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Review

Facing Heavy Metal Stress, What Are the Positive Responses of Melatonin in Plants: A Review

by
Xianghan Cheng
†,
Xiaolei Liu
†,
Feifei Liu
,
Yuantong Yang
and
Taiji Kou
*
College of Agriculture, Henan University of Science and Technology, Luoyang 471023, China
*
Author to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Agronomy 2024, 14(9), 2094; https://doi.org/10.3390/agronomy14092094
Submission received: 20 August 2024 / Revised: 5 September 2024 / Accepted: 12 September 2024 / Published: 13 September 2024
(This article belongs to the Section Plant-Crop Biology and Biochemistry)
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Abstract

:
With the growth of the population and the development of modern industry and the economy, the problem of heavy metal pollution in cultivated soil has become increasingly prominent. Moreover, heavy metal poses a serious threat to plant growth due to its characteristics of difficult degradation, high mobility, easy enrichment, and potential toxicity and has become a social topic. Melatonin is a new type of plant hormone widely present in animals, plants, fungi, and bacteria, and its biological role has begun investigated in the last dozen years. Facing heavy metal stress, melatonin can play a pleiotropic role in the physiological processes of plants, such as stress resistance and growth regulation, mitigate the damage caused by stress on plants, and provide a new research idea for alleviating heavy metal stress in plants. From the aspects of the plant phenotype, physiology, element absorption, and molecular structure, this paper, therefore, mainly reviews the effects of melatonin on plants subjected to heavy metal stress and the mechanism of melatonin alleviating heavy metal stress and then puts forward future research directions. This information may be of great significance to the normal growth of crops under heavy metal stress and will provide an important theoretical basis for the genetic improvement of crop resistance in the future.

1. Introduction

With the development of modern industry and the economy, heavy metal pollution has attracted great attention and become a social problem all over the world [1,2]. Globally, there are about 10 million soil contaminated plots, more than 50% of which are reported to be contaminated by heavy metals [3,4], and more than 20 million hectares of land are reported to be contaminated by the heavy metals cadmium (Cd), lead (Pb), copper (Cu), zinc (Zn), hydragyrum (Hg), arsenic (As), chromium (Cr), cobalt (Co), and nickel (Ni) [5,6]. It has been reported that about 500,000 of the 3.5 million potentially contaminated soil sites in the European Union were reported to be highly contaminated with heavy metals [7]; about 600,000 ha of brown land in the United States were contaminated with heavy metals [8,9].
Among these heavy-metal-polluted soil resources, cultivated land resources are closely related to human survival because land is an important material basis for food production and food security as well as for related agricultural production activities [2,10,11]. According to “Geochemical Survey Report of China’s Cultivated Land (2015)”, 2.5% of the cultivated land resources were moderately and severely polluted by heavy metals, covering an area of 34.88 million mu; 5.7% were lightly polluted by heavy metals, covering an area of 78.99 million mu. Moreover, heavy metal pollutants in the land cannot be degraded by soil microorganisms and it is easy for them to accumulate in large quantities in the soil–crop system [12], then directly affect the normal growth, development, and metabolism of plants and finally enter the human body through enrichment in the food chain, threatening human health [13,14,15]. Therefore, it is urgent to find ways to alleviate heavy metal stress in plants.
Melatonin (N-Acetyl-5-methoxytryptamine) is a novel hormone found widely in plants. Although melatonin has been found in nature for more than 60 years [16], it has only been detected in higher plants for 30 years [17], and relative studies on its biological role have only been begun in the last 15 years. In recent years, a large number of studies have confirmed that in the face of abiotic stress factors such as low temperature [18], high temperature [19], drought [20], flood [21], salinity [22], heavy metal pollution [23,24,25], and ultraviolet radiation [26], this hormone can directly play a multipotent role in the physiological processes of plants, such as antioxidant and growth regulation, so as to alleviate the harm caused by stress to plants.
Currently, there have been many relevant studies on melatonin as a regulator to cope with environmental stress. However, these previous studies have focused too much on the regulatory effects of melatonin in alleviating a plant’s resistance to temperature, drought, salinity, moisture, and other stresses and have not conducted a comprehensive and detailed review of the regulatory mechanism of heavy metal stress. So, facing the increasingly prominent problem of heavy metal stress, what are the positive responses of melatonin in plants? This paper mainly reviews the effects of melatonin on plants subjected to heavy metal stress and the mechanism of melatonin alleviating heavy metal stress, from the aspects of the plant phenotype, physiology, and molecular and element absorption, and then puts forward future research directions. This information may provide theoretical reference for future studies on melatonin alleviating heavy metal stress in crops and the genetic improvement of crop resistance.

2. Current Situation of Soil Heavy Metal Pollution and Its Harm to Plants

With the growth of the population and the development of modern industry and the economy (mining, mineral smelting, application of pesticides and fertilizers, etc.), the problem of heavy metal pollution in cultivated soil has become increasingly prominent. Take China, for example: in the 1980s, the over-standard rate of heavy metal spots in the cultivated soil of China was 7.16%, among which the pollution proportions of Cd and Ni were the highest at 1.32% and 3.85%, respectively [27]. In 2014, the national soil pollution survey bulletin showed (Table 1) that the over-standard rate of heavy metal points in the cultivated soil of China was 19.4%, of which 13.7%, 2.8%, 1.8%, and 1.1% were mild, moderate, and severe pollution points, and the main pollutants were Cd, Ni, Cu, As, Hg, and Pb [28]. However, in 2018, the over-standard rate of heavy metal spots in the cultivated soil of China increased to 21.49%, of which the proportions of mild, moderate, and severe polluted spots were 13.97%, 2.50%, and 5.02%, respectively. Moreover, the main pollutants were Cd, Ni, Cu, Zn, and Hg, and their rates of exceeding the standard were 17.39%, 8.41%, 4.04%, 2.84%, and 2.56%, respectively [27]. Nearly 10 million ha of agricultural land has been polluted, resulting in the loss of about 12 million tons of grain crops [29]. Compared with the 1980s, the over-standard rate of heavy metals in the cultivated soil of China has increased by 14 percentage points, of which the pollution proportions of Cd, Ni, Cu, Zn, and Hg have increased by 16.07%, 4.56%, 3.68%, 2.24%, and 1.96%, respectively, and this number is still increasing year by year. Moreover, agricultural grain output in China has been sharply reduced at the rate of 10 million tons per year, and the yields of grains contaminated by heavy metals have reached tens of millions of tons, which has directly led to heavy economic losses [30,31].
Once heavy metal ions enter plant tissues, they seriously affect the phenotypes and physiological and ecological characteristics of plants and have a great influence on the growth and development of crops. As shown in Figure 1, in terms of the phenotype in plants, according to the growth processes of plants, it has mainly been displayed that reducing the seed germination rate [32,33]; inhibiting root elongation, leading to root atrophy and even death [34]; suppressing the growth of branches and stems [35], with leaves turning yellow and dry and showing senescence [36]; and disrupting the flowering cycles of plants [37], reducing production and quality [38], are effects of heavy metal ions. In terms of physiological and ecological characteristics in plants, it has mainly been displayed that these ions lead to the lipid peroxidation of cell membranes and then affect SOD (Superoxide dismutase), CAT (Catalase), POD (Peroxidase), APX (Ascorbic acid peroxidase), NR (Nitrate reductase), and GR (Glutathione reductase), reducing the chlorophyll content and photosynthetic efficiency (the photosynthetic rate refers to the rate at which plants fix carbon dioxide through photosynthesis and convert it into organic matter per unit time.), inhibiting respiration and nitrogen metabolism, increasing protein solubility and proline content, and suppressing the absorption of nutrients.
In summary, there is an increasing trend of heavy metal pollution in cultivated land, which not only poses a serious threat to plant growth but also causes huge economic losses. Therefore, it is urgent to find ways to alleviate heavy metal pollution in plants.

3. Current Research Status of Melatonin in Stress Resistance

Melatonin (also known as pineal hormone) belongs to the category of indole heterocyclic compounds and is a new type of plant hormone widely present in animals, plants, fungi, and bacteria. Melatonin not only affects the processes of seed germination, root development, photosynthesis, leaf water/CO2 exchange [39], the circadian rhythm, the photoperiodic response, maturity, and aging (Figure 2) but is also similar to other plant hormones, which can show a series of possible cellular and physiological effects, such as these changes in cell membrane permeability mediated by intracellular Ca2+ and ion transporters; stomatal opening and/or closing; and the metabolism of carbohydrates, lipids, and nitrogen, as well as osmotic protective metabolites [40,41].
When affected by adverse conditions such as strong light, salinity, temperature, drought, and water and heavy metal stress, melatonin can also directly act as an effective antioxidant to resist abiotic stress in plants, reduce the levels of reactive oxygen species (ROS) and reactive nitrogen species (RNS), and detoxify a variety of chemical pollutants. For example, under strong light conditions, melatonin can reduce light damage in Arabidopsis by upregulating the expression of cytokinin synthesis genes (IPT3, IPT5, and LOG7) and signal transduction genes (AHK2, AHK3, ARR1, ARR4, ARR5, and ARR12) [42]. Under salt stress, exogenous melatonin can alleviate the inhibition of salt stress in cotton (Gossypium hirsutum L.) [43], alfalfa (Medicago sativa L.) [44], banana (Musa acuminata L.) [45], mustard (Brassica juncea L.) [22], and corn (Zea mays L.) [46] by regulating the active oxygen scavenging system, ATP-binding cassette transporter synthesis, plant hormone signal transduction, endogenous melatonin gene expression, and expression of transcription factors MYB, TGA, and WRKY3. Whether under high or low temperature stress, melatonin can improve the cold tolerance of cucumber seeds (Cucumis sativus L.) and the heat resistance of rice seeds by regulating the antioxidant enzyme activity of the seeds of cucumber and rice under stress and thereby promote seed germination [15,19]. Under drought stress, melatonin can reduce the damage of alfalfa and enhance its drought tolerance under drought stress by regulating nitro oxidation homeostasis and the proline metabolism system [47]. And similar significant effects have also been observed in plants such as “Naganofuji No.2” apples and sugar beet seedlings [48]. Under water stress, melatonin can control the content of ROS and RNS and actively alter molecular defense capabilities, thereby improving plant tolerance to water stress [21].
Similarly, in plants under heavy metal stress, melatonin also enhances stress resistance; however, a comprehensive and detailed overview of the regulatory mechanism of heavy metal stress has not been observed. This paper mainly reviews the effects of melatonin on plants subjected to heavy metal stress and the mechanism of melatonin alleviating heavy metal stress, from the aspects of the plant phenotype, physiology, and molecular and element absorption, and provides theoretical reference for future studies on melatonin alleviating heavy metal stress in crops and the genetic improvement of crop resistance. Related studies on the response of the phenotype, physiology, and molecular and element absorption of plants under heavy metal stress are listed in Table 2 (the specific effects are described in the further sections).

4. What Positive Responses Has Melatonin Had in Plants under Heavy Metal Stress?

4.1. From the Perspective of Plant Phenotype, How Does Melatonin Alleviate Plant Damage under Heavy Metal Stress?

4.1.1. Seed Germination

Seed germination requires sufficient material and energy, such as in the form of carbohydrates, amino acids, and nutrient elements. However, under heavy metal stress, starch is fixed, nutrient absorption is limited, and the mobilization of reserve materials is hindered. Previous research has found that melatonin can alleviate this obstruction under heavy metal stress conditions and significantly promote seed germination (Figure 2b). For example, for wheat seeds (Triticum aestivum L.) under chromium stress, melatonin can increase the germination rate and promote subsequent growth in a concentration-dependent manner within a certain concentration range by enhancing wheat reserve mobilization and antioxidant metabolism [33]. These results are similar to those from the research conducted by Chen et al. on cotton seeds, which found that melatonin also affects seed germination in a dose-dependent manner within a certain concentration range [67]. However, it is worth noting that for different crops, the application of the same concentration of melatonin may also exhibit different effects [68]. In addition, for seeds, melatonin soaking treatment can also promote seed germination under heavy metal stress and protect seedlings from heavy metal ion toxicity [69].

4.1.2. Growth and Development

Faced with heavy metal stress in the soil, plant roots are primary sites of plant–heavy-metal interaction. Melatonin can maintain the root structure and promote root growth (Figure 2a) by regulating the expression of enzymes, genes, and hormone receptors related to rooting, branching, and cell wall formation. For example, for melon and pea seedlings under Cu stress, and wheat seedlings under Cd stress, melatonin could promote cell-wall-formation-related gene expression by upregulating the expression of peroxidase and heat shock 70 kDa protein; downregulating the expression of xyloglucan endotrans glucose/hydroxylase, dirigent protein, thyroid-like protein, and subtilisin-like protein family protein; and alleviating root growth inhibition and maintaining the root structure, thereby increasing plant tolerance and survival rates under heavy metal stress [34,36,70].
In addition, under heavy metal stress, melatonin can also enhance aboveground growth and yield (Figure 2a) by enhancing the photosynthetic rate and delaying leaf senescence to enhance carbon assimilation ability. For example, the application of exogenous melatonin could significantly increase the plant height, fresh weight, and dry weight of naked oats (Avena nuda L.) under cadmium stress, thereby promoting plant growth [24,33]. Exogenous melatonin can effectively alleviate the dwarf phenotype of tomato (Solanum lycopersicum L.) under excessive Cu stress, increase tomato branch and leaf growth, and thereby limit the impact of excessive Cu on plant growth [35]. Melatonin can also reduce the absorption and migration of Cd and As, alleviate the toxicity of Cd and As to rice (Oryza sativa L.) during the flowering period, and thereby increase the rice yield [37]. And melatonin may regulate the flowering cycle [71] and floral aroma production of many species in a concentration-dependent manner [71,72]. Other related studies on the role of melatonin in reducing the appearance of plant growth under heavy metal stress are summarized in Table 2.
Generally, for plants under heavy metal stress, melatonin can protect the root structure, promote root development, and increase plant height, the number of branches, and the leaf area, thereby improving plant tolerance to heavy metals and promoting plant growth and development.

4.1.3. Maturity and Aging

In the face of heavy metal stress, research on the effects of melatonin on plant phenotypes mainly focuses on the early stages of growth and development while there is little research on the maturation and aging of crops in the later stages of growth and development. On the one hand, in the early stages of plant growth and development, melatonin alleviates the toxic effects of heavy metals (Section 4.1.1 and Section 4.1.2) and improves crop yield and quality in the later stages of growth. On the other hand, melatonin itself can promote plant fruit growth and the quality of the yield by regulating the mechanisms of photosynthesis and carbohydrate metabolism, maintaining normal nutrient accumulation and transportation, and so on. For example, soaking seeds with melatonin can delay leaf senescence and promote root development in wheat plants, thereby increasing wheat yield [73]. Spraying melatonin on tomato leaves can not only increase the contents of total soluble sugar, vitamin C, and lycopene in fruit but also increase tomato yield [74]. After root irrigation with melatonin, ‘Zaosu’ pear can increase the sugar content in the fruit during the fruit development period, mainly because melatonin promotes the accumulation of early starch content; regulates the activities of invertase, sucrose synthase, and sucrose phosphate synthase; and increases the sucrose and sorbitol content in the fruit [75]. In addition, during the process of leaf aging, melatonin can also increase the instability of chlorophyll protein complexes by specifically synthesizing or activating proteases, thereby releasing chlorophyll and delaying aging.
In summary, from the perspective of the plant phenotype, melatonin alleviates the harm of heavy metal stress to plants by increasing the seed germination rate, promoting aboveground and underground growth and development (especially root system), and delaying plant maturity and aging.

4.2. From the Perspective of Physiology, How Does Melatonin Alleviate Heavy Metal Stress in Plants?

For heavy metal stress in plants, the current research on the physiological response of melatonin mainly focuses on antioxidant stress and photosynthetic efficiency.

4.2.1. Regulatory Effect of Melatonin on Plant Antioxidant System

There is an antioxidant system in plants that is responsible for clearing free radicals such as ROS and RNS. Under normal plant growth conditions, it maintains a dynamic balance between the production and clearance of reactive oxygen species. However, when plants are subjected to heavy metal stress, the dynamic balance of ROS production and clearance is disrupted [76]. Plants directly or indirectly produce reactive oxygen species, causing them to be subjected to oxidative stress, which can lead to cell membrane lipid peroxidation, DNA damage, protein denaturation, carbohydrate oxidation, pigment decomposition, and enzyme activity damage, as well as to the disruption of plant cell homeostasis [77]. In response to this phenomenon, previous researchers have attempted to solve it with melatonin. This is because melatonin is an efficient endogenous free radical scavenger that can effectively eliminate hydroxyl radicals (·OH−), nitro radicals (·ONOO−), lipid peroxidation radicals (LOO−), superoxide anion radicals (O2−), hydrogen peroxide (H2O2), and nitric oxide radicals (NO−) [78]. And its antioxidant capacity is twice that of vitamin E, four times that of glutathione (GSH), and fourteen times that of mannitol [79].
Melatonin is an effective free radical scavenger, acting as the first line of defense against internal and environmental oxidative stressors [80]. How does melatonin interact with heavy metal stress signals and ROS? A relationship diagram has been organized to explain its interaction mechanism (Figure 3). The interaction has been roughly divided into three pathways, but the three pathways may occur simultaneously. I. As an amphiphilic molecule that freely penetrates the cell membrane, melatonin can directly clear ROS. And in response to heavy metal stress, plants themselves will also produce more endogenous melatonin, which promotes increases in antioxidant levels (glutathione, ascorbic acid, proline, VC, VE, flavonoids, etc.) and the activity of related enzymes (SOD, POD, CAT, APX, GPX, GR, etc.), thereby indirectly clearing ROS and reducing the impact of oxidative stress caused by heavy metals on plant growth and development. II. Melatonin can chelate toxic metals to alleviate the stress caused by heavy metals. Stress is first recognized by receptors present in plant cell membranes, followed by a series of signaling cascades. The details are as follows: (1) after being recognized by the receptor, the secondary messengers Ca2+ and ROS are first generated to participate in the transmission of heavy metal stress signals; (2) subsequently, melatonin and heavy-metal-stress-signaling molecules can induce the levels of related transcription factors, most of which are stress-related transcription factors, including WRKY, NAC-domain-containing proteins, and zinc-finger-related transcription factors. This process will be described in more detail in Section 4.3. (3) Furthermore, melatonin regulates the expression of redox-related genes and plant-stress-defense-related genes, such as chlorophylase-related gene CLHl, chlorophyll-A-oxygenase-related gene PAO, and ion-balance-related gene NHXl/AKTl. This indicates that melatonin may play a role in protecting important molecules such as nucleic acids, proteins, and lipids from oxidative damage. However, the specific downstream signal of the melatonin receptor is not yet clear and the gene expression signaling pathway is also unclear. III. In the third part, melatonin can be directly perceived by receptors and may participate in other physiological functions. For example, melatonin can interact with plant hormones such as jasmonic acid and salicylic acid, which are closely related to defense responses, and jointly participate in regulating plant growth and development.
Currently, there have been many studies on the effect of melatonin on enhancing antioxidant systems in plants under heavy metal stress, summarized in Table 2. For example, one study found that under Cr stress, melatonin increased the activity of SOD, POD, APX, and CAT enzymes in wheats and enhanced the antioxidant capacity, therefore reducing oxidative damage [33]. Under Cu stress, exogenous melatonin increased the proline content and cell permeability in kiwifruit seedling leaves, thereby maintaining a high water potential and turgor pressure. It also enhanced the content of total polyphenol compounds (TPC), total flavonoid content (TFC), total flavanol content (TFAC), and ascorbic acid (AsA) in kiwifruit seedling leaves, clearing free radicals in a timely manner and raising the antioxidant capacity [56]. Under Al and Cd stress, melatonin could enhance the antioxidant capacity and biomass of Brassica napus seedlings and enhance plant tolerance to Al and Cd stress [53]. Under Cd stress, exogenous melatonin (soil and foliar applications) reduced Cd toxicity and enhanced crop tolerance to Cd stress by increasing growth and antioxidant defense systems [57]. These results are similar to those of other researchers who studied the regulation of antioxidant systems by melatonin in radish (Raphanus sativus L.) under Pb stress [65], mushroom under Cd stress [59], tomato under Cu stress [35], and fragrant rice under combined stress from Pb and Cd [60].
In summary, melatonin can directly or indirectly scavenge reactive oxygen species, reduce the levels of ROS and lipid oxidation in plant leaves under heavy metal stress, and increase the levels of antioxidants and the expression of related enzymes and genes, thereby alleviating toxicity and improving tolerance.

4.2.2. Regulatory Effect of Melatonin on Plant Photosynthetic System

Photosynthesis is the foundation of plant survival, growth, and development, and its photochemical reactions are completed through electron transfer chains between Photosystem I (PS I) and Photosystem II (PS II) [82]. The regulation of electron transfer in the PSI cycle is believed to be crucial for photosynthesis and plant growth, with the function of protecting both photosystems from excessive reductions in the number of chloroplasts (excessive chloroplast degradation refers to the phenomenon wherein chloroplasts in plant cells decompose abnormally fast due to environmental pressure, genetic factors, hormone imbalance, or pathogen infection, which leads to impaired photosynthesis and hindered plant growth.) [83]. However, the damage caused by heavy metals to the plant photosynthetic system is mainly caused by the destruction of the chloroplast bilayer membrane structure of the leaves, causing the disintegration of the grana stacking structure [84], inhibiting the electron transfer activity of PS I and PS II, and reducing the chlorophyll content, ultimately leading to a decrease in the photosynthetic rate [85,86]. Melatonin significantly alleviates the damage caused by heavy metal stress to the plant photosynthetic system, regulates the photosynthetic system, and promotes photosynthesis.
Melatonin can regulate the photosynthetic system in plants under heavy metal stress, mainly through the following three aspects (Figure 4): (1) melatonin regulates the systems of PS I and PS II under heavy metal stress, promoting photochemical efficiency (Fv/Fm); (2) melatonin inhibits chlorophyll loss in plant leaves under heavy metal stress and increases the chlorophyll content; and (3) melatonin increases stomatal conductance and the CO2 absorption capacity under heavy metal stress and increases the net photosynthetic rate (Pn) and transpiration rate (Tr). For example, previous studies have found that melatonin significantly improves the PSI and PSII efficiency of rapeseed under chromium (Cr) stress, and rapeseed varieties that are resistant to chromium stress exhibit a better ability to protect PSII [81]. Melatonin could enhance both the chlorophyll content of naked oat seedlings under cadmium (Cd) stress [24] as well as the relative chlorophyll content and photosynthetic capacity of aromatic rice under plumbum and cadmium (Pb-Cd) compound stress [60]. In addition, under cadmium (Cd) stress, exogenous melatonin significantly increased the net photosynthetic rate and transpiration rate in eggplants, reducing the damage to the photosynthetic organs of eggplants under Cd stress [63]. Moreover, with increases in the melatonin concentration, the photosynthetic capacity of eggplant seedlings increased. For perennial ryegrass under heavy metal stress, melatonin enhanced the plant chlorophyll content, photochemical efficiency, net photosynthetic rate, and cell membrane stability, thereby alleviating leaf senescence [87,88].
The above results indicate that melatonin can not only regulate the systems of PS I and PS II but also inhibit chlorophyll loss and improve photochemical efficiency, thereby enhancing photosynthesis and promoting morphogenesis, growth, and development in plants. Up to now, all relevant studies on melatonin regulating the photosynthetic systems of plants under heavy metal stress have been compiled in Table 2, indicating that exogenous melatonin can improve the photosynthetic systems of plants under heavy metal stress.
To summarize, from the physiological perspective, melatonin can reduce oxidative damage by improving the levels of antioxidant enzymes and scavenging free radicals, enhance the photosynthetic capacity by increasing the content of chlorophyll and improving photosynthetic efficiency, and finally alleviate the heavy metal stress faced by plants. And in most cases, these two improvements coexist.

4.3. From the Perspective of Molecular Biology, How Does Melatonin Alleviate Heavy Metal Stress in Plants?

As a biological stimulator, melatonin can change the expression of redox network genes involved in the anti-stress response and strengthen plants by optimizing photosynthesis-related parameters and inhibiting aging genes [89]. Moreover, abiotic stressors that induce anti-stress genes will also cause endogenous melatonin levels to increase [90]. As is well known, the response of cells to stress is mainly triggered by the interaction between extracellular substances and plasma membrane proteins. This means that stress is first perceived by receptors on the plant cell membrane. Then, the signal is transmitted downstream to generate secondary messengers including calcium and ROS. Melatonin will change the expression of genes involved in signal transduction steps in this process [91] (Figure 3, signal transduction part). However, the research on melatonin in signal perception and transmission has been still unclear. Researchers have found a melatonin plant receptor, CAND2/PMTR1, but there have been few studies on the direct downstream signals activated by this receptor after it binds melatonin. Whether there are other melatonin receptors is also a scientific problem that needs to be solved urgently. So, the signal conduction part in Figure 3 is represented by “?”.
In recent years, researchers have discovered the plant melatonin receptor CAND2/PMTR1 in Arabidopsis thaliana. The successful identification of this receptor is considered to be a turning point in plant research. The function and signal pathway of plant melatonin has become part of a receptor-based regulation strategy [92]. CAND2/PMTR1 is located on the plasma membrane, has a receptor-like topology, and interacts with G protein subunit (GPA1) and its expression in different tissues is induced by melatonin [93]. Melatonin controls stomatal closure and regulates H2O2 production by the CAND2/PMTR1-mediated signal pathway [94]. In addition, PMTR1 homologues have been identified in several plant species and have been found to regulate seed germination and seedling growth, stomatal closure, leaf senescence, and several stress responses [95,96,97]. However, there have been few studies on the direct downstream signals activated by the receptor CAND2/PMTR1 binding to melatonin. Whether there are other melatonin receptors is also a scientific problem that needs to be solved urgently. Melatonin plays a role as a signaling molecule in plants by the melatonin receptor and its downstream signal transduction pathway.
Under heavy metal stress, calcium, MAPK, and plant hormone signaling pathways crosstalk with each other [98,99]. Heavy metal stress leads to a significant accumulation of ROS, which, especially H2O2, can trigger the activation of Ca2+ signaling pathways and MAPK cascade reactions and produce ROS through positive feedback regulation [100,101,102,103]. Many calcium-sensitive proteins such as calmodulin (CaMs), calcineurin-B-like proteins (CBLs), and Ca2+-dependent protein kinases (CDPKs) can sense high levels of cytoplasmic Ca2+ [104]. Calcium ions crosstalk with the MAPK signaling pathway through MAPK phosphorylation and the activation of CDPK [105]. Previous studies have shown that the melatonin receptor may be required to activate MAPK cascade reaction [106] and then stress signals are transmitted to different downstream transcription factors through MAPK cascade reactions [78,107].
When stress signals are transmitted downstream to activate transcription factors, melatonin will participate in regulating the level of transcription factors to improve the damage caused by heavy metals. During this process, several transcription factor superfamilies are mainly involved in reactions related to heavy metal stress, plant development, hormone signal transduction, etc. such as MYB (plant homologue of Myb proto oncogene), MRKY (a plant protein bound to a specific DNA sequence by a WRKYGQK peptide), and NAC (Apical meristem/ATAF1-2/cup-shaped cotyledon protein). And some signal transduction pathways related to heavy metal stress will be activated under stress and alleviate the damage to plants through their mutual cooperation or antagonism, such as mitogen-activated protein kinases (MAPKs), Jasmonic acid (JA), salicylic acid (SA), etc.; these are commonly found in plants [108,109,110].
Transcription factors can regulate the expression of different target genes including stress genes encoding metal transporters and heat shock proteins (HSPs), melatonin synthesis genes, antioxidant-enzyme-related genes, nutrient-element-related genes, etc. [111,112,113,114,115,116,117]. Among them, the structures, functions, and regulatory mechanisms of metal transporters vary, but they are all target protein genes that can specifically bind to a certain metal ion and transport it to a specific part of the cell [118]. For example, P-type heavy metal ATPase (P-type ATPase) transporters can transport metal ions such as Cu+, Ag+, Cd2+, Pb2+, Zn2+, Co2+, etc. while the ZIP (ZRT, IRT-like proteins) transporter family can transport divalent metal ions such as Zn2+, Fe2+, etc. Heavy metal stress enhances the expression of HSPs in plants, which can enhance their tolerance to metal toxicity. Genes related to melatonin synthesis can promote endogenous melatonin synthesis, including TDC, T5H, SNAT, ASMT, and COMT [119]. Antioxidant-enzyme-related genes can improve antioxidant enzyme activity and reduce oxidative damage, and these include SOD (Cu/Zn-SOD, Fe-SOD, etc.), CAT (Mn-CAT, CAT-POD, etc.), GPX (GPX1, etc.) POD, APX-encoding antioxidant enzyme genes, LOX, POX, and other Lipoxygenase genes. Nutrient-element-related genes are mostly genes involved in the efficient absorption and utilization of nitrogen, phosphorus, and potassium, and these include DEP1, RGA1, RGB1, NRT1.1B, NRT2.3, TOND1, VPT1, CK2β3, HAK5, and so on [120,121,122,123,124].
Under heavy metal stress, melatonin can improve a series of physiological reactions including growth and development, photosynthesis, antioxidant stress, and mineral element transport; alleviate oxidative damage; and improve plant tolerance to heavy metals by regulating the levels of transcription factors and gene expression described above.
In this paper, the related studies on melatonin’s regulation of plant transcription factors and gene expression under heavy metal stress have been summarized in Table 2 [34,59,125,126]. For example, transcription factors such as WRKYs, NACs, and MYBs in rice might be involved in the response to high concentrations of Cd stress in rice [127]. In a study, under Cd stress, the MYB transcription factor OsMYB45 was highly expressed in rice leaves, rice husks, stamens, pistils, and lateral roots; increased the hydrogen peroxide content and antioxidant enzyme activity; and enhanced the Cd metal tolerance of rice [128]. Xu et al. [129] found, through the conjoint analysis of miRNA and transcriptomes, that melatonin treatment can induce the upregulated expression of RsMT1 gene in radish seedlings under Cd stress, thereby enhancing the tolerance of radish to Cd. Under Cd and Pb stress, the expression of the lipoperoxidase gene LOX and POX in naked oat seedlings increased significantly after the exogenous application of melatonin; the expression level of the Asmap1 gene in the MAPK cascade reaction was significantly upregulated; the transcription factors NAC and WRKY1 also improved to varying degrees [61]. This shows that melatonin can alleviate the adverse environment of Cd and Pd in the growth processes of naked oat seedlings. In addition, melatonin could also reduce Cu toxicity by inducing the expression of several defense genes (CAT, APX, GR, and MDHAR) and MT-biosynthesis-related genes (TDC, SNAT, and COMT) in tomato plants under Cu stress [35]. The above results indicate that melatonin not only participates in metal detoxification but also participates in the regulation of cell redox homeostasis.
In summary, at the molecular level, the current research on the impact of exogenous melatonin on heavy metal stress has mainly focused on resisting the adverse effects of heavy metal stress by activating and regulating MYB, MRKY, NAC, and other transcription factors, as well as MAPK cascade reactions and other signal transduction pathways under heavy metal stress, so as to alleviate the toxicity of plants.

4.4. From the Perspective of Nutrient Absorption, How Does Melatonin Alleviate Heavy Metal Stress in Plants?

Nutrient elements constitute an important material foundation for plant growth and development. The excessive intake of heavy metal elements will certainly interfere with the absorption and utilization of nutrient elements, thus affecting both the final yields and quality of crops as well as the energy consumption, input–output ratio, and sustainable development of agriculture. Therefore, it is very necessary to review how melatonin alleviates heavy metal stress in plants from the perspective of nutrient absorption.
As is well known, the roots of plants are specialized organs for the absorption and transportation of mineral nutrients and are also important organs for sensing the external nutritional status [130]. Therefore, the mechanism of coordination between the structure and function of the roots and the nutritional status in plants is crucial. However, heavy metal stress in soil can generate a large amount of ROS, causing oxidative stress and altering the plant cell structure. Among these two effects, due to the first inhibition of plant roots by heavy metals, the root structure is first damaged, seriously affecting the absorption and transportation of mineral nutrients. For example, research has found that Cu stress inhibits plant root development; improves cell membrane permeability; causes K+ and PO43− plasma to leak out; and reduces the contents of P, K, Ca, and other nutrients in plant roots [131]. These results are similar to the research results from Lidon and Henriques [132], who pointed out that Cu stress can inhibit the absorption of trace elements such as Mn, Fe, and Ca in plants. However, the application of melatonin can significantly improve this situation. For example, under Ni stress, the contents of macroelements (N, P, Ca, Mg, S) and micronutrients (Fe, Mn, Zn) in tomato seedlings were found to be significantly reduced while melatonin could significantly increase the contents of these nutrients under Ni stress, alleviate oxidative stress by inhibiting the accumulation of ROS, improve the root architecture and the exudation of organic acid anions, and possibly inhibit excessive metal transport and accumulation [133]. In addition, a similar result was reported in wheat [134], that is, melatonin increases the essential mineral nutrients of plants under Cd stress, thus eventually triggering growth in plants. These results suggest that melatonin may be an important substance to promote ion homeostasis in plants.
The different nutrient elements in plants are not independently regulated, and transcription factors and related genes play important roles in them. A series of important functional genes related to plant nutrients and their mechanisms of action have been identified and elucidated, including numerous genes related to nutrient absorption, transportation, and distribution, such as Pstol1, SPX1, OsHMA4, etc. [135,136,137]. In addition, they also include some heavy-metal-related genes such as OsN-RAMP5, OPT3, WKRY6, etc. [138,139,140]. The oxidative stress caused by heavy metal stress in plants can cause DNA damage, affecting some important functional genes related to nutrient absorption, transportation, and distribution; hindering nutrient absorption; interfering with metabolism; and inhibiting growth and reproduction [141]. Melatonin plays an important role in alleviating this kind of plant injury. Under heavy metal stress, melatonin may regulate some transporter genes in the NRT, AMT, PHT, SUT, ZIP, YSL, and ABC families. The transport proteins of the NRT family, AMT family, PHT family, SUT family, and ZIP family are responsible for nitrate, ammonium, phosphate, sulfate, and zinc uptake and transport, respectively [142,143,144,145,146,147]. The transport proteins of the YSL and ABC families are mainly involved in the transport of various metal ions in plants, such as Fe, Zn, Cu, Ni, and Mn [148,149]. For example, in a study, the application of melatonin reversed the toxic effect of Cu2+. The contents of K, Mg, and Ca in the root and P in the leaves of cucumber were close to the values observed in CK. At the same time, melatonin increased the content of Mn in the root [150]. The results show that melatonin may play a role in balancing nutrients by regulating the content of nutrient elements by regulating the relevant transporter genes.
Heavy metal stress can also reduce nutrient uptake and transport by affecting plant photosynthesis and carbohydrate metabolism. Research found that Cd stress treatment reduced the N content in the leaves of garden water celery (Lepidium sativum L.), leading to disrupted coordination between C, S, and N metabolism, leading to poor plant growth and sensitivity to Cd stress [151]. However, melatonin enabled plants to maintain nutrient absorption flux, improve plant metabolism, and significantly reduce growth inhibition [78]. For example, the application of melatonin significantly enhanced the growth traits of plants under Ni stress, increased chlorophyll content and photosynthetic efficiency, reduced Ni accumulation, and improved the steady states of mineral nutrients [133]. Under Cd stress, melatonin increased the chlorophyll content in cotton, promoted photosynthesis, and enhanced the contents of some nutrients (Ca, Mg, Fe, Zn, Na, Mn), which would also have reduced the contents of the K, P, and S elements and, to some extent, decreased the damage of Cd to cotton plants [25]. Melatonin increased the content of soluble sugar, soluble protein, and chlorophyll in zinnia seedlings under Cr stress and decreased the accumulation of Cr [152]. Melatonin resisted heavy metal stress in plants, improved the inhibition brought by heavy metal stress, promoted the absorption and transport of mineral nutrients, and regulated the accumulation of mineral elements. In this paper, melatonin’s effects in improving the absorption and transport of mineral nutrients in plants under heavy metal stress have been summarized in Table 2.
In summary, from the perspective of nutrient absorption, current research shows that melatonin can promote nutrient absorption by clearing ROS and upregulating the expression of genes related to element absorption and transport and can also enable plants to maintain a nutrient absorption flux; regulate mineral element accumulation, transportation, and distribution; and reduce growth inhibition by regulating photosynthesis and the carbohydrate metabolism mechanism.

5. Conclusions and Future Research Directions

Currently, an increasing trend in heavy metal content has been found in arable soil, which poses a serious threat to plants. Therefore, it is urgent to find ways to alleviate the harm caused by heavy metal pollution to plants. Melatonin has been widely studied as a growth regulator and antioxidant in plants. In plants, melatonin also plays an important anti-stress role in the face of heavy metal stress. Melatonin mainly improves the antioxidant stress response and regulates photosynthesis and the carbohydrate metabolism by activating and regulating MYB, MRKY, NAC, and other transcription factors and signal transduction pathways related to heavy metal stress so as to improve the germination rates of seeds and promote the balanced absorption of nutrients, plant growth and development, and the maturity and senescence of late development, ultimately alleviating the heavy metal toxicity of plants.
Although much progress has been made in the research on melatonin in plants, there are still some problems to be studied.
(1)
The research and application of melatonin related to crops should be strengthened. In cultivated soil, crops are mainly planted. With the increasing trend of heavy metal content in cultivated soil, melatonin can improve the tolerance of plants to heavy metals. Therefore, it is necessary to strengthen the research and application of melatonin in the absorption and accumulation of nutrients, yield, and the quality of crops (especially staple grains) so as to truly apply melatonin in production to solve practical problems.
(2)
The mechanism of the interaction between melatonin and other plant hormones should be make clear. Melatonin may participate in other plant reactions after being directly perceived by receptors. For example, JA and SA, which are closely related to the defense response, may interact with melatonin to participate in the regulation of plant growth and development, but whether there is a cross between JA, SA, and the MAPK cascade reaction of melatonin remains to be further studied.
(3)
Melatonin-hormone signal perception and transmission should be explored. Although researchers have cloned a melatonin plant receptor, CAND2/PMTR1, in recent years, there have been few studies on the direct downstream signals activated after the receptor binds melatonin. The question of whether there are other melatonin receptors is also a scientific problem that needs to be solved urgently.
(4)
The selection of crop varieties with high melatonin contents and screening of stress resistance genes should be carried out. These constitute an attractive and challenging research direction to select crop varieties with high melatonin contents and develop crops with resistance to reversion genes by using the existing research results on melatonin and combining the traditional breeding theory and experience.

Author Contributions

Conceptualization and investigation, X.C. and X.L.; software, X.C. and F.L.; formal analysis and data curation, X.L., F.L. and Y.Y.; writing—original draft, X.C. and X.L.; writing—review and editing, X.C. and T.K.; project administration, T.K.; funding acquisition, X.C. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by the National Nature Science Foundation of China (No. 32401741), Joint Fund for Science and Technology Research and Development Plan of Henan Province (Application Research and Development Category) (No. 232103810058), and PhD Startup Foundation of the Henan University of Science and Technology (No. 13480101).

Conflicts of Interest

The authors report no declarations of interest.

Correction Statement

This article has been republished with a minor correction to the Funding statement. This change does not affect the scientific content of the article.

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Figure 1. Effects of heavy metal stress on plant growth, development, and physiological and ecological characteristics. Abbreviations: HM, heavy metal; SOD, Superoxide dismutase; CAT, Catalase; POD, Peroxidase; ADH, Alcohol dehydrogenase.
Figure 1. Effects of heavy metal stress on plant growth, development, and physiological and ecological characteristics. Abbreviations: HM, heavy metal; SOD, Superoxide dismutase; CAT, Catalase; POD, Peroxidase; ADH, Alcohol dehydrogenase.
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Figure 2. The role of melatonin as a growth-promoting regulator and antioxidant in plant growth and development. (a) The effects of melatonin on plant growth, root development, flowering cycle, photosynthesis, circadian rhythm, and nutrient uptake and (b) the effect of melatonin on plant seed germination. (The blue arrow in Figure 2a indicates melatonin transport from the root system to the ground).
Figure 2. The role of melatonin as a growth-promoting regulator and antioxidant in plant growth and development. (a) The effects of melatonin on plant growth, root development, flowering cycle, photosynthesis, circadian rhythm, and nutrient uptake and (b) the effect of melatonin on plant seed germination. (The blue arrow in Figure 2a indicates melatonin transport from the root system to the ground).
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Figure 3. Plot of melatonin and heavy metal stress signals and ROS interactions. (I). Melatonin can directly or indirectly remove ROS and reduce the effect of heavy metal oxidative stress on plant growth and development. (II). Melatonin can chelate the toxic metals to reduce the stress caused by heavy metals. Stress is first recognized by receptors in the plant cell membrane, followed by a series of signaling cascades. First, Ca2+ and ROS are generated and involved in the transmission of heavy metal stress signals, whereafter levels of related transcription factors can be induced by melatonin and heavy-metal-stress-signaling molecules. Then, melatonin regulates the expression of redox-related genes and plant stress defense, such as in the form of CLHl (the chlorophyll-enzyme-related gene), PAO (chlorophyll-A-oxygenase-related gene), and NHXl/AKTl (ion balance-related gene). However, the specific downstream symbol is not clear, as shown in the figure of “?”. (III). Melatonin can be directly sensed by the receptors and may be involved in other physiological functions. (Refer to [81].).
Figure 3. Plot of melatonin and heavy metal stress signals and ROS interactions. (I). Melatonin can directly or indirectly remove ROS and reduce the effect of heavy metal oxidative stress on plant growth and development. (II). Melatonin can chelate the toxic metals to reduce the stress caused by heavy metals. Stress is first recognized by receptors in the plant cell membrane, followed by a series of signaling cascades. First, Ca2+ and ROS are generated and involved in the transmission of heavy metal stress signals, whereafter levels of related transcription factors can be induced by melatonin and heavy-metal-stress-signaling molecules. Then, melatonin regulates the expression of redox-related genes and plant stress defense, such as in the form of CLHl (the chlorophyll-enzyme-related gene), PAO (chlorophyll-A-oxygenase-related gene), and NHXl/AKTl (ion balance-related gene). However, the specific downstream symbol is not clear, as shown in the figure of “?”. (III). Melatonin can be directly sensed by the receptors and may be involved in other physiological functions. (Refer to [81].).
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Figure 4. Effects of melatonin on plant photosynthetic system under heavy metal stress. (The blue arrow indicates melatonin transport from the root system to the ground).
Figure 4. Effects of melatonin on plant photosynthetic system under heavy metal stress. (The blue arrow indicates melatonin transport from the root system to the ground).
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Table 1. The proportions of inorganic pollutants exceeding the standard in 2014 from National Soil Pollution Investigation Bulletin.
Table 1. The proportions of inorganic pollutants exceeding the standard in 2014 from National Soil Pollution Investigation Bulletin.
Pollutant TypePoint Exceeding the Standard Rate (%)Proportion of Pollution Points of Different Degrees (%)
LightMildModerateSerious
Cd7.005.200.800.500.50
Hg1.601.200.200.100.10
As2.702.000.400.200.10
Cu2.101.600.300.150.05
Pb1.501.100.200.100.10
Cr1.100.900.150.040.01
Zn0.900.750.080.050.02
Ni4.803.900.500.300.10
Note: In this bulletin, the excess rates of points refer to the proportions of the numbers of soil excess points to the total number of investigated points. (Source: [28].).
Table 2. Summary of related studies about melatonin in the physiological aspects of antioxidant system, photosynthetic system, gene expression, and nutrient element absorption in higher plants treated with toxicity of excessive heavy metal contents.
Table 2. Summary of related studies about melatonin in the physiological aspects of antioxidant system, photosynthetic system, gene expression, and nutrient element absorption in higher plants treated with toxicity of excessive heavy metal contents.
Physiological LevelHeavy MetalCropsApplication WaysMelatonin
Concentration		EffectSpecific IndexReferences
PhenotypeCrWheatsoaking seed100 μM (50 grains)↑germination rate[33]
CuBrassica oleracea rubrumsoaking seed1 μM; 10 μM (100 grains)↑germination rate[49]
CuMelon seedlingssoaking seed300 μmol/L (1000 grains)↑root growth inhibition,
root structure		[34]
CuTomatospraying leaf100 µM (6 plants)↑tomato branch and leaf growth[35]
CdWheat seedlingssoaking seed100 µM (150 grains)↑primary root growth[36]
CdRicespraying leaf100 μM (9 plants)↑repression of Cd in flowering rice[50]
CdNaked oatroot irrigation50 μM; 100 μM (32 plants)↑plant height, fresh weight, and dry weight[24]
CdChickpeasoaking seed10 μM↑seed germination and root elongation[51]
CdPlatycladus orientalis seedlingsspraying leaf200 μmol/L (4 plants)↑seedling height, leaf length, leaf width, and stem width[52]
Al; CdKale-shaped rapesoaking seed50 μM; 100 μM (100 grains)↑germination rate of seeds, bud length, and root length[53]
Antioxidant systemAlWheathydroponics10 μM (21 plants)↑SOD, POD, CAT, AsA, GSH, Proline, DPPH, FRAP, GSH/GSSG, AsA/DAH, H2O2, and MDA[54]
CrSwede type rapesoaking seed10 μM (10 grains)↑SOD, POD, CAT, APX, H2O2, and MDA[55]
CrWheatsoaking seed100 μM (50 grains)↑SOD, POD, CAT, APX, the pro-oxidant NADPH-oxidase, H2O2, O2−[33]
CuMonkey peachroot irrigation0.1 μmol/L (3 plants)↑proline, TPC, TFC, TFAC, AsA, DPPH, and FRAP[56]
CuTomatospraying leaf100 μM (6 plants)↑SOD, POD, CAT, APX, FRAP, GSH/GSSG, and ASA/DHA[35]
CdPearl millespraying leaf100 μmol/L; 200 μmol/L↑proline, SOD, POD, CAT, APX, H2O2, and MDA[57]
CdChickpeasoaking seed10 μM↑APX, MDHAR, DHAR, GSH, GSH-PX, the pro-oxidant NADPH-oxidase, NADH-oxidase activities, and H2O2[58]
CdMushroomshydroponics100 μM↑proline, SOD, POD, CAT, APX, GR, H2O2, and O2−[59]
Al; CdKale-shaped rapesoaking seed50 μM; 100 μM (100 grains)↑SOD, POD, CAT, APX, H2O2, and MDA[53]
Pb-Cd compoundAromatic Ricespraying leaf; root irrigation50 μmol/L; 300 μmol/L (25 plants)↑AsA, GSH, SOD, POD, CAT, H2O2, and MDA[60]
Cd; PbOat wheat seedlingsroot irrigation100 μM↑proline, SOD, POD, CAT, H2O2, O2−, and MDA[61]
Photosynthetic systemCrSwede type rapesoaking seed10 μM (10 grains)↑improving the PSI and PSII efficiency[55]
CdTomatospraying leaf100 μM (6 plants)↑chlorophyll content and photosynthetic rate[62]
CdEggplantspraying leaf150 μmol/L (2 plants)↑LUE, Pn, Tr, Gs, and Ci[63]
CdNaked oat seedlingshydroponics50 μM; 100 μM (32 plants)↑chlorophyll content[24]
CdPlatycladus orientalis seedlingsspraying leaf200 μmol/L (4 plants)↑chlorophyll content[52]
Al; CdKale-shaped rapesoaking seed50 μM; 100 μM (100 grains)↑photosynthetic rate[53]
Pb-Cd compoundAromatic Ricespraying leaf; root irrigation50 μmol/L; 300 μmol/L (25 plants)↑chlorophyll content[60]
NiTomatospraying leaf100 μM (10 plants)↑chlorophyll content, photosynthetic rate, and blade gas-exchange parameters[64]
Gene expressionCuMelon seedlingssoaking seed300 μmol/L (1000 grains)↑AP2/ERF, BBR/BP, HD-ZIP, and transcription factor family[34]
CuTomatospraying leaf100 μM (6 plants)↑CAT, APX, GR, MDHAR relative gene expression, TDC, SNAT, and COMT[35]
CdMushroomshydroponics100 μM (8 plants)↑CAT, SOD, POD, GR, and APX relative gene expression[59]
CdNaked oat seedlingshydroponics50 μM; 100 μM (32 plants)↑LOX, POX, Asmap1, NAC, and WRKY1[24]
CdPlatycladus orientalis seedlingsspraying leaf200 μmol/L (4 plants)↑POD, GST, APX, and ADH[52]
CdChickpeasoaking seed10 μM↑G6PDH and RBOHF[58]
PbRadishspraying leaf50 μM↑RsWRKY41, RsMYB2, RsAPX2, RsPOD52, and RsGST[65]
Cd; PbOat wheat seedlingsroot irrigation100 μM↑LOX, POX, and Asmap1[61]
Al; CdKale-shaped rapesoaking seed50 μM; 100 μM (100 grains)↑BnCOMT-1, BnCOMT-5, BnCOMT-8, BnCOMT-4, and BnCOMT-6[53]
Nutrient absorptionCuCucumberhydroponics0.01 μmol/L (15 plants)↑K, Mg, Ca, P, and Mn[66]
CdCottonspraying leaf50 μM↑Ca, Mg, Fe, Zn, N, Mn
K, P, and S		[25]
NiTomatospraying leaf100 μM (10 plants)↑N, P, Ca, Mg, S, Fe, Mn, and Zn[64]
Note: ↑ indicates positive improvement effect in plants under heavy metal stress. A detailed description of the results of phenotype, antioxidant system, photosynthetic system, gene expression, and mineral nutrient absorption is presented in Section 4. Abbreviations: SOD, Superoxide dismutase; CAT, Catalase; POD, Peroxidase; ADH, Alcohol dehydrogenase; APX, Ascorbate peroxidase; AsA, Ascorbic acid; GSH, Glutathion; MDA, Malondialdehyde; TPC, total polyphenol compounds; TFC, total flavonoid content; TFAC, total flavanol content; DPPH, Diphenyl picryl hydrazinyl radical; FRAP, Ferric-reducing antioxidant power; GSH/GSSG, Glutathione/Oxidized glutathione; ASA/DHA, Ascorbic acid/Dehydrotype ascorbic acid; MDHAR, Monodehydroascorbate reductase; DHAR, Dehydroascorbate reductase; GSH-PX, Glutathione peroxidase, GR, Gluathione reductase; LUE, Lightuseefficiency; Pn, net photosynthetic rate; Tr, transpiration rate; Gs, stomatal conductance; Ci, intercellular CO2 concentration; TDC, Tryptophan decarboxylase; SNAT, Serotonin N-acetyltransferase; COMT, Catechol-O-methyltransferase; LOX, Lipoxygenase; POX, Peroxidase; Asmap1, the mitogen-activated protein kinase genes; G6PDH, Glucose-6-phosphate dehydrogenase; RBOHF, the respiratory burst oxidase homolog protein F. NAC, WRKY, and MYB are transcription factor genes.
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Cheng, X.; Liu, X.; Liu, F.; Yang, Y.; Kou, T. Facing Heavy Metal Stress, What Are the Positive Responses of Melatonin in Plants: A Review. Agronomy 2024, 14, 2094. https://doi.org/10.3390/agronomy14092094

AMA Style

Cheng X, Liu X, Liu F, Yang Y, Kou T. Facing Heavy Metal Stress, What Are the Positive Responses of Melatonin in Plants: A Review. Agronomy. 2024; 14(9):2094. https://doi.org/10.3390/agronomy14092094

Chicago/Turabian Style

Cheng, Xianghan, Xiaolei Liu, Feifei Liu, Yuantong Yang, and Taiji Kou. 2024. "Facing Heavy Metal Stress, What Are the Positive Responses of Melatonin in Plants: A Review" Agronomy 14, no. 9: 2094. https://doi.org/10.3390/agronomy14092094

APA Style

Cheng, X., Liu, X., Liu, F., Yang, Y., & Kou, T. (2024). Facing Heavy Metal Stress, What Are the Positive Responses of Melatonin in Plants: A Review. Agronomy, 14(9), 2094. https://doi.org/10.3390/agronomy14092094

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