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Article

Exogenous Application of Methyl Jasmonate at the Booting Stage Improves Rice’s Heat Tolerance by Enhancing Antioxidant and Photosynthetic Activities

by
She Tang
1,2,
Yufei Zhao
1,
Xuan Ran
1,
Hao Guo
1,
Tongyang Yin
1,
Yingying Shen
1,
Wenzhe Liu
1 and
Yanfeng Ding
1,2,*
1
College of Agronomy, Nanjing Agricultural University, Nanjing 210095, China
2
Jiangsu Collaborative Innovation Centre for Modern Crop Production, Nanjing 210095, China
*
Author to whom correspondence should be addressed.
Agronomy 2022, 12(7), 1573; https://0-doi-org.brum.beds.ac.uk/10.3390/agronomy12071573
Submission received: 27 May 2022 / Revised: 26 June 2022 / Accepted: 27 June 2022 / Published: 29 June 2022
(This article belongs to the Special Issue Advances in Rice Physioecology and Sustainable Cultivation)
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Abstract

:
With the intensification of global warming, high temperatures during rice’s growth and development could further lead to a deterioration in rice yields. Therefore, it is particularly important to further clarify the response of the rice booting stage to high temperatures, and to explore reasonable countermeasures on this basis to reduce yield losses. Methyl jasmonate (MeJA) is a derivative of jasmonates and is widely used for stress resistance. However, the role of MeJA in alleviating high temperatures during the rice booting stage has not been given enough attention. This study aimed to further evaluate the alleviation effect of methyl jasmonate on high-temperature stress during the key growth period of local conventional japonica rice. The results showed that high temperatures (37.5 °C/27.0 °C) at the booting stage had a significant impact on the antioxidant system of rice and also significantly reduced the photosynthetic capacity of the plant, resulting in a decrease in the final yields. The exogenous spraying of 0.1 mmol/L MeJA at the booting stage could effectively alleviate the influence of high-temperature stress on rice photosynthesis. Exogenous MeJA increased the stomatal conductance (Gs) of rice leaves under high-temperature stress, and correspondingly increased the transpiration rate (Tr) and decreased the organ temperature of rice plants, thereby reducing the damage to the actual photochemical efficiency (ΦPSII) caused by high temperatures. By increasing the carotenoid content (Car) and reducing the malondialdehyde content (MDA), the antioxidant capacity of the plants was restored to a certain extent under exogenous MeJA, and the yield factor showed an increase in the number of grains per panicle and the seed-setting rate of Wuyunjing 24, which alleviated the booting stage yield losses induced by high-temperature stress. In conclusion, the application of exogenous MeJA at the booting stage alleviated the negative consequences of high temperatures by enhancing the plants’ antioxidant and photosynthetic capacity. Therefore, MeJA may have a potential role in mitigating the challenges of global warming in rice production.

1. Introduction

The impact of global climate change on agricultural production has gradually emerged [1,2], and the impact of frequently high temperatures on the growth and development process of rice is more obvious, which may further lead to yield reduction [3,4]. The fifth IPCC (Intergovernmental Panel on Climate Change) assessment report of the Intergovernmental Panel on Climate Change in 2014 showed that extreme high-temperature weather will become more frequent, which would inevitably threaten food security [5]. The lower reaches of the Yangtze River in China are one of the main planting areas of japonica rice, and the probability of encountering high temperatures during the reproductive and growing period of rice in this area is increasing significantly [6]. The booting stage is an important period for the differentiation of young spikelet and organ formation in rice, which is crucial for yield formation and is also the most sensitive period to high temperatures [7,8]. High temperatures during this stage would induce the impaired development of spikelet [9,10], decreased pollen viability [11], impaired fertilization, abnormally accelerated grain filling, and ultimately reduced rice yield [12]. With the intensification of global warming, high temperatures are becoming an important threat restricting rice production [13]. Therefore, the development of effective defensive measures that could increase the heat resistance of rice is an urgent need.
Plants may resist short-term high-temperature stress, and an appropriate range of high temperatures would damage the antioxidant system itself and reduce the ability to scavenge reactive oxygen species. Under high-temperature stress conditions, the accumulation of reactive oxygen species in plant tissues leads to lipid peroxidation of the cell membrane, which changes the structure of the plasma membrane, increases the permeability of the plasma membrane, which would further induce the stability of the membrane’s deterioration, and promotes protein decomposition and denaturing [14,15]. This process is not only detrimental to the normal growth and development of plants, but also has a negative effect on the photosynthetic capacity of plants [16,17,18]. Photosynthesis refers to the physiological process in which plants convert carbon dioxide and water into organic matter and oxygen by absorbing light energy. However, the photosynthetic system is sensitive to adversity, and photosynthesis is also the primary physiological process for plants damaged by high temperatures [19]. The energy conversion of plant photosynthesis is accomplished through the synergistic action of two photosystems, photosystem I (PSI) and photosystem II (PSII) [20]. The two-system coordination mechanism formed by plants after years of evolution can be used to adapt to changes in the growth environment. In particular, PSII is the most sensitive element in the electron transport chain to heat stress, and the actual photochemical efficiency (ΦPSII) is an important chlorophyll fluorescence parameter, reflecting the potential activity of PSII, which is sensitive to high-temperature stress and is widely used as an indicator for evaluating plant heat tolerance [21,22,23]. Zhang et al. [24] showed that the reaction center of PSII could be seriously damaged in heat-sensitive varieties, and the photosynthetic rate was decreased significantly when exposed to high temperatures. Tan et al. [25] found that short-term high temperatures can lead to a significant decrease in the photon quantum yield (APY), maximum photochemical efficiency (Fv/Fm), and photosynthetic efficiency. Previous studies have found that high temperatures would induce a decrease in the Fv/Fm, ΦPSII, and electron transport rate (ETR), and an increase in non-photochemical quenching coefficients (NPQ) and other heat dissipations, and these changes ultimately lead to a decrease in plant photosynthetic efficiency, and ultimately induced a loss in crop yield [26,27,28]. Therefore, it is necessary to evaluate the impact of high temperatures on plants’ photosynthetic organs and photosynthetic efficiency and provide a research basis for the proposal of reasonable mitigation measures.
Previous studies have shown the spraying of exogenous chemical-regulating substances is an effective way to improve the stress tolerance of plants [29,30]. Jasmonates is one of those plant growth regulators that could regulate relatively well the signaling of abscisic acid and ethylene and have the potential to alleviate the heat stress damages. Methyl jasmonate (MeJA) is a derivative of jasmonates and is widely used for stress resistance in plants as a chemical regulatory substance, such as droughts, low temperatures, high temperatures, salinity, pests, and diseases [31]. According to previous studies, exogenous MeJA could effectively enhance the activities of antioxidant enzymes, soluble sugar, and proline accumulation in plants under abiotic stress [32,33,34]. Under the background of global climate warming, the probability of extreme high-temperature weather increases significantly, which will have a persistent effect on crop production. Therefore, the establishment of reasonable control measures is particularly important. Although MeJA has been extensively studied under a variety of adversities, such as hypothermia, sputum damage, and salting, there are few reports on the role of exogenous MeJA in alleviating high-temperature stress during this important period of rice booting. In our previous study, the application of exogenous MeJA at the grain filling stage could effectively improve the rice’s stress resistance and promote the increase in grain weight and the reduction in yield losses, and greatly alleviated the deterioration in rice quality under high temperatures. According to the relevant results, we believe that this measure has a positive effect on alleviating the growth and development of rice under high-temperature stress. Therefore, the purpose of this study is to further evaluate the effect of exogenous MeJA under high-temperature stress at the critical booting stage of rice, and the results are of great value for further proposing reasonable and reliable measures to deal with climate change.

2. Materials and Methods

2.1. Plant Materials, Site Description, and Experiment Design

This study was conducted at the experimental station of Nanjing Agricultural University, located at Baolin farm, Danyang City, Jiangsu province (31°54′31″ N, 119°28′21″ E). Two conventional japonica rice varieties, Wuyunjing 24 and Ningjing 3, with their excellent qualities as rice produced in the downstream of Yangtze River delta region, were used in this study. In order to facilitate the experimental treatment, the sowing dates of the two varieties were adjusted to ensure a simultaneous growth period. Plants with the same growing trend were transplanted at the three-leaf stage into plastic pots, each containing 15 kg of air-drying clay loam. The clay loam (pH = 6.3) contained 1.3 g·kg−1 total nitrogen, 110.92 mg·kg−1 available potassium, and 11.64 mg·kg−1 available phosphorus. Water and fertilizer management were based on the local accurate quantitative cultivation measures. A total of 4 treatments were conducted as follows: MeJA spraying under high temperatures (MH), water spraying under high temperatures (WH), water spraying under room temperature (CK), and MeJA spraying under room temperature (MN). Three replicates were set up for each treatment, and rice plants were high-temperature treated for seven consecutive days, started from the jointing stage, and were removed from the greenhouse to continue growing. The high-temperature treatment was 37.5 °C/27.0 °C (day/night), compared with the average natural ambient temperature of 26.1 °C/22.4 °C (day/night). The treatment duration was set to 7:00 to 19:00 during the day and 19:00 to 7:00 at night. Foliar spraying was conducted with 0.1 mmol/L MeJA purchased from Sigma-Aldrich (Sigma-Aldrich, Shanghai, China) on the day of the high-temperature treatment and on the next day between 16:00 and 17:00. MeJA solution was added with Tween-20 (0.01 mmol/L) to enhance the foliar adhesion. A ZDR-20 model temperature recorder produced by Hangzhou Zeda Instrument Co., Ltd. (Hangzhou Zeda Instrument Co., Ltd, Hangzhou, China) was used to record the temperature and humidity during the experiment.

2.2. Leaf Photosynthetic and Chlorophyll Fluorescence Parameters

The net photosynthetic rate (Pn), stomatal conductance (Gs), transpiration rate (Tr) and intercellular CO2 concentration (Ci) were measured directly in the middle of the flag leaf with the LI-6400 portable photosynthesis instrument (LI-COR BioSciences) at 9:00–11:00 a.m. The chlorophyll fluorescence parameters were determined by replacing the photosynthetic leaf chamber with the fluorescence-measuring leaf chamber. The dark reaction was used to measure the darkness of the middle part of the front leaf after 15 min of dark adaptation, and then the photochemical quenching coefficient (qP), actual photochemical efficiency (ΦPSII) and electron transport rate (ETR) were measured according to the description by Tang [29], respectively. Three replicates of relevant parameters in each treatment were measured three times to ensure the reliability of the data.

2.3. Antioxidant Capacity and Malondialdehyde (MDA) Content

At 1, 2, 4, 7, and 6 days after high-temperature treatment (day 13 post-treatment), the top 3 leaves were collected for determination of their physiological parameters. Leave samples were snap frozen in liquid nitrogen for 30 s and stored at −40 °C. Samples were homogenized with a pH = 7.0 phosphate buffer in an ice bath and then subjected to refrigerated centrifugation to obtain a crude enzyme solution for measuring antioxidant enzymes and MDA. The activity of superoxide dismutase (SOD) and peroxidase (POD) was measured with the nitro blue tetrazolium (NBT) photoreduction method [35] and guaiacol method [36], respectively; determination of the ascorbate peroxidase (APX) and catalase (CAT) was completed according to Nakano and Asada [37] and Bergmeyer [38], respectively; measurement of the MDA content was conducted with the thiobarbituric acid (TBA) method [39].

2.4. Soluble Sugar Content

Rice leaves were collected on day 1, 2, 4, 7, and 6 days after high-temperature treatment. Leaf samples were dried in a circulation oven at 105 °C for 30 min and stored in an oven at 80 °C. Detailed protocols were used according to the anthrone colorimetry method described by Zhang [40]. The mean was regarded as having soluble sugar content with three biological replicates.

2.5. Leaf Carotenoid (Car) Content

After the spectral reflectance was collected, the leaf sample was quickly placed in a fresh-keeping bag, frozen in liquid nitrogen. For the extraction and calculation of leaf Car, refer to Arnon [41] and Lichtenthaler [42]. Samples were smashed and mixed, and weighed approximately 0.10 g. The mixture was extracted with a mixture of absolute ethanol and acetone 1:1 in the dark, and absorbance at 645 and 663 nm was measured with a Hitachi (HITACHI) U-2800 UV-Vis spectrophotometer to calculate the Car content. The mean was regarded as having carotenoid content with three biological replicates.

2.6. Determination of Cytokinin (CTK) and Abscisic Acid (ABA)

The contents of CTK and ABA were determined according to the requirements of the CTK and ABA kits (Jiancheng, Nanjing, China). A 1 g sample was grinded in a liquid nitrogen quick-freeze, and then 2 ml 80% methanol solution containing 1 mmol/L di-tert-butyl-p-cresol (BTH) was added. The homogenate was transferred to a 10 mL centrifuge tube. After 4 h at 4 °C, centrifugation at 3500 r/min for 20 min was performed. The supernatant was added to the precipitate with 2 mL of the extract. After centrifugation at 4 °C for 1 h, the supernatant was combined, and the supernatant passed the C-18 solid phase extraction column. CTK and ABA were further measured by an enzyme-linked immunosorbent assay producted by SimpleStep ELISA kit (Abcam, Shanghai, China).

2.7. Yield Components, Milling Quality, and Appearance Quality

At the maturity stage, the grain number, seed setting rate, and 1000-grain weight per panicle were measured in each treatment, and the data were used to calculate the final yield for each treatment. Rice grain samples harvested at physiological maturity were air dried at room temperature before shelling and milling. The brown rice percentage (BRP) and milled rice percentage (MRP) were determined by the processing machinery SY88-TH & SY88-TRF (Wuxi Shanglong Grain Equipment Co., Ltd., Wuxi, China), according to the national standard for rice quality evaluation GB/T 17891/1999, the People’s Republic of China (NBQTC, 1999). The grain weight was measured using the one-percent balance scales. The grain size characteristics (length, width, and thickness) of brown rice were measured by a digital vernier calipers (CD-15CP; Mitutoyo Corp., Kawasaki, Japan). The chalk characteristics of brown rice were observed with a cleanliness testbed consisting of a chalky rate, chalky area, and chalkiness according to the China National Standard GB/T 17897-1999.

2.8. Statistics and Analysis

Data were analyzed as a completely randomized design following ANOVA, and the mean values were compared by Duncan’s multiple range test (DMRT) (p ≤ 0.05). Data sorting and analysis and figure preparation were performed using Microsoft Excel 2010 (Microsoft, Redmond, WA, USA) and OriginPro 8. (OriginLab, Inc., Northampton, MA, USA) SPSS 20.0 (SPSS, Inc., Chicago, IL, USA) was used for statistical analysis.

3. Results

3.1. Effects of Spraying MeJA at Booting Stage on Rice Leaf’s Temperature under High-Temperature Stress

High-temperature stress treatment at the booting stage significantly increased the temperature of the top three leaves of the two varieties. Compared with CK, spraying of exogenous MeJA had no significant effect on the leaf temperature at normal temperatures in both the Wuyunjing 24 and Ningjing 3 variety. Under high-temperature treatment conditions, exogenous MeJA significantly reduced the temperature of the top three leaves of Ningjing 3, and it had a similar effect on Wuyunjing 24, but only significantly reduced the temperature of the inverted 2nd leaves of Wuyunjing 24 (Figure 1). Compared with WH, the temperature of the inverted 1st, 2nd, 3nd leaf of Ningjing 3 is decreased by 2.32, 1.84 and 1.4 °C, respectively, by spraying MeJA, and the temperature of the inverted 2nd leaf of Wuyunjing 24 is decreased by 1.28 °C. The results showed that MeJA could reduce the temperature of high-temperature rice leaves during the booting stage, but there were differences in the effect of different varieties.

3.2. Effects of Spraying MeJA at the Booting Stage on the Photosynthesis and Chlorophyll Fluorescence Parameters of Rice under High-Temperature Stress

The results showed that high-temperature stress significantly reduced the net photosynthesis rate (Pn), stomatal conductance (Gs), and intercellular CO2 concentration (Ci) of Ningjing 3 and Wuyunjing 24. The transpiration rate showed the inconsistent performance of the two varieties under high-temperature stress (Table 1). Under normal temperatures, exogenous MeJA had no significant effect on the net photosynthesis rate and stomatal conductance. However, the intercellular CO2 concentration of Ningjing 3 and the transpiration rate of Wuyunjing 24 decreased. Under high-temperature stress conditions, the application of exogenous MeJA had significant effects on Ningjing 3. The net photosynthetic rate, stomatal conductance, intercellular CO2 concentration, and transpiration rate (Tr) of MH (high-temperature and sprayed with MeJA) treatment were increased by 15.43%, 23.27%, 8.65% and 5.23% compared to WH (high-temperature and sprayed with water), respectively. Exogenous MeJA sufficiently increased the net photosynthetic rate, stomatal conductance, and intercellular CO2 concentration in Wuyunjing 24 leaves, with an increase of 13.07%, 50.45%, 13.67%, respectively, but had no significant effect on the transpiration rate.
The actual photochemical efficiency (ΦPSII) is an important chlorophyll fluorescence parameter, reflecting the potential activity of PSII, and the ΦPSII is sensitive to high-temperature stress. Therefore, the effect of high-temperature stress on the photosynthesis system can be diagnosed according to the change in ΦPSII. Results showed that the contents of ΦPSII in the two varieties were significantly decreased on day 1 and day 3 of the high-temperature treatment (Figure 2). Specifically, ΦPSII of Ningjing 3 was decreased by 32.26% and 31.54%, respectively while ΦPSII of Wuyunjing 24 was decreased by 21.37% and 56.17%, respectively. There was no significant effect on the 2 varieties on day 6 and day 9 under the high-temperature treatment. The spraying of MeJA had no significant influence on the photosystem II under normal temperature conditions, while under high temperatures, exogenous MeJA could significantly increase the photochemical efficiency in both varieties. Among them, under a high-temperature treatment, the ΦPSII value of Ningjing 3 was increased by 24.79% on day 3, and by 39.49% on day 1 and 62.65% on day 3 for Wuyunjing 24. The results indicated that exogenous MeJA could effectively alleviate the high-temperature damages to the photosynthetic system at the rice booting stage.

3.3. Effects of Exogenous MeJA at Booting Stage on Antioxidant Capacity of Rice Leaves under High-Temperature Stress

Results indicated the superoxide dismutase (SOD) activities showed a trend of increasing first and then decreasing under the high-temperature treatment from day 1 to day 7. The activity of SOD rebounded during the recovery period (13 days after the high-temperature treatment), and the performance trends for both varieties are the same. For Ningjing 3, there was no significant difference between the natural temperature and sprayed with water (CK) and the natural temperature and sprayed with MeJA (MN) treatments during the entire experimental period. The SOD activity of the MN treatment was improved during the recovery period. During the first 2 days of the high-temperature treatment, the SOD activities of the high-temperature and sprayed with MeJA (MH) and heat stress and sprayed with water (WH) treatments were lower than that of the control CK. The SOD activities of MH and WH showed an increasing trend during the first 4 days. On the 4th day of the high-temperature treatment, the SOD activity of the MH treatment was increased by 8.90% compared with the WH treatment. However, in the late stage of the high-temperature treatment, the SOD activity under the exogenous MeJA treatment continued to be higher than that under the control treatment. The SOD activity of Wuyunjing 24 was lower in WH treatment than that of CK during the whole high-temperature treatment and the recovery period, and reached a significant level (decreased by 28.72%) on the 7th day of high-temperature treatment. There was no significant difference between the normal-temperature MH and CK treatments. The SOD activity of the MH and WH treatments were all lower than the CK. Spraying MeJA significantly increased the SOD activity by 39.32% during high-temperature stress compared with water spraying treatment at the end of the high-temperature treatment.
The catalase (CAT) activity of Wuyunjing 24 showed an overall trend of rising first and then decreasing in all four treatments. The activity of CAT was significantly higher compared to CK on the 2nd and 4th day of treatment, and the activities were increased by 28.78% and 12.53%, respectively. There was no significant difference between exogenous MeJA under the high-temperature and CK treatments, while exogenous MeJA further increased the activity of CAT on the 1st, 2nd, and 4th days by 10.57%, 7.84%, and 16.88% under the high-temperature treatment compared to the WH treatment, respectively. However, no significant difference was detected during the whole period. For Ningjing 3, the CAT activities of the WH, MH, and MN treatments all showed a trend of rising first and then decreasing. On the 4th day of the high-temperature treatment, the CAT activity of WH was significantly increased by 80.02%, and MN had an increase of 25.29% compared with CK. Exogenous MeJA significantly increased the CAT activity by 108.35% under high temperatures when compared with CK. The POD (peroxidase) activity of Wuyunjing 24 showed a tendency of decreasing first and then rising in all of the four treatments. Under normal temperatures (CK and MN), POD activity continued to decline and reached the lowest POD activity value on the 4th day of treatment. There was no significant difference in POD activity between the CK and MN treatments. Under the high-temperature treatment (MH and WH), the activity of POD continued to decrease significantly and the lowest activity value was detected on the 2nd day of treatment compared with CK. The POD activity of the MH treatment was increased by 38.98% compared with WH. During the recovery period, the POD activity of the four treatments all increased, and the POD activity of the high-temperature treatment group was significantly lower than that of CK and MN. For Ningjing 3, the POD activity of the CK and MN treatments was not significantly changed and stabilized from day 1 to day 7, while WH and MH showed an overall trend of decreasing first and then increasing. The POD activities rebounded substantially during the recovery period in all four treatments. The ascorbate peroxidase (APX) activity of both varieties showed a similar trend of rising first and then decreasing. The APX activity of Wuyunjing 24 on the 2nd, 4th, 7th, and 13th days of the high-temperature treatment were significantly lower than that of the control by 8.93%, 3.12%, 15.32%, and 30.88%, respectively. The APX activity of the MN treatment was significantly lower than that of CK on the 2nd day, and the difference was not statistically significant in other periods. Compared with WH, the APX activity of MH was increased by 23.28%, 61.43%, 12.10%, and 7.60% on days 1, 4, 7, and 13, respectively. The APX activities of the two varieties were still in a decreasing trend during the recovery period (Figure 3).

3.4. Effects of Exogenous MeJA at Booting Stage on the Content of Malondialdehyde (MDA) and Soluble Sugar of Rice Leaves under High-Temperature Stress

MDA is the product of the cell membrane after being peroxidized by reactive oxygen species and reflects the harmful effect of adversity on plants. The MDA content of both varieties showed a trend of first decreasing and then increasing during the high-temperature treatment (Figure 4). After the recovery period, the MDA content of both varieties decreased. The content of MDA in Ningjing 3 was significantly reduced during the first 4 days under high-temperature treatment (WH and MH). The content of MDA in WH was decreased by 11.26% on the 4th day under high-temperature treatment and was increased by 24.62% on day 7 compared with CK. The MDA content of the MH treatment was lower overall than WH and was reduced by 12.04% on the 7th day under high temperatures. The MDA contents of Wuyunjing 24 were increased by 70.58%, 17.06%, and 18.66% on days 2, 4, and 7 under high temperatures compared with CK. Exogenous MeJA at normal temperatures had no significant effect on the MDA content compared with the high-temperature treatment. The application of MeJA significantly reduced the content of MDA by 21.98%, 55.43%, 8.38%, and 21.38% on day 1, 2, 4, and 7 under high-temperature conditions.
Soluble sugar is a protective substance that regulates osmotic pressure and could further maintain the osmotic balance and the stability of the membrane. The results showed that high-temperature stress reduced the content of soluble sugar in leaves, and showed a downward trend with the increase in the high-temperature stress time (Figure 4). Exogenous MeJA significantly increased the soluble sugar content of Wuyunjing 24 under high temperatures compared with spraying fresh water, and the content of soluble sugar was significantly higher than that of CK during the recovery period. The change trend for the soluble sugar content of Ningjing 3 in each treatment was consistent with that of Wuyunjing 24. Compared with the normal-temperature treatment, exogenous MeJA increased the soluble sugar content in rice leaves under high temperatures. However, the difference in the recovery period was not significant compared with the other treatments.

3.5. Effects of Exogenous MeJA at the Booting Stage on the Content of Endogenous Hormone Cytokinin (CTK) and Abscisic Acid (ABA) of Rice Leaves under High-Temperature Stress

The results showed that the carotenoid (Car) content of Ningjing 3 showed a continuous downward trend after 1 to 7 days of high-temperature treatment, and its content recovered during the recovery period (Figure 5). The application of exogenous MeJA effectively increased the carotenoid content by11.80% compared to that of high temperatures. During the recovery period, the carotenoid contents of the MH and WH treatments were relatively higher than that of CK and MN. For Wuyunjing 24, the carotenoid contents of the CK, WH, and MN treatments generally showed a downward trend during the high-temperature treatment, while exogenous MeJA maintained a higher carotenoid content in rice plants under the high-temperature treatment. Compared with CK, the high-temperature treatment significantly increased the ABA content of Ningjing 3 by 20.17%. Exogenous MeJA at normal temperatures also slightly increased the ABA content compared with CK (Figure 6). In comparison, the spraying of water under high temperatures increased the ABA content by 2.65% compared with the MH treatment. The ABA content of Wuyunjing 24 in the WH treatment was slightly higher than that of the CK treatment, but the difference was not significant. The ABA content in the MN treatment was lower than that of CK, with a decrease of 3.85%. Under high-temperature treatment conditions, exogenous MeJA significantly increased the ABA content by 17.00% compared with the MH treatment. The results for the CTK contents of both varieties were increased significantly (31.25% in Ningjing 3 and 3.99% in Wuyunjing 24, respectively) under high temperatures compared with the treatment sprayed with clear water under normal temperatures. The responses of the two varieties to the exogenous MeJA at normal temperatures (MN) were inconsistent. The MN treatment significantly increased the CTK content of Ningjing 3, while the effect on Wuyunjing 24 was the opposite. The CTK content of MeJA-treated Ningjing 3 was significantly higher under high-temperature stress than that of CK, with an increase of 13.55%, but it was not significantly increased compared with WH. In addition, the application of exogenous MeJA significantly increased the CTK content of Wuyunjing 24 by 12.65% under high-temperature stress compared to that treated with clear water.

3.6. Effects of Exogenous MeJA at Booting Stage on Rice Yield and Quality under High-Temperature Stress

High temperature significantly reduced the number of grains per panicle, 1000-grain weight, and grain yield for both varieties, but had no significant effect on the panicle numbers (Table 2). In contrast, Wuyunjing 24 was less affected by high-temperature stress, with a yield loss of 43.31%, and the yield of Ningjing 3 was reduced by 48.31% compared to the CK. Under normal temperatures, exogenous MeJA significantly reduced the 1000-grain weight of 2 varieties, and had no significant effect on the panicle numbers, number of grains per panicle, and seed-setting rate. Furthermore, exogenous MeJA had no significant effect on rice yields at room temperature. Exogenous MeJA significantly improved the seed-setting rate of Wuyunjing 24 under high temperatures, while no significant effect was detected in Ningjing 3. For both varieties, the grain weight of MeJA-treated (MH) rice plants were higher than water treatment under high temperatures (WH). Exogenous MeJA significantly alleviated the yield losses of Wuyunjing 24 (20.41%) under high-temperature stress, while the yield of Ningjing 3 did not reach a significant level. The results showed that MeJA treatment could reduce the loss in rice yields caused by high-temperature stress at the booting stage, but the effect was different among different varieties. The results for rice quality indicated that exogenous MeJA at the booting stage under high temperatures significantly increased the head rice rate and reduced the chalky grain rate and chalkiness for both varieties compared to the CK. Meanwhile, exogenous MeJA significantly reduced the length and width of the rice grain, and further reduced the aspect ratio of the grain’s length/width. Exogenous application of MeJA had no significant effect on the appearance quality and milling quality of the two varieties at room temperature. Under high-temperature stress, spraying water could also significantly reduce the chalky traits and increase the percentage for the head rice rate in both varieties during the booting stage (Table 3). However, this alleviation effect in terms of quality appears to be less than that of exogenous MeJA.

4. Discussion

The global climate is undergoing a significant change characterized by warming, and the frequent occurrence of extreme climates has had a profound impact on agriculture. Rice is the staple food source of Asian residents. Therefore, in order to achieve multiple goals such as high quality and high yields, it is urgent to strengthen the research on the response and adaptation of the rice production system, and on this basis, propose a reasonable technical approach in responding to climate change. The effect of high temperatures on the physiological characteristics of rice could eventually be reflected in the grain yield and quality. According to rice’s morphological characteristics, the reproductive growth period is divided into the early reproductive growth stage (starting of panicles differentiation booting) and the middle and later stages of reproductive growth (earing-grain ripening). There is no clear boundary between the middle and late stages of reproductive growth [43]. High-temperature stress at the early reproductive growth stage (booting stage) of rice could reduce the number of spikelets per panicle, seed-setting rate, and grain weight, all of which constitute a loss in the final yield of rice [44]. From the perspective of antioxidant capacity and photosynthetic production during rice growth and development, the damages of high temperatures to the above systems are the fundamental reason for the reduction in yields. Under normal circumstances, active oxygen production and scavenging system substances in plants are in a dynamic equilibrium state. When plants were subjected to adverse stress, a large number of reactive oxygen species were induced, and cell membrane lipids would be damaged immediately by reactive oxygen species [45,46]. The reactive oxygen species (ROS) metabolism is a universal response to environmental stresses in plants. Accumulation of ROS induced by an adverse environment could seriously damage the cellular membrane and internal function components. Malondialdehyde (MDA) is one of the products of membrane lipid peroxidation, and the accumulation of MDA can be used as a physiological index to measure the extent of plant organ damage caused by adverse stress [47]. In this study, the MDA content in rice leaves was firstly decreased and then increased under the high-temperature treatment. However, the content of MDA in the MeJA treatment maintained the same level as the CK high-temperature stress, which indicated that exogenous MeJA could have a significant effect on mitigating high-temperature damages to membrane lipids. The content of MDA is closely related to the activity of antioxidant enzymes and the content of non-enzymatic antioxidants. In this study, the activities of superoxide dismutase (SOD), ascorbate peroxidase (APX), and catalase (CAT) all showed a general trend of increasing first and then decreasing under high-temperature stress conditions, which was contrary to the content changes of MDA. The increased activities of antioxidant enzymes in the early stage of high temperatures promptly removed the excess reactive oxygen. With the increase in stress periods, the capacity of antioxidant enzymes decreased, and the MDA content began to increase, further confirming the protective effect of antioxidant enzymes on the membrane system. Liu and Huang [48] reported the peroxidase (POD) activity was opposite to the activity trend of CAT and SOD. POD has similar functions to APX and CAT that can convert hydrogen peroxide into water. In this study, the POD activity under high temperatures showed an opposite tendency of decreasing first and then increasing, in contrast to the CAT, and that may be related to the antagonistic effects of the POD, APX, and CAT involved in the plant defensive systems [49]. Exogenous MeJA have been proved to have ROS-scavenging and membrane-protecting properties in various plant species, which can enhance thermotolerance by mediating the expression of genes in the antioxidant enzyme system [50,51]. Our results showed exogenous MeJA could maintain the higher activities of antioxidant enzymes under high-temperature stress, and this process could be accompanied with signaling cascades that start with signal perception and result in a variety of stress responses [52]. Carotenoids (Car) are a type of chlorophyll and an antioxidant substance, and high temperatures induced the increase in the Car content of rice leaves. The synthesis of the increased content of Car could increase the capacity of plants in removing active oxygen species [53]. The application of exogenous MeJA further increased the Car content in rice leaves, but it showed a downward trend during the later growth and development stage. This may be due to prolonged stress and senescence times in plants that further reduced the ability of plants to synthesize carotenoids [54]. The role of CTK (cytokinin) in delaying the senescence and its analogues in the improvement of plants’ stress resistance have been reported in various plant species [55]. Leaf senescence has been proved to be closely related to hormone interactions. Among them, ABA (abscisic acid) is generally thought to promote leaf senescence, while previous studies have shown that CTK can partially or completely overcome the role of ABA during this process. Plant senescence would induce the increase in the ABA content of plant organs, and decrease the CTK content transported from roots, which would further accelerate leaf senescence. In this study, the contents of ABA and CTK in Ningjing 3 and Wuyunjing 24 were significantly increased under high-temperature stress. After spraying them with MeJA, the CTK content of Wuyunjing 24 and the ABA content of both varieties were significantly increased or maintained high endogenous hormone levels under high-temperature stress, indicating that the exogenous MeJA may have balanced hormone levels under stress conditions, so as to further strengthen the protection of the leaf membrane system and chlorophyll.
Previous studies have reported that the inhibition of photosynthesis under high temperatures was mainly realized through the stomatal restriction factors, such as decreased stomatal conductance, resulting in a decreased photosynthetic rate and increased intercellular carbon dioxide concentration. Studies also found that the decline in the photosynthetic rate could also be caused by non-stomatal factors. The inactivation of Rubisco activase and the reduction in carboxylase activity [56,57], reduction in the chlorophyll a/b ratio, and reduction in the chlorophyll-proteosome binding capacity under high-temperature stress may all affect plant photosynthetic capacity [58]. Our results showed that high temperatures led to a decrease in the net photosynthetic rate of rice at the booting stage, which was related to the decrease in the stomatal conductance and intercellular carbon dioxide concentration. The destruction of photosynthetic systems by high-temperature stress mainly occurred in the reaction center of the thylakoid membrane of chloroplasts, and photosynthetic system II was extremely sensitive to high-temperature stress. In this study, the photosynthetic apparatus was damaged by the high temperatures, which further induced the significantly reduced activity of leaf photosystem II and the plant’s photosynthesis rate. Exogenous MeJA effectively alleviated the decrease in photosynthesis by reducing the temperature of the leaf under high-temperature conditions by effectively increasing the stomatal conductance and transpiration rate of the leaves. At the same time, the increased antioxidant capacity of the antioxidant system also relieves damage to the chloroplast’s cell membrane under high-temperature stress. Although there is a certain number of studies that considered the exogenous hormones as playing important roles in plant defenses against environmental stress, the “mode of action” remains unclear due to the complicated complex metabolic pathways involved in the plant growth and development process. Plant evolution contains the development of a series of highly coordinated systems and resulted in the adaptations to the stresses. This process is accompanied with signaling cascades that starts with signal perception and result in a variety of stress responses [59]. For example, stress signals are perceived by sensors located at the plasma membrane in the signal transduction pathway and result in the release or activation of various secondary messengers, such as calcium (Ca), ROS (reactive oxygen species), and inositol phosphates, which transmits the stress signals and activates downstream components, e.g., protein kinases and protein phosphatases. These proteins orchestrate the balance of protein phosphorylation and play a key role in the regulation of transcription factors (TFs), and are further involved in the physiological, biochemical, molecular, and genetic changes in plants [60,61,62,63]. Therefore, the mechanism for the increased leaf transpiration rate and reduced leaf conductance induced by exogenous MeJA still needs further evaluation.
Previous studies have mainly focused on the impact of high temperatures on rice yields during the reproductive growth stage, and there are few reports on the effect of high temperatures on rice quality formation during this period. The results of this study showed that high temperatures at the booting stage could also significantly affect the quality of rice. The head rice rate was significantly increased under high temperatures, while the grain length and width, chalkiness, and chalky grain rate were all significantly reduced (Figure 7). The decrease in chalkiness and the chalky grain rate and the increase in the head rice rate may be due to the significant decrease in the number of grains and the decreased size of individual grains under high-temperature conditions. In addition, exogenous MeJA maintained the photosynthetic capacity of rice leaves, and that ensured the assimilation supply (source) to grain, and the reduced grain number leads to a reduction in the storage capacity (sink). In this case, the assimilated supply for each grain was more abundant than under normal temperature conditions, especially the grains in the lower part of the ear, leading to the improvement in related quality traits [64]. Contrary to our expectations, the results showed that exogenous MeJA had no significant effect on rice quality under high-temperature conditions. Whether this phenomenon persists still needs to be verified, and the relevant mechanisms remain to be determined in future studies.

5. Conclusions

Under global climate change, the impact of frequent high temperatures on crop production has become increasingly apparent. Although there are differences in adversity performance due to differences in the heat tolerance of cultivars, encountering high temperatures during rice booting inevitably led to a substantial decrease in yields. Yield losses were mainly due to the decreased antioxidant and photosynthetic capacity of rice plants caused by high-temperature stress. Therefore, the exploration of reasonable and effective countermeasures is particularly important. The results of this study demonstrated that exogenous MeJA could alleviate the inhibition of photosynthesis by alleviating damage to the photosynthetic system PSII under high temperatures. Furthermore, by increasing the activities of antioxidant enzymes (SOD, POD, APX, CAT) and the content of non-enzymatic antioxidant carotenoids and endogenous hormone signals, exogenous MeJA improved the stress resistance of plants to high temperatures. Exogenous MeJA may also be involved in more complex plant stress metabolic pathways, and the mechanisms remain to be further clarified.

Author Contributions

S.T. and Y.D. conceived the experiments, S.T. designed the experiments and wrote the paper, Y.Z., X.R., H.G., T.Y., Y.S. and W.L. performed the experiments, Y.Z. edited the manuscript. All authors have read and agreed to the published version of the manuscript.

Funding

This work was funded by the National Natural Science Foundation of China (Grant No. 32071949 & 31701366). This work was also supported by the National Key R&D Program, Ministry of Science and Technology, China (Grant No. 2017YFD0300100, 2017YFD0300103 & 2017YFD0300107). We also received support from the Collaborative Innovation Center for Modern Crop Production co-sponsored by Province and Ministry (CIC-MCP) and the Fundamental Research Funds for the Central Universities, China (Grant No. KJQN201802).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Data recorded in the current study are available in all Tables and Figures of the manuscript.

Conflicts of Interest

The authors declare no conflict of interest.

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Agronomy 12 01573 g001 550
Figure 1. Leaf temperature of different treatments. Note: CK: natural temperature and sprayed with water; MN: natural temperature and sprayed with MeJA; WH: heat stress and sprayed with water; MH: high temperature and sprayed with MeJA. Bars are the standard deviation. Values followed by different letters are significantly different at the 5% probability level.
Figure 1. Leaf temperature of different treatments. Note: CK: natural temperature and sprayed with water; MN: natural temperature and sprayed with MeJA; WH: heat stress and sprayed with water; MH: high temperature and sprayed with MeJA. Bars are the standard deviation. Values followed by different letters are significantly different at the 5% probability level.
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Figure 2. Effects of exogenous MeJA on ΦPSII, ETR, and qP of rice flag leaf at the booting stage under high temperatures. Note: CK: natural temperature and sprayed with water; MN: natural temperature and sprayed with MeJA; WH: heat stress and sprayed with water; MH: high temperature and sprayed with MeJA. ΦPSII: actual photochemical efficiency; ETR: photosynthetic electron transport rate; qP: photochemical quenching coefficient. Bars are the standard deviation. Values followed by different letters are significantly different at the 5% probability level.
Figure 2. Effects of exogenous MeJA on ΦPSII, ETR, and qP of rice flag leaf at the booting stage under high temperatures. Note: CK: natural temperature and sprayed with water; MN: natural temperature and sprayed with MeJA; WH: heat stress and sprayed with water; MH: high temperature and sprayed with MeJA. ΦPSII: actual photochemical efficiency; ETR: photosynthetic electron transport rate; qP: photochemical quenching coefficient. Bars are the standard deviation. Values followed by different letters are significantly different at the 5% probability level.
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Figure 3. Effects of exogenous MeJA on the activities of SOD, POD, CAT, and APX of rice leaves at the booting stage under high temperatures. Note: CK: natural temperature and sprayed with water; MN: natural temperature and sprayed with MeJA; WH: heat stress and sprayed with water; MH: high temperature and sprayed with MeJA. SOD: superoxide dismutase; POD: peroxidase; CAT: catalase; APX: ascorbate peroxidase. Bars are the standard deviation. Values followed by different letters are significantly different at the 5% probability level.
Figure 3. Effects of exogenous MeJA on the activities of SOD, POD, CAT, and APX of rice leaves at the booting stage under high temperatures. Note: CK: natural temperature and sprayed with water; MN: natural temperature and sprayed with MeJA; WH: heat stress and sprayed with water; MH: high temperature and sprayed with MeJA. SOD: superoxide dismutase; POD: peroxidase; CAT: catalase; APX: ascorbate peroxidase. Bars are the standard deviation. Values followed by different letters are significantly different at the 5% probability level.
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Figure 4. Effects of exogenous MeJA on the content of MDA and soluble sugar of rice leaves at the booting stage under high temperatures. Note: CK: natural temperature and sprayed with water; MN: natural temperature and sprayed with MeJA; WH: heat stress and sprayed with water; MH: high temperature and sprayed with MeJA. MDA: malondialdehyde. Bars are the standard deviation. Values followed by different letters are significantly different at the 5% probability Level.
Figure 4. Effects of exogenous MeJA on the content of MDA and soluble sugar of rice leaves at the booting stage under high temperatures. Note: CK: natural temperature and sprayed with water; MN: natural temperature and sprayed with MeJA; WH: heat stress and sprayed with water; MH: high temperature and sprayed with MeJA. MDA: malondialdehyde. Bars are the standard deviation. Values followed by different letters are significantly different at the 5% probability Level.
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Figure 5. Effects of exogenous MeJA on the carotenoid content (Car) of rice leaves at the booting stage under high temperatures. Note: CK: natural temperature and sprayed with water; MN: natural temperature and sprayed with MeJA; WH: heat stress and sprayed with water; MH: high temperature and sprayed with MeJA. Bars are the standard deviation. Values followed by different letters are significantly different at the 5% probability level.
Figure 5. Effects of exogenous MeJA on the carotenoid content (Car) of rice leaves at the booting stage under high temperatures. Note: CK: natural temperature and sprayed with water; MN: natural temperature and sprayed with MeJA; WH: heat stress and sprayed with water; MH: high temperature and sprayed with MeJA. Bars are the standard deviation. Values followed by different letters are significantly different at the 5% probability level.
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Figure 6. Effects of exogenous MeJA on the content of CTK and ABA of rice leaves at the booting stage under high temperatures. Note: CK: natural temperature and sprayed with water; MN: natural temperature and sprayed with MeJA; WH: heat stress and sprayed with water; MH: high temperature and sprayed with MeJA. ABA: abscisic acid; CTK: cytokinin. Bars are the standard deviation. Values followed by different letters are significantly different at 5% probability level.
Figure 6. Effects of exogenous MeJA on the content of CTK and ABA of rice leaves at the booting stage under high temperatures. Note: CK: natural temperature and sprayed with water; MN: natural temperature and sprayed with MeJA; WH: heat stress and sprayed with water; MH: high temperature and sprayed with MeJA. ABA: abscisic acid; CTK: cytokinin. Bars are the standard deviation. Values followed by different letters are significantly different at 5% probability level.
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Figure 7. Illustration of high-temperature and exogenous MeJA on rice quality traits. Note: CK: natural temperature and sprayed with water; MN: natural temperature and sprayed with MeJA; WH: heat stress and sprayed with water; MH: high temperature and sprayed with MeJA.
Figure 7. Illustration of high-temperature and exogenous MeJA on rice quality traits. Note: CK: natural temperature and sprayed with water; MN: natural temperature and sprayed with MeJA; WH: heat stress and sprayed with water; MH: high temperature and sprayed with MeJA.
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Table
Table 1. Effects of exogenous MeJA on photosynthesis and chlorophyll fluorescence parameters under high temperatures.
Table 1. Effects of exogenous MeJA on photosynthesis and chlorophyll fluorescence parameters under high temperatures.
VarietyTreatmentsPn
(μmol·m−2·s−1)		Gs
(mol ·m−2·s−1)		Ci
(μmol·mol−1)		Tr
(mmol·m−2·s−1)
Ningjing 3CK20.27 ± 1.42 ab0.347 ± 0.01 a238.0 ± 6.56 ab5.58 ± 0.64 b
MN21.03 ± 1.61 a0.347 ± 0.0 a245.0 ± 8.19 a4.48 ± 0.14 c
WH16.20 ± 0.61 c0.245 ± 0.01 c210.5 ± 2.31 c7.27 ± 0.32 a
MH18.70 ± 0.66 b0.302 ± 0.02 b228.7 ± 1.53 b7.65 ± 0.06 a
Wuyunjing 24CK18.74 ± 0.89 a0.411 ± 0.03 a260.4 ± 16.15 a7.05 ± 1.04 a
MN20.13 ± 1.99 a0.381 ± 0.06 ab231.5 ± 2.08 b6.48 ± 0.05 a
WH16.30 ± 1.48 b0.224 ± 0.01 c203.5 ± 0.58 c6.81 ± 0.01 a
MH18.43 ± 0.75 a0.337 ± 0.04 ab231.3 ± 1.15 b7.05 ± 0.11 a
Note: CK: natural temperature and sprayed with water; MN: natural temperature and sprayed with MeJA; WH: heat stress and sprayed with water; MH: high temperature and sprayed with MeJA. Pn: net photosynthetic rate, Gs: stomatal conductance; Ci: intercellular carbon dioxide concentration; Tr: transpiration rate. Values followed by different letters are significantly different at the 5% probability level.
Table
Table 2. Effects of exogenous MeJA on rice yields and yield components under high temperatures.
Table 2. Effects of exogenous MeJA on rice yields and yield components under high temperatures.
VarietyTreatmentsPaniclesGrains per PanicleFilled Grain Rate (%)1000-Grain Weight (g)Grain Yield (g·Pot−1)
Ningjing 3CK33.27 ± 2.39 a172.59 ± 41.92 a97.60 ± 0.01 a26.30 ± 0.53 a148.41 ± 44.13 a
MN36.88 ± 1.2 a159.70 ± 3.38 a98.34 ± 0.00 a24.32 ± 0.35 b141.00 ± 9.05 a
WH34.53 ± 2.72 a96.79 ± 7.61 b97.23 ± 0.01 a23.69 ± 0.09 bc76.71 ± 3.44 b
MH35.9 ± 0.70 a97.72 ± 6.87 b97.02 ± 0.00 a23.16 ± 0.25 c78.91 ± 6.00 b
Wuyunjing 24CK30.3 ± 0.51 a185.68 ± 13.59 a96.33 ± 0.01 a26.96 ± 0.48 a129.42 ± 0.67 a
MN29.56 ± 0.87 a188.12 ± 4.75 a93.19 ± 0.01 a24.14 ± 0.96 b124.99 ± 3.13 a
WH29.47 ± 0.21 a127.18 ± 3.71 b83.29 ± 0.08 b23.62 ± 0.22 b73.36 ± 8.84 c
MH29.28 ± 0.60 a137.58 ± 7.77 b93.68 ± 0.01 a23.58 ± 0.45 b88.33 ± 3.58 b
Note: CK: natural temperature and sprayed with water; MN: natural temperature and sprayed with MeJA; WH: heat stress and sprayed with water; MH: high temperature and sprayed with MeJA. Values followed by different letters are significantly different at the 5% probability level.
Table
Table 3. Effects of exogenous MeJA on rice milling and appearance quality under high temperatures.
Table 3. Effects of exogenous MeJA on rice milling and appearance quality under high temperatures.
VarietyTreatmentsBrown Rice Rate %Milled Rice Rate %Head Rice Rate %Grain Length (mm)Grain Width (mm)Grain Length/WidthChalky Grain Rate (%)Chalkiness (%)
Ningjing 3CK83.29 ± 0.79 a71.18 ± 0.48 ab67.28 ± 0.68 b5.32 ± 0.00 a2.79 ± 0.00 a1.92 ± 0.02 a30.67 ± 1.61 a7.47 ± 1.45 a
MN82.70 ± 1.30 a69.50 ± 1.49 a65.08 ± 1.47 b5.36 ± 0.00 a2.80 ± 0.00 a1.90 ± 0.03 ab29.00 ± 1.32 a6.14 ± 2.11 a
WH83.60 ± 0.52 a72.14 ± 1.25 b69.08 ± 2.65 a5.02 ± 0.01 b2.71 ± 0.00 b1.85 ± 0.02 b7.83 ± 1.89 b0.49 ± 0.30 b
MH83.44 ± 0.21 a70.34 ± 0.27 ab69.10 ± 0.84 a5.04 ± 0.01 b2.68 ± 0.00 b1.88 ± 0.02 ab5.33 ± 1.44 b0.25 ± 0.13 b
Wuyunjing 24CK83.34 ± 0.48 ab68.35 ± 1.49 a64.46 ± 1.32 b4.64 ± 0.01 a3.11 ± 0.00 a1.49 ± 0.02 a30.00 ± 6.25 a5.86 ± 1.28 a
MN82.87 ± 0.47 b69.41 ± 2.71 a66.47 ± 3.59 ab4.65 ± 0.01 a3.09 ± 0.00 a1.51 ± 0.02 a29.67 ± 1.15 a5.56 ± 1.64 a
WH83.65 ± 0.20 a71.10 ± 0.81 a69.96 ± 1.14 a4.47 ± 0.01 b3.00 ± 0.00 b1.49 ± 0.02 a14.67 ± 0.76 b1.53 ± 0.41 b
MH83.43 ± 0.05 ab70.872.55 a69.59 ± 3.15 a4.40 ± 0.00 b2.98 ± 0.00 b1.48 ± 0.01 a9.50 ± 2.18 b1.38 ± 0.20 b
Note: CK: natural temperature and sprayed with water; MN: natural temperature and sprayed with MeJA; WH: heat stress and sprayed with water; MH: high temperature and sprayed with MeJA. Values followed by different letters are significantly different at the 5% probability level.
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Tang, S.; Zhao, Y.; Ran, X.; Guo, H.; Yin, T.; Shen, Y.; Liu, W.; Ding, Y. Exogenous Application of Methyl Jasmonate at the Booting Stage Improves Rice’s Heat Tolerance by Enhancing Antioxidant and Photosynthetic Activities. Agronomy 2022, 12, 1573. https://0-doi-org.brum.beds.ac.uk/10.3390/agronomy12071573

AMA Style

Tang S, Zhao Y, Ran X, Guo H, Yin T, Shen Y, Liu W, Ding Y. Exogenous Application of Methyl Jasmonate at the Booting Stage Improves Rice’s Heat Tolerance by Enhancing Antioxidant and Photosynthetic Activities. Agronomy. 2022; 12(7):1573. https://0-doi-org.brum.beds.ac.uk/10.3390/agronomy12071573

Chicago/Turabian Style

Tang, She, Yufei Zhao, Xuan Ran, Hao Guo, Tongyang Yin, Yingying Shen, Wenzhe Liu, and Yanfeng Ding. 2022. "Exogenous Application of Methyl Jasmonate at the Booting Stage Improves Rice’s Heat Tolerance by Enhancing Antioxidant and Photosynthetic Activities" Agronomy 12, no. 7: 1573. https://0-doi-org.brum.beds.ac.uk/10.3390/agronomy12071573

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