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Article

Exogenous Salicylic Acid Alleviates Water Deficit Stress by Protecting Photosynthetic System in Maize Seedlings

by
Longfei Xin
1,2,
Jiajia Wang
1,* and
Qinghua Yang
2,*
1
College of Agronomy, Xinyang Agriculture and Forestry University, Xinyang 464000, China
2
College of Agronomy, Henan Agricultural University, Zhengzhou 450046, China
*
Authors to whom correspondence should be addressed.
Agronomy 2023, 13(9), 2443; https://doi.org/10.3390/agronomy13092443
Submission received: 9 August 2023 / Revised: 7 September 2023 / Accepted: 18 September 2023 / Published: 21 September 2023
(This article belongs to the Section Plant-Crop Biology and Biochemistry)
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Abstract

:
Water deficit is a significant abiotic stress affecting crop growth and production. While many studies have indicated that salicylic acid (SA) plays a crucial role in mitigating the detrimental effects of environmental stress on plants, its mechanism regulating the photosynthetic adaptability of maize seedlings under water deficit is still unclear. This study aimed to investigate the impact of exogenous SA on maize seedling performance under polyethylene glycol (PEG)-induced water deficit. The results showed that PEG treatment destroyed the integrity of chloroplast and reduced chlorophyll content and photosynthesis rate (Pn), leading to growth retardation of maize seedlings with lower biomass accumulation and leaf relative water content (RWC). Moreover, chlorophyll fluorescence index, including potential photochemical activity (Fv/Fo), maximum Photosystem II (PSII) quantum yield (Fv/Fm), and energy captured by PSII reaction center for electron transfer (Eto/RC), were decreased, but energy dissipated by unit reaction center (DIo/RC) was enhanced in maize seedlings under water deficit. In addition, PEG treatment also significantly declined the activity of Rubisco and Rubisco activase (RCA) in maize seedlings. In contrast, SA treatment enhanced the content of chlorophyll, as well as the transcription level of psbA, and RCA and Rubisco small subunit (rbcS) reduced the damaging effects of PEG treatment by protecting the integrity of chloroplast and repairing the damaged PSII reaction center, thus positively regulating photosynthetic reaction and water-deficit tolerance in maize seedlings. Our data implied that SA played an important regulatory role in plant resistance to water-deficit stress, and the result will further supply the regulatory network of SA-mediated photosynthetic adaptability.

1. Introduction

Water deficit caused by drought is one of the most serious threats to plant growth and production worldwide [1,2,3,4]. In response to stressful environments, plants are constantly making adjustments, leading to numerous morphological, physiological, and biochemical changes, such as stomatal movement, osmotic adjustment, and reactive oxygen species (ROS)-mediated antioxidant defense system [1,3,5,6]. In recent years, plants’ response to water-deficit stress has become the focus of plant–environment interaction research, and various response mechanisms operating in plants have been found [7,8,9,10,11,12]. However, it is still a major challenge to effectively apply these results to field production. Among them, exogenous plant growth regulators (PGRs) have been considered an effective means to improve drought tolerance in plants [3,13,14]. Therefore, an in-depth analysis of the role of PGRs on environmental stress response and its mechanism is urgently needed.
Salicylic acid (SA) is a phenolic hormone in plants that affects seed germination and growth, stomata movement, leaf senescence, and fruit yield and is involved in plant defense responses to biotic and abiotic stresses [15,16]. The biosynthesis of SA in vivo is achieved through the phenylalanine ammonia lyase (PAL) pathway and the Isochorismate synthase (ICS) pathway [17,18,19]. In vitro, SA is an important PGR in plants’ defense response to diverse stressful environments [20,21]. SA reduces the accumulation of toxic compounds and programmed cell death (PCD) through ROS signaling, nitrogen metabolism, and other processes, thereby reducing the damage of abiotic and biotic stresses to plants [20,22]. In addition, with ROS and glutathione (GSH), SA participates in the transcriptional regulation of defense genes, inducing defense responses such as PCD and stomata closure, thereby affecting metabolic processes [23]. SIZ1 is a positive regulator of drought resistance [24,25]. Studies have found that SA-mediated SIZ1 activity in Arabidopsis regulated stomatal closure and enhanced drought tolerance [20]. SA enhanced plant performance under salt stress in Mungbean by regulating the photosynthetic process and antioxidant defense activity [26,27]. While SA played an important role in protecting against heat, drought, and salt stress and in photosynthesis in mustard [28], wheat [29], grape [30], and Arabidopsis [31], its mechanism of regulating photosynthetic adaptability of maize seedlings under water deficit is still unclear. Most reports have focused on the mechanisms linking antioxidant capacity, stomatal movement, and abscisic acid (ABA) signal transduction. The specific function of SA in alleviating the damage of water deficit in relation to photosynthesis in maize needs further study.
The imbalance of water metabolism in vivo caused by drought destroys the photosynthetic organs, affects the photosynthetic process, and threatens the survival of plants [32]. Photosystem II (PSII), a multiprotein–pigment complex composed of multiple subunits on the thylakoid membrane, plays a critical role in photosynthesis [33]. In addition, the PSII reaction center is the primary target of abiotic stress damage and is very sensitive to environmental stresses [34,35,36]. Previous studies have found that the influence of drought on the photosynthetic process and chlorophyll (Chl) a fluorescence parameter might result from the inhibition of photosynthetic electron transport or damage of the PSII reaction center [35]. Chloroplast gene psbA encodes the D1 subunit protein, which plays a vital role in the repair of damaged PSII reaction center [36,37]. It was reported that the D1 protein not only provides binding sites for various coenzyme factors, maintaining the stability of the PSII complex conformation but also participates in charge separation and electron transfer [38,39]. Despite their importance, little attention has been paid to SA-mediated regulatory networks controlling plant photosynthetic adaptability to water deficit. In addition, the associations between SA and water-deficit-tolerant ability in maize seedlings remained unclear. Hence, exploring the regulatory mechanism of SA on the PSII reaction center is of great significance in improving the photosynthetic adaptability in maize seedlings under water deficit.
This study was undertaken to gain insight into the interaction between SA and water-deficit-resistant ability in maize seedlings via physiological analysis and to explore SA-mediated photosynthetic response to water-deficit stress in terms of seedling morphology, RWC, chlorophyll content, chloroplast ultrastructure, chlorophyll fluorescence, photosynthetic parameters, Rubisco and RCA activity, and transcripts level of genes corresponding to photosynthetic process under different stresses. The results of this research will help to explain the regulatory mechanism of exogenous SA in the photosynthetic response under water-deficit stress and deliver a resolution for maize improvement programs under stressful environments.

2. Materials and Methods

2.1. Plant Materials and Growth Conditions

This study used the water-sensitive maize variety Zhuyu 309 (Zhu 07 × 78599-3). First, the uniform maize seeds were surface disinfected with 1.5% sodium hypochlorite for 15 min, then rinsed repeatedly with deionized water 4–6 times. After sterilization, the seeds were soaked for 8 h and germinated for 4 d in the dark. Uniform seedlings were selected and then transferred to one-half of Hoagland’s nutrient solution with twelve seedlings per plastic box and twelve plastic boxes in total. After being cultured to the three-leaf stage, the maize seedlings were transferred to full-strength Hoagland’s nutrient solution. All plants were grown in an incubator under the following conditions: the day/night temperature of 28 °C/20 °C ± 2 °C, the light/dark period of 16/8 h, light intensity of 300 μmol·m−2·s−1, and air humidity of 70 ± 5%.
A completely randomized design was used in the experiment, which included four treatment groups with three independent biological replicates per treatment. The seedlings in the control (CK) were watered with full-strength Hoagland solution. The seedlings in the SA treatment (SA) were sprayed with 5 mM of SA in a full-strength Hoagland solution. The seedlings in the PEG treatment (PEG) were subjected to 20% (w/v) polyethylene glycol (PEG6000). The seedlings under SA and PEG treatments (SA + PEG) were sprayed with 5 mM of SA and 20% (w/v) PEG6000. Three days after treatments, the latest fully grown young leaves were harvested for morphological and physiological measurements.

2.2. Determination of Maize Seedling Biomass

The whole seedlings of different treatments were divided into aboveground and underground parts, and the dry and fresh weights were measured, respectively.

2.3. Measurements of Leaf Relative Water Content (RWC)

Leaf samples from different treatments were used for RWC assay according to the previously described method [35]. First, the fresh weight (mf) of leaves was measured. The leaves were then immersed in distilled water for several hours to allow them to absorb water and become saturated. Turgid weight (mt) was measured when the weight of immersed leaves no longer increased. After that, the leaves were dried to measure the dry weight (md). The RWC level was calculated according to the Equation (1):
RWC (%) = (mf − md) ×100/ (mt − md)

2.4. Measurements of Chlorophyll Content and Photosynthetic Parameters

Fresh leaf samples without veins from different treatments were cut into small pieces and used to determine chlorophyll content. The measurement was conducted according to the methods described previously [40].
Photosynthetic parameters such as the net photosynthesis rate (Pn), stomatal conductance (Gs), intercellular CO2 concentration (Ci), and transpiration rate (Tr) in leaves of maize seedlings were measured with a Li-6400XT portable system (LI-COR, Lincoln, NE, USA) in the morning between 9:00 and 11:00. All measurements were conducted according to the instrument operation manual.

2.5. Measurement of Chlorophyll Fluorescence

Chlorophyll fluorescence measurements were performed by the Handy PEA-plant efficiency analyzer (Hansatech Instruments Ltd., Norfolk, UK) according to the methods reported previously [41]. All parameters were measured on the middle of the second completely unfolded leaf of maize seedlings after 15–20 min dark adaptation.

2.6. Observation of Chloroplast Ultrastructure

Chloroplast ultrastructure of leaves under different treatments was observed by transmission electron microscopy (TEM) assay. After treatment, the same part of leaf samples was cut into small rectangular pieces of 1 mm × 2 mm with a blade, fixed in 3% glutaraldehyde fixative, dehydrated, and embedded with epoxy resin, and then sliced with a Leica EM UC6 ultra-thin slicer (Leica, Wetzlar, Germany). Finally, the chloroplast structure was observed using a Hitachi H-7500 (Hitachi Ltd., Tokyo, Japan) electron microscope.

2.7. Determination of Rubisco and RCA Activity

The activity of Rubisco activase (RCA) and Ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) in plants was measured using appropriate kits from COMIN (http://www.cominbio.com/index.html, accessed on 16 October 2021) following the manufacturer’s instructions.

2.8. RNA Extraction and Quantitative Real-Time PCR

Total RNA was extracted using Trizol reagent (Invitrogen, Carlsbad, CA, USA) following the manufacturer’s instructions. First-strand complementary DNA (cDNA) was synthesized using the AMV First-Strand cDNA Synthesis Kit (Sangon Biotech, Shanghai, China) as instructed by the manufacturer. Quantitative real-time PCR (qRT-PCR) assays were conducted using 2× SG Fast qPCR Master Mix (High Rox) (Sangon Biotech, Shanghai, Shanghai, China) and amplified by gene-specific primers (Table S1) with actin as an internal control. Reaction mixtures include 50–500 ng first-strand cDNA, 0.2 μM forward primer, 0.2 μM reverse primer, and nuclease-free water to a final volume of 20 μL. The qRT-PCR was performed on an Applied Biosystems 5700 real-time system with appropriate reaction conditions. The expression level was calculated according to the method described previously [42].

2.9. Statistical Analysis

Data analysis was performed in GraphPad Prism 8 (GraphPad Software Inc., San Diego, CA, USA). Significant differences were determined with Duncan’s multiple range tests (p < 0.05). In addition, correlations among the different measured traits were assessed using Spearman’s correlation analysis.

3. Results

3.1. Exogenous SA Could Alleviate the Inhibition of Water Deficit on Biomass Accumulation of Maize Seedlings

The fresh weight (FW) and dry weight (DW) of the shoots and roots of maize seedlings were measured under different conditions. Compared with the CK group, a decrease of about 47.73% and 18.18% was observed in the shoot FW and shoot DW, respectively, in seedlings under SA + PEG conditions; however, a sharp decrease of about 57.55% and 27.24% were observed under individual PEG conditions (Figure 1A,B). A similar trend was observed for the RWC levels in the leaves of maize plants. Individual PEG treatment decreased RWC levels by 21.27%, and PEG treatment decreased RWC levels in SA-sprayed seedlings by 15.95% (Figure 1C). Compared with the CK condition, individual SA treatment had little effect on leaf RWC and biomass accumulation of maize seedlings. These results showed that PEG-induced water deficit inhibited the growth of maize seedlings, while SA could alleviate the deficit-caused inhibition of water and its effect on the maize seedling growth, thus effectively alleviating the water loss of maize plants caused by PEG and improving the water retention of leaves.

3.2. Exogenous SA Improved Photosynthetic Efficiency in Maize Seedlings under Water Deficit

To investigate the impact of SA on photosynthesis in leaves of maize seedlings under water deficit, we measured gas exchange parameters in seedlings under different treatments. In comparison to the CK condition, the parameters related to Pn, Tr, and Gs in PEG-treated plants decreased by 55.52%, 63.24%, and 57.38%, respectively; however, the decrease in SA-sprayed seedlings under the PEG condition was about 34.98%, 26.49%, and 40.71%, respectively (Figure 2A–C). In contrast, compared with the CK condition, an increase of 31.33% in Ci was observed in SA-sprayed plants under PEG treatment, and a much higher increase of 45.07% in Ci was observed in seedlings under individual PEG treatment (Figure 2D). Gas exchange parameters in individual SA-treated seedlings were similar to those of the CK condition (Figure 2). These results suggested that SA treatment could significantly inhibit the decrease in Pn, Tr, and Gs in maize plants under PEG treatment and maintain high photosynthetic productivity.

3.3. Exogenous SA Reduced the Degradation of Chlorophyll in Leaves of Maize Seedlings under Water Deficit

We further measured chlorophyll content in the leaves of maize seedlings under different treatments. As shown in Figure 3, compared with the CK condition, PEG treatment decreased the contents of chlorophyll a, chlorophyll b, carotenoid, and total chlorophyll in SA-sprayed seedlings by 9.69%, 6.57%, 25.28%, and 10.79%, respectively; however, individual PEG treatment decreased those by 14.99%, 6.97%, 35.69%, and 15.35%, respectively (Figure 3), suggesting that SA treatment could slow down the degradation of chlorophyll, which might help maintain the photosynthetic efficiency in maize seedlings under PEG treatment.

3.4. Exogenous SA Positively Regulated Photosynthetic Reaction Process in Maize Seedlings under Water Deficit

To further explore the SA-mediated photosynthetic adaptability mechanism, we analyzed the fluorescence parameters in the leaves of maize seedlings under different treatments. Under non-stress conditions, the SA spraying had little effect on chlorophyll fluorescence parameters in leaves (Figure 4). Additionally, compared with the CK condition, a decline of about 20.14%, 4.13%, and 16.57% in the Fv/Fo, Fv/Fm, and Eto/RC in SA-sprayed seedlings under PEG condition was observed, respectively; however, their sharp decline of about 27.96%, 6.63%, and 30.69%, respectively, under individual PEG treatment was also observed (Figure 4A–C). DIo/RC in maize seedlings under individual PEG treatment was significantly higher than in other treatments (Figure 4D). These data indicated that PEG-induced water deficit affected the activity of the PSII reaction center and the proportion of light energy captured by leaves. However, SA treatment could alleviate the photoinhibition, protect the PSII reaction center, and reduce the degree of damage to the PSII reaction center.

3.5. Exogenous SA Introduced to Maintain the Integrity of Chloroplast Ultrastructure in Maize Seedlings under Water Deficit

Chloroplasts are central organelles responsible for photosynthesis, and the normal development of chloroplast is a prerequisite for photosynthesis of green plants [43]. It was found that the chloroplasts are involved in the plants’ adaptive regulation of drought stress by sensing changes in the environment [32].In order to further evaluate whether chloroplast development was affected by PEG-induced water deficit and exogenous SA, we observed the chloroplast ultrastructure in leaves of maize seedlings under different treatments with transmission electron microscopy. We observed normal chloroplasts under CK and individual SA conditions, which were long oval or boat-shaped, arranged along the edge of the cell with dense and well-structured granum-thylakoid (Figure 5A,B). By contrast, individual PEG condition was found to result in severely disrupted chloroplasts, which were expanded from long oval to round, with decomposed chloroplast membrane, scattered granum-thylakoid, and distorted grana and stroma lamellae (Figure 5C). However, a less disrupted chloroplast was observed in SA-sprayed maize seedlings under PEG treatment, with more neat grana thylakoid stacking, clearer grana, and stroma lamellae, compared with seedlings under individual PEG treatment (Figure 5D).

3.6. Exogenous SA Inhibited the Decline of Rubisco Activity and RCA Activity in Maize Seedlings under Water Deficit

We next found that PEG-induced water deficit inhibited Rubisco and RCA activities in the leaves of maize seedlings (Figure 6). Compared with the CK condition, a decline of about 28.27% in Rubisco activity and 11.52% in RCA activity in SA-sprayed maize plants was observed under PEG treatment (Figure 6A,B). However, individual PEG conditions resulted in a much higher reduction in activities of Rubisco and RCA, which were 48.86% and 39.43%, respectively, lower than those in seedlings of CK (Figure 6A,B).
In order to evaluate the response mechanism of maize seedlings to SA under PEG-induced water-deficit stress, we analyzed the transcripts level of the D1 protein-encoding gene psbA. The psbA transcripts were downregulated under different treatments; a higher decrease was observed under individual PEG conditions (57.35%), followed by SA-sprayed seedlings under PEG treatment (22.57%) (Figure 7A). This finding was consistent with observed differences in levels of chlorophyll fluorescence—a marker of PSII reaction center damage—in leaves from each treatment (Figure 4). We also analyzed the transcript levels of genes such as the RCA gene, rbcL, and rbcS, corresponding to the Rubisco and RCA activities. Compared with the CK condition, the transcripts of RCA, rbcL, and rbcS gene in SA-sprayed maize plants under the PEG condition decreased to the extent of 39.55%, 58.53%, and 9.48%, respectively (Figure 7B–D). Whereas, under individual PEG treatment, the reduction was about 75.56%, 61.35%, and 47.94%, respectively (Figure 7B–D).

3.7. Analysis of the Correlations between Different Measured Traits of Maize Seedlings under Different Treatments

We further conducted Spearman’s correlation analysis between the different measured traits (Figure 8). There was a significant correlation between photosynthetic parameters and many other indicators. Pn, Tr, and Gs were all negatively correlated with root DW and Ci (p < 0.05) but positively correlated with other indicators except DIo/RC (p < 0.05). There was no significant correlation between DIo/RC and other indicators (p > 0.05). The results suggest that PEG and SA + PEG had significant effects on the growth and photosynthetic characteristics of maize seedlings, and there were significant interactions among different traits.

4. Discussion

4.1. Exogenous SA Alleviates Decreases in Photosynthesis under Water Deficit by Stabilizing Chloroplast Structure and Slowing Down the Decline of Chlorophyll Content

Drought affects many plant growth and development processes, perhaps most significantly the photosynthesis [32]. Chlorophyll is a member of the lipid-containing pigment family, located on the thylakoid membrane of the chloroplast, and directly involved in energy conversion processes in photosynthesis, such as the absorption, transmission, and distribution of photosynthetic light energy [44,45,46]. Chlorophyll is essential for photosynthesis because it allows plants to obtain energy from light, and to some extent, its content reflects the degree of photosynthesis [47]. Numerous studies suggested that drought stress leads to reduced photosynthetic pigment content and photosynthesis in plant leaves [35,48]. Similar results were obtained in the present work, where the water deficit led to a significant decrease in chlorophyll content in the leaves of maize seedlings, possibly due to the inhibition of chlorophyll synthesis and the acceleration of decomposition. However, SA treatment could significantly alleviate the decrease in chlorophyll content in leaves of maize seedlings under drought stress, especially chlorophyll a and carotenoid. These results indicated that under water deficit, SA treatment slowed down the decomposition of chlorophyll a in leaves of maize seedlings and then promoted the ability of chlorophyll to absorb and convert light energy and photochemical reaction. These might result from the role of SA in reducing leaf water loss and promoting its internal growth and metabolism during drought. Our study showed that the SA spraying under normal conditions did not result in substantial changes in the chlorophyll content in the leaves of maize seedlings. However, it was found that the application of SA on detached leaves caused a decrease in chlorophyll content and accelerated leaf senescence in Arabidopsis, which might be attributed to the distinct physiological response of salicylic acid depending on the treatment duration, application concentration, plant species, and their growth status [15,49,50].
Stomata, the plants’ main channels for exchanging gas and dissipating water to the external environment, play a key role in photosynthesis [51]. The main reason for the decrease in the photosynthetic rate of plant leaves is stomatal and non-stomatal limitations, and whether the decrease in photosynthetic rate is related to stomatal limitation can be judged according to the changes in Gs and Ci [52]. In this study, water deficit caused a significant decrease in Pn and Gs, while a significant increase in Ci was observed, compared with the control, indicating that the decrease in Pn in the maize seedling leaves was mainly controlled by non-stomatal limitation. This might be due to membrane lipid peroxidation caused by water deficit, which could further destroy the chloroplast membrane and lead to the weakening of the assimilation ability of mesophyll cells and the increase in Ci concentration [39]. Our observation of the chloroplasts’ ultrastructure in the leaves of maize seedlings under different treatments also confirmed this speculation. In this study, water deficit destroyed the chloroplast structure of maize seedlings, damaged photosynthetic organs, and affected the photosynthetic process. However, SA-sprayed maize seedlings experienced the least PEG-induced chloroplast damage, with more neat grana thylakoid stacking and clearer grana and matrix lamellae, indicating that SA treatment could protect the integrity of the chloroplast in leaves under PEG treatment, reducing the water-deficit damage to the photosynthetic apparatus and thereby maintaining the photosynthetic performance of seedlings, increasing the assimilation capacity of mesophyll cells, and maintain higher photosynthetic rate.

4.2. Exogenous SA Contributed to Maintain Higher Photosynthetic Capacity in Maize Seedlings under Water Deficit by Protecting PSII Reaction Centers

The chloroplast gene psbA was responsible for reproducing new D1 proteins to repair the damaged PSII [53]. It was reported that abiotic stresses, such as high temperature and strong light, caused a significant decrease in psbA transcripts in wheat leaves [53]. In this study, we found that water-deficit stress led to a significant decrease in psbA transcripts, but spraying the maize seedlings with SA inhibited the decline of psbA transcripts during water deficit. We speculated that psbA transcription induced by SA spraying might enhance the de novo synthesis of the D1 protein for the replacement of injured protein and dissipate more excess light energy [54], suggesting that SA might function as a signal molecule involved in turnover regulation of D1 protein under environmental stresses.
It is well established that the production of excessive excitation energy under water-deficit conditions causes impaired electron transfer to the PSII reaction center as opposed to the increase in heat dissipation, occurrence of photoinhibition, reduction in light energy utilization efficiency, and the imbalance in excitation energy distribution between PSI and PSII [55]. Chl a fluorescence kinetics technology, an effective and noninvasive method generally used to quantify the photochemical efficiency of PSII, is now commonly employed in detecting the stress damage to the PSII reaction center [56,57,58]. It was reported that plants had developed various processes to alleviate the damage caused by excessive excitation energy to the PSII reaction center, such as changing energy absorption, trapping, electron transport, and dissipation per cross section [35,59]. Notably, in this study, the changes in chlorophyll fluorescence parameters—indicators of PSII structure and function—might be due to the variations in damaged PSII reaction centers in PEG treatment, suggesting that the photosynthetic apparatus and cell membrane system were damaged by PEG-induced water deficit. Furthermore, the chlorophyll degradation under the PEG treatment aggravated the damage of the electron transport chain that could cause excessive accumulation of ROS [60], while the exogenous SA protection of the photosystem could reverse the water-deficit caused inhibition of the potential activity of PSII in maize seedlings. In addition, exogenous SA could reduce the energy dissipated by the reaction center, allocate more energy to electron transfer, and repair the electron transfer to the PSII reaction center, thereby increasing the generation of energies needed for countering PEG-induced water deficit.

4.3. Exogenous SA Improved the Efficiency of Photosynthetic Carbon Fixation by Activating Photosynthetic Enzymes

Rubisco inhabits the chloroplast stroma and functions as a key enzyme in the photosynthetic carbon assimilation related to energy metabolism [61]. Rubisco has dual functions; it can catalyze the first major carbon fixation reaction in the Calvin photosynthesis cycle and catalyze Ribulose-1,5-bisphosphate (RuBP) into the photorespiration pathway [55]. Recent studies have demonstrated that although the content of Rubisco accounts for more than 50% of soluble protein in leaves, its catalytic efficiency is very low, and the carboxylation activity of Rubisco must be activated by molecular chaperone RCA in vivo [62]. During the current study, we found that the activities of Rubisco and RCA in maize seedlings decreased under PEG treatment, followed by the decrease in net photosynthetic rate, which was associated with previous studies showing that water deficit reduced the activities of Rubisco and RCA in plants, thereby inhibiting their photosynthesis [63]. It was found that SA pretreatment alleviated the reduction in Pn during heat stress by maintaining a high Rubisco activation state and maintained PSII function to accelerate the recovery of Pn in grapevine leaves [30]. Therefore, we speculated that the protection of SA in PEG-treated maize seedlings could be achieved by affecting the activity of photosynthesis-related proteins and maintaining the PSII function.
Rubisco’s large and small subunits were encoded rbcL and rbcS, respectively, and transported to the chloroplast and assembled into a Rubisco enzyme with 16 subunits [64]. It was found that under PEG treatment, rice seedlings compensated for the damage to their encoded protein subunits caused by reactive oxygen species by increasing the transcription levels of rbcL and rbcS [65]. In barley, Rubisco activase A was reported to have a critical regulation role in drought and salinity combined stress tolerance [66]. It was found that the expression level of the RCA gene was almost unchanged during short-term drought and salt stresses but significantly downregulated by gradually increasing drought stress in early seedling samples [64]. The expression level of genes corresponding to the photosynthetic process in plants was regulated by many factors and might also be closely related to the regulation of other substances. In this study, the differential expression of rbcL, rbcS, and RCA transcripts under different treatments might lead to activity differences between Rubisco and RCA.
It has been reported that the SA pathways regulating the photosynthetic system in abiotic stress include proline metabolism, ethylene formation, proline metabolism and ethylene formation, Ascorbate (AsA) -glutathione (GSH) cycle metabolism, antioxidant metabolism, and nitrogen and sulfur assimilation [27,28,29]. In this study, the damage to chloroplast structure and the decrease in light energy utilization efficiency caused by water deficit might result from the excessive accumulation of ROS, a by-product of chloroplast metabolism under stressful conditions [60,67]. Interestingly, it was found that the ROS-mediated signaling pathway is one of the chloroplast retrograde signal transduction pathways, which plays a vital role in plant response to drought [60]. It was also reported that there is an antagonistic effect between SA and chloroplast retrograde signal transduction [31]. Research showed that the nucleotide phosphatase (SAL1)-3′-phosphoadenosine-5′-phosphate (PAP) chloroplast retrogrades signaling regulates plant drought stress response by regulating stomatal movement [68]. Meanwhile, it was found that the SAL1-PAP chloroplast retrograde signaling pathway is also regulated by SA and JA-mediated signaling pathways [69]. Therefore, we speculate that SA, as an important stress signal molecule, might interact with ROS signal transduction and chloroplast retrograde signaling pathway in some way to maintain chloroplast protein quantity control, protect the photosynthetic system, and improve water-deficit resistance. However, chloroplast retrograde signaling is a complex signal-regulatory network involving the interaction between many signal molecules and regulatory pathways. How SA interacts with these signaling pathways to regulate chloroplast retrograde signaling pathways and maintain the function of chloroplasts under stresses still needs in-depth research.

5. Conclusions

In conclusion, SA plays a critical role in the response of photosynthesis to water deficit. However, the regulation mechanism of SA as a signal molecule involved in the adaptability of maize seedlings to water deficit still needs to be further explored.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/agronomy13092443/s1, Table S1: List of the specific primers used for qRT-PCR.

Author Contributions

Project administration, L.X., J.W., and Q.Y.; funding acquisition, L.X.; supervision, L.X., and Q.Y.; investigation, L.X., and J.W.; data curation, L.X., and J.W.; writing—original draft preparation, L.X., J.W., and Q.Y.; writing—review and editing, L.X., J.W., and Q.Y. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by grants from the Key Technology Developing Program of Henan Province (222102110338), the Youth Fund Project of Xinyang Agriculture and Forestry University (2019LG013), and the Young Backbone Teachers Training Program of Xinyang Agriculture and Forestry University (2021).

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Phenotypes analysis of maize plants under different treatments. (A) Fresh weight of shoot and root in maize seedlings under different treatments. (B) Dry weight of shoot and root in maize seedlings under different treatments. (C) Leaf RWC level in maize seedlings under different treatments. Data are given as means ± standard deviation (SD). Significant differences were determined by the Duncan’s multiple range test (p < 0.05) and represented by different lowercase letters.
Figure 1. Phenotypes analysis of maize plants under different treatments. (A) Fresh weight of shoot and root in maize seedlings under different treatments. (B) Dry weight of shoot and root in maize seedlings under different treatments. (C) Leaf RWC level in maize seedlings under different treatments. Data are given as means ± standard deviation (SD). Significant differences were determined by the Duncan’s multiple range test (p < 0.05) and represented by different lowercase letters.
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Figure 2. Gas exchange parameters in leaves of maize seedlings under different treatments. (A) Photosynthetic rate (Pn), (B) transpiration rate (Tr), (C) stomatal conductance (Gs), and (D) intercellular CO2 concentration (Ci) in leaves of maize seedlings under different treatments. Significant differences were determined by the Duncan’s multiple range test (p < 0.05) and represented by different lowercase letters.
Figure 2. Gas exchange parameters in leaves of maize seedlings under different treatments. (A) Photosynthetic rate (Pn), (B) transpiration rate (Tr), (C) stomatal conductance (Gs), and (D) intercellular CO2 concentration (Ci) in leaves of maize seedlings under different treatments. Significant differences were determined by the Duncan’s multiple range test (p < 0.05) and represented by different lowercase letters.
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Figure 3. Chlorophyll content in the leaves of maize seedlings under different treatments. (A) Chlorophyll a content, (B) chlorophyll b content, (C) carotenoid content, and (D) total chlorophyll content in the leaves of maize seedlings under different treatments. Data are given as means ± SD. Significant differences were determined by the Duncan’s multiple range test (p < 0.05) and represented by different lowercase letters.
Figure 3. Chlorophyll content in the leaves of maize seedlings under different treatments. (A) Chlorophyll a content, (B) chlorophyll b content, (C) carotenoid content, and (D) total chlorophyll content in the leaves of maize seedlings under different treatments. Data are given as means ± SD. Significant differences were determined by the Duncan’s multiple range test (p < 0.05) and represented by different lowercase letters.
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Figure 4. Chlorophyll fluorescence parameters in the leaves of maize seedlings under different treatments. (A) Fv/Fo, (B) Fv/Fm, (C) Eto/RC, and (D) DIo/RC in the leaves of maize seedlings under different treatments. Data are given as means ± SD. Significant differences were determined by the Duncan’s multiple range test (p < 0.05) and represented by different lowercase letters.
Figure 4. Chlorophyll fluorescence parameters in the leaves of maize seedlings under different treatments. (A) Fv/Fo, (B) Fv/Fm, (C) Eto/RC, and (D) DIo/RC in the leaves of maize seedlings under different treatments. Data are given as means ± SD. Significant differences were determined by the Duncan’s multiple range test (p < 0.05) and represented by different lowercase letters.
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Figure 5. Chloroplast ultrastructure in leaves of maize seedlings under different treatments. (A) CK; (B) SA; (C) PEG; (D) SA + PEG; bar = 1 μm. CM, chloroplast membrane; GL, Grana lamellae; SL, Stroma lamellae; OG, Osmiophilic granule.
Figure 5. Chloroplast ultrastructure in leaves of maize seedlings under different treatments. (A) CK; (B) SA; (C) PEG; (D) SA + PEG; bar = 1 μm. CM, chloroplast membrane; GL, Grana lamellae; SL, Stroma lamellae; OG, Osmiophilic granule.
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Figure 6. The enzyme activity of (A) Rubisco activase (RCA) and (B) Rubisco in leaves of maize seedlings under different treatments. Data are given as means ± SD. Significant differences were determined by the Duncan’s multiple range test (p < 0.05) and represented by different lowercase letters.
Figure 6. The enzyme activity of (A) Rubisco activase (RCA) and (B) Rubisco in leaves of maize seedlings under different treatments. Data are given as means ± SD. Significant differences were determined by the Duncan’s multiple range test (p < 0.05) and represented by different lowercase letters.
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Figure 7. The relative expression level of (A) psbA, (B) RCA, (C) rbcL, and (D) rbcS in leaves of maize seedlings under different treatments. Data are given as means ± SD. Significant differences were determined by the Duncan’s multiple range test (p < 0.05) and represented by different lowercase letters.
Figure 7. The relative expression level of (A) psbA, (B) RCA, (C) rbcL, and (D) rbcS in leaves of maize seedlings under different treatments. Data are given as means ± SD. Significant differences were determined by the Duncan’s multiple range test (p < 0.05) and represented by different lowercase letters.
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Figure 8. Spearman’s correlation analysis between different measured traits.
Figure 8. Spearman’s correlation analysis between different measured traits.
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Xin, L.; Wang, J.; Yang, Q. Exogenous Salicylic Acid Alleviates Water Deficit Stress by Protecting Photosynthetic System in Maize Seedlings. Agronomy 2023, 13, 2443. https://doi.org/10.3390/agronomy13092443

AMA Style

Xin L, Wang J, Yang Q. Exogenous Salicylic Acid Alleviates Water Deficit Stress by Protecting Photosynthetic System in Maize Seedlings. Agronomy. 2023; 13(9):2443. https://doi.org/10.3390/agronomy13092443

Chicago/Turabian Style

Xin, Longfei, Jiajia Wang, and Qinghua Yang. 2023. "Exogenous Salicylic Acid Alleviates Water Deficit Stress by Protecting Photosynthetic System in Maize Seedlings" Agronomy 13, no. 9: 2443. https://doi.org/10.3390/agronomy13092443

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