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Article

Exogenous Melatonin Alleviates Osmotic Stress by Enhancing Antioxidant Metabolism, Photosynthetic Maintenance, and Hormone Homeostasis in Forage Oat (Avena sativa) Seedlings

by
Jingbo Yu
1,
Xingyu Luo
1,
Qingping Zhou
1,
Zhou Li
2,* and
Shiyong Chen
1,3,*
1
Sichuan Zoige Alpine Wetland Ecosystem National Observation and Research Station, Southwest Minzu University, Chengdu 610041, China
2
College of Grassland Science and Technology, Sichuan Agricultural University, Chengdu 611130, China
3
College of Animal and Veterinary Sciences, Southwest Minzu University, Chengdu 610041, China
*
Authors to whom correspondence should be addressed.
Grasses 2024, 3(3), 190-204; https://doi.org/10.3390/grasses3030014
Submission received: 2 July 2024 / Revised: 23 August 2024 / Accepted: 28 August 2024 / Published: 3 September 2024
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Abstract

:
Melatonin (MT) is a multifunctional hormone that enhances crop resilience against various abiotic stresses. However, its regulatory mechanism of osmotic tolerance in forage oats (Avena sativa) plants under water-limited scenarios is still unclear. This study aimed to delineate the impact of MT pretreatment on the morphological, physiological, and biochemical functions of oat seedlings under osmotic stress. Our findings demonstrated that exogenous treatment of MT noticeably elevated leaf area while decreasing the root/shoot ratio of oat seedlings subjected to osmotic stress. Osmotic-induced 38.22% or 48.37% decrease in relative water content could be significantly alleviated by MT pretreatment on day 7 or day 14, respectively. MT treatment also significantly mitigated osmotic-induced decreases in photosynthetic parameters including net photosynthetic rate, stomatic conductance, and intercellular CO2 concentration as well as various chlorophyll fluorescence parameters, which could contribute to enhanced accumulations of free proline and soluble sugars in seedlings after being subjected to a prolonged duration of osmotic stress. Furthermore, MT markedly improved antioxidant enzyme activities including superoxide dismutase, ascorbate peroxidase, catalase, and peroxidase along with the accumulation of ascorbic acid contributing to a significant reduction in reactive oxygen species under osmotic stress. In addition, the MT application induced a 978.12%, 33.54%, or 30.59% increase in endogenous MT, indole acetic acid, or gibberellic acid content under osmotic stress but did not affect the accumulation of abscisic acid. These findings suggest that an optimal concentration of MT (100 μmol·L−1) could relieve osmotic stress via improvement in osmotic adjustment, the enzymatic antioxidant defense system, and endogenous hormonal balance, thereby contributing to enhanced photosynthetic functions and growth of oat seedlings under water-limited conditions.

1. Introduction

For several centuries, it has been elucidated that drought presents a significant limitation to agricultural yields in arid and semi-arid areas worldwide. Reports about crop losses are increasing each year, especially in developing countries due to drought, hence imparting a major obstacle to food security [1]. In plant research, osmotic solutions are used to simulate drought stress conditions and reveal the growth-repressing mechanisms. Polyethylene glycol 6000 (PEG-6000) is widely used as an osmotic regulator to induce osmotic stress by simulating water potential [2]. Its effectiveness in studying the effects of osmotic stress has been well-documented across various crop species, including wheat (Triticum aestivum), rice (Oryza sativa), and barley (Hordeum vulgare), etc. [3,4,5]. Osmotic stress considerably reduced protection against dehydration, thereby resulting in reduced morphological, physiological, and biochemical functions of plants [6]. To counter the hazardous effects of osmotic stress, plants have naturally evolved various strategies to escape or alleviate water deficit. For example, osmotic stress triggers the overproduction of specific reactive oxygen species (ROS), namely superoxide anion (O2−.) and hydrogen peroxide (H2O2) in plants, which are responsible for oxidative stress and even programmed cell death [7]. Therefore, plants tend to enhance both enzymatic and non-enzymatic antioxidants within the antioxidant defense system to minimize ROS accumulation under osmotic stress [8,9,10]. Additionally, osmotic stress disrupted phytohormone metabolism and also decreased photosynthesis, transpiration, and water use efficiency [11,12]. Hence, exploring the underlying mechanisms conferring osmotic stress tolerance in plants has become an important objective in crop breeding and management.
Plant growth regulators (PGRs) are involved in plant growth, development, and stress tolerance [13,14,15]. Melatonin (MT) is recognized as a natural indoleamine hormone in relation to plant development [16,17], photosynthetic performance [18], leaf senescence [19], and fruit ripening and storage [20]. Numerous research studies have been carried out to indicate the physiological functions of MT in plants associated with the modulation of resilience against various abiotic stressors, for instance, drought [21], cold [22], and salinity [23]. MT acted directly as a potent antioxidant to enhance plant tolerance by reducing ROS accumulation [24,25]. Hong et al. noticed that exogenous MT largely inhibited chlorophyll (Chl) degradation and the expression of senescence-related genes in rice, contributing to delayed leaf senescence [19]. In maize (Zea mays) seedlings, exogenous application of MT enhanced biochar efficiency under drought stress [26]. Exogenous MT activated antioxidant enzymes such as ascorbate peroxidase (APX), catalase (CAT), superoxide dismutase (SOD), peroxidase (POD), dehydroascorbate reductase (DHAR), and glutathione reductase (GR), thereby inhibiting ROS accumulation in leaves under osmotic stress [27].
Oat (Avena sativa) stands as a vital cosmopolitan compact crop with high nutritional content and a wide range of adaptability to drought [28,29]. As an essential forage crop, oat cultivation is increasing with increasing demand from rapidly growing animal husbandry in the world [30,31]. Conversely, the shortage of water resources restricts oat growth and production worldwide. Although previous research has examined the effects of melatonin on Avena nuda and Avena sativa under osmotic stress, as well as its role in alleviating other stress effects, these studies have not fully provided a detailed analysis of how melatonin influences key physiological and biochemical responses and interactions between melatonin and endogenous hormones [32,33,34]. Therefore, the current study intended to reveal the impacts of exogenous MT on alleviating osmotic-induced damage to oat plants based on analyses of growth and physiological parameters and to further explore the potential functions of MT in improving the osmotic stress of oats related to alterations in photosynthetic performance, antioxidant metabolism, and endogenous phytohormones.

2. Materials and Methods

2.1. Plant Materials and Treatments

Oat seeds (cultivar “Qing Yan No.1”) were obtained from the Southwest Minzu University, China. Seeds were disinfected in 75% ethanol for 10 min and subsequently rinsed twice with deionized water. After this, seeds were sowed on quartz sands in plastic containers (21 × 15 × 6 cm) which were placed within a plant growth chamber (MRC-350B-LED, Nanda Wanhao Technology Co., Ltd., Nanjing, China) with 600 μmol·m−2·s−1 PAR (Photosynthetically Active Radiation), 16 h/8 h photoperiod, 23/19 °C (day/night), and 65% relative humidity. At 7 days post-germination, Hoagland nutrient solution was applied to the seedlings until two-leaf stage [35]. Prior to osmotic stress, a group of seedlings was cultivated with 100 μmol·L−1 MT solution, while the other remained unaffected. At two-leaf stage, all plants were divided into three treatments as follows: (1) control (C): seedlings were cultured normally with Hoagland nutrient solution; (2) drought treatment (D): seedlings were cultivated in 15% PEG-6000 (Polyethylene Glycol-6000) that was dissolved in Hoagland nutrient solution; (3) drought + MT treatment (D + MT): seedlings were cultivated with 100 μmol·L−1 melatonin solution and later cultivated in Hoagland’s solution containing 15% PEG 6000. Each treatment comprised four biological replicates and was carried out under completely randomized design (CRD).

2.2. Determination of Morphological Traits

The length–width coefficient method was utilized to estimate the leaf area. The root/shoot ratio reflected the correlation between the underground and aboveground parts. Separately, the fresh weights (FW) of roots and shoots were determined using a balance. After this, samples were dried at 105 °C for 30 min and later at 80 °C for 72 h to measure their dry weight (DW). Root/shoot ratio was determined by the ratio of root DW to shoot DW. Plant height was measured by using a ruler, and six plants were selected as independent biological replications.

2.3. Determination of Photosynthetic Characteristics, Leaf Water Status, and Osmolytes

Chl content was determined by acetone–ethanol mixture extraction method [36]. Fresh leaf tissues (0.2 g) were finely sliced into small fragments, soaked in 10 mL of 80% acetone and 10 mL of 95% ethanol, and stored in a dark place. The absorbance of extracts was measured at 663 and 645 nm (OD663 and OD645). Chl content was calculated using the formula illustrated by Arnon [37]. Net photosynthesis rate (Pn), stomatal conductance (GS), intercellular CO2 concentration (Ci), transpiration rate (Tr), optimal/maximal PSII efficiency (Fv/Fm), electron transport rate (ETR), photochemical quenching (qP), non-photochemical quenching (qN), actual photochemical efficiency (ΦPSII), and photochemical efficiency of PSII (Fv’/Fm’) of the third functional leaf of oat seedlings were measured every two days from 0 d to 15 d of osmotic stress between 9:00 AM and 10:00 AM using the LI-6800 portable photosynthesizer system (LI-COR, LI-COR Biosciences Co., Ltd., Lincoln, NE 68504, USA).
Leaf relative water content (RWC) was determined following the method of Barrs et al. [38]. Fresh leaf tissues (0.1 g) were excised and weighed mechanically to get the FW. Later, samples were dipped in deionized water for one-day interval, and turgid weight (TW) was recorded. DW of the leaf samples was ascertained by oven-drying at 75 °C for a duration of 72 h. The RWC (%) was calculated as RWC (%) = [(FW − DW)/(TW − DW)] × 100. According to the sulfuric acid-anthrone colorimetric method, soluble sugar content (SSC) was determined [39]. Free proline (Pro) content in seedlings was estimated using the sulfosalicylic acid-acid ninhydrin method [40].

2.4. Determination of Oxidative Damage and Cell Membrane Stability

O2−∙ content was determined using the procedure described by Velikova et al. [41], and the O2− content was noted spectrophotometerically at 530 nm. H2O2 content was estimated using the method described by Yu et al. [42]. The H2O2 content was measured by observing the absorbance at 390 nm. Malondialdehyde (MDA) content in seedlings was measured following the thiobarbituric acid method [43]. Relative conductivity (REC) was determined by a conductivity meter (DDS-307A, Precision & Scientific Instrument Co., Ltd., Shanghai, China), and 0.1 g of fresh leaf samples was kept in a test tube with 10 mL of deionized water for 24 h at room temperature. After this, the initial conductivity (S1) was measured. The final conductivity (S2) of solution was measured after it was boiled in a water bath at 105 °C for 2 h. REC (%) was calculated based on REC (%) = (S1/S2) × 100% [44].

2.5. Determination of Antioxidant Enzyme Activities and Non-Enzymatic Antioxidants

The POD activity was measured according to the guaiacol method [45], and the absorbance was measured at 460 nm. The activity of SOD was measured by noting the photochemical reduction rate of Nitro-Blue tetrazolium chloride at 560 nm [46]. The CAT activity was assessed following the protocol described by Chance and Maehly [45], and the absorbance was recorded at 240 nm. The APX activity was measured spectrophotometerically at 290 nm by the method described by Nakano et al. [47]. The reduced forms of ascorbic acid (ASA) or glutathione (GSH) were determined by using the kit (Art. No. ASA-1-W or Art. No. GSH-1-W) base on the method of 5,5′-dithiobis-(2-nitrobenzoic acid) (DTNB) [48] or the red phenanthroline method [49] in accordance with the manufacturer’s instructions (Suzhou Comin Biotechnology Co., Ltd., Suzhou, China), respectively.

2.6. Determination of Endogenous Hormones

To estimate the hormone content, leaf samples (0.2 g) were meticulously pulverized into a fine powder using a mortar and pestle, and then these powders were subsequently mixed with 1 mL of 80% (v/v) methanol at 4 °C for a duration of 12 h. After being centrifuged at 4 °C and 8000× g for 10 min, supernatants were used to detect endogenous hormonal contents including gibberellin (GA3), indoleacetic acid (IAA), abscisic acid (ABA), and endogenous MT by using HPLC–MS/MS analysis as described in previous studies [50,51].

2.7. Statistical Analysis

Statistical analyses were conducted using one-way ANOVA, followed by Duncan’s test in SPSS version 22.0 (SPSS, Chicago, IL, USA). The means were tested using the least significant difference test (LSD test) at p ≤ 0.05. Figures were drawn using Origin 2021 software (Origin Lab, Northampton, MA, USA).

3. Results

3.1. Effects of Melatonin on Water Status and Morphology under Osmotic Stress

Leaf relative water content continued to decline with the prolonged osmotic stress, and MT-treated plants (D + MT) demonstrated a 38.22% or 48.37% upsurge in relative water content than untreated plants (D) on the 7th or 14th day of osmotic stress, respectively (Figure 1A). MT pretreatment induced significant increases in soluble sugar content and free proline content in oat plants subjected to osmotic stress (Figure 1B,C). Pro content in the D + MT treatment was 1.7 times higher as compared with the D treatment on the 7th or 14th day of osmotic stress, respectively (Figure 1B). Soluble sugar content in the D treatments increased by 1.24 times as compared with the control on the 7th day, and the soluble sugar content in MT-treated plants exhibited a 1.26-fold increase in comparison to the MT-untreated plants (Figure 1C). Osmotic stress causes a significant reduction in plant height and leaf area but improves the root/shoot ratio of oat plants (Figure 2A–C). Seedling height was not affected by the MT, but MT treatment significantly alleviated the reduction in leaf area induced by osmotic stress while a notable deterioration in the root/shoot ratio was observed (Figure 2A–C).

3.2. Effects of Melatonin on Oxidative Damage and Antioxidant Metabolism under Osmotic Stress

Osmotic stress induced oxidative injury to seedlings, as demonstrated by higher H2O2, O2−, malondialdehyde content, and relative conductivity levels (Figure 3A–D). On the 7th day of osmotic stress, the MT-treated seedlings exhibited a significant decrease in the H2O2 and O2− contents, when compared to untreated seedlings under water scarcity, respectively (Figure 3A,B). On the 14th day, the accumulation of H2O2 and O2− was further alleviated by the MT treatment and decreased by 1.38-fold and 3.74-fold, when relative to osmotic-stressed seedlings without MT treatment, respectively (Figure 3A,B). Malondialdehyde content and relative conductivity increased significantly under osmotic stress (Figure 3C,D). The malondialdehyde content exhibited a significant decline in the D + MT treatment, with decreases of 33.74% or 72.51%, while REC in the D + MT treatment declined by 3.40-fold or 2.29-fold on the 7th and 14th day, respectively (Figure 3C,D).
The enzymatic antioxidant activity (SOD, CAT, POD, and APX) markedly increased in osmotic-stressed oat seedlings (Figure 4A–D). MT application significantly increased the activities of these four antioxidant enzymes under osmotic stress (Figure 4A–D). On the 14th day of osmotic stress, the superoxide dismutase activity in the D + MT treatment was significantly elevated relative to the D treatment (Figure 4A). Water-stressed seedlings with MT application increased catalase or peroxidase activity by 1.27 or 1.26 times on the 14th day of osmotic stress compared to the osmotic-stressed seedlings without the MT application, respectively (Figure 4B,C). On the 7th and 14th days of osmotic stress, ascorbic acid content in the D + MT treatment was elevated by 44.11% and 20.66%, respectively, when compared to the D treatment (Figure 5A). GSH content in oat seedlings showed a marked increase upon osmotic stress exposure (Figure 5B). On the 7th day of osmotic stress, in comparison to the control, the increments in GSH content for the D + MT and D treatments were 1.93-fold and 1.54-fold, respectively (Figure 5B). On the 14th day of osmotic stress, the glutathione contents in the D + MT and D treatments showed further increases as compared with the control (Figure 5B).

3.3. Effects of Melatonin on Photosynthetic Parameters and Photochemical Efficiency under Osmotic Stress

On the 7th day, osmotic stress resulted in a significant reduction in total chlorophyll content, chlorophyll a, and chlorophyll b in all plants, as well as no significant differences in total chlorophyll and chlorophyll a content between the D and D + MT treatments (Figure 6A–C). On the 14th day, in contrast to the D treatment, the D + MT treatment displayed enhanced levels of chlorophyll a, chlorophyll b, total chlorophyll, and carotenoid contents. (Figure 6A–D). Pn, Gs, and Ci gradually decreased with increasing osmotic stress time, whereas the D + MT maintained significantly higher Pn, Gs, and Ci compared to the D treatment during osmotic stress (Figure 7A–C). Osmotic stress also resulted in a significant reduction in Tr in the D treatment, but the effect of osmotic stress on Tr in the D + MT was not as obvious as Tr in the D on the 12th and 15th days (Figure 7D). On the 9th day of osmotic stress, Pn, Gs, Tr, and Ci in the D + MT treatment increased by 84.31%, 158.87%, 24.90%, or 6.45% as compared to the D treatment, respectively (Figure 7A–D). Fluorescence parameters were affected negatively by osmotic stress (Figure 8A–F). As the osmotic stress continued, the Fv/Fm, ETR, qP, qN, Fv’/Fm’, and ΦPSII exhibited a declining trend across all plants (Figure 8A–F). On the 9th and 12th days of osmotic stress, the D + MT treatment exhibited significantly higher F/Fm, ETR, qP, qN, and ΦPSII compared to the D treatment, respectively (Figure 8A–D,F), while Fv’/Fm’ exhibited no significant variations between the D and the D + MT (Figure 8E).

3.4. Effects of Melatonin on Endogenous Hormone under Osmotic Stress

Among the three treatments (C, D, and D + T), MT content was the highest in D + MT and the lowest in C (Figure 9A). The content of MT in the D treatment was 1.59 times higher than the C. However, D + MT treatment showed 9.78 times higher MT content as compared with the control (Figure 9A). While osmotic stress notably reduced IAA content in plants without MT application, it had no significant impact on the IAA content in the D + MT treatment (Figure 9B). Osmotic stress induced a significant increase in the accumulation of ABA in all plants, but exogenous application of MT exhibited no significant influence on ABA content under osmotic stress (Figure 9C). In comparison to the control, the GA3 content was significantly reduced in the D treatment. In contrast, the D + MT treatment registered a significant 30.59% increase in GA3 content compared to the D treatment (Figure 9D).

4. Discussion

Drought stands as a predominant abiotic stressor, limiting crop development and productivity [52]. Previously, Gao et al. noted that MT treatment in the root zone significantly alleviated osmotic-induced declines in the fresh and dry weight of naked oat plants but did affect plant height [27], which was consistent with our present research. Interestingly, the osmotic-stress-induced increase in the root/shoot ratio could be significantly weakened by the MT application in oat plants. It has been demonstrated that an improvement in the root/shoot ratio contributed to enhanced drought tolerance in different plant species, since more roots will be propitious to obtain more available water from soil [53,54,55]. The water status in plants is frequently assessed using leaf RWC. Accumulations of osmo-protectant compounds such as free Pro and soluble sugars were beneficial to osmotic balance in plants subjected to drought stress [56]. It was observed that the exogenous application of MT significantly improved accumulations of free Pro and soluble sugar in the current study, indicating that the MT regulated osmotic balance to decrease water loss in leaves. A recent study by EL-Bauome et al. similarly showed that foliar application of MT enhanced accumulations of Pro and soluble sugars associated with the mitigation of drought-induced declines in leaf RWC and aboveground growth of cauliflower (Brassica oleracea) plants [57]. This offers insight into why, during sustained osmotic stress, oat plants treated with MT prioritized increased aboveground growth over a higher root/shoot ratio: MT-treated oat plants suffered from less water deficit in leaves than untreated plants during the same period of osmotic stress.
Chl is the chief pigment that is responsible for the absorption, transfer, and conversion of light energy. Its content reflects the efficiency of photosynthetic carbon sequestration and the sensitivity of plants to drought stress [58,59]. Wang et al. found that the exogenous supply of MT could significantly alleviate Chl degradation and photoinhibition, thus effectively slowing down the aging process of apple (Malus domestica) plants under drought stress [60], which matches the evidence presented in our current research. Drought-induced Chl degradation directly resulted in losses in photosynthetic functions such as reduced photosynthesis and Chl fluorescence in sorghum (Sorghum bicolor) leaves [61]. Previous findings suggest that Pn, Gs, Tr, Fv/Fm, qP, and ETR significantly reduced when wheat plants were subjected to drought stress [62,63]. It is widely recognized that reduced photosynthesis is mainly an effect of stomatal and non-stomatal limitation [64]. Osmotic stress significantly decreased photosynthetic (Pn, Gs, Ci, or Tr) and photochemical (Fv/Fm, ETR, qP, or ΦPSII) parameters in oat plants. Gradual declines in Pn and Fv/Fm were followed by gradual decreases in Gs and Ci during a prolonged period of osmotic stress, indicating drought-induced photoinhibition in oat plants was mainly due to stomatal limitation. However, the MT pretreatment significantly alleviated the negative effects of drought on photosynthetic and photochemical indicators in oat plants subjected to osmotic stress. It could be inferred that MT improved osmotic adjustment, contributing to an improved water status in the leaves of oat plants under osmotic stress, which provided a better intracellular environment for photosynthetic performance. In addition, photosynthetic maintenance will contribute to better biosynthesis and metabolism of photosynthetic products such as soluble sugars for growth and osmotic adjustment during long-term osmotic stress.
Osmotic stress also interferes with electron transfer to molecular oxygen in leaf chloroplasts, resulting in the production of ROS that is responsible for oxidative damage, photosynthetic inhibition, and eventually cell death [65,66,67]. Plants have evolved an indigenous defense system comprising enzymatic (SOD, POD, CAT, or APX) and non-enzymatic antioxidants (ASA and GSH) to minimize ROS-induced oxidative stress. SOD is responsible for the dismutation of O2− to form H2O2 and O2, whereas POD, CAT, and APX are important enzymes associated with H2O2 quenching [68]. Osmotic stress exhibited a significantly enhanced production of H2O2, O2−, and MDA, leading to a damaged cell membrane system as reflected by increased EL levels in oat seedlings. Exogenous application of MT markedly reduced drought-induced oxidative damage and the loss in cell membrane stability associated with significant increases in SOD, CAT, POD, and APX activities in oat plants subjected to osmotic stress. Corresponding findings were reported by Hossain et al. in buckwheat (Fagopyrum tataricum) under drought stress [69]. Furthermore, GSH and ASA, recognized as essential non-enzymatic antioxidants in the ASA-GSH cycle, have been reported to effectively scavenge ROS under stress conditions [68]. Here, we found that osmotic stress led to a significant decrease in ASA content but increased GSH content in oat plants. However, the effect of MT on ASA and GSH was different. The findings indicated that MT-regulated antioxidant defense in oat plants was mainly related to the activation of various antioxidant enzymes and ASA instead of accumulations of non-enzymatic antioxidants including GSH under osmotic stress. These results are consistent with the study conducted by Imran et al., which found that an exogenous supply of MT mitigated the excessive ROS-induced oxidative damage by strengthening SOD, CAT, POD, and APX activities in soybean (Glycine max) plants under water stress, which provided a better cellular redox state for growth [70].
Plant tolerance to drought could be improved by exogenous application of MT, salt, heat, cold, flooding, or heavy metal toxicity by regulating endogenous MT biosynthesis [71,72]. The results of this study indicate that osmotic stress enhances endogenous MT levels in seedlings; however, it does not improve tolerance under high osmotic pressure. In this study, exogenous application of MT stimulated the production of endogenous MT, similar to observations in rice [73]. Consequently, exogenous MT not only increased endogenous MT content but also appeared to regulate the antioxidant system and limit reactive oxygen species (ROS) generation. Furthermore, the exogenous administration of MT significantly influenced the biosynthesis of other plant hormones, such as gibberellins (GA) and abscisic acid (ABA). Previous research by Li et al. suggested that the MT significantly reduced endogenous ABA biosynthesis but enhanced antioxidant enzyme activities to detoxify H2O2 in two Malus species under drought stress [72]. Drought-induced accumulation of ABA in soybean plants could be inhibited by MT application, whereas MT enhanced endogenous salicylic acid and jasmonic acid contents. This indicates a potential link between MT-regulated drought tolerance and the mediation of endogenous phytohormones [70]. The present study also demonstrated that drought resulted in significant rises in endogenous MT and ABA contents but decreased IAA and GA3 contents in oat seedlings. However, the MT application significantly alleviated drought-induced declines in IAA and GA3 contents in oat leaves. It is well known that osmotic stress directly induces the ABA synthesis to regulate stomatal closure, thereby reducing transpiration and water loss [74]. The beneficial roles of GA3 and IAA have been also widely studied. For example, the supply of exogenous GA3 mitigated drought-induced injury to rapeseed (Brassica napus) associated with enhanced multiple antioxidant enzyme activities and accumulations of soluble sugar and free Pro [75]. Moreover, an appropriate dose of IAA supply could significantly mitigate drought damage to white clover (Trifolium repens) through inducing the accumulation of free amino acids such as Pro for osmotic adjustment and also enhancing the antioxidant defense system [76]. The MT-induced tolerance in oat seedlings could be associated with higher endogenous GA3 and IAA levels since they are essential for regulating plant growth and defense against stress. However, an in-depth mechanism is still required to clearly demonstrate the interaction of melatonin and other endogenous hormones when plants endure prolonged osmotic stress.

5. Conclusions

In summary, the exogenous application of MT is an efficient technique to mitigate drought-induced growth retardant of oat seedlings. The MT pretreatment significantly improved accumulations of Pro and soluble sugars associated with higher leaf RWC under osmotic stress, which provided a better intracellular environment for photosynthetic performance. In addition, exogenous MT significantly improved enzymatic antioxidant activities, hence reducing drought-induced oxidative damage in oat seedlings. MT-regulated increases in endogenous MT, IAA, and GA3 could be one of the key mechanisms related to enhanced drought tolerance and growth of oat seedlings in water-scarce environments, but it still demands in-depth exploration of the interaction of melatonin and other endogenous hormones in future studies.

Author Contributions

Conceptualization, J.Y., Z.L., and S.C.; methodology, J.Y. and Z.L.; software, J.Y. and S.C.; validation, J.Y. and Q.Z.; formal analysis, J.Y. and X.L.; investigation, X.L.; resources, Q.Z.; data curation, J.Y. and X.L.; writing—original draft preparation, J.Y. and X.L.; writing—review and editing, Z.L. and S.C.; supervision, S.C. and Z.L.; funding acquisition, Q.Z. and S.C. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Key Research & Development Program of Sichuan province (2021YFYZ0013, 2023NZZJ0002).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Data are contained within the article.

Conflicts of Interest

The authors declare no conflicts of interest.

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Figure 1. Effects of exogenous melatonin (MT) on (A) relative water content, (B) free proline content, and (C) soluble sugar content in leaves of oat seedlings under osmotic stress. Different letters above columns show significant difference by LSD (p < 0.05) on given day. Vertical bars indicate ± SE of mean (n = 4). C, control; D, osmotic stress; D + MT, osmotic-stressed seedlings were pretreated with 100 μmol·L−1 of MT.
Figure 1. Effects of exogenous melatonin (MT) on (A) relative water content, (B) free proline content, and (C) soluble sugar content in leaves of oat seedlings under osmotic stress. Different letters above columns show significant difference by LSD (p < 0.05) on given day. Vertical bars indicate ± SE of mean (n = 4). C, control; D, osmotic stress; D + MT, osmotic-stressed seedlings were pretreated with 100 μmol·L−1 of MT.
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Figure 2. Effects of exogenous melatonin (MT) on (A) seedling height, (B) leaf area, and (C) root/shoot ratio in oat seedlings under osmotic stress. Different letters above columns show significant difference by LSD (p < 0.05) on given day. Vertical bars indicate ±SE of mean (n = 4). C, control; D, osmotic stress; D + MT, osmotic-stressed seedlings were pretreated with 100 μmol·L−1 of MT.
Figure 2. Effects of exogenous melatonin (MT) on (A) seedling height, (B) leaf area, and (C) root/shoot ratio in oat seedlings under osmotic stress. Different letters above columns show significant difference by LSD (p < 0.05) on given day. Vertical bars indicate ±SE of mean (n = 4). C, control; D, osmotic stress; D + MT, osmotic-stressed seedlings were pretreated with 100 μmol·L−1 of MT.
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Figure 3. Effects of exogenous melatonin (MT) on (A) hydrogen peroxide (H2O2), (B) superoxide anion (O2−), (C) relative conductivity, and (D) malondialdehyde content in leaves of oat seedlings under osmotic stress. Different letters above columns show significant difference by LSD (p < 0.05) on given day. Vertical bars indicate ±SE of mean (n = 4). C, control; D, osmotic stress; D + MT, osmotic-stressed seedlings were pretreated with 100 μmol·L−1 of MT.
Figure 3. Effects of exogenous melatonin (MT) on (A) hydrogen peroxide (H2O2), (B) superoxide anion (O2−), (C) relative conductivity, and (D) malondialdehyde content in leaves of oat seedlings under osmotic stress. Different letters above columns show significant difference by LSD (p < 0.05) on given day. Vertical bars indicate ±SE of mean (n = 4). C, control; D, osmotic stress; D + MT, osmotic-stressed seedlings were pretreated with 100 μmol·L−1 of MT.
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Figure 4. Effects of exogenous melatonin (MT) on (A) superoxide dismutase (SOD), (B) catalase (CAT), (C) peroxidase (POD), and (D) ascorbate peroxidase (APX) activities in leaves of oat seedlings under osmotic stress. Different letters above columns show significant difference by LSD (p < 0.05) on given day. Vertical bars indicate ±SE of mean (n = 4). C, control; D, osmotic stress; D + MT, osmotic-stressed seedlings were pretreated with 100 μmol·L−1 of MT.
Figure 4. Effects of exogenous melatonin (MT) on (A) superoxide dismutase (SOD), (B) catalase (CAT), (C) peroxidase (POD), and (D) ascorbate peroxidase (APX) activities in leaves of oat seedlings under osmotic stress. Different letters above columns show significant difference by LSD (p < 0.05) on given day. Vertical bars indicate ±SE of mean (n = 4). C, control; D, osmotic stress; D + MT, osmotic-stressed seedlings were pretreated with 100 μmol·L−1 of MT.
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Figure 5. Effects of exogenous melatonin (MT) on (A) ascorbic acid (ASA) and (B) glutathione (GSH) contents in leaves of oat seedlings under osmotic stress. Different letters above columns show significant difference by LSD (p < 0.05) on given day. Vertical bars indicate ±SE of mean (n = 4). C, control; D, osmotic stress; D + MT, osmotic-stressed seedlings were pretreated with 100 μmol·L−1 of MT.
Figure 5. Effects of exogenous melatonin (MT) on (A) ascorbic acid (ASA) and (B) glutathione (GSH) contents in leaves of oat seedlings under osmotic stress. Different letters above columns show significant difference by LSD (p < 0.05) on given day. Vertical bars indicate ±SE of mean (n = 4). C, control; D, osmotic stress; D + MT, osmotic-stressed seedlings were pretreated with 100 μmol·L−1 of MT.
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Figure 6. Effects of exogenous melatonin (MT) on (A) total chlorophyll content, (B) chlorophyll a, (C) chlorophyll b, and (D) carotenoid in leaves of oat seedlings under osmotic stress. Different letters above columns show significant difference by LSD (p < 0.05) on given day. Vertical bars indicate ±SE of mean (n = 4). C, control; D, osmotic stress; D + MT, osmotic-stressed seedlings were pretreated with 100 μmol·L−1 of MT.
Figure 6. Effects of exogenous melatonin (MT) on (A) total chlorophyll content, (B) chlorophyll a, (C) chlorophyll b, and (D) carotenoid in leaves of oat seedlings under osmotic stress. Different letters above columns show significant difference by LSD (p < 0.05) on given day. Vertical bars indicate ±SE of mean (n = 4). C, control; D, osmotic stress; D + MT, osmotic-stressed seedlings were pretreated with 100 μmol·L−1 of MT.
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Figure 7. Effects of exogenous melatonin (MT) on (A) photosynthesis rate (Pn), (B) stomatal conductance (Gs), (C) intercellular CO2 concentration (Ci), and (D) transpiration rate (Tr) in leaves of oat seedlings under osmotic stress. Vertical bars indicate ±SE of the mean (n = 4). C, control; D, osmotic stress; D + MT, osmotic-stressed seedlings were pretreated with 100 μmol·L−1 of MT.
Figure 7. Effects of exogenous melatonin (MT) on (A) photosynthesis rate (Pn), (B) stomatal conductance (Gs), (C) intercellular CO2 concentration (Ci), and (D) transpiration rate (Tr) in leaves of oat seedlings under osmotic stress. Vertical bars indicate ±SE of the mean (n = 4). C, control; D, osmotic stress; D + MT, osmotic-stressed seedlings were pretreated with 100 μmol·L−1 of MT.
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Figure 8. Effects of exogenous melatonin (MT) on (A) optimal/maximal PSII efficiency (Fv/Fm), (B) electron transport rate (ETR), (C) photochemical quenching (qP), (D) non-photochemical quenching (qN), (E) photochemical efficiency of PSII (Fv’/Fm’), and (F) actual photochemical efficiency (ΦPSII) in leaves of oat seedlings under osmotic stress. Different letters above columns show significant difference by LSD (p < 0.05) on given day. Vertical bars indicate ±SE of mean (n = 4). C, control; D, osmotic stress; D + MT, osmotic-stressed seedlings were pretreated with 100 μmol·L−1 of MT.
Figure 8. Effects of exogenous melatonin (MT) on (A) optimal/maximal PSII efficiency (Fv/Fm), (B) electron transport rate (ETR), (C) photochemical quenching (qP), (D) non-photochemical quenching (qN), (E) photochemical efficiency of PSII (Fv’/Fm’), and (F) actual photochemical efficiency (ΦPSII) in leaves of oat seedlings under osmotic stress. Different letters above columns show significant difference by LSD (p < 0.05) on given day. Vertical bars indicate ±SE of mean (n = 4). C, control; D, osmotic stress; D + MT, osmotic-stressed seedlings were pretreated with 100 μmol·L−1 of MT.
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Figure 9. Effects of exogenous melatonin (MT) on (A) MT content, (B) indole-3-acetic acid (IAA) content, (C) abscisic acid (ABA) content, and (D) gibberellin (GA3) content in leaves of oat seedlings under osmotic stress. Different letters above columns show significant difference by LSD (p < 0.05) on given day. Vertical bars indicate ±SE of mean (n = 4). C, control; D, osmotic stress; D + MT, osmotic-stressed seedlings were pretreated with 100 μmol·L−1 of MT.
Figure 9. Effects of exogenous melatonin (MT) on (A) MT content, (B) indole-3-acetic acid (IAA) content, (C) abscisic acid (ABA) content, and (D) gibberellin (GA3) content in leaves of oat seedlings under osmotic stress. Different letters above columns show significant difference by LSD (p < 0.05) on given day. Vertical bars indicate ±SE of mean (n = 4). C, control; D, osmotic stress; D + MT, osmotic-stressed seedlings were pretreated with 100 μmol·L−1 of MT.
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MDPI and ACS Style

Yu, J.; Luo, X.; Zhou, Q.; Li, Z.; Chen, S. Exogenous Melatonin Alleviates Osmotic Stress by Enhancing Antioxidant Metabolism, Photosynthetic Maintenance, and Hormone Homeostasis in Forage Oat (Avena sativa) Seedlings. Grasses 2024, 3, 190-204. https://doi.org/10.3390/grasses3030014

AMA Style

Yu J, Luo X, Zhou Q, Li Z, Chen S. Exogenous Melatonin Alleviates Osmotic Stress by Enhancing Antioxidant Metabolism, Photosynthetic Maintenance, and Hormone Homeostasis in Forage Oat (Avena sativa) Seedlings. Grasses. 2024; 3(3):190-204. https://doi.org/10.3390/grasses3030014

Chicago/Turabian Style

Yu, Jingbo, Xingyu Luo, Qingping Zhou, Zhou Li, and Shiyong Chen. 2024. "Exogenous Melatonin Alleviates Osmotic Stress by Enhancing Antioxidant Metabolism, Photosynthetic Maintenance, and Hormone Homeostasis in Forage Oat (Avena sativa) Seedlings" Grasses 3, no. 3: 190-204. https://doi.org/10.3390/grasses3030014

APA Style

Yu, J., Luo, X., Zhou, Q., Li, Z., & Chen, S. (2024). Exogenous Melatonin Alleviates Osmotic Stress by Enhancing Antioxidant Metabolism, Photosynthetic Maintenance, and Hormone Homeostasis in Forage Oat (Avena sativa) Seedlings. Grasses, 3(3), 190-204. https://doi.org/10.3390/grasses3030014

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