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Review

Tolerance of Forage Grass to Abiotic Stresses by Melatonin Application: Effects, Mechanisms, and Progresses

by
Yufeng Fan
1,2,
Lingling Li
1,2,
Fenghui Guo
3 and
Xiangyang Hou
1,2,*
1
College of Grassland Science, Shanxi Agricultural University, Jinzhong 030801, China
2
Key Laboratory of Model Innovation in Forage Production Efficiency, Ministry of Agriculture and Rural Affairs, Jinzhong 030801, China
3
Industrial Crop Research Institute, Shanxi Agricultural University, Fenyang 032200, China
*
Author to whom correspondence should be addressed.
Agriculture 2024, 14(2), 171; https://doi.org/10.3390/agriculture14020171
Submission received: 13 December 2023 / Revised: 19 January 2024 / Accepted: 19 January 2024 / Published: 23 January 2024
(This article belongs to the Section Crop Production)
Browse Figure
Versions Notes

Abstract

:
Climate change related abiotic stress has been potentially impacting the quantity and quality of forage grass. Melatonin, a multifunctional molecule that has been found to be present in all plants examined to date, plays a crucial role in improving forage grass tolerance to both biotic and abiotic stresses. However, research on melatonin’s role in forage grass is still developing. In this review, the effects of melatonin application on abiotic stress are the primary topic, and we try to find relative mechanisms. In order to determine whether melatonin has a good effect on forage grass, we compared and summarized the adapting ability of different forage grasses under abiotic stress after melatonin application in aspects of growth and development, photosynthesis, antioxidant systems, plant hormone interactions, and ion homeostasis. According to part of the data, we found that different forage grasses exhibited varying responses to endogenous melatonin content and exogenous melatonin dose applications. Meanwhile, the regulatory mechanisms of melatonin application include the expression of chlorophyll synthesis and degradation genes, electron transport and phosphorylation genes, stress regulation pathway genes, and plant hormone synthesis genes. We propose possible future studies that can further explore the metabolic pathways of melatonin and the molecular mechanisms of melatonin regulation of abiotic stress in forage grass. Specifically, research can focus on elucidating the signaling pathways, gene expression of regulatory networks, and interactions with other plant hormones. This will provide valuable theoretical and practical guidance for adapting to climate change and forage grass development.

1. Introduction

Global climate change is continuing to threaten and disrupt the growth patterns of various organisms [1]. According to statistics, rising temperatures due to climate change have led to a 15% decrease in global wheat production, and drought has further exacerbated the sharp decline in plant productivity [2]. For example, the 2012 La Niña event caused a 30% decrease in corn production in the United States, due to severe drought conditions [3]. Even more concerning is the fact that non-biological stressors resulting from global climate change have already led to over 60% decrease in global crop yields. Predictions indicate that future climate change is expected to result in higher temperatures and reduced rainfall in southern Australia, leading to a slight increase in grass production by 2030 but a 19% decrease by 2070 [4]. These extreme and frequent abiotic stress conditions can inflict irreversible damage on plants, and this damage is expected to worsen under future climate change conditions [5]. Thus, there is an urgent need to identify effective measures and methods to mitigate the damage caused by abiotic stress and address climate change, which has emerged as a critical concern in the scientific community.
Grasslands cover a significant portion of the earth’s lands, even including the oceans. As one of the most economically beneficial and essential crops, forage grass plays a crucial role in ecosystems and feed crops [6]. Approximately 26% of the global land is used for forage grass, with one-third of arable land dedicated to grass production, contributing to 40% of the global agricultural GDP [7]. However, global climate change, with increased CO2 concentrations, rising temperatures, altered precipitation patterns, and more frequent extreme weather events, has subjected grasslands to frequent abiotic stresses, such as drought, salinity, high temperatures, and heavy metal contamination [8]. As a result, the productivity and quality of forage grass have significantly declined. Future global climate change will continue to impact natural grassland ecosystems and livestock systems, leading to increasingly severe damage from abiotic stress.
Melatonin (N-acetyl-5-methoxytryptamine), a versatile small molecule, is widely present in humans, animals, and plants [9]. Studies have shown that melatonin can influence the entire life cycle of plants, from seed germination to growth, maturation, aging, and recovery from stress [10]. The biosynthesis of melatonin begins with the production of tryptophan through the oxalate pathway in chloroplasts, which is then converted into serotonin via the catalysis from biosynthetic enzymes, and finally is synthesized into melatonin [11]. The biosynthetic enzymes of melatonin mainly include tryptophan decarboxylase (TDC), tryptophan hydroxylase, tryptamine 5-hydroxylase (T5H), serotonin N-acetyltransferase (SNAT), N-Acetyl serotonin methyltransferase (ASMT), arylalkylamine N-acetyltransferase, and hydroxyindole-O-methyltransferase (HIOMT) [12]. The TDC enzyme plays an important role in melatonin biosynthesis by catalyzing the conversion of tryptophan into tryptamine. The T5H enzyme then initiates the conversion of tryptamine into serotonin. At the same time, T5H can convert tryptophan into 5-hydroxytryptophan, which is then converted into serotonin under the catalysis of aromatic-L-amino acid decarboxylase (AADC). SNAT and HIOMT enzymes convert serotonin into N-acetyl serotonin or N-acetyl tryptamine in chloroplasts or mitochondria. The final step in melatonin biosynthesis is the synthesis of melatonin through the O-methylation of N-acetyl serotonin by the action of ASMT [13].
Moreover, melatonin, as an antioxidant, can alleviate damage caused by abiotic stress, regulate photosynthesis, ion balance, and stress signal transduction, and directly enhance the activity of various antioxidant enzymes and enzymes involved in photosynthesis in plant cells, thus protecting plants from cell damage caused by oxidative stress [14]. Therefore, it is predicted that melatonin will play an important role in helping plants adapt to adverse environmental conditions, particularly in the current context of climate change. Even though there are numerous papers already published on other plants, this review seeks to summarize and analyze existing research findings for forage grass and assess the effects and strategies of melatonin in terms of growth and development, photosynthetic capacity, antioxidant ability, interactions with hormones, and ion homeostasis (Figure 1). Meanwhile, we focus on addressing the following questions: (1) What relationship exists between melatonin and the growth and development of forage grass? (2) Which aspects of forage grass does melatonin regulate under abiotic stress? How is it affected? (3) What molecular mechanisms and metabolic pathways are regulated by melatonin in forage grass under abiotic stress? (4) Does melatonin have the potential to become an important avenue for forage grass to adapt to abiotic stress? All these questions triggered our interest in finding answers. Ultimately, we aim to determine whether melatonin has a positive effect on aiding forage grass in adapting to abiotic environments and organizing the regulatory network.

2. Melatonin Regulates the Growth and Development of Forage Grass

The characteristics of forage grass that is growing well include lush overall growth, large and dense leaves, thick and strong stems, and a stable and lush underground root system [15]. The quality of the growth conditions directly impacts the quality of forage grass, which, in turn, affects the availability of high-quality feed for the livestock industry [16]. It also indirectly affects humans’ healthy intake of meat and milk protein through the adequate supply of forage grass. However, under the influence of drought, alkali salt, and heavy metal stresses, the growth time for forage grass is short, the leaves and stems are short and thin, the overall growth shape is small, and the resistance is weak [17]. We found that melatonin possibly plays a certain role in alleviating growth and development problems under abiotic stress and has significant effects.

2.1. Seed Germination and Seedling Growth

Seed germination and seedling growth (including root and stem growth) are two important stages of forage grass growth and development [18]. The regulating effect of melatonin is manifested in the germination rate (GR), germination potential (GP), germination index (GI), plant height (PH) stem thickness (ST), and root length (RL) in the stage of seed germination and seedlings. They all show good results compared to untreated ones after melatonin treatment. For example, after pretreatment with 300 μmol/L melatonin, the GR and GP of hybridization pennisetum seeds under 150 mM NaCl salt stress increased by 20% and 10%, respectively [19]. Under the condition of PEG-23% drought treatment and 75 μmol/L exogenous melatonin treatment for 24 h, the GR, GP, GI, and vitality index of ‘WuSu No.1’ awnless brome seeds increased by 34.24%, 68.71%, 69.61%, and 78.14%, respectively [20]. Under the condition of 0.15 mM NaCl salt stress treatment, the GR and GP of alfalfa seed of the ‘Chifeng’ variety increased by 53.8% and 53.5%, respectively, and the GI increased by 55.8% after the supplementation of 300 μmol/L melatonin pretreatment [21]. Under drought stress, the growth of ‘Sanditi’ alfalfa seedlings showed improvement in PH, ST, and RL after 100 μmol/L melatonin treatment [22]. Similarly, oat was improved by melatonin treatment under salt stress; their PH, ST, RL, fresh weight (FW), dry weight (DW), and relative water content significantly improved [23].
The effects of melatonin on forage grass might even be stronger than other crops. For example, under the condition of 200 mM sodium chloride (NaCl) salt stress, the germination rate, germination potential, and germination index of the alfalfa seeds of the XinjiangDaye variety decreased by 25%, 59%, and 63%. However, the germination rate, germination potential, and germination index of the alfalfa seeds increased by 20.97%, 18.67%, and 231% after 50 μmol/L exogenous melatonin pretreatment [24]. Under the condition of salt stress, the seed germination rate of the ‘Zhongmu No. 2’ alfalfa was reduced by 55%, while the germination rate and germination potential increased by 42% and 19.9% after 50 μmol/L exogenous melatonin pretreatment [25]. However, drought stress reduced the germination rate of cotton seeds by 60%, and exogenous melatonin treatment only increased the germination rate by 11% and the vitality index by 17% [26]. After 100 mM NaCl stress for 32 h, the rice seed germination rate was reduced by 28%, and 5 μmol/L melatonin pretreatment increased it by 20% [27], which is good but obviously, the effect of melatonin on forage grass is better (Table 1).

2.2. The Mechanism of Melatonin Regulation in the Growth and Development Stage

Melatonin exerts noticeable effects on the germination and growth stages of forage grass plant seeds. Its primary mechanism of action involves the regulation of stress-related gene expression, thereby enhancing germination and promoting resistance to stress, as well as facilitating overall growth and development. However, further research is still needed on which pathways are affected by the expression of these partial genes. Exogenous melatonin treatment promoted the up-regulation of alfalfa stress-related genes Dehydration-Responsive Element (DRE), Auxin Response Factor (ARF), Homeodomain-Leucine Zipper (HD-ZF), Myeloblastosis (MYB), and Refinder of the Embryo Morphogenesis (REM) [35]. In alfalfa grown under cadmium stress conditions, the application of exogenous melatonin stimulated the upregulation of ABC transporter and PCR2 transcripts and reduced the accumulation of cadmium content [36]. A study showed that MsASMT1 is a melatonin receptor gene, and overexpression of MsASMT1 could increase the endogenous melatonin content and promote the growth of alfalfa. At the same time, if the expression of this gene is silenced, the effect of melatonin in alleviating salt stress will be reduced or even disappear, and the overexpression of this gene will effectively alleviate salt stress on alfalfa [15]. Therefore, both endogenous melatonin content and exogenous melatonin treatment of forage grass play an important role in the growth process and stress resistance of forage grass.
In this section, the growth and development of forage grass, including seed germination and seedling growth, are vital stages that significantly influence the overall quality and productivity of forage grass. The regulatory effects of melatonin on these growth stages, as evidenced by its impact on the germination rate, germination potential, and growth parameters of seedlings under various stress conditions, demonstrate the significant potential of melatonin in enhancing stress resistance and promoting the growth of forage grass. Melatonin’s role in regulating stress-related genes and enhancing stress resistance further underscores its importance in mitigating the adverse effects of abiotic stress on forage grass growth and development. Moreover, the identification of melatonin receptor genes and their impact on endogenous melatonin content and stress alleviation highlights the intricate molecular mechanisms underlying melatonin’s influence on forage grass. To gain a comprehensive understanding, further research is necessary to elucidate the specific pathways affected by the expression of stress-related genes and the role of melatonin receptor genes in promoting the growth and stress resistance of forage grass.

3. Melatonin Regulates the Photosynthesis of Forage Grass

3.1. The Effects of Melatonin Application on Photosynthesis

Photosynthesis is a very important pathway in the growth and development of any plant. Plants convert light energy into chemical energy [37]. Whether this process works normally is one of the criteria for normal plant growth [38]. Photosynthetic pigments play an important role in the photosynthesis process. Under abiotic conditions, the photosynthesis of forage grass will be affected. The reason is mainly because abiotic stress destroys the homeostasis of normally growing forage grass. The most obvious manifestation is the release and over accumulation of reactive oxygen species in the body. When reactive oxygen species (ROS) are excessively accumulated, the biosynthesis of chlorophyll will be disrupted, and the chlorophyll content and the light absorption and photochemical efficiency will be reduced, further leading to a series of photosynthetic imbalances and deterioration [39]. Therefore, being able to effectively maintain the chlorophyll content and the stability of the photosynthetic electron transport chain to remove reactive oxygen species is the main starting point for regulating abiotic stress damage and ensuring the normal operation of photosynthesis [40]. After melatonin treatment of alfalfa under salt stress, it was found that melatonin has obvious effects on increasing the chlorophyll content and maintaining photosynthesis. For example, under 15% PEG drought stress, Bara 310SC and Longdong alfalfa show the above indexes are improved after exogenous melatonin treatment. Specifically, although drought stress causes the chlorophyll content of ‘Bara 310SC’ and Longdong alfalfa to decrease by 26.86% and 33.63%, after 100 μmol/L melatonin treatment, they increased by 22.92% and 58.22%. Therefore, the effect of melatonin treatment is significant. A study found that 400 μmol/L melatonin treatment has little effect on the increase in photosynthetic pigment content and even might cause an inhibitory effect [32].

3.2. The Mechanism of Melatonin Regulation on Photosynthesis

The mechanisms whereby melatonin regulates photosynthesis in forage grass include (1) melatonin regulating the expression of genes related to chlorophyll synthesis and degradation, and (2) melatonin regulating the operation of the photosynthetic transfer chain and related components. For example, under drought stress, the expression of the chlorophyll degradation genes Chlorophyllase (Chlase), Pheophytinase (PPH), and Chlorophyll peroxidase (Chl-PRX) in Agrostis stolonifera after melatonin treatment was found to be significantly reduced, and at the same time, the activity of chlorophyll degradation gene enzymes was significantly reduced [41]. Under high-temperature stress, the expression of the senescence-related genes LpSAG12.1 and Lph36 in perennial ryegrass treated with melatonin was significantly inhibited, resulting in a decrease in chlorophyll content [27]. Therefore, melatonin affects chlorophyll content directly by regulating the expression of chlorophyll synthesis and degradation genes and indirectly affects chlorophyll content by regulating the expression of aging-related genes (Table 2).
Photosynthetic electron transport is an important process of photosynthesis and is easily damaged. The photosystem II (PSII) is an important thylakoid membrane protein in the photosynthetic electron transport chain. It is a large multi-subunit pigment-protein complex. It is also an important part of the photosynthetic electron transfer process. When drought causes the electron transfer of PSII to be inhibited, ROS accumulate excessively in the thylakoid membrane, reducing the electron transfer efficiency of PSII. However, when researchers used melatonin to treat wheat grown under drought conditions, they found that the degradation of proteins on the thylakoid membrane caused by drought was inhibited, and D1, Lhcb5, Lhcb6, PsbQ, and PsbS protein levels increased; it also promoted the dephosphorylation of LCHII, CP43, and D1 to protect the photophosphorylation system [28]. Carbon assimilation is driven by CO2 and limited by low levels or the activation of photosystem I (PS I). The study found that melatonin can enhance α-amylase activity under cold stress. β-amylase activity promotes carbon assimilation in the CHL b-deficient mutant ANK32B of wheat, enhances ATPase activity and sucrose synthesis, and maintains a high-chlorophyll content. Moreover, enhancing starch degradation in maternal plants after melatonin pretreatment is an effective way to enhance the cold resistance of wheat offspring. Melatonin controls the photosynthetic carbon cycle and regulates stomatal movement by regulating sugar metabolism, gluconeogenesis pathways, and transient starch degradation and transport. Changes in stomatal conductance under drought stress will directly affect the transpiration rate.
In this section, the impact of abiotic stress on the photosynthesis of forage grass, particularly in relation to chlorophyll content and the stability of the photosynthetic electron transport chain, underscores the crucial role of maintaining normal photosynthetic function under adverse conditions. Melatonin treatment has been shown to have a significant effect on increasing chlorophyll content and regulating the expression of genes related to chlorophyll synthesis and degradation, as well as the operation of the photosynthetic electron transport chain and related components. These findings highlight the potential of melatonin in mitigating abiotic stress-induced damage to the photosynthetic process and ensuring its normal operation. Further research on the specific mechanisms by which melatonin regulates photosynthesis in forage grass will provide valuable insights into its role in enhancing stress tolerance and promoting plant growth.

4. Melatonin Regulates the Antioxidant Mechanism of Forage Grass

The Effects of Melatonin on Antioxidant Mechanism

Abiotic stress causes an increase in the content of reactive oxygen in plants, which leads to the disruption of cell integrity and metabolic pathways. Previous studies have demonstrated that melatonin can improve the ROS clearance efficiency under abiotic stress conditions [43]. Melatonin may help to reduce ROS in two ways: (1) melatonin regulates the activity of different enzymatic and non-enzymatic antioxidants; and (2) melatonin itself can directly scavenge ROS [44]. The antioxidant nature of melatonin is due to the redox active properties of the molecule, as well as metabolites originating during its metabolism [45], including cyclic 3-hydrox-ymelatonin, N1-acetyl-N2-formyl-5-methoxykynuramine, N1-acetyl-5-methoxykynuramine, 6-hydroxymelatonin, and 2-hydroxymelatonin [46]. More interestingly, one molecule of melatonin can simultaneously clear multiple ROS, while the ratio of other antioxidants is only 1:1 or lower. In the ROS, the hydroxyl radical (·OH) is one of the most toxic species. But melatonin’s role as a ·OH radical scavenger is quite amazing [47]. The other is the antioxidant properties of the two side chains of the melatonin molecule: the carbonyl part of the C3 amide functional group and the nitrogen in the carbonyl group play a key role in quenching. Thus, the reaction of melatonin with ROS involves electron supply to form melatonin cationic radicals, nitrogen atom supply to hydrogen, nitrosation, addition reaction, substitution, and ROS reduction [45]. Physiological and mechanistic explanations of melatonin-mediated scavenging of ·OH radicals include the addition of ·OH radicals to the C3 site of the indole ring, tautomerism of enolimide to ketoamine, cyclization between the C2 and N sites of the indole ring, and the reaction of the side chain of the ring with a second ·OH radical to form cyclic 3-hydroxymelatonin and water [47]. Those findings showed that melatonin has the capacity to save and help forage grass to adapt to the environment.
When forage grass is attacked by stresses that cause active oxygen accumulation, research shows that it is able to clear the active oxygen by enhancing its antioxidant and non-enzymatic activities [43]. Melatonin can remove reactive oxygen species. For example, Under drought stress, Studies on alfalfa [32], tall fescue [48], oat [49], and perennial ryegrass [50] all show that exogenous melatonin treatment could enhance the activities of antioxidant enzymes, such as superoxide dismutase (SOD), catalase (CAT), and peroxidase (POD), and reduce malondialdehyde (MDA), H2O2, O21, and other active oxygen species. Further studies found that melatonin induced an increase in SOD, APX, CAT, and POD coding gene transcriptional levels and their activities [51]. Similar results were found for salt stress or heavy metal toxicity [52]. For example, 20 μmol/L melatonin treatment of Bermudagrass can reduce the accumulation of reactive oxygen species and the content of malondialdehyde, increase the content of glutathione, and regulate the activities of glyoxalase (Gly I and Gly II) systems to alleviate lead stress [13]. Further development is needed to study the mechanism of regulating the clearance of reactive oxygen species mediated by melatonin.
In this section, the role of melatonin in clearing reactive oxygen species (ROS) and enhancing antioxidant and non-enzymatic activities in forage grass under various abiotic stress conditions is pivotal for maintaining cell integrity and metabolic pathways. Melatonin’s dual mechanism of regulating the activity of enzymatic and non-enzymatic antioxidants, as well as directly scavenging ROS, has been extensively demonstrated in various studies. Furthermore, the physiological and mechanistic explanations of melatonin’s scavenging of ·OH radicals underscore its remarkable antioxidant properties. These findings highlight melatonin’s significant potential to aid forage grass in adapting to environmental stresses. Further research is warranted to delve into the precise mechanisms by which melatonin regulates the clearance of reactive oxygen species, providing valuable insights into its role in stress adaptation.

5. Melatonin Regulates Ion Homeostasis of Forage Grass

5.1. The Effects of Melatonin on Ion Homeostasis

Absorption of ions by plants and maintenance of ion homeostasis in the body are two of the important factors for survival under stress. Under stress, melatonin can help to regulate the ion absorption and ion transporters of forage grass, including Na+, K+, and Cl− transporters, as well as phosphate and sulfur ions to help forage grass establish ion homeostasis [53]. For example, under salt stress, exogenous melatonin treatment promotes plasma absorption of nitrogen, phosphorus, potassium, calcium, and magnesium in alfalfa [54]. Under salt stress, melatonin treatment reduces Na+ accumulation and promotes K+ absorption. For example, under salt stress, the accumulation of Na+ was reduced in stems and roots, the absorption of K+ increased in stems, and more significantly, the ratio of K+/Na+ increased in stems and roots after pretreatment with 50 μmol/L melatonin in alfalfa [55]. Under cadmium stress, Ca2+ and K+ contents significantly increased after treatment with melatonin (50 μmol/L and 100 μmol/L) in wheat seedling leaves [39]. Under salt stress, the absorption of N, P, and K plasma increased in wheat significantly, the accumulation of Na+ is reduced, and the ratios of K+/Na+, Ca2+/Na+ and Mg2+/Na+ are increased after the combined treatment of salicylic acid and melatonin [56].

5.2. The Mechanism of Melatonin Regulation on Ion Homeostasis

Ions are transported into the plant by H+ pumps, ion channels, and ion channel proteins. So, what role does melatonin play in the activity of ion channels and ion channel-related proteins? Studies have shown that melatonin can improve the absorption and content of sulfur by upregulating genes involved in sulfur transport and metabolism, including sulfur transporters such as ATP thioacylase, 5′-adenylate sulfate reductase, sulfite reductase and O-acetylserine-mercaptan hydrolase [57]. Melatonin also can mediate the regulation of H+-ATPase activity, which directly affects nutrient and ion absorption and transport, including up-regulation in the gene expression of enzymes, such as HA2, HA3, HA4, HA8, and HA9 [58]. Under the stimulation of ROS, melatonin regulates the level of Ca2+ signaling by activating NADPH oxidase activity, thereby promoting Ca2+ inflow and maintaining ion homeostasis in vivo. For example, melatonin regulates gene transcription of Ca2+ signaling in alfalfa (cyclic nucleotide-gated channel CGs; CAM/calmodulin-like proteins, CAM/CMLs, and calc-dependent protein kinases (CDPKs)) [59].
In summary, the role of melatonin in regulating ion absorption and ion transporters in forage grass under various stress conditions is a critical factor for establishing ion homeostasis. Notably, melatonin treatment has been shown to impact the absorption and content of essential ions, such as Na+, K+, Cl−, phosphate, sulfur, Ca2+, and many others. Furthermore, melatonin’s influence on ion channel-related proteins, including H+-ATPase activity and Ca2+ signaling, demonstrates its multifaceted role in maintaining ion homeostasis. The following section will delve into the specific mechanisms by which melatonin can modulate ion channel activity and related protein expression, providing a comprehensive understanding of its impact on ion homeostasis in forage grass.

6. Melatonin Interacts with Other Plant Hormones

6.1. The Effects of Melatonin on Other Plant Hormones

Hormones are produced in the plant, and act on a certain tissue at a certain time, playing a role in growth regulation; so, each hormone exists in the plant body at the same time and there is a certain connection and interaction. Melatonin is one of the endogenous plant hormones of crops, which has been proven to be inseparable from other plant hormones. Melatonin is involved in the synthesis and degradation of other plant endogenous hormones and plays a regulatory role. A large number of studies in other crop fields have found that there are interaction relationships between melatonin and other hormones, such as indole-3-acetic acid (IAA), gibberellin (GA), abscisic acid (ABA), jasmonic acid (JA), salicylic acid (SA), and cytokinin (CK). (1) Melatonin treatment enhances the accumulation of distal root auxin signals and regulates auxin biosynthesis to control root structure and promote lateral root development [60]. (2) Melatonin concentration affects the IAA biosynthesis; high concentrations inhibit the promotion effect of low concentrations [61]. (3) Stress can promote an increase in ABA levels, and melatonin can mediate ABA metabolism and inhibit ABA synthesis [62]. (4) GA and ABA are antagonists. Melatonin can regulate ABA catabolic genes, GA biosynthesis genes, and ABA biosynthesis genes [63]. The interaction between melatonin and JA or SA has also been well documented for the upstream signaling pathways of defense genes involved in JA and SA biosynthesis [64]. (5) Melatonin regulates the expression of JA biosynthesis genes (AOC and LoxD) and genes in JA signaling pathways. (6) Melatonin triggers plant immunity, thereby promoting melatonin-mediated SA synthesis [33].

6.2. The Mechanism of Melatonin Regulation on Other Plant Hormones

Above all we can see that melatonin seems to be an important part of the hormone signaling pathway. There are two relationships between melatonin and other hormones in the pasture field: (1) the relationship between the change in melatonin levels and the content of other hormones; and (2) the relationship between the change in melatonin levels and the biosynthetic expression of other hormones. Exogenous melatonin treatment had a significant effect on IAA content in alfalfa leaves. At 150 mM NaCl, 10 µM melatonin treatment induced a salinity increase, increased auxin content, and significantly increased endogenous melatonin accumulation in alfalfa leaves. High-salt concentration increased IAA content in roots, and exogenous melatonin further increased IAA levels. Under 200 mM NaCl, 15 µM melatonin increased the content of IAA in roots. Salt stress causes a significant increase in IAA/MT ratios in roots and leaves, whereas melatonin treatment reduces IAA/MT ratios in alfalfa leaves [65]. Under drought stress, exogenous melatonin treatment also promoted an increase in IAA and GA3 contents in oat leaves and inhibited the increase of ABA content [23]. Under normal conditions, exogenous melatonin treatment may inhibit seed germination and increase abscisic acid content by up-regulating the expression of abscisic acid related synthesis genes. Under normal growth and development conditions, melatonin treatment synergistically inhibited the germination of Arabidopsis seeds with ABA and up-regulated the expression of NCED3 and ABA2 genes related to ABA synthesis. Melatonin and GA3 produce antagonistic effects and jointly regulate the expression of ABO5 and GASA6 genes related to seed germination [66]. In wild ryegrass (Elymus nutans), the expression of cold-response genes (CBF9, CBF14, and COR14a) in the ABA independent pathway was upregulated after exogenous melatonin treatment, while additional treatment with the ABA biosynthesis inhibitor fluridone significantly inhibited melatonin induced ABA accumulation, suggesting that ABA-dependent pathways also contribute to melatonin induced cold tolerance [42]. Under high-temperature conditions, exogenous melatonin treatment regulated the up-regulation of cytokinin (CK) biosynthesis genes LpIPT2 and LpOG1 and their signaling response transcription factors (B-type ARRs), the transcription of key transcription factors in the ABA signaling pathway encoded by LpABI3 and LpABI5, and the ABA biosynthesis genes LpZEP and LpNCE. The expression of D1 decreased, while the endogenous melatonin content increased [28]. Under drought conditions, the content of jasmonic acid (JA) increased after 100 μmol/L melatonin treatment, and the expression of JA genes (LOX1.5 and LOX2.1) and two transcription factors (HY5 and MYB86) were up-regulated. Moreover, the expression of genes related to lignin biosynthesis (4CL2, P5CS1 and CCR2) and genes related to starch and sucrose metabolism (PME53 and SUS4) were up-regulated [67]. There is an important correlation between the change in melatonin levels and IAA, ABA, CK, JA, and other hormones, and the melatonin treatment concentration can regulate the expression of these hormone synthesis genes and degradation genes.
In this section, the intricate relationship between melatonin and other plant hormones, including IAA, ABA, GA, JA, SA, and CK, is shown to be a crucial aspect of hormone signaling pathways in forage grass. Melatonin’s influence on the biosynthesis, content, and signaling pathways of these hormones underscores its importance in regulating various physiological processes, particularly in response to stress conditions. The intricate interplay between melatonin and other hormones, as evidenced by numerous studies in different crop fields, highlights the complex and multifaceted role of melatonin in hormone regulation. Future research in the field of forage grass should continue to explore the dynamic interactions between melatonin and other hormones, as well as their molecular mechanisms, to further elucidate their combined impact on plant physiology and stress responses.

7. Conclusions

Abiotic stress is always a threat to the growth and development of forage grass. In general, the road along melatonin research on forage grass to adapt to future climate change-related abiotic stress is still difficult. In recent years, scholars have made some achievements in the field of forage grass, but it is still insufficient. Previous studies have shown that different species of forage grasses have different tolerance to abiotic stress. For example, under the same stress conditions and when treated with the same concentration of exogenous melatonin, different varieties of alfalfa show different alleviating effects of melatonin. The interesting thing is that the alleviating effects of melatonin on the growth and development of forage grass were even higher than those in other plants, such as cotton. Therefore, it triggered a question about how to apply melatonin properly and whether different varieties and under different stresses will be different. In the future, if a large number of studies exist, we will have the ability to use the data and statistics, eventually being able to correctly apply melatonin based on conditions: the study of different varieties of forage grass still needs further detailed exploration and classification.
Secondly, the silencing and inhibition of melatonin receptor genes can lead to the reduction in or even loss of the effects of melatonin treatment, which indicates that melatonin plays an important role in coping with abiotic stress. Melatonin treatment also showed significant effects on photosynthesis, antioxidant capacity, and ion homeostasis, including chlorophyll synthesis and degradation, enhancement of antioxidant enzyme activity, and ion transport. However, above all aspects, there is still significant room for exploring the metabolic pathways and molecular mechanisms of melatonin. Further studies on the melatonin synthesis process and related pathways, metabolic pathways, and molecular mechanisms in forage grass are of great significance in the future.
In conclusion, (1) melatonin has an important correlation in the growth and development of forage grass, but the endogenous melatonin content of various varieties and materials and its correlation with life and stress resistance must be an important direction for future research. (2) Under abiotic stress, for the growth and development of forage grass or for the physiological and biochemical response, melatonin treatment can significantly alleviate stress damage and improve stress resistance, and its effect is significantly or even stronger than that in other plants. (3) The regulating mechanisms of melatonin treatment include the up-regulation and expression of stress-related genes to alleviate stress and regulate the expression of photosynthesis, antioxidants, ion homeostasis, and other hormone-related synthesis genes to adapt to abiotic stress (Table 2). (4) According to current research results about melatonin on forage grass, it is certain that melatonin will become an effective weapon that can be applied for the adaptation from abiotic stresses one day; maybe it is a long way away, but it still can be achieved.
All in all, this review will help forage grass researchers to further study the mechanisms of melatonin regulation of forage grass stress resistance to alleviate stress damage, judge and understand the dosage of melatonin, and encourage researchers to further explore the metabolic pathways of melatonin and related molecular mechanisms in the forage grass field.

Funding

This research was funded The central government guides local science and technology development fund projects by grant number Project No. YDZJSX2022A038 and Key research and development projects in Shanxi Province, Project No. 202102140601006. And The APC was funded by The central government guides local science and technology development fund projects by grant number Project No. YDZJSX2022A038 and Key research and development projects in Shanxi Province, Project No. 202102140601006.

Conflicts of Interest

We declare no conflicts of interest.

References

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Agriculture 14 00171 g001
Figure 1. Melatonin mitigation of abiotic stresses in forage grass.
Figure 1. Melatonin mitigation of abiotic stresses in forage grass.
Agriculture 14 00171 g001
Table 1. The effects of melatonin application on different plant.
Table 1. The effects of melatonin application on different plant.
PlantType of StressMEL LevelMain EffectsRef
PennisetumSalt300 μmol/LThe germination rate and germination potential of seeds increased by 20% and 10%, respectively[19]
Awnless bromeDrought75 μmol/L-24 hThe germination rate, germination potential, germination index, and vitality index of seeds significantly improved[20]
Agrostis stoloniferaDrought20 μmol/LIncreased light efficiency and chlorophyll content decreased the expression of chlorophyll degrading genes[27]
Perennial ryegrassDrought100 μmol/LIncreased chlorophyll content, enhanced antioxidant enzyme activity, and removed reactive oxygen species[28]
WheatSalt200 μmol/LThe chlorophyll content of varieties Shahkar-13 and Khaista17 increased by 25% and 37%, respectively[29]
WheatAluminum30 μmol/LMelatonin treatment decreased root tip-Al contents by 19.0% and 15.5%[30]
WheatHeat100 μmol/LMT treatment reduced H2O2 by 47.2%, O2 by 52.8%, and TBARS by 48.1%. [31]
‘Chifeng’Salt300 μmol/LThe germination rate and germination potential of seeds increased by 53.8% and 53.5%, and the germination index increased by 55.8%[21]
‘Sanditi’Drought100 μmol/LSeedling height, stem diameter and root length significantly increased[22]
‘Xiangjiangdaye’Salt50 μmol/LThe germination rate, germination potential, and germination index increased by 20.97%, 18.67%, and 231%, respectively[24]
‘Zhongmu No.2’Salt50 μmol/LThe germination rate and germination potential of seeds increased by 42% and 19.9%, respectively[25]
‘Bara310S’Drought100 μmol/LThe chlorophyll content increased by 22.92%, and the photosynthetic efficiency improved[32]
‘Longdong’Drought100 μmol/LThe chlorophyll content increased by 58.22%, and the photosynthetic efficiency improved[32]
CottonSalt50 μmol/LThe germination rate and vigor index of seeds increased by 11% and 17%, respectively[26]
RiceSalt5 μmol/LThe seed germination rate increased by 20%[25]
WatermelonSalt150 μmol/LPn and Gs increased by 40.8% and 21.6%, respectively[33]
MaizeSalt1 μmol/LImproved light and efficiency, and Pn increased by 19%[34]
Table 2. The Effects of Melatonin on Related Genes.
Table 2. The Effects of Melatonin on Related Genes.
PlantsMain GeneEffectRef
alfalfaDRE, ARF, HD-ZF, MYB, REMstress-related genes alleviate salt stress damage[35]
alfalfaMsASMT1melatonin receptor gene, overexpression could increase the endogenous melatonin content[15]
Agrostis stoloniferaChlorophyllase (Chlase), Pheophytinase (PPH), Chlorophyll peroxidase (Chl-PRX)under drought stress, reduced the expression of chlorophyll degradation genes[41]
perennial ryegrassLpSAG12.1 and Lph36Under high-temperature stress, inhibited the expression of chlorophyll degradation genes[27]
Lolium multiflorumCBF9, CBF14, and COR14acold-response genes[42]
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Fan, Y.; Li, L.; Guo, F.; Hou, X. Tolerance of Forage Grass to Abiotic Stresses by Melatonin Application: Effects, Mechanisms, and Progresses. Agriculture 2024, 14, 171. https://doi.org/10.3390/agriculture14020171

AMA Style

Fan Y, Li L, Guo F, Hou X. Tolerance of Forage Grass to Abiotic Stresses by Melatonin Application: Effects, Mechanisms, and Progresses. Agriculture. 2024; 14(2):171. https://doi.org/10.3390/agriculture14020171

Chicago/Turabian Style

Fan, Yufeng, Lingling Li, Fenghui Guo, and Xiangyang Hou. 2024. "Tolerance of Forage Grass to Abiotic Stresses by Melatonin Application: Effects, Mechanisms, and Progresses" Agriculture 14, no. 2: 171. https://doi.org/10.3390/agriculture14020171

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