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Article

Salicylic Acid Reduces Wheat Yield Loss Caused by High Temperature Stress by Enhancing the Photosynthetic Performance of the Flag Leaves

by
Yonghui Fan
1,2,†,
Zhaoyan Lv
3,†,
Yuxing Li
1,2,
Boya Qin
1,2,
Qingyu Song
4,
Liangliang Ma
1,2,
Qianqian Wu
1,2,
Wenjing Zhang
1,2,
Shangyu Ma
1,2,
Chuanxi Ma
1,2,* and
Zhenglai Huang
1,2,*
1
Key Laboratory of Wheat Biology and Genetic Improvement on South Yellow and Huai River Valley, Ministry of Agriculture, Hefei 230036, China
2
College of Agronomy, Anhui Agricultural University, Hefei 230036, China
3
College of Horticulture, Anhui Agricultural University, Hefei 230036, China
4
College of Plant Protection, Anhui Agricultural University, Hefei 230036, China
*
Authors to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Agronomy 2022, 12(6), 1386; https://doi.org/10.3390/agronomy12061386
Submission received: 22 April 2022 / Revised: 31 May 2022 / Accepted: 3 June 2022 / Published: 9 June 2022
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Versions Notes

Abstract

:
High temperature stress during grain filling substantially decreases wheat productivity; thus, to ensure food security, heat tolerance in wheat must be developed. It remains unclear whether exogenous salicylic acid (SA) can induce tolerance to high temperatures in wheat at the grain-filling stage. In this study, a two-year pot culture experiment using the wheat cultivar ‘Yangmai 18’ was conducted from 2018 to 2020. The plants were pre-sprayed with SA from the heading stage (SAH), anthesis stage (SAA), 5 days after anthesis (DAA; SA5), and 10 DAA (SA10). After that, the wheat plants were subjected to high temperature stress (G) simulated using a passive warming method during the period between 15 and 19 DAA. The results showed that, compared with the normal temperature control group (NN), high temperature stress at the grain-filling stage significantly reduced the yield and photosynthetic capacity of wheat. The application of SA at different stages reduced the yield loss and the damage to the photosynthetic capacity caused by high temperature stress; the effectiveness of the treatments in descending order was SAAG > SA5G > SA10G > SAHG. Exogenous SA treatment increased the amount and proportion of dry matter distributed in the stem sheaths and leaves and grains, and decreased the amount and proportion of dry matter distributed in the rachises and glumes at the maturity stage, thereby reducing the yield loss under high temperature stress. The application of SA significantly increased the leaf area, stomatal density, chlorophyll content, soluble protein content, maximum photochemical efficiency (Fv/Fm), actual photochemical efficiency (ΦPSII), and activity of sucrose phosphate synthase (SPS) of the wheat flag leaves under high temperature stress at the grain-filling stage, thereby improving the photosynthetic performance of the flag leaves under stress. In summary, exogenous SA significantly restored the photosynthetic capacity of wheat flag leaves injured by post-anthesis high temperature stress, which effectively alleviated the inhibition of wheat growth caused by the stress and ultimately reduced the yield loss. Spraying SA at the anthesis stage had the greatest effect abating the loss of yield and reduced photosynthetic performance under high temperature stress.

1. Introduction

Due to long-term and significant greenhouse gas emissions, the temperature of the earth’s atmosphere increased by 0.6 °C in the 20th century [1] and will continue to rise by 1.4–5.8 °C in the 21st century [2]. Wheat is adapted to a cool growth environment and 18–22 °C is the suitable temperature for grain-filling [3]. In the Huanghuai wheat area, which is one of the main wheat production areas in China, high temperature and high humidity weather frequently occurs in the late stage of wheat growth. Days with an average daily temperature higher than the optimal grain-filling temperature of wheat account for 1/3 of the period from heading to maturity. Especially in the mid and late stages of grain filling, the temperature rises sharply. When there is continuous high temperature during this period, high temperature-forced maturity occurs, which causes premature senescence of the leaves, a shortened grain-filling period, and reduced grain weight [4].
Studies have shown that SA plays an important role in the response of plants to biotic or abiotic stress. For example, it activates resistant responses and induces the resistance of plants to abiotic stress such as drought [5], salinity [6], low temperature [7], ozone [8], and ultraviolet radiation [9]. SA can enhance stress resistance, reduce ethylene synthesis, and inhibit the activities of related enzymes so as to avoid the programmed cell death that can be initiated by endogenous ethylene under stress [10,11,12], thereby improving the stress resistance of plants. In cucumber, under low temperatures and weak light, SA can protect the photosynthetic system and ensure normal photosynthesis by abating the decrease in the net photosynthetic rate (Pn) and photochemical efficiency (Fv/Fm) of the leaves, thereby reducing the damage caused by the stress to plants [13]. Dawood et al. [14] reported that the application of exogenous SA induced the energy supply in olive seedlings, promoted cell growth and division, strengthened repair systems, prevented the adverse effects of the decline of organ function on plant growth, and enhanced resistance to external stress. So far, the majority of studies on the effects of exogenous SA on plants have focused on horticultural crops [15,16,17,18], while studies aimed at resolving high-temperature stress in wheat production have mostly focused on the application of plant growth regulators such as polyamines [19], trehalose [20], and abscisic acid [21]. It is still unclear if exogenous SA can induce the tolerance to high temperatures in wheat at the grain-filling stage.
Photosynthesis is the physiological process that is harmed first under high temperatures. Studies have shown that the effect of SA on the photosynthetic system under high temperature stress mainly manifests in the protection of the chloroplasts. For example, SA maintains the stability of the photosynthetic pigments and photosystems (PSI, PSII) and maintains the ability of plants to normally perform carbon assimilation so as to achieve normal growth [22]. It was reported that SA improves heat tolerance mainly by influencing the photosynthetic system and redox level in rice seedlings [23]. Ananieva et al. [22] found that after treatment with 500 µmol/L SA, barley seedlings showed an increased photosynthetic rate and a reduced level of membrane damage and membrane lipid peroxidation caused by high temperature stress, which was mainly due to the ability of SA to initiate the overall antioxidant defense system. Aftab et al. [24] treated soybean seedlings in a greenhouse with different concentrations of SA and found that after the application of 100 µmol/L SA, the photosynthetic rate of the seedlings was maintained at an increased level for 5 days. In addition, the foliar application of 100 μM exogenous SA maintained a higher photosynthetic rate, stomatal conductance (Gs), PSII efficiency, and rubisco activity in grape leaves under high temperature stress, and following the stress, SA alleviated the reduction in leaf photosynthetic rate and the damage to PSII functioning [4]. Dat et al. [25] found that high temperature hardening at 45 °C for 1 h in the dark significantly increased the SA content of the stems of mustard seedlings, and further research revealed that spraying a low concentration (100 μM) of SA on the leaves increased the activity of antioxidant enzymes, thereby enhancing the heat tolerance of mustard seedlings. Several studies have demonstrated that SA is able to enhance plant resistance to stresses, but these experiments were mostly conducted at the seedling stage, and few studies have focused on the effect of high temperature stress on the photosynthetic capacity of the wheat leaves at late growth stages.
In our study, exogenous SA was pre-sprayed at different periods, including the heading stage, anthesis stage, and 5 and 10 days after anthesis (DAA). A high-temperature environment was simulated in the middle of the grain-filling stage. The effect of the pre-application of exogenous SA under high temperature stress was investigated by evaluating the yield and yield components, dry matter accumulation and distribution, and the photosynthetic performance of the flag leaves to provide a theoretical basis for further elucidation of the mechanism of high temperature resistance and for developing suitable cultivation technology for wheat production under high temperatures.

2. Materials and Methods

2.1. Experimental Design

The experiment was carried out from 2019 to 2020 in Nongcui Garden (31.83° N, 117.24° E), an on-campus experimental base of Anhui Agricultural University, Shushan District, Hefei, Anhui Province. The field was flat and had a deep layer of yellow-brown loam with medium fertility. The soil pH value of the 0–20 cm soil layer was 6.5. The chemical characteristics of the soil in 2018–2020 are shown in Table 1.
The wheat cultivar ‘Yangmai 18′, which is a local cultivar that shows good productivity and adaptability in this area, was used in this study. The experiment adopted a pot culture technique with in situ backfilling soil (the 0–20 cm soil layer in field was used to fill polyethylene culture pots that were then embedded in the experimental field with their bottoms positioned 20 cm below the ground surface). Each culture pot (30 cm in height and 25 cm in diameter) was filled with 7.5 kg sieved soil. In order to meet the nutrient requirements of the plants, 6 g compound fertilizer (N:P:K at 17:17:17) was applied per pot. Nitrogen fertilizer was applied twice and the ratio of base fertilizer to topdressing fertilizer was 5:5. The topdressing fertilizer was applied at the jointing stage. Twenty wheat seeds were sown in each pot on 7 November 2018and 4 November 2019. At the three-leaf stage (three leaves plus one developing leaf), the seedlings were thinned to 8 plants per pot. Each treatment had 3 replicates and contained 21 pots, and the 6 treatments totaled 126 pots. The same wheat cultivar was grown in the agricultural production field around the experimental field. The planting and cultivation management followed that used for high-yield fields.
The concentration of SA applied was 0.1 mmol·L−1, which was the optimal concentration identified in a previous experiment. From the heading stage (SAH), anthesis stage (SAA), and at 5 and 10 DAA, foliar application was performed once a day at dusk (spraying for 4 days consecutively at each application time) until the adaxial and abaxial surfaces of the leaves were wet (a layer of small water droplets was formed and about to fall). The control group was sprayed with the same amount of distilled water (Table 1). The experiment adopted a randomized block design. All solutions for spraying were adjusted to pH 6.0 ± 0.1 with 1 mmol·L−1 KOH, and each 100 mL solution contained 0.02 mL Tween-20.
At 15 DAA, the control (NN) and high temperature treatment (G) were set. A passive warming shed [26,27] was used to simulate a high temperature environment. The pot-cultured plants previously sprayed with SA were treated in a high temperature environment around the clock in a warming shed for 5 days (15–19 DAA). To control the extent of the temperature increase in the shed, the plastic film cover was rolled up by 30 cm at noon daily to facilitate ventilation in the shed. The experiment contained 6 treatments. The schematic representation of experimental design and treatments is shown in Figure 1. The temperature and humidity of the air in the wheat canopy were continuously recorded every 10 min with an intelligent temperature and humidity data logger Elitech RC-4HC (Jiangsu Jingchuang Electric, Xuzhou, China). During the growing period from 2018 to 2019, the average temperature increase for high temperature stress at the grain-filling stage was 5.7 °C. During the growing period from 2019 to 2020, the average temperature increase for high temperature stress at the grain-filling stage was 6.0 °C. The temperature and humidity data during the treatment are shown in Figure 2. Following the high temperature treatment, the shed was removed to allow the wheat plants to grow under natural conditions.

2.2. Sampling Method and Measurement

Uniform spikes flowering on the same day were tagged for sampling. Twenty plants were sampled in each plot at the maturity stages. They were separated into leaf, stem, spike-stalk and glume, and grain; dried in an oven for 30 min at 105 °C; and then dried at 85 °C to obtain a constant weight for dry weight determination. At 5, 10, 15, 20, and 25 DAA, 10 tagged spikes were sampled. The flag leaves were taken from the tagged wheat plants, immediately frozen in liquid nitrogen, and then stored in a −80 °C freezer for enzyme activity determination.

2.2.1. Determination of Grain Yield and Yield Components

At the maturity stage, plants in six pots from each treatment were sampled to investigate the number of effective ears and number of grains per ear. The yield was calculated and the 1000-grain weight was determined.

2.2.2. Determination of Dry Matter Accumulation and Transportation

After anthesis, in each plot, 6 pots of wheat ears that bloomed on the same day and that had the same growth rate were selected and labeled. At the anthesis stage and maturity stage, the aboveground parts of 20 single stems of the labeled plants were sampled and their leaves, leaf sheaths and stalks, and ears (at the maturity stage the rachises and glumes and grains of the ears were separated) were separated. After treatment at 105 °C for 30 min, they were dried at 80 °C and then weighed.

2.2.3. Determination of the Net Photosynthetic Rate

The net photosynthetic rate of flag leaves was determined on the 5, 10, 15, 20, and 25 DAA. From each treatment, 12 flag leaves with the same growth state and similar light-receiving direction were sampled. A LI-6400 portable photosynthesis system (Li-Cor Inc., Lincoln, NE, USA) was used to determine the net photosynthetic rate (Pn) of the wheat leaves. The Pn was measured on the flag leaf between 9:00 p.m. and 11:00 a.m. on a sunny day. A leaf chamber equipped with a red/blue LED light source was used. All measurements were recorded at a constant flow rate of 500 mL min−1 and CO2 concentration of approximately 380 μmol mol−1, under a photosynthetically active radiation of 1000 μmol m−2 s−1 and relative humidity of 60%. During the measurements, the environmental conditions were recorded according to Sharkey et al. [28] and Mu et al. [29].

2.2.4. Stomatal Density and Leaf Area

A membrane blotting method was used to measure the stomatal density on the abaxial surface of a leaf [30,31]. Transparent nail polish was smeared on the abaxial surface of a leaf under light. After drying, the nail polish formed a membrane and was then peeled from the leaf with transparent tape and placed on a glass slide for observation under a microscope. The number of stomata was counted using a grid ocular micrometer. Ten leaves from each treatment were used to prepare the slides. the number of stomata in a field of view was counted and then the ocular micrometer was placed on the stage to measure the diameter (d) of the field of view. The area of the field of view was calculated using equation S = π(d · 2−1)2. Stomatal density was calculated based on the average number of stomata per unit area of field view. Leaf area measurements were made using a LI-3000 area meter (Li-Cor Inc., Lincoln, NE, USA).

2.2.5. Chlorophyll Fluorescence Parameters

A chlorophyll fluorometer PAM-2500 (Heinz Walz GmbH, Effeltrich, Germany) was used for measuring the chlorophyll fluorescence of the flag leaves. The minimum and maximum chlorophyll fluorescence (Fo and Fm) were measured after dark adaptation for 30 min. The steady-state chlorophyll fluorescence (Fs) was measured after the activation of an illumination of 1200 µmol m−2 s−1 for 10 min, and then a strong flash was applied and the maximum fluorescence (Fm′) under light adaptation was recorded. After, the leaves were shaded for dark adaptation for 3 s, the far-red light was turned on, and the initial fluorescence (Fo′) under light adaptation was measured. The maximum photochemical efficiency (Fv/Fm) and actual photochemical efficiency of PSII (ΦPSII) were calculated according to the method reported by Genty et al. [32].

2.2.6. Chlorophyll Content

One gram of leaf material was cut into several sections and placed in 50 mL extraction solution (acetone:ethanol v:v = 1:1) and incubated at 25 °C for 24 h under dark conditions. The absorbance of the extract was measured at 470, 663, and 645 nm wavelengths. The chlorophyll content was calculated using the equation reported by Zheng et al. [33].

2.2.7. Soluble Protein Content and Sucrose Phosphate Synthase (SPS) Activity

Soluble protein content was measured using the modified method from Bradford [34]. Frozen samples of 0.5 g were ground and placed in a sodium phosphate buffer (50 mM, pH 7.0). The extracts were centrifuged (4000× g, 10 min, and 4 °C). Soluble proteins were quantified using the supernatants of samples with bovine serum albumin as a standard. A micro-scale determination was performed using the kit BC0605 produced by Beijing Solarbio Science and Technology (Beijing, China).

2.3. Statistical Analysis

All data are expressed as the means of three replicates. One-way analysis of variance (ANOVA) was performed to compare treatments within the same year’s experiment. Differences between treatments were tested at the 0.05 probability level (p) by Duncan’s multiple range test. Statistical analyses were conducted using SPSS statistical software (SPSS ver. 10, SPSS, Chicago, IL, USA). The results were plotted using Origin 8.5(OriginLab Corporation, Northampton, MA, USA).

3. Results and Analysis

3.1. Yield and Yield Components

The data in Table 2 show that compared with NN, high temperature stress at the grain-filling stage significantly reduced the number of grains per ear, the 1000-grain weight, and the yield of wheat. Compared with NG, SA pre-spraying at different stages increased the 1000-grain weight and yield of wheat under all treatment conditions (SAHG, SAAG, SA5G and SA10G). In 2018–2019, SAAG treatment significantly increased the 1000-grain weight and yield by 13.76% and 11.48%, respectively, while SA5G significantly increased by 13.67% and 10.75%, respectively, as compared with NG. In 2019–2020, SAAG treatment significantly increased the 1000-grain weight and yield by 8.80% and 7.15%, respectively, while SA5G significantly increased by 12.89% and 7.62%, respectively, as compared with NG. This indicated that pre-spraying with SA reduced the loss of wheat yield under high temperature stress. SAAG treatment had the best remission effect of SA pre-spraying on yield loss under stress, followed by SA5G, SA10G, and SAHG accordingly. Compared with NN, high temperature stress at the grain-filling stage significantly reduced the 1000-grain weight and the number of grains per ear. The 1000-grain weight of wheat in the SAHG, SAAG, SA5G, and SA10G treatments was higher than that in NG. SA pre-spraying at the anthesis stage had the best effect on abating the reduction of the 1000-grain weight of wheat under high temperature stress at the grain-filling stage.

3.2. Distribution and Proportion of Dry Matter in the Wheat Organs at the Maturity Stage

The data in Table 3 show that compared with NN, high temperature stress at the grain-filling stage significantly reduced the amount and proportion of dry matter distributed in the stem sheaths and leaves and grains at the maturity stage, and significantly increased the amount and proportion distributed in the rachises and glumes. The amount and proportion of dry matter distributed in the stem sheaths, leaves, and grains at the maturity stage in SAHG, SAAG, SA5G, and SA10G were higher, while those in the rachises and glumes were lower than those in NG, indicating that the pre-application of SA effectively increased the accumulation of dry matter as well as the amount and proportion of dry matter distributed in those organs at the maturity stage under high temperature stress. SAAG had the best effect on abating the stress caused by the reduction of dry matter distribution in these wheat organs at the maturity stage.

3.3. Flag-Leaf Area

The flag-leaf areas in the SAAG treatment were 11.95% and 5.89% higher than in NN at 5 and 10 DAA, respectively (Figure 3). At 15 DAA, the flag-leaf area in SAHG, SAAG, SA5G, and SA10G was significantly greater by 5.36%, 13.16%, 9.13%, and 5.17%, respectively, as compared with NN. At 25 DAA, the flag-leaf area in NG was significantly lower than that in NN. The flag-leaf area in all the SA pre-spraying treatments was significantly higher than in NG; the highest increase in flag-leaf area was found in the SAAG treatment by 78.98%, indicating that SA pre-application abated the reduction of the flag-leaf area under high temperature stress. SAAG treatment was best at abating the stress causing flag-leaf area reduction, followed by SA5G, SA10G, and SAHG accordingly, which indicates that the pre-spraying of SA at the anthesis stage was the most effective approach for reducing leaf senescence under high temperature stress.

3.4. Net Photosynthetic Rate and Stomatal Density of the Flag Leaves

Figure 4A shows that at 20 DAA, the net photosynthetic rate of the flag leaves in NG was significantly lower by 35.50% compared with NN. The net photosynthetic rates of the flag leaves in SAHG, SAAG, SA5G, and SA10G were 17.40%, 30.43%, 13.79%, and 7.51% higher than in NG, respectively, indicating that pre-spraying with SA abated the decreased net photosynthetic rate of the wheat flag leaves under high temperature stress. SAAG was the most effective treatment for alleviating the stress caused by the reduction in the net photosynthetic rate of the wheat flag leaves. A similar trend was also observed regarding the stomatal density of the flag leaves in these treatments in Figure 4B. High temperature stress at the grain-filling stage significantly reduced the stomatal density of the flag leaves and pre-spraying SA at the anthesis stage resulted in the greatest increase in the stomatal density of the flag leaves under high temperature stress at the grain-filling stage, by 32.00%.

3.5. Maximum and Actual Photochemical Efficiency of the Flag Leaves

Figure 5 indicates that at 5 DAA, SAHG treatment significantly increased the Fv/Fm and ΦPSII of the flag leaves by 4.86% and 7.15%, respectively, while SAHG significantly increased by 10.04% and 12.42%, respectively, as compared with NN. At 10 DAA, the Fv/Fm and ΦPSII of the flag leaves in the SAHG, SAAG, and SA5G treatments were significantly greater than those in the control group. At 15 DAA, the Fv/Fm and ΦPSII of the flag leaves in SAHG, SAAG, SA5G, and SA10G were significantly greater than those in the control group. At 25 DAA, the maximum photochemical efficiency, actual photochemical efficiency, Fv/Fm, and ΦPSII of the wheat flag leaves in NG were significantly lower by 8.92% and 14.02%, respectively, as compared with NN. The Fv/Fm and ΦPSII of the wheat flag leaves in all the SA pre-spraying treatments were higher than those in NG; the SAAG treatment showed the highest increase by 8.04% and 12.58%, respectively, indicating that the pre-application of SA alleviated the weakening of the photosynthetic capacity of the flag leaves under high temperature stress and as a result, the stability of the photosynthetic system was maintained.

3.6. Chlorophyll Content, Soluble Protein Content, and Sucrose Phosphate Synthase (SPS) Activity of the Flag Leaves

Figure 6A shows that prior to high temperature stress at the grain-filling stage (5, 10, and 15 DAA), the chlorophyll content of the wheat flag leaves in SAHG, SAAG, SA5G, and SA10G was significantly higher than that in NN. After high temperature stress at the grain-filling stage (25 DAA), compared with NN, NG had significantly reduced chlorophyll content in the wheat flag leaves, by 31.97%. The chlorophyll content of the wheat flag leaves in all the SA pre-spraying treatments was significantly higher than that in NG, and SA pre-spraying at the anthesis stage was best at abating the reduction of chlorophyll content, by 37.14%.
Figure 6B demonstrates that at 5 DAA, SAAG treatment significantly increased the soluble protein content of the flag leaves by 12.58%, as compared with NN. At 10 DAA, the soluble protein content of the flag leaves in the SAHG, SAAG, and SA5G treatments was respectively 8.19%, 19.40%, and 11.89% higher than that in NN. At 15 DAA, the soluble protein content of the flag leaves in the SAAG, SA5G, and SA10G treatments was respectively 21.24%, 19.99%, and 10.18% higher than that in NN. At 25 DAA, compared with NN, NG significantly reduced the soluble protein content of the wheat flag leaves by 46.07%, and after SA pre-application, the soluble protein content of the wheat flag leaves was significantly higher than that in NG. Pre-application of SA at the anthesis stage (SAAG) resulted in the highest increase in soluble protein content of the wheat flag leave compared with NG, by 73.45%.
Figure 6C shows that the SPS activity of the flag leaves in the SAHG, SAAG, SA5G, and SA10G treatments before high temperature stress at the grain-filling stage (5, 10, and 15 DAA) was higher than that in NN, and the pre-application of SA at the anthesis stage resulted in significantly higher SPS activity compared with NN. After high temperature stress at the grain-filling stage (25 DAA), NG had significantly reduced SPS activity in the flag leaves compared with NN, by 60.68%. The SPS activity of the flag leaves in the SA pre-spraying treatments SAAG, SA5G, and SA10G was respectively 132.85%, 101.05%, and 57.51% higher than that in NG, and SAAG showed the best effect on alleviating the stress caused by decrease in SPS activity, followed by SA5G, SA10G, and SAHG accordingly.

4. Discussion

In recent years, against the backdrop of global warming, events such as heat damage and severe yield reduction or harvest failure have become increasingly frequent. Managing the impact of high temperature damage on crop production and improving the heat resistance of crops have become pertinent research topics in crop science. Several studies have shown that the use of exogenous substances to induce heat resistance in crops may represent an important breakthrough and countermeasure in enhancing crop heat resistance [35]. Studies have demonstrated that the application of exogenous SA significantly increases the yield of wheat under water logging conditions [36], promotes the growth and increases the yield of salt-tolerant spring wheat under controlled salt stress conditions in pots [37], and increases barley yield under salinity conditions in the field [38]. The influence of exogenous SA on stress resistance was also confirmed in our study. We found that exogenous SA significantly increased the yield of wheat under high temperature stress, and SA pre-application at the anthesis stage was the best at abating the reduction in wheat yield caused by high temperature stress at the grain-filling stage. In the present study, compared with NG, pre-spraying SA significantly increased the yield of wheat under all treatment conditions (by 2.34%, 13.67%, 10.75%, and 6.60% in SAHG, SAAG, SA5G, and SA10G, respectively). SA is an economical exogenous substance costing approximately $4.0 per 500 g. We calculated the expenses associated with SA spaying and yield loss based on real-time SA and wheat prices. At the concentration of SA used in the present experiments, the cost of SA is approximately 0.40 USD hm−2 [39,40]. Converting potted yields to field yields according to the seeding density in field production (2.25 × 106 seeds hm−2), we found that, compared with the high temperature treatment without SA spraying (NG), the yield under SA pre-spraying at different stages can be increased by approximately 2.34% (SAHG)–13.67% (SAAG), and the economic loss reduction is higher than the price of SA. That is, the expenses associated with SA spraying are compensated by avoiding yield loss due to high temperatures. “Source” and “sink” are the two aspects of yield formation. The yield depends not only on the capacity of the “sink,” but also on the production of the “source” and the transportation capacity of photosynthetic products [41]. High temperature stress inhibits the photosynthesis of the leaves, which are the “source” organs, resulting in insufficient “source” material for grain-filling and a decrease in dry matter accumulation in wheat [42,43]. In our study, after high temperature stress, the amount and proportion of dry matter distributed to the stem sheaths and leaves and grains significantly decreased, while the amount and proportion of dry matter distributed to the rachises and glumes increased significantly at the maturity stage, indicating that high temperature stress at the grain-filling stage affected the dry matter accumulation in the wheat organs and ultimately influenced wheat yield. This might be because high temperature stress caused damage to the wheat photosynthetic organs, resulting in the production of peroxides and causing failure in the conversion of nutrients to dry matter in non-reproductive organs such as the leaves and stem sheaths [44,45]. Plaut et al. [46] reported that post-anthesis high temperature stress reduces the photosynthetic rate in the leaves, resulting in a decrease in the rate of dry matter accumulation, ultimately affecting the size of the grains. The results of our study showed that SA pre-application increased the transport of dry matter from the rachises and glumes to the grains, which was conducive to alleviating the grain weight and yield loss under high temperature stress.
Zhu et al. [47] suggested that the level of photosynthetic efficiency is an important indicator of crop yield. High temperature stress inhibits plant growth and causes the accumulation of secondary metabolites, degradation of chlorophyll, and damage of the photosynthetic system, resulting in the low efficiency of the PSII reaction center in absorbing, transferring, and converting light energy, ultimately causing a decrease in the photosynthetic rate [48,49,50,51]. Zheng et al. [52] noted that SA protected the photosynthetic system of wheat under high temperature and strong light. In our study, exogenous SA abated the reduction of wheat flag-leaf area under high temperature stress and the loss of the effective area of the flag leaves for capturing light energy, thereby delaying the senescence of the flag leaves. Chlorophyll and carotenoids are the major pigments in plant photosynthesis, and chlorophyll plays a critical role in the absorption, transmission, and transformation of light energy. Our study showed that the chlorophyll content and soluble protein content of the plants decreased under high temperature stress, and exogenous SA pre-application abated the reduction in chlorophyll content of the wheat flag leaves under high temperature stress. SA increased the net photosynthetic rate and chlorophyll content of the flag leaves, which may be due to the participation of SA in protecting the integrity of the chloroplast membrane structure and regulating the balance of the antioxidant system in the chloroplasts. PSII is the primary site of photo-inhibitory damage [53,54]. We found that high temperature stress significantly decreased the Fv/Fm of the leaves and that spraying of exogenous SA significantly increased the Fv/Fm of the wheat flag leaves under high temperature stress. By increasing the Fv/Fm and ΦPSII of the wheat flag leaves, application of exogenous SA improved the potential photosynthetic capacity and light energy utilization efficiency, laying a foundation for the accumulation of photosynthetic products and delayed the rate of flag leaf senescence, thereby maintaining the stability of the photosynthetic system [55]. In our study, SA treatment increased the stomatal density, which allowed the plants to effectively absorb and retain water and prevented dehydration damage to the plants by controlling the excessive evaporation of water to ensure water supply to the leaves for photosynthesis under high temperature stress. SA abated the decline of the number of stomata, which resulted in a higher level of carbon dioxide fixation and organic matter accumulation, leading to a reduction of yield loss [56,57]. Yang et al. [58] found that under high temperature stress, plants showed closed stomata, damaged chloroplasts, and decreased chlorophyll content. SA causes the production of a large number of heat shock proteins (HSPs) under heat stress, which help the plant to maintain the activity of antioxidant enzymes, reduce the oxidative stress damage induced by high temperature, ensure the stability of cell membranes, and enhance the ability of the chloroplasts to absorb and utilize light energy. As a result, damage to chloroplasts caused by high temperature stress was alleviated and the heat resistance of plants improved. Following SA pre-application, the chlorophyll content, stomatal density, and flag-leaf area of the wheat plants increased and the potential photosynthetic capacity and light energy utilization efficiency of the photosynthetic system were improved, which ensured the normal functioning of photosynthesis, promoted the formation and transport of photosynthetic products, and increased the accumulation of dry matter. Therefore, the yield loss under high temperature stress was abated.
Soluble protein, an important osmotic regulator in plant cells, plays an important role in plant metabolism, growth, and development, and the heat resistance of plants is related to the rate of protein synthesis and degradation. Due to its strong hydrophilicity, increases in soluble protein under high temperature stress are beneficial for maintaining the intracellular water balance [59,60]. Studies have shown that high temperature stress reduces the soluble protein content in wheat [61]. As an osmotic substance, soluble protein has a role in maintaining the cell membrane. High temperature stress results in decreased soluble protein content and increased levels of reactive oxygen species, which damages the cell membranes [62]. Zhu et al. [63] found that with the extension of the duration of high temperature stress, soybean seedlings showed a significantly lower soluble protein content compared with the control group. In our study, the soluble protein content of wheat decreased under high temperature stress, and after SA pretreatment, the soluble protein content of the wheat flag leaves was significantly higher than that under high temperature stress. The soluble protein content of plant leaves reflects nitrogen accumulation, and nitrogen content has a significant positive correlation with photosynthetic capacity [64]. SA increased the soluble protein content of the wheat flag leaves, which was conducive to increasing flag leaf photosynthetic capacity and yield formation [65]. Photosynthetic products in wheat leaves mainly exist in the form of sucrose and are transported to other organs. Sucrose synthesis depends on SPS, and the accumulation of sucrose and the distribution of photosynthetic products are directly influenced by the activity of SPS. Yuan et al. [66] found that at different growth stages, the total sugar and sucrose contents in tomato fruits were significantly reduced under high temperature stress. We also found that the SPS activity of the flag leaves was reduced under high temperature stress. Starch is the main storage carbohydrate in higher plants. The synthesis of starch depends on the supply of sucrose, while the accumulation of starch depends on the rate of starch synthesis and degradation, which is closely related to the activity of SPS and amylase [67]. In our study, following SA pre-spraying at different stages, the SPS activity of the flag leaves in all the treatments was significantly higher than that in the high temperature stress treatment. SA pre-spraying at the anthesis stage was best at abating the decreased activity of SPS in the flag leaves under high temperature stress. El-Tayeb et al. [68] reported that SPS activity directly affects the distribution of photosynthetic products between starch and sucrose, which is negatively correlated with starch accumulation and positively correlated with sucrose formation. SA significantly increased the activity of SPS in the flag leaves and promoted carbon catabolism, including the decomposition of starch, which was then converted into sucrose and transported to the grains, leading to increased wheat yield. In summary, high temperature stress decreased the sugar and nitrogen content of the flag leaves. The foliar application of SA increased the sugar and nitrogen content by increasing the soluble protein content and SPS activity, thereby enhancing the resistance of wheat to high temperature stress.

5. Conclusions

The application of SA at different stages reduced the yield loss and damage to the photosynthetic capacity caused by high temperature stress; the effectiveness of the treatments in descending order was SAAG > SA5G > SA10G > SAHG. Exogenous SA significantly restored the photosynthetic capacity of wheat flag leaves damaged by post-anthesis high temperature stress, which effectively alleviated the inhibition of wheat growth caused by the stress and ultimately reduced the yield loss.

Author Contributions

Y.F., Z.L. and Y.L. initiated the manuscript. B.Q., Q.S., L.M., Q.W., W.Z. and S.M. performed experiments. C.M. and Z.H. conceptualized the idea and revised the manuscript. All authors have read and agreed to the published version of the manuscript.

Funding

Project of Natural Science Foundation of Anhui Province: 2008085qc118, National Natural Science Foundation of China: U19A2021, Major Science and Technology Special Project of Anhui Province: S202003a06020035, Jiangsu Collaborative Innovation Center for Modern Crop Production: JCIC-MCP.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Acknowledgments

This work was supported by the Project of Natural Science Foundation of Anhui Province (2008085qc118), National Natural Science Foundation of China (U19A2021), and Major Science and Technology Special Project of Anhui Province (S202003a06020035). We acknowledge support from the Jiangsu Collaborative Innovation Center for Modern Crop Production (JCIC-MCP).

Conflicts of Interest

The authors declare that they have no conflict of interest.

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Agronomy 12 01386 g001 550
Figure 1. Schematic representation of experimental design and treatments. DAA refers to days after anthesis. NN is the control (normal growth conditions outside the shed). NG represents non-SA spraying and high temperature stress at the grain-filling stage. SAHG represents exogenous SA spraying at the heading stage and high temperature stress at the grain-filling stage. SAAG represents exogenous SA spraying at the anthesis stage and high temperature stress at the grain-filling stage. SA5G and SA10G represent treatments whereby exogenous SA was sprayed starting from 5 and 10 DAA and high temperature stress at the grain-filling stage.
Figure 1. Schematic representation of experimental design and treatments. DAA refers to days after anthesis. NN is the control (normal growth conditions outside the shed). NG represents non-SA spraying and high temperature stress at the grain-filling stage. SAHG represents exogenous SA spraying at the heading stage and high temperature stress at the grain-filling stage. SAAG represents exogenous SA spraying at the anthesis stage and high temperature stress at the grain-filling stage. SA5G and SA10G represent treatments whereby exogenous SA was sprayed starting from 5 and 10 DAA and high temperature stress at the grain-filling stage.
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Figure 2. The temperature and humidity changes in the canopy during the treatment.
Figure 2. The temperature and humidity changes in the canopy during the treatment.
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Figure 3. Effects of exogenous salicylic acid (SA) spraying on the flag leaf area of wheat under high temperature stress at the grain-filling stage in 2018–2019. NN is the control (normal growth conditions outside the shed). NG represents non-SA spraying and high temperature stress at the grain-filling stage. SAHG represents exogenous SA spraying at the heading stage and high temperature stress at the grain-filling stage. SAAG represents exogenous SA spraying at the anthesis stage and high temperature stress at the grain-filling stage. SA5G and SA10G represent treatments whereby exogenous SA was sprayed starting from 5 and 10 DAA and high temperature stress at the grain-filling stage. Different lowercase letters denote statistically significant differences (p < 0.05, Duncan’s multiple range test) among treatments. Results are expressed as mean ± SE (n = 3).
Figure 3. Effects of exogenous salicylic acid (SA) spraying on the flag leaf area of wheat under high temperature stress at the grain-filling stage in 2018–2019. NN is the control (normal growth conditions outside the shed). NG represents non-SA spraying and high temperature stress at the grain-filling stage. SAHG represents exogenous SA spraying at the heading stage and high temperature stress at the grain-filling stage. SAAG represents exogenous SA spraying at the anthesis stage and high temperature stress at the grain-filling stage. SA5G and SA10G represent treatments whereby exogenous SA was sprayed starting from 5 and 10 DAA and high temperature stress at the grain-filling stage. Different lowercase letters denote statistically significant differences (p < 0.05, Duncan’s multiple range test) among treatments. Results are expressed as mean ± SE (n = 3).
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Figure 4. Effect of exogenous salicylic acid (SA) spraying on the net photosynthetic rate (A) and stomatal density (B) of the flag leaves of wheat under high temperature stress at the grain-filling stage (20 days after anthesis) in 2018–2019. NN is the control (normal growth conditions outside the shed). NG represents non-SA spraying and high temperature stress at the grain-filling stage. SAHG represents exogenous SA spraying at the heading stage and high temperature stress at the grain-filling stage. SAAG represents exogenous SA spraying at the anthesis stage and high temperature stress at the grain-filling stage. SA5G and SA10G represent treatments whereby exogenous SA was sprayed starting from 5 and 10 DAA and high temperature stress at the grain-filling stage. Different lowercase letters denote statistically significant differences (p < 0.05, Duncan’s multiple range test) among treatments. Results are expressed as mean ± SE (n = 3).
Figure 4. Effect of exogenous salicylic acid (SA) spraying on the net photosynthetic rate (A) and stomatal density (B) of the flag leaves of wheat under high temperature stress at the grain-filling stage (20 days after anthesis) in 2018–2019. NN is the control (normal growth conditions outside the shed). NG represents non-SA spraying and high temperature stress at the grain-filling stage. SAHG represents exogenous SA spraying at the heading stage and high temperature stress at the grain-filling stage. SAAG represents exogenous SA spraying at the anthesis stage and high temperature stress at the grain-filling stage. SA5G and SA10G represent treatments whereby exogenous SA was sprayed starting from 5 and 10 DAA and high temperature stress at the grain-filling stage. Different lowercase letters denote statistically significant differences (p < 0.05, Duncan’s multiple range test) among treatments. Results are expressed as mean ± SE (n = 3).
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Figure 5. Effects of exogenous salicylic acid (SA) spraying on the maximum photochemical efficiency (A) and actual photochemical efficiency (B) of the flag leaves under high temperature stress during the grain-filling period in 2018–2019. NN is the control (normal growth conditions outside the shed). NG represents non-SA spraying and high temperature stress at the grain-filling stage. SAHG represents exogenous SA spraying at the heading stage and high temperature stress at the grain-filling stage. SAAG represents exogenous SA spraying at the anthesis stage and high temperature stress at the grain-filling stage. SA5G and SA10G represent treatments whereby exogenous SA was sprayed starting from 5 and 10 DAA and high temperature stress at the grain-filling stage. Different lowercase letters denote statistically significant differences (p < 0.05, Duncan’s multiple range test) among treatments. Results are expressed as mean ± SE (n = 3).
Figure 5. Effects of exogenous salicylic acid (SA) spraying on the maximum photochemical efficiency (A) and actual photochemical efficiency (B) of the flag leaves under high temperature stress during the grain-filling period in 2018–2019. NN is the control (normal growth conditions outside the shed). NG represents non-SA spraying and high temperature stress at the grain-filling stage. SAHG represents exogenous SA spraying at the heading stage and high temperature stress at the grain-filling stage. SAAG represents exogenous SA spraying at the anthesis stage and high temperature stress at the grain-filling stage. SA5G and SA10G represent treatments whereby exogenous SA was sprayed starting from 5 and 10 DAA and high temperature stress at the grain-filling stage. Different lowercase letters denote statistically significant differences (p < 0.05, Duncan’s multiple range test) among treatments. Results are expressed as mean ± SE (n = 3).
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Figure 6. Effects of exogenous salicylic acid (SA) spraying on the chlorophyll content (A), soluble protein content (B), and sucrose phosphate synthase activity (C) of the flag leaves of wheat under high temperature stress during the grain-filling period in 2018–2019. NN is the control (normal growth conditions outside the shed). NG represents non-SA spraying and high temperature stress at the grain-filling stage. SAHG represents exogenous SA spraying at the heading stage and high temperature stress at the grain-filling stage. SAAG represents exogenous SA spraying at the anthesis stage and high temperature stress at the grain-filling stage. SA5G and SA10G represent treatments whereby exogenous SA was sprayed starting from 5 and 10 DAA and high temperature stress at the grain-filling stage. Different lowercase letters denote statistically significant differences (p < 0.05, Duncan’s multiple range test) among treatments. Results are expressed as mean ± SE (n = 3).
Figure 6. Effects of exogenous salicylic acid (SA) spraying on the chlorophyll content (A), soluble protein content (B), and sucrose phosphate synthase activity (C) of the flag leaves of wheat under high temperature stress during the grain-filling period in 2018–2019. NN is the control (normal growth conditions outside the shed). NG represents non-SA spraying and high temperature stress at the grain-filling stage. SAHG represents exogenous SA spraying at the heading stage and high temperature stress at the grain-filling stage. SAAG represents exogenous SA spraying at the anthesis stage and high temperature stress at the grain-filling stage. SA5G and SA10G represent treatments whereby exogenous SA was sprayed starting from 5 and 10 DAA and high temperature stress at the grain-filling stage. Different lowercase letters denote statistically significant differences (p < 0.05, Duncan’s multiple range test) among treatments. Results are expressed as mean ± SE (n = 3).
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Table
Table 1. Presentation of the chemical characteristics of the soil in 2018–2020.
Table 1. Presentation of the chemical characteristics of the soil in 2018–2020.
YearsOrganic Matter
(g kg−1)		Available Nitrogen
(mg kg−1)		Available Phosphorus
(mg kg−1)		Available Potassium
(mg kg−1)
2018–201913.986.213.471.5
2019–202015.290.616.579.6
Table
Table 2. Effects of exogenous salicylic acid (SA) spraying on wheat yield and yield components under high temperature stress during the grain-filling period in 2018–2020.
Table 2. Effects of exogenous salicylic acid (SA) spraying on wheat yield and yield components under high temperature stress during the grain-filling period in 2018–2020.
YearsTreatmentSpikes Pot−1Kernels Spike−11000-Kernel Weight (g)Yield (g pot−1)
2018–2019NN24.67 ± 0.3349.33 ± 0.33 a42.54 ± 0.12 a50.38 ± 0.41 a
NG24.67 ± 0.3347.00 ± 0.00 c35.49 ± 0.63 d42.81 ± 0.39 d
SAHG24.00 ± 0.0047.33 ± 0.33 bc36.61 ± 0.29 c43.81 ± 0.78 d
SAAG24.33 ± 0.3348.67 ± 0.33 ab40.37 ± 0.34 b48.66 ± 0.67 b
SA5G24.00 ± 0.0048.33 ± 0.33 abc39.56 ± 0.12 b47.41 ± 0.22 b
SA10G23.67 ± 0.3347.67 ± 0.33 bc37.25 ± 0.25 c45.63 ± 0.67 c
2019–2020NN23.33 ± 0.3350.33 ± 0.88 a43.71 ± 0.27 a51.85 ± 0.37 a
NG24.00 ± 0.0048.00 ± 0.00 d37.77 ± 0.33 c43.85 ± 0.21 e
SAHG24.00 ± 0.0048.33 ± 0.33 d38.24 ± 1.19 c44.49 ± 0.75 de
SAAG23.67 ± 0.3349.67 ± 0.33 ab41.09 ± 0.49 b49.51 ± 0.59 b
SA5G24.00 ± 0.0049.00 ± 0.00 bc40.47 ± 0.38 b47.20 ± 0.67 c
SA10G24.33 ± 0.3348.67 ± 0.33 cd39.59 ± 0.76 bc45.57 ± 0.28 d
NN is the control (normal growth conditions outside the shed). NG represents non-SA spraying and high temperature stress at the grain-filling stage. SAHG represents exogenous SA spraying at the heading stage and high temperature stress at the grain-filling stage. SAAG represents exogenous SA spraying at the anthesis stage and high temperature stress at the grain-filling stage. SA5G and SA10G represent treatments whereby exogenous SA was sprayed starting from 5 and 10 DAA and high temperature stress at the grain-filling stage. Different lowercase letters denote statistically significant differences (p < 0.05, Duncan’s multiple range test) among treatments. Results are expressed as mean ± SE (n = 3).
Table
Table 3. Effects of exogenous salicylic acid (SA) spraying on the amount and proportion of dry matter in various organs of wheat at the mature stage under high temperature stress during the grain-filling stage in 2018–2020.
Table 3. Effects of exogenous salicylic acid (SA) spraying on the amount and proportion of dry matter in various organs of wheat at the mature stage under high temperature stress during the grain-filling stage in 2018–2020.
YearsTreatmentStem and LeafSpike Stalk and GlumeGrain
Amount
(g stem−1)		Proportion
(%)		Amount
(g stem−1)		Proportion
(%)		Amount
(g stem−1)		Proportion
(%)
2018–2019NN1.67 ± 0.13 a38.39 ± 0.24 a0.65 ± 0.02 e14.94 ± 0.66 d2.03 ± 0.02 a46.67 ± 0.35 b
NG1.26 ± 0.04 bc32.47 ± 0.13 d0.90 ± 0.02 a23.20 ± 0.45 a1.72 ± 0.02 d44.33 ± 0.97 c
SAHG1.31 ± 0.04 bc33.25 ± 0.34 c0.83 ± 0.02 b21.07 ± 1.01 b1.82 ± 0.02 c46.19 ± 0.89 bc
SAAG1.49 ± 0.05 ab35.90 ± 0.45 b0.67 ± 0.01 e16.14 ± 0.41 cd1.99 ± 0.04 ab47.95 ± 0.12 a
SA5G1.43 ± 0.02 b34.88 ± 0.52 b0.71 ± 0.01 d17.32 ± 0.76 c1.96 ± 0.03 ab47.80 ± 0.23 a
SA10G1.38 ± 0.03 b33.99 ± 0.23 c0.77 ± 0.01 c18.97 ± 0.91 bc1.91 ± 0.02 b47.04 ± 0.39 ab
2019–2020NN1.56 ± 0.06 a35.29 ± 0.12 a0.64 ± 0.01 e14.48 ± 0.55 c2.22 ± 0.02 a50.23 ± 0.35 a
NG1.21 ± 0.02 d31.16 ± 0.20 d0.86 ± 0.02 a22.16 ± 0.42 a1.81 ± 0.03 d46.65 ± 0.37 b
SAHG1.25 ± 0.02 d32.05 ± 0.21 c0.81 ± 0.02 b20.77 ± 0.99 ab1.84 ± 0.02 d47.18 ± 0.21 c
SAAG1.48 ± 0.03 ab35.24 ± 0.19 a0.67 ± 0.01 d15.95 ± 1.31 bc2.05 ± 0.01 b48.81 ± 0.32 b
SA5G1.41 ± 0.03 bc34.90 ± 0.16 a0.68 ± 0.01 d16.83 ± 1.17 bc1.95 ± 0.02 c48.27 ± 0.23 b
SA10G1.35 ± 0.03 c34.26 ± 0.19 b0.73 ± 0.01 c18.53 ± 0.96 b1.86 ± 0.02 d47.21 ± 0.19 c
NN is the control (normal growth conditions outside the shed). NG represents non-SA spraying and high temperature stress at the grain-filling stage. SAHG represents exogenous SA spraying at the heading stage and high temperature stress at the grain-filling stage. SAAG represents exogenous SA spraying at the anthesis stage and high temperature stress at the grain-filling stage. SA5G and SA10G represent treatments whereby exogenous SA was sprayed starting from 5 and 10 DAA and high temperature stress at the grain-filling stage. Different lowercase letters denote statistically significant differences (p < 0.05, Duncan’s multiple range test) among treatments. Results are expressed as mean ± SE (n = 3).
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Fan, Y.; Lv, Z.; Li, Y.; Qin, B.; Song, Q.; Ma, L.; Wu, Q.; Zhang, W.; Ma, S.; Ma, C.; et al. Salicylic Acid Reduces Wheat Yield Loss Caused by High Temperature Stress by Enhancing the Photosynthetic Performance of the Flag Leaves. Agronomy 2022, 12, 1386. https://doi.org/10.3390/agronomy12061386

AMA Style

Fan Y, Lv Z, Li Y, Qin B, Song Q, Ma L, Wu Q, Zhang W, Ma S, Ma C, et al. Salicylic Acid Reduces Wheat Yield Loss Caused by High Temperature Stress by Enhancing the Photosynthetic Performance of the Flag Leaves. Agronomy. 2022; 12(6):1386. https://doi.org/10.3390/agronomy12061386

Chicago/Turabian Style

Fan, Yonghui, Zhaoyan Lv, Yuxing Li, Boya Qin, Qingyu Song, Liangliang Ma, Qianqian Wu, Wenjing Zhang, Shangyu Ma, Chuanxi Ma, and et al. 2022. "Salicylic Acid Reduces Wheat Yield Loss Caused by High Temperature Stress by Enhancing the Photosynthetic Performance of the Flag Leaves" Agronomy 12, no. 6: 1386. https://doi.org/10.3390/agronomy12061386

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