peptides and 0.4% biosurfactant rhamnolipid (PR). (v) The tea leaves were treated with 6 g L−1 small peptides and 0.4% of the biosurfactant sophorolipid (PS). During the experiment, the tea plants were sprayed every five days, and after three days, the temperature was set to 42 °C/36 °C in a high-temperature environment, followed by a return to normal temperature after six days. The small peptides were provided by Shandong Tianjiu Biotechnology Co., Ltd. (Heze, China), which were made of high-purity soybean protein via enzymatic digestion, separation, concentration, sterilization, and spray drying. Its molecular weight was less than 600 Da. The rhamnolipid used in the experiment was a substance with biological metabolic properties produced by Pseudomonas or Burkholderia [73]. Sophorolipid is a microbial secondary metabolite produced by Candida using sugar and vegetable oil as carbon sources through the fermentation process under certain conditions [74,75,76]. Rhamnolipid was provided by Shaanxi Ruijie Biotechnology Co., Ltd. (Xi’an, China), and sophorolipid was provided by Shandong Yousuo Chemical Technology Co., Ltd (Heze, China). Both biosurfactants are non-toxic, harmless, biodegradable, and edible. Moreover, their industrial production has reached a high degree of maturity. During the experiment, the leaves of the same part of each group of tea plants were taken for the determination of physiological and biochemical indexes and the contents of amino acids and hormones; only 2–3 leaves of each tea plant were taken for determination.

4.2. Determination of Antioxidant Enzyme Activity, MDA and SS Content, and Survival Rate

The superoxide dismutase (SOD) activity, peroxidase (POD) activity, malondialdehyde (MDA) content, and soluble sugar (SS) content were measured at various time points during and after high-temperature stress in this study. Specifically, we measured these indicators before the onset of high-temperature stress, three days after the onset of high-temperature stress, six days after the onset of high-temperature stress, and three days after returning to normal temperature. All measurements were performed according to the scientific research kit provided by Suzhou Grace Biotechnology Co., Ltd. (Suzhou, China) (the scientific research kit number was SOD: G0101W, POD: G0107W, MDA: G0109W, SS: G0501W). The survival rate was the ratio of surviving tea plants to the total tea plants after the end of the experiment. In this experiment, the death of the tea plants was defined as all leaves withered and no buds available for further growth. A total of 60 tea plants in each treatment were divided into three groups, and the survival rate of each group was counted, respectively. The single-factor variance test was used to analyze significant differences, and the significant differences are expressed by different letters (p < 0.05).

4.3. Determination of Photosynthetic Pigment and Fv/Fm

The chlorophyll a (Chl a) content, chlorophyll b (Chl b) content, chlorophyll a/b (Chl a/b) ratio, carotenoid (Caro) content, and maximum photochemical efficiency of the photosystem II (Fv/Fm) of the tea leaves were measured at different time points under high-temperature stress. Specifically, we measured these indicators before high-temperature stress, after three days, and after six days and three days afterward returned to the usual condition. The contents of Chl a, Chl b, and Caro were determined according to the scientific research kit provided by Suzhou Grace Biotechnology Co., Ltd. (Suzhou, China) (the scientific research kit number was G0601W). For the Fv/Fm efficiency, the second developed leaf was acclimated in the dark for 30 min, and the data were calculated by using an FP110-LM/D instrument (PSI, Drásov, Czech Republic).

4.4. Determination of Phytohormones and Amino Acids

The determination of phytohormones and amino acid content was also carried out in the present work under high-temperature stress for three days. After obtaining the variable importance in projection (VIP) based on the orthogonal partial least-squares-discriminant Analysis (OPLS-DA) model, metabolites with fold change ≥ 2 and fold change ≤ 0.5 were selected, and the difference was considered significant (Fold change = the average value of the experimental group/the average value of the control group. When the average value of the control group is 0, the fold change is infinite, expressed as Inf). For the regulation of the identified metabolites in different pathways, we used the KEGG compound database (http://www.kegg.jp/kegg/compound/) (accessed on 16 December 2022) and mapped them to the KEGG pathway database (http://www.kegg.jp/kegg/pathway.html) (accessed on 16 December 2022). We mapped the significant metabolic pathways to the metabolite concentration analysis (MSEA) dataset and assessed the significance of the results by performing hypergeometric tests using the following formula:
P = 1 − ∑ i = 0 m − 1 M i N − m n − i N n
where N represents the total number of metabolites with KEGG annotations, n represents the number of differential metabolites in N, M represents the number of metabolites in a specific KEGG pathway, and m represents the number of differential metabolites in M in the KEGG pathway. The phytohormone and amino acid content was evaluated by Maiwei Biotechnology Co., Ltd. (Wuhan, China) using the AB Scienx QTRAP 6500 LC-MS/MS platform (SCIEX, Framingham, MA, USA).

4.5. Statistical Analysis

Statistical analysis was conducted using the SPSS 20.0 software (SPSS Inc., Chicago, IL, USA) and the GraphPad Prism 9.4.0 software (GraphPad Software, San Diego, CA, USA). All data are expressed as the means ± the standard deviations (n ≥ 3). The significant differences were determined by using Duncan’s multiple-range tests (p < 0.05).

5. Conclusions

Based on our findings, we concluded that the exogenous small peptides and surfactants significantly enhanced the thermotolerance of tea plants and increased their survival rate under high-temperature stress. The effectiveness of small peptides can be further boosted by surfactants, with biosurfactants such as rhamnolipid and sophorolipid exhibiting superior performance to chemical surfactants such as tween-20. Notably, there were no significant differences observed in the performance between the two biosurfactants. The primary effects of small peptides and surfactants on tea plants were as follows: (1) enhancing the antioxidant system of tea plants by increasing the activities of POD and SOD, while reducing MDA content; (2) elevating the levels of Chl a, Caro, the Chl a/b ratio, and the Fv/Fm value, thereby protecting the photosynthetic system of the tea plants; (3) up-regulating GA expression while down-regulating the expression of JA, SL, IAA, and CTK to enhance the thermotolerance of the tea plants; (4) enhancing the thermotolerance of the tea plants by inducing an increase in amino acid content such as L-Carnosine and N-Glycyl-L-Leucine and regulating metabolic pathways such as Beta-Alanine metabolism, Thiamine metabolism, and Glutathione metabolism. Overall, these findings may have practical implications for the cultivation of tea plants under high-temperature stress.

Supplementary Materials

The following Supporting Information can be downloaded at: https://0-www-mdpi-com.brum.beds.ac.uk/article/10.3390/plants12152817/s1, Table S1: Significantly different hormones and amino acids between treatment groups and the control.

Author Contributions

H.C. conducted the experiment, analyzed the data, and wrote the manuscript. Y.S. collected the samples. Z.D. and Y.W. put forward the hypotheses and designed the experiments. S.Z., Y.S. and K.F. reviewed the manuscript. H.L. participated in the experimental design and guided the research. All authors have read and agreed to the published version of the manuscript.

Funding

The research was funded by the Technology System of Modern Agricultural Industry in Shandong Province (SDAIT-19-01), the Special Foundation for Distinguished Taishan Scholar of Shandong Province (No. ts201712057), the Livelihood Project of Qingdao City (21-1-4-ny-2-nsh), the Special Talent Program of SAAS (CXGC2023A11), and the Agricultural Improved Variety Project of Shandong Province (2020LZGC010).

Data Availability Statement

The data presented in this study are available within the article.

Conflicts of Interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

References

  1. Mathur, S.; Agrawal, D.; Jajoo, A. Photosynthesis: Response to High Temperature Stress. J. Photochem. Photobiol. B Biol. 2014, 137, 116–126. [Google Scholar] [CrossRef] [PubMed]
  2. Khan, A.H.; Ma, Y.; Wu, Y.; Akbar, A.; Shaban, M.; Ullah, A.; Deng, J.; Khan, A.S.; Chi, H.; Zhu, L.; et al. High-Temperature Stress Suppresses Allene Oxide Cyclase 2 and Causes Male Sterility in Cotton by Disrupting Jasmonic Acid Signaling. Crop J. 2023, 11, 33–45. [Google Scholar] [CrossRef]
  3. Lü, G.; Wu, Y.; Bai, W.; Ma, B.; Wang, C.; Song, J. Influence of High Temperature Stress on Net Photosynthesis, Dry Matter Partitioning and Rice Grain Yield at Flowering and Grain Filling Stages. J. Integr. Agric. 2013, 12, 603–609. [Google Scholar] [CrossRef]
  4. Ullah, F.; Haq, I.; Gul, H.; Hafeez, M.; Guncan, A.; Tariq, K.; Desneux, N.; Zhao, Z.; Li, Z. Impact of Temperature Stress on Demographic Traits and Population Projection of Bactrocera dorsalis. Entomol. Gen. 2022, 42, 949–957. [Google Scholar] [CrossRef]
  5. Shi, W.; Zhang, X.; Yang, J.; Impa, S.M.; Wang, D.; Lai, Y.; Yang, Z.; Xu, H.; Wu, J.; Zhang, J.; et al. Irrigating with Cooler Water Does Not Reverse High Temperature Impact on Grain Yield and Quality in Hybrid Rice. Crop J. 2022, 11, 904–913. [Google Scholar] [CrossRef]
  6. Yan, Y.; Jeong, S.; Park, C.-E.; Mueller, N.D.; Piao, S.; Park, H.; Joo, J.; Chen, X.; Wang, X.; Liu, J.; et al. Effects of Extreme Temperature on China’s Tea Production. Environ. Res. Lett. 2021, 16, 044040. [Google Scholar] [CrossRef]
  7. Olsson, V.; Joos, L.; Zhu, S.; Gevaert, K.; Butenko, M.A.; De Smet, I. Look Closely, the Beautiful May Be Small: Precursor-Derived Peptides in Plants. Annu. Rev. Plant Biol. 2018, 70, 153–186. [Google Scholar] [CrossRef] [Green Version]
  8. Kang, J.; Wang, X.; Ishida, T.; Grienenberger, E.; Zheng, Q.; Wang, J.; Zhang, Y.; Chen, W.; Chen, M.; Song, X.-F.; et al. A Group of CLE Peptides Regulates de Novo Shoot Regeneration in Arabidopsis thaliana. New Phytol. 2022, 235, 2300–2312. [Google Scholar] [CrossRef]
  9. Zhang, Y.; Tan, S.; Gao, Y.; Kan, C.; Wang, H.; Yang, Q.; Xia, X.; Ishida, T.; Sawa, S.; Guo, H.; et al. CLE42 Delays Leaf Senescence by Antagonizing Ethylene Pathway in Arabidopsis. New Phytol. 2022, 235, 550–562. [Google Scholar] [CrossRef]
  10. Liu, Z.; Hou, S.; Rodrigues, O.; Wang, P.; Luo, D.; Munemasa, S.; Lei, J.; Liu, J.; Ortiz-Morea, F.A.; Wang, X. Phytocytokine Signalling Reopens Stomata in Plant Immunity and Water Loss. Nature 2022, 605, 332–339. [Google Scholar] [CrossRef]
  11. Takahashi, F.; Suzuki, T.; Osakabe, Y.; Betsuyaku, S.; Kondo, Y.; Dohmae, N.; Fukuda, H.; Yamaguchi-Shinozaki, K.; Shinozaki, K. A Small Peptide Modulates Stomatal Control via Abscisic Acid in Long-Distance Signalling. Nature 2018, 556, 235–238. [Google Scholar] [CrossRef] [PubMed]
  12. Christmann, A.; Grill, E. Peptide Signal Alerts Plants to Drought. Nature 2018, 556, 178–179. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  13. Ogawa-Ohnishi, M.; Yamashita, T.; Kakita, M.; Nakayama, T.; Ohkubo, Y.; Hayashi, Y.; Yamashita, Y.; Nomura, T.; Noda, S.; Shinohara, H.; et al. Peptide Ligand-Mediated Trade-off between Plant Growth and Stress Response. Science 2022, 378, 175–180. [Google Scholar] [CrossRef] [PubMed]
  14. Ormancey, M.; Guillotin, B.; Clemente, H.S.; Thuleau, P.; Plaza, S.; Combier, J.P. Use of MicroRNA-Encoded Peptides to Improve Agronomic Traits. Plant Biotechnol. J. 2021, 19, 1687–1689. [Google Scholar] [CrossRef]
  15. Appah, S.; Jia, W.; Ou, M.; Wang, P.; Asante, E.A. Analysis of Potential Impaction and Phytotoxicity of Surfactant-Plant Surface Interaction in Pesticide Application. Crop Prot. 2020, 127, 104961. [Google Scholar] [CrossRef]
  16. Sachdev, D.P.; Cameotra, S.S. Biosurfactants in Agriculture. Appl. Microbiol. Biotechnol. 2013, 97, 1005–1016. [Google Scholar] [CrossRef] [Green Version]
  17. Guo, B.-F.; Guo, Y.; Wang, J.; Zhang, L.-J.; Jin, L.-G.; Hong, H.-L.; Chang, R.-Z.; Qiu, L.-J. Co-Treatment with Surfactant and Sonication Significantly Improves Agrobacterium-Mediated Resistant Bud Formation and Transient Expression Efficiency in Soybean. J. Integr. Agric. 2015, 14, 1242–1250. [Google Scholar] [CrossRef]
  18. Wu, S.-S.; Tseng, C.-T.; Yang, Y.-H.; Liu, Y.-C.; Chang, J.-C.; Gyawali, P.; Li, Y.-H.; Yang, T.-H.; Tsai, Y.-F.; Tang, L.-C.; et al. Potential of a Combination of Entomopathogenic Fungal Strains and a Non-Ionic Surfactant to Control the Fall Armyworm (Spodoptera frugiperda). J. Asia-Pac. Entomol. 2022, 25, 102001. [Google Scholar] [CrossRef]
  19. Barman, D.; Ghimire, O.P.; Chinnusamy, V.; Kumar, R.R.; Arora, A. Amelioration of Heat Stress during Reproductive Stage in Rice by Melatonin. Indian J. Agric. Sci. 2019, 89, 91–96. [Google Scholar] [CrossRef]
  20. Wilson, R.A.; Gupta, S.; Sangha, M.K.; Kaur, G. Effect of Heat Stress on Enzymatic and Non-Enzymatic Antioxidants in Brassica rapa. J. Environ. Biol. 2019, 40, 119–124. [Google Scholar] [CrossRef]
  21. Gong, H.-L.; Chen, Q.-Q. Exogenous Sucrose Protects Potato Seedlings Against Heat Stress by Enhancing the Antioxidant Defense System. J. Soil Sci. Plant Nutr. 2021, 21, 1511–1519. [Google Scholar] [CrossRef]
  22. Yuan, X.K.; Yang, Z.Q.; Li, Y.X.; Liu, Q.; Han, W. Effects of Different Levels of Water Stress on Leaf Photosynthetic Characteristics and Antioxidant Enzyme Activities of Greenhouse Tomato. Photosynthetica 2016, 54, 28–39. [Google Scholar] [CrossRef]
  23. Chen, J.-H.; Tang, M.; Jin, X.-Q.; Li, H.; Chen, L.-S.; Wang, Q.-L.; Sun, A.-Z.; Yi, Y.; Guo, F.-Q. Regulation of Calvin–Benson Cycle Enzymes under High Temperature Stress. aBIOTECH 2022, 3, 65–77. [Google Scholar] [CrossRef] [PubMed]
  24. Ru, C.; Hu, X.; Chen, D.; Wang, W.; Song, T. Heat and Drought Priming Induce Tolerance to Subsequent Heat and Drought Stress by Regulating Leaf Photosynthesis, Root Morphology, and Antioxidant Defense in Maize Seedlings. Environ. Exp. Bot. 2022, 202, 105010. [Google Scholar] [CrossRef]
  25. Sonjaroon, W.; Jutamanee, K.; Khamsuk, O.; Thussagunpanit, J.; Kaveeta, L.; Suksamrarn, A. Impact of Brassinosteroid Mimic on Photosynthesis, Carbohydrate Content and Rice Seed Set at Reproductive Stage under Heat Stress. Agric. Nat. Resour. 2018, 52, 234–240. [Google Scholar] [CrossRef]
  26. Ru, C.; Hu, X.; Chen, D.; Wang, W.; Zhen, J. Photosynthetic, Antioxidant Activities, and Osmoregulatory Responses in Winter Wheat Differ during the Stress and Recovery Periods under Heat, Drought, and Combined Stress. Plant Sci. 2023, 327, 111557. [Google Scholar] [CrossRef]
  27. Zahra, N.; Hafeez, M.B.; Ghaffar, A.; Kausar, A.; Zeidi, M.A.; Siddique, K.H.M.; Farooq, M. Plant Photosynthesis under Heat Stress: Effects and Management. Environ. Exp. Bot. 2023, 206, 105178. [Google Scholar] [CrossRef]
  28. Ge, C.; Yu, X.; Kan, M.; Qu, C. Adaption of Ulva pertusa to Multiple-Contamination of Heavy Metals and Nutrients: Biological Mechanism of Outbreak of Ulva Sp. Green Tide. Mar. Pollut. Bull. 2017, 125, 250–253. [Google Scholar] [CrossRef]
  29. Liu, J.; Zhao, Y.; Song, H.; Chen, J.; Long, Y. Antagonism or Synergism? Combined Effects of Enhanced UV-B Radiation and Acid Rain on Photosynthesis in Seedlings of Two C4 Plants. Acta Ecol. Sin. 2020, 40, 72–80. [Google Scholar] [CrossRef]
  30. Bouargalne, Y.; Raguénès-Nicol, C.; Guilbaud, F.; Cheron, A.; Clouet, V.; Deleu, C.; Le Cahérec, F. New Insights into Chlorophyll-WSCP (Water-Soluble Chlorophyll Proteins) Interactions: The Case Study of BnD22 (Brassica napus Drought-Induced 22 KDa). Plant Physiol. Biochem. 2022, 181, 71–80. [Google Scholar] [CrossRef]
  31. Sun, M.; Zhao, C.; Shang, H.; Hao, Y.; Han, L.; Qian, K.; White, J.C.; Ma, C.; Xing, B. ZnO Quantum Dots Outperform Nanoscale and Bulk Particles for Enhancing Tomato (Solanum lycopersicum) Growth and Nutritional Values. Sci. Total Environ. 2023, 857, 159330. [Google Scholar] [CrossRef] [PubMed]
  32. Poor, P.; Nawaz, K.; Gupta, R.; Ashfaque, F.; Khan, M.I.R. Ethylene Involvement in the Regulation of Heat Stress Tolerance in Plants. Plant Cell Rep. 2022, 41, 675–698. [Google Scholar] [CrossRef] [PubMed]
  33. Prerostova, S.; Dobrev, P.I.; Kramna, B.; Gaudinova, A.; Knirsch, V.; Spichal, L.; Zatloukal, M.; Vankova, R. Heat Acclimation and Inhibition of Cytokinin Degradation Positively Affect Heat Stress Tolerance of Arabidopsis. Front. Plant Sci. 2020, 11, 87. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  34. Guo, T.; Gull, S.; Ali, M.M.; Yousef, A.F.; Ercisli, S.; Kalaji, H.M.; Telesinski, A.; Auriga, A.; Wrobel, J.; Radwan, N.S.; et al. Heat Stress Mitigation in Tomato (Solanum lycopersicum L.) through Foliar Application of Gibberellic Acid. Sci. Rep. 2022, 12, 11324. [Google Scholar] [CrossRef]
  35. Li, N.; Euring, D.; Cha, J.Y.; Lin, Z.; Lu, M.; Huang, L.-J.; Kim, W.Y. Plant Hormone-Mediated Regulation of Heat Tolerance in Response to Global Climate Change. Front. Plant Sci. 2021, 11, 627969. [Google Scholar] [CrossRef]
  36. Jha, U.C.; Nayyar, H.; Siddique, K.H.M. Role of Phytohormones in Regulating Heat Stress Acclimation in Agricultural Crops. J. Plant Growth Regul. 2022, 41, 1041–1064. [Google Scholar] [CrossRef]
  37. Da Costa, M.V.J.; Ramegowda, V.; Sreeman, S.; Nataraja, K.N. Targeted Phytohormone Profiling Identifies Potential Regulators of Spikelet Sterility in Rice under Combined Drought and Heat Stress. Int. J. Mol. Sci. 2021, 22, 11690. [Google Scholar] [CrossRef]
  38. Saleem, M.; Asghar, H.N.; Khan, M.Y.; Zahir, Z.A. Gibberellic Acid in Combination with Pressmud Enhances the Growth of Sunflower and Stabilizes Chromium(VI)-Contaminated Soil. Environ. Sci. Pollut. Res. 2015, 22, 10610–10617. [Google Scholar] [CrossRef]
  39. Hedden, P.; Thomas, S.G. Gibberellin Biosynthesis and Its Regulation. Biochem. J. 2012, 444, 11–25. [Google Scholar] [CrossRef] [Green Version]
  40. Vanstraelen, M.; Benková, E. Hormonal Interactions in the Regulation of Plant Development. Annu. Rev. Cell Dev. Biol. 2012, 28, 463–487. [Google Scholar] [CrossRef]
  41. Richards, D.E.; King, K.E.; Aitali, A.T.; Harberd, N.P. HOW GIBBERELLIN REGULATES PLANT GROWTH AND DEVELOPMENT: A Molecular Genetic Analysis of Gibberellin Signaling. Annu. Rev. Plant Physiol. Plant Mol. Biol. 2001, 52, 67–88. [Google Scholar] [CrossRef] [Green Version]
  42. Achard, P.; Gong, F.; Cheminant, S.; Alioua, M.; Hedden, P.; Genschik, P. The Cold-Inducible CBF1 Factor-Dependent Signaling Pathway Modulates the Accumulation of the Growth-Repressing DELLA Proteins via Its Effect on Gibberellin Metabolism. Plant Cell 2008, 20, 2117–2129. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  43. Magome, H.; Yamaguchi, S.; Hanada, A.; Kamiya, Y.; Oda, K. The DDF1 Transcriptional Activator Upregulates Expression of a Gibberellin-Deactivating Gene, GA2ox7, under High-Salinity Stress in Arabidopsis. Plant J. 2008, 56, 613–626. [Google Scholar] [CrossRef] [PubMed]
  44. Sun, T. The Molecular Mechanism and Evolution of the GA–GID1–DELLA Signaling Module in Plants. Curr. Biol. 2011, 21, R338–R345. [Google Scholar] [CrossRef] [Green Version]
  45. Ahmad, B.; Jaleel, H.; Shabbir, A.; Khan, M.; Haroon, Y.S. Concomitant Application of Depolymerized Chitosan and GA3 Modulates Photosynthesis, Essential Oil and Menthol Production in Peppermint (Mentha piperita L.). Sci. Hortic. 2019, 246, 371–379. [Google Scholar] [CrossRef]
  46. Pirbalouti, A.G.; Sajjadi, S.E.; Parang, K. A Review (Research and Patents) on Jasmonic Acid and Its Derivatives. Arch. Pharm. 2014, 347, 229–239. [Google Scholar] [CrossRef]
  47. Jang, G.; Yoon, Y.; Choi, Y.D. Crosstalk with Jasmonic Acid Integrates Multiple Responses in Plant Development. Int. J. Mol. Sci. 2020, 21, 305. [Google Scholar] [CrossRef] [Green Version]
  48. Kaya, A.; Doganlar, Z.B. Exogenous Jasmonic Acid Induces Stress Tolerance in Tobacco (Nicotiana tabacum) Exposed to Imazapic. Ecotox. Environ. Safe. 2016, 124, 470–479. [Google Scholar] [CrossRef]
  49. Ilyas, N.; Gull, R.; Mazhar, R.; Saeed, M.; Kanwal, S.; Shabir, S.; Bibi, F. Influence of Salicylic Acid and Jasmonic Acid on Wheat Under Drought Stress. Commun. Soil Sci. Plant Anal. 2017, 48, 2715–2723. [Google Scholar] [CrossRef]
  50. Kim, H.; Seomun, S.; Yoon, Y.; Jang, G. Jasmonic Acid in Plant Abiotic Stress Tolerance and Interaction with Abscisic Acid. Agronomy 2021, 11, 1886. [Google Scholar] [CrossRef]
  51. Kamal, A.H.M.; Komatsu, S. Jasmonic Acid Induced Protein Response to Biophoton Emissions and Flooding Stress in Soybean. J. Proteom. 2016, 133, 33–47. [Google Scholar] [CrossRef]
  52. Liu, H.; Timko, M.P. Jasmonic Acid Signaling and Molecular Crosstalk with Other Phytohormones. Int. J. Mol. Sci. 2021, 22, 2914. [Google Scholar] [CrossRef] [PubMed]
  53. Ruan, J.; Zhou, Y.; Zhou, M.; Yan, J.; Khurshid, M.; Weng, W.; Cheng, J.; Zhang, K. Jasmonic Acid Signaling Pathway in Plants. Int. J. Mol. Sci. 2019, 20, 2479. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  54. Liu, B.; Zhang, Y.; Wang, S.; Wang, W.; Xu, X.; Wu, J.; Fang, Y.; Ju, Y. Effects of Strigolactone and Abscisic Acid on the Quality and Antioxidant Activity of Grapes (Vitis vinifera L.) and Wines. Food Chem. X 2022, 16, 100496. [Google Scholar] [CrossRef] [PubMed]
  55. Wang, W.; Min, Z.; Wu, J.; Liu, B.; Xu, X.; Fang, Y.; Ju, Y. Physiological and Transcriptomic Analysis of Cabernet Sauvginon (Vitis vinifera L.) Reveals the Alleviating Effect of Exogenous Strigolactones on the Response of Grapevine to Drought Stress. Plant Physiol. Biochem. 2021, 167, 400–409. [Google Scholar] [CrossRef] [PubMed]
  56. Wang, D.-W.; Xi, Z. Strigolactone Agonists/Antagonists for Agricultural Applications: New Opportunities. Adv. Agrochem 2022, 1, 61–72. [Google Scholar] [CrossRef]
  57. Kaniganti, S.; Bhattacharya, J.; Petla, B.P.; Reddy, P.S. Strigolactone, a Neglected Plant Hormone, with a Great Potential for Crop Improvement: Crosstalk with Other Plant Hormones. Environ. Exp. Bot. 2022, 204, 105072. [Google Scholar] [CrossRef]
  58. Prandi, C.; Kapulnik, Y.; Koltai, H. Strigolactones: Phytohormones with Promising Biomedical Applications. Eur. J. Org. Chem. 2021, 2021, 4019–4026. [Google Scholar] [CrossRef]
  59. Chen, X.; Shi, X.; Ai, Q.; Han, J.; Wang, H.; Fu, Q. Transcriptomic and Metabolomic Analyses Reveal that Exogenous Strigolactones Alleviate the Response of Melon Root to Cadmium Stress. Hortic. Plant J. 2022, 8, 637–649. [Google Scholar] [CrossRef]
  60. Zamljen, T.; Medic, A.; Hudina, M.; Veberic, R.; Slatnar, A. Biostimulative Effect of Amino Acids on the Enzymatic and Metabolic Response of Two Capsicum Annuum L. Cultivars Grown under Salt Stress. Sci. Hortic. 2023, 309, 111713. [Google Scholar] [CrossRef]
  61. Ji, Y.; Yue, L.; Cao, X.; Chen, F.; Li, J.; Zhang, J.; Wang, C.; Wang, Z.; Xing, B. Carbon Dots Promoted Soybean Photosynthesis and Amino Acid Biosynthesis under Drought Stress: Reactive Oxygen Species Scavenging and Nitrogen Metabolism. Sci. Total Environ. 2023, 856, 159125. [Google Scholar] [CrossRef] [PubMed]
  62. Yang, Z.; Zhu, L.; Zhao, X.; Cheng, Y. Effects of Salinity Stress on Osmotic Pressure, Free Amino Acids, and Immune-Associated Parameters of the Juvenile Chinese Mitten Crab, Eriocheir Sinensis. Aquaculture 2022, 549, 737776. [Google Scholar] [CrossRef]
  63. Zhu, G.; Cheng, D.; Wang, X.; Guo, Q.; Zhang, Q.; Zhang, J.; Tu, Q.; Li, W. Free Amino Acids, Carbon and Nitrogen Isotopic Compositions Responses to Cadmium Stress in Two Castor (Ricinus communis L.) Species. Plant Physiol. Biochem. 2022, 184, 40–46. [Google Scholar] [CrossRef]
  64. Aydin, A.; Kurt, F.; Hürkan, K. Key Aromatic Amino Acid Players in Soybean (Glycine Max) Genome under Drought and Salt Stresses. Biocatal. Agric. Biotechnol. 2021, 35, 102094. [Google Scholar] [CrossRef]
  65. Shim, J.S.; Jeong, H.I.; Bang, S.W.; Jung, S.E.; Kim, G.; Kim, Y.S.; Redillas, M.C.F.R.; Oh, S.-J.; Seo, J.S.; Kim, J.-K. Drought-Induced Branched-Chain Amino Acid Aminotransferase Enhances Drought Tolerance in Rice. Plant Physiol. 2022, 191, 1435–1447. [Google Scholar] [CrossRef] [PubMed]
  66. Chen, Y.; Huang, W.; Zhang, F.; Luo, X.; Hu, B.; Xie, J. Metabolomic Profiling of Dongxiang Wild Rice Under Salinity Demonstrates the Significant Role of Amino Acids in Rice Salt Stress. Front. Plant Sci. 2021, 12, 729004. [Google Scholar] [CrossRef]
  67. Hamada, A.M.; Jonsson, L.M.V. Thiamine Treatments Alleviate Aphid Infestations in Barley and Pea. Phytochemistry 2013, 94, 135–141. [Google Scholar] [CrossRef]
  68. Zhou, J.; Sun, A.; Xing, D. Modulation of Cellular Redox Status by Thiamine-Activated NADPH Oxidase Confers Arabidopsis Resistance to Sclerotinia sclerotiorum. J. Exp. Bot. 2013, 64, 3261–3272. [Google Scholar] [CrossRef]
  69. Minhas, A.P.; Tuli, R.; Puri, S. Pathway Editing Targets for Thiamine Biofortification in Rice Grains. Front. Plant Sci. 2018, 9, 975. [Google Scholar] [CrossRef] [Green Version]
  70. Thanwisai, L.; Kim Tran, H.T.; Siripornadulsil, W.; Siripornadulsil, S. A Cadmium-Tolerant Endophytic Bacterium Reduces Oxidative Stress and Cd Uptake in KDML105 Rice Seedlings by Inducing Glutathione Reductase-Related Activity and Increasing the Proline Content. Plant Physiol. Biochem. 2022, 192, 72–86. [Google Scholar] [CrossRef]
  71. Ramzan, M.; Shah, A.A.; Ahmed, M.Z.; Bukhari, M.A.; Ali, L.; Casini, R.; Elansary, H.O. Exogenous Application of Glutathione and Gamma Amino-Butyric Acid Alleviates Salt Stress through Improvement in Antioxidative Defense System and Modulation of CaXTHs Stress-Related Genes. South Afr. J. Bot. 2023, 157, 266–273. [Google Scholar] [CrossRef]
  72. Devnarain, N.; Crampton, B.G.; Olivier, N.; van der Westhuyzen, C.; Becker, J.V.W.; O’Kennedy, M.M. Transcriptomic Analysis of a Sorghum Bicolor Landrace Identifies a Role for Beta-Alanine Betaine Biosynthesis in Drought Tolerance. South Afr. J. Bot. 2019, 127, 244–255. [Google Scholar] [CrossRef]
  73. Zhao, F.; Yuan, M.; Lei, L.; Li, C.; Xu, X. Enhanced Production of Mono-Rhamnolipid in Pseudomonas Aeruginosa and Application Potential in Agriculture and Petroleum Industry. Bioresour. Technol. 2021, 323, 124605. [Google Scholar] [CrossRef] [PubMed]
  74. Dierickx, S.; Castelein, M.; Remmery, J.; De Clercq, V.; Lodens, S.; Baccile, N.; De Maeseneire, S.L.; Roelants, S.L.K.W.; Soetaert, W.K. From Bumblebee to Bioeconomy: Recent Developments and Perspectives for Sophorolipid Biosynthesis. Biotechnol. Adv. 2022, 54, 107788. [Google Scholar] [CrossRef]
  75. Farias, C.B.B.; Almeida, F.C.G.; Silva, I.A.; Souza, T.C.; Meira, H.M.; Soares da Silva, R.d.C.F.; Luna, J.M.; Santos, V.A.; Converti, A.; Banat, I.M.; et al. Production of Green Surfactants: Market Prospects. Electron. J. Biotechnol. 2021, 51, 28–39. [Google Scholar] [CrossRef]
  76. Qazi, M.A.; Wang, Q.; Dai, Z. Sophorolipids Bioproduction in the Yeast Starmerella bombicola: Current Trends and Perspectives. Bioresour. Technol. 2022, 346, 126593. [Google Scholar] [CrossRef]
Plants 12 02817 g001 550
Figure 1. (A) Tea plant status treated with CK (spraying clean water on the leaf surface) after 6 days of high-temperature stress. (B) Tea plant status treated with P0 (spraying small peptides on the leaves) after 6 days of high-temperature stress. (C) The tea plant state of PT (spraying small peptides and tween-20 on the leaves) treatment after 6 days of high-temperature stress. (D) Tea plant status treated with PR (spraying small peptides and rhamnolipid on the leaves) after 6 days of high-temperature stress. (E) Tea plant status under PS (spraying small peptides and sophorolipid on the leaves) treatment after 6 days of high-temperature stress. (F) Leaf status of the second leaf of tea plants in each treatment group after 6 days of high-temperature stress.
Figure 1. (A) Tea plant status treated with CK (spraying clean water on the leaf surface) after 6 days of high-temperature stress. (B) Tea plant status treated with P0 (spraying small peptides on the leaves) after 6 days of high-temperature stress. (C) The tea plant state of PT (spraying small peptides and tween-20 on the leaves) treatment after 6 days of high-temperature stress. (D) Tea plant status treated with PR (spraying small peptides and rhamnolipid on the leaves) after 6 days of high-temperature stress. (E) Tea plant status under PS (spraying small peptides and sophorolipid on the leaves) treatment after 6 days of high-temperature stress. (F) Leaf status of the second leaf of tea plants in each treatment group after 6 days of high-temperature stress.
Plants 12 02817 g001
Plants 12 02817 g002 550
Figure 2. Peroxidase (POD) activity, superoxide dismutase (SOD) activity, malondialdehyde (MDA) content, and soluble sugar (SS) content of each treatment (CK, P0, PT, PR, and PS) before high-temperature stress, 3 days after high-temperature stress, 6 days after high-temperature stress, and 3 days after temperature recovery. Different letters indicate the significant difference between the control plant group and each treatment group under the given high-temperature stress time (p < 0.05). “0” represents before high-temperature stress; “1” represents 3 days after high-temperature stress; “2” represents 6 days after high-temperature stress; “3” represents 3 days after temperature recovery.
Figure 2. Peroxidase (POD) activity, superoxide dismutase (SOD) activity, malondialdehyde (MDA) content, and soluble sugar (SS) content of each treatment (CK, P0, PT, PR, and PS) before high-temperature stress, 3 days after high-temperature stress, 6 days after high-temperature stress, and 3 days after temperature recovery. Different letters indicate the significant difference between the control plant group and each treatment group under the given high-temperature stress time (p < 0.05). “0” represents before high-temperature stress; “1” represents 3 days after high-temperature stress; “2” represents 6 days after high-temperature stress; “3” represents 3 days after temperature recovery.
Plants 12 02817 g002
Plants 12 02817 g003 550
Figure 3. Chlorophyll a (Chl a) content, chlorophyll b (Chl b) content, chlorophyll a/chlorophyll b (Chl a/b) ratio, carotenoid (Caro) content, and Fv/Fm value among treatments (CK, P0, PT, PR, and PS) before high-temperature stress, 3 days after high-temperature stress, 6 days after high-temperature stress, and 3 days after temperature recovery. Different letters indicate the significant difference between the control plant group and each treatment group under the given high-temperature stress time (p < 0.05). “0” represents before high-temperature stress; “1” represents 3 days after high-temperature stress; “2” represents 6 days after high-temperature stress; “3” represents 3 days after temperature recovery.
Figure 3. Chlorophyll a (Chl a) content, chlorophyll b (Chl b) content, chlorophyll a/chlorophyll b (Chl a/b) ratio, carotenoid (Caro) content, and Fv/Fm value among treatments (CK, P0, PT, PR, and PS) before high-temperature stress, 3 days after high-temperature stress, 6 days after high-temperature stress, and 3 days after temperature recovery. Different letters indicate the significant difference between the control plant group and each treatment group under the given high-temperature stress time (p < 0.05). “0” represents before high-temperature stress; “1” represents 3 days after high-temperature stress; “2” represents 6 days after high-temperature stress; “3” represents 3 days after temperature recovery.
Plants 12 02817 g003
Plants 12 02817 g004 550
Figure 4. Diterpenoid biosynthesis; red represents a compound with a significant increase in content.
Figure 4. Diterpenoid biosynthesis; red represents a compound with a significant increase in content.
Plants 12 02817 g004
Plants 12 02817 g005 550
Figure 5. (A) The significant difference of amino acid expression between P0 and CK. (B) Differential amino acid expression between PT and CK. (C) Differential amino acid expression between PR and CK. (D) The radar chart of differential amino acid expression between PS and CK only shows the top 10 amino acids with the largest difference. The grid line corresponds to the value of the differential multiple, and the green shadow is composed of the line of the differential multiple corresponding to each substance.
Figure 5. (A) The significant difference of amino acid expression between P0 and CK. (B) Differential amino acid expression between PT and CK. (C) Differential amino acid expression between PR and CK. (D) The radar chart of differential amino acid expression between PS and CK only shows the top 10 amino acids with the largest difference. The grid line corresponds to the value of the differential multiple, and the green shadow is composed of the line of the differential multiple corresponding to each substance.
Plants 12 02817 g005
Plants 12 02817 g006 550
Figure 6. (A) The difference of amino acid metabolism pathway between P0 and CK. (B) The difference of amino acid metabolism pathway between PT and CK. (C) Difference of amino acid metabolism pathway between PR and CK. (D) The difference of amino acid metabolism pathway between PS and CK. The abscissa represents the corresponding Rich factor for each pathway. The Rich factor is the ratio of the number of differential metabolites in the corresponding pathway to the total number of metabolites annotated by the pathway. The higher the value, the greater the enrichment degree is. The ordinate is the path name, and the color of the point is the p-value. The redder the point, the more significant the enrichment is. The size of the dot represents the number of enriched differential metabolites. The red dotted line represents the metabolic pathway with p < 0.05.
Figure 6. (A) The difference of amino acid metabolism pathway between P0 and CK. (B) The difference of amino acid metabolism pathway between PT and CK. (C) Difference of amino acid metabolism pathway between PR and CK. (D) The difference of amino acid metabolism pathway between PS and CK. The abscissa represents the corresponding Rich factor for each pathway. The Rich factor is the ratio of the number of differential metabolites in the corresponding pathway to the total number of metabolites annotated by the pathway. The higher the value, the greater the enrichment degree is. The ordinate is the path name, and the color of the point is the p-value. The redder the point, the more significant the enrichment is. The size of the dot represents the number of enriched differential metabolites. The red dotted line represents the metabolic pathway with p < 0.05.
Plants 12 02817 g006
Plants 12 02817 g007 550
Figure 7. (A) Beta-Alanine metabolism, (B) Thiamine metabolism, and (C) Glutathione metabolism, Red represents a compound with a significant increase in content. Green represents a compound with a significantly reduced content.
Figure 7. (A) Beta-Alanine metabolism, (B) Thiamine metabolism, and (C) Glutathione metabolism, Red represents a compound with a significant increase in content. Green represents a compound with a significantly reduced content.
Plants 12 02817 g007
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Chen, H.; Song, Y.; Li, H.; Zaman, S.; Fan, K.; Ding, Z.; Wang, Y. Enhancing the Adaptability of Tea Plants (Camellia sinensis L.) to High-Temperature Stress with Small Peptides and Biosurfactants. Plants 2023, 12, 2817. https://0-doi-org.brum.beds.ac.uk/10.3390/plants12152817

AMA Style

Chen H, Song Y, Li H, Zaman S, Fan K, Ding Z, Wang Y. Enhancing the Adaptability of Tea Plants (Camellia sinensis L.) to High-Temperature Stress with Small Peptides and Biosurfactants. Plants. 2023; 12(15):2817. https://0-doi-org.brum.beds.ac.uk/10.3390/plants12152817

Chicago/Turabian Style

Chen, Hao, Yujie Song, He Li, Shah Zaman, Kai Fan, Zhaotang Ding, and Yu Wang. 2023. "Enhancing the Adaptability of Tea Plants (Camellia sinensis L.) to High-Temperature Stress with Small Peptides and Biosurfactants" Plants 12, no. 15: 2817. https://0-doi-org.brum.beds.ac.uk/10.3390/plants12152817

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop