Abstract
Melatonin plays a crucial role in enhancing plant resilience to environmental stresses by regulating physiological and biochemical responses. This review provides an overview of melatonin biosynthesis, signaling pathways, and its interactions with phytohormones, highlighting its multifunctional roles across various crop species. We summarize recent discoveries regarding the biosynthetic pathways of melatonin and its crucial metabolites, emphasizing the importance of tryptophan and serotonin in this process. Furthermore, we discuss the intricate crosstalk between melatonin and phytohormones, particularly auxins, cytokinins, and brassinosteroids, which collectively influence root development, growth, and stress tolerance, among other traits. The antioxidant activity of melatonin and its derivatives, along with their impact on photosynthesis, has also been thoroughly discussed. Notably, melatonin’s regulatory actions promote root growth, thereby improving water and nutrient absorption under stress conditions. The identification of candidate genes and a putative receptor provides a foundation for future studies aimed at elucidating the molecular mechanisms underlying melatonin signaling in crop species. Ultimately, this review underscores the potential of harnessing melatonin in crop improvement strategies to enhance resilience to abiotic stresses while promoting sustainable agricultural practices.
Keywords: Antioxidant systems, Crop resilience, Melatonin, Melatonin derivatives, Phytohormones, Root growth
Introduction
To mitigate the effects of stress, plants have developed a variety of adaptive mechanisms, including the production of biomolecules that modulate physiological and biochemical responses (Khan et al. 2022). Among these regulatory molecules, melatonin (N-acetyl-5-methoxytryptamine) has garnered significant attention in recent years (Zeng et al. 2022). According to the Scopus database (1995–2024), over half of the reports on melatonin in agricultural and biological sciences have been published in the past 5 years (Scopus.com, accessed June 2024). Melatonin’s multidirectional action in plants, including its regulation of gene expression, enhancement of antioxidant defense systems, and interactions with phytohormones, allows plants to fine-tune metabolic processes and effectively respond to stress signals (Arnao and Hernández-Ruiz 2021). Notably, melatonin’s regulation of phytohormone networks, particularly brassinosteroid (BR) signaling pathways, holds vast potential for increasing plant tolerance to environmental stresses. BRs play a crucial role in regulating root development, a key factor for survival in water-limited environments (Sun et al. 2021; Wei and Li 2016).
This review summarizes recent advances in understanding melatonin biosynthesis, metabolism, signaling, and functions across various crop species. Moreover, it discusses the impact of melatonin on plant growth, development, and stress tolerance, with a special focus on its role in hormonal regulation. Additionally, it explores the dynamic interaction between melatonin and phytohormones in regulating root growth, offering valuable insights into potential strategies for crop improvement.
Melatonin biosynthesis and catabolism
Melatonin biosynthesis begins with tryptophan, which is initially converted to serotonin through a two-step process involving decarboxylation and hydroxylation (Back et al. 2016; Erland 2024). In the cytoplasm, tryptophan decarboxylase (TDC) converts tryptophan into tryptamine, which is then hydroxylated to serotonin by tryptamine 5-hydroxylase (T5H), an enzyme located in the endoplasmic reticulum (Fig. 1). Subsequently, serotonin is converted into N-acetylserotonin by serotonin N-acetyltransferase (SNAT), an enzyme primarily found in chloroplasts. Melatonin is then synthesized from N-acetylserotonin by cytosolic N-acetylserotonin methyltransferase (ASMT) or caffeic acid O-methyltransferase (COMT) (Xie et al. 2022). COMT, an enzyme with a broad substrate spectrum, exhibits low specificity for N-acetylserotonin (Wang et al. 2019). Therefore, COMT-mediated methylation of N-acetylserotonin is limited by the enzyme’s preference for other substrates, allowing ASMT to play a dominant role in this process (Byeon et al. 2015a; Back et al. 2016; Huang et al. 2024). Nonetheless, numerous studies on crop plants, including Oryza sativa (Huangfu et al. 2022), Citrullus lanatus (Chang et al. 2021), Nicotiana tabacum (Yao et al. 2022), Gossypium hirsutum L. (Zhang et al. 2024), Solanum lycopersicum L. (Ahammed et al. 2019; Sun et al. 2020a), and Camellia sinensis (Pham et al. 2024), highlight the significance of COMT in melatonin synthesis.
Fig. 1.
Melatonin biosynthesis in plants. Dashed arrows indicate hypothetical biosynthetic pathways. TDC, tryptophan decarboxylase; TPH, tryptophan hydroxylase; T5H, tryptamine 5-hydroxylase; SNAT, serotonin N-acetyltransferase; ASMT, N-acetylserotonin methyltransferase; COMT, caffeic acid O-methyltransferase (figure drafted on the base of Yu et al. 2018; Khan et al. 2023a, using BioRender tool at http://biorender.com)
Under stress conditions or during plant senescence, when serotonin accumulates to high levels, it can be converted to 5-methoxytryptamine by ASMT/COMT and subsequently to melatonin by SNAT, causing the final step of biosynthesis to occur in chloroplasts (Fig. 1) (Choi et al. 2017; Lee et al. 2014; Liu et al. 2022a). Melatonin production may also take place in other cellular compartments. For example, mitochondria isolated from Arabidopsis thaliana with a SNAT isoform cloned from Malus zumi retained the ability to produce melatonin after serotonin treatment (Wang et al. 2017). However, other studies indicate that SNATs are mainly localized in chloroplasts (Byeon et al. 2014; Yu et al. 2019). Tan and Reiter (2020) propose that under stress conditions, melatonin synthesis could shift from chloroplasts to mitochondria when the former is compromised.
Melatonin synthesis pathway in plants shares certain elements with those found in other organisms (Zhao et al. 2019a). In both plants and animals, melatonin synthesis begins with tryptophan, which is converted to serotonin; however, the intermediates and enzymes involved in these processes differ significantly. In animals, the pathway initiates with the conversion of tryptophan into 5-hydroxytryptophan by tryptophan hydroxylase (TPH), followed by transformation into serotonin via aromatic L-amino acid decarboxylase. Subsequently, serotonin is converted into N-acetylserotonin by SNAT or arylamine N-acetyltransferase (AANAT), and finally, N-acetylserotonin is converted into melatonin by ASMT or hydroxyindole-O-methyltransferase (Kim et al. 2024). The biosynthetic pathway of melatonin in bacteria is expected to be analogous to that in animals, following the 5-hydroxytryptophan route. For instance, Ma et al. (2017) revealed that in Pseudomonas fluorescens, isotopic tryptophan was incorporated into 5-hydroxytryptophan, but not into tryptamine. Similarly, Jiao et al. (2016) reported that Bacillus amyloliquefaciens produced various melatonin intermediates, including 5-hydroxytryptophan, but not tryptamine. In contrast, Muñiz‐Calvo et al. (2019) found that in Saccharomyces cerevisiae, tryptophan is converted directly into tryptamine without undergoing hydroxylation. Additionally, S. cerevisiae possesses enzymes such as AANAT and polyamine acetyltransferase, which, along with the detection of 5-methoxytryptamine as an intermediate, suggest that in yeasts melatonin may be synthesized directly from this compound (Bisquert et al. 2023; Que et al. 2020).
Notably, there may be an alternative route for melatonin synthesis in plants that bypasses the involvement of T5H. In rice mutants lacking T5H activity, which blocks serotonin production, both melatonin and 5-hydroxytryptophan, an intermediate in serotonin synthesis in animals, were found to increase (Park et al. 2012). These findings suggest the possible existence of a similar pathway in plants, although TPH, the enzyme responsible for 5-hydroxytryptophan production, has not yet been identified in plants (Tan et al. 2016a). For TPH1 and TPH2 genes, which are highly conserved among vertebrates (Xu et al. 2019), we applied a sequence alignment-based method (www.blast.ncbi.nlm.nih.gov); however, no homologs were detected in monocots such as Triticum aestivum L. and Hordeum vulgare L. (Table 1), nor in the dicot Glycine max L. These species were selected for analysis as representatives of economically important crops with complex genomes. It has been proposed that a putative TPH-like in plants could generate 5-hydroxytryptophan, which is then converted into serotonin by TDC (Park et al. 2008; Mannino et al. 2021). While direct evidence of TPH as a functional enzyme in plants is lacking, the existence of alternative pathways for melatonin biosynthesis suggests a complexity that warrants further investigation. Moreover, there may be an as-yet-undiscovered melatonin biosynthesis pathway that bypasses serotonin entirely. Arnao et al. (2023) proposed a melatonin biosynthesis route involving SNAT, which converts tryptamine to N-acetyltryptamine. Subsequently, N-acetyltryptamine can be converted into N-acetylserotonin by T5H, although this pathway is yet to be confirmed in plants. To date, SNAT-mediated production of N-acetyltryptamine was experimentally validated in the cyanobacterium Synechocystis sp. by Byeon et al. (2013). The potential SNAT-mediated conversion of tryptamine in plants requires further research, as it could eliminate the inhibitory effect of serotonin on melatonin production (Back et al. 2016).
Table 1.
Genes encoding enzymes involved in melatonin biosynthesis and degradation in O. sativa and their potential orthologs in cereal species
In the National Center for Biotechnology Information database, accession numbers beginning with the ‘XM’ prefix represent mRNA transcripts predicted by gene prediction algorithms during the genome annotation process (http://www.ncbi.nlm.nih.gov). A complete list of gene accession prefixes can be found in the DNA Data Bank of Japan database at http://www.ddbj.nig.ac.jp/documents/prefix-e
aGenes involved in melatonin biosynthesis and catabolism reported by Okazaki et al. (2010), Byeon et al. (2015a, 2016), Lee et al. (2016), Wei et al. (2016), Hong et al. (2018)
bO-methyltransferase with ASMT activity, according to Hong et al. (2018)
cOs2-ODD11 and Os2-ODD33 with proven M2H and M3H activity by Lee et al. (2016), Wei et al. (2016)
Enzymatic and non-enzymatic conversion of melatonin in plants
The melatonin molecule possesses methoxy and acetyl side chains, which contribute to its amphiphilic nature, allowing it to easily cross biological membranes and access various compartments within plant cells. Once in specific cellular compartments, melatonin can undergo both enzymatic and non-enzymatic transformations (Mannino et al. 2021). The primary products of melatonin’s enzymatic modifications in plants include its hydroxylated derivatives: 2-hydroxymelatonin (2-OHM) and cyclic 3-hydroxymelatonin (C3-OHM), followed by the metabolite N1-acetyl-N2-formyl-5-methoxykynuramine (AFMK) (Fig. 2).
Fig. 2.
Main melatonin metabolites in plants. M2H, melatonin 2-hydroxylase; M3H, melatonin 3-hydroxylase; IDO, indoleamine-2,3-dioxygenase; 1O2, singlet oxygen; ·OH, hydroxyl radical (figure drafted on the base of Hardeland 2017; Back 2021, using BioRender tool at http://biorender.com)
The enzymes responsible for melatonin conversion are distributed across different cellular compartments. Melatonin 2-hydroxylase (M2H), which produces 2-OHM, is mainly located in chloroplasts, while melatonin 3-hydroxylase (M3H) and indoleamine-2,3-dioxygenase (IDO), which generate C3-OHM and AFMK, respectively, are observed in the cytoplasm. Both M2H and M3H exhibit higher catalytic efficiency in plants compared to melatonin biosynthetic enzymes such as SNAT and ASMT (Hardeland 2017; Back 2021). A quantitative analysis of 2-OHM in 24 plant species, including 11 crop plants, revealed that its average content was significantly higher than that of melatonin (Byeon et al. 2015b). Lee et al. (2016) further demonstrated that the catalytic efficiency of M3H in O. sativa exceeded that of M2H, resulting in C3-OHM levels more than tenfold higher than 2-OHM. In contrast, AFMK was produced at a considerably lower level compared to the two previously mentioned melatonin derivatives. These findings indicate that melatonin undergoes rapid metabolism within plant cells, predominantly forming 2-OHM and C3-OHM.
The same metabolites can also form through the non-enzymatic transformation of melatonin caused by free radicals and other reactive compounds generated during oxidative stress. Melatonin has a high reduction potential due to its electron-rich indole ring, enabling it to react with various oxygen- and nitrogen-based free radicals in plant cells. For instance, hydroxylation of melatonin via reactions with two hydroxyl radicals can occur at any unsubstituted carbon atom on the indole ring, leading to the formation of metabolites such as 2-OHM and C3-OHM. AFMK can then be produced when C3-OHM reacts with two hydroxyl radicals (Hardeland 2016). However, studies by Lee et al. (2016) revealed that treating O. sativa with C3-OHM did not result in AFMK production, suggesting that in plants, AFMK may be primarily synthesized from melatonin via IDO or alternative pathways. Hardeland (2017) indicated that AFMK can be formed through various non-enzymatic processes, either from melatonin itself or through its metabolites. One such pathway involves the direct reaction of melatonin with singlet oxygen (Fig. 2). Furthermore, melatonin-derived metabolites are likely formed under ultraviolet radiation (UVR) exposure, as the absorption of UVR by melatonin’s aromatic indole ring may induce chemical bonds cleavage and structural transformations. In a cell-free system, it was demonstrated that UVR induces melatonin catabolism, leading to the formation of derivatives such as AFMK and 2-OHM (Fischer et al. 2006). UVR also excites various cellular components, transferring energy to molecular oxygen and generating singlet oxygen, which then reacts with melatonin. As UVR influences the melatonin molecule both directly and indirectly, its metabolism is promoted during light exposure (Pospíšil et al. 2019; Slominski et al. 2017a, 2018). Notably, tryptophan, similar to melatonin, can also undergo conversion by UVR and reactive oxygen species (ROS), with 5-hydroxytryptophan as a product (Slominski et al. 2012; Bellmaine et al. 2020). The nonenzymatic synthesis pathway of 5-hydroxytryptophan could explain the existence of an alternative melatonin synthesis pathway via 5-hydroxytryptophan, despite the absence of the TPH enzyme in plants.
Pleiotropic effects of melatonin derivatives
Melatonin transformation to its derivatives leads to biologically relevant effects. For instance, the antioxidant properties of AFMK have been widely described in human studies. It has been shown that AFMK itself is not as potent antioxidant as melatonin; however, its derivative, N1-acetyl-5-methoxykynuramine, exhibits stronger antioxidative effects (Hardeland 2017; Janjetovic et al. 2014; Tan et al. 2015; Bocheva et al. 2022). However, it remains unclear whether AFMK plays a significant role in plant antioxidant defense. Tan et al. (2007) observed that higher levels of AFMK were formed in Eichhornia crassipes plants exposed to high light intensity, suggesting its potential role in photoprotection against UVR. In contrast, metabolites such as 2-OHM and C3-OHM have been studied in more detail. Lee and Back (2022) demonstrated that C3-OHM exhibits significantly higher antioxidant activity than melatonin and 2-OHM in A. thaliana. This finding aligns with the earlier prediction by Pérez-González et al. (2017) regarding the low antioxidant activity of 2-OHM, based on its structural features. According to Korkmaz et al. (2023), 2-OHM reduces oxidative damage in Capsicum annuum L. by increasing proline levels and the activity of antioxidant enzymes. A similar effect was observed in Cucumis sativus L., where 2-OHM induced antioxidants accumulation and the expression of stress-responsive genes (Shah et al. 2019). C3-OHM, beyond its antioxidant properties, has been linked to the regulation of flowering-related gene expression in A. thaliana (Lee and Back 2022). These findings indicate that the pleiotropic effects of melatonin in plants are likely not only due to the properties of melatonin itself, but also result from its derivatives.
In silico identification of melatonin biosynthetic and catabolic genes in crop plants
Knowledge about melatonin synthesis and degradation in plants primarily derives from studies on O. sativa (Back 2021). Orthologs of O. sativa melatonin biosynthetic genes have been identified in silico for various plant species (Bhowal et al. 2021; Yang et al. 2022); however, catabolic genes remain largely unexplored in many crops, including cereals. In this study, using experimentally confirmed O. sativa gene sequences involved in melatonin biosynthesis and catabolism, along with a sequence alignment-based method (http://www.blast.ncbi.nlm.nih.gov), we identified their putative orthologs in H. vulgare and T. aestivum (Table 1). Sequences were filtered based on the criteria of over 50% query coverage and 70% identity. For melatonin catabolic genes encoding 2-oxoglutarate-dependent dioxygenases, 2-ODD11, which exhibits both M2H and M3H activities, and 2-ODD21, with M3H activity (Lee et al. 2016; Wei et al. 2016), query coverage was lowered to 23% to facilitate the identification of potential orthologs.
No orthologs of the rice gene encoding the IDO enzyme were found in either H. vulgare or T. aestivum (Table 1). The presence of signature domains (pyridoxal-dependent decarboxylase, PF00282; cytochrome P450, PF00067; acetyltransferase, PF00583; O-methyltransferase domains, PF08100 and PF00891; leucine carboxyl methyltransferase, PF04072; 2-oxoglutarate-dependent dioxygenase domains, PF14226 and PF03171) confirmed the putative identity of the identified orthologs. All candidate genes identified through in silico analysis require further research to confirm their functional roles in melatonin biosynthesis and degradation.
Melatonin signaling
Melatonin signaling and its downstream effectors coordinate a variety of plant developmental processes, including seed germination, vegetative growth, flowering, and senescence (Tiwari et al. 2021). By influencing metabolites accumulation, osmoregulation, photosynthesis, mitochondrial respiration, redox homeostasis, and interactions with phytohormones, melatonin enables plants to fine-tune their responses to environmental stresses and ensure optimal growth (Fig. 3) (Sun et al. 2021; Gao et al. 2023).
Fig. 3.
Model of melatonin action in plants in response to stress (figure drafted on the base of Arnao and Hernández-Ruiz 2021; Tiwari et al. 2021, using BioRender tool at http://biorender.com)
Through its putative receptor, Cand2, mitogen-activated protein kinase (MAPK) cascades, and downstream transcription factors, melatonin influences the expression of genes related to plant growth, development, and stress responses (Gao et al. 2023). Notably, plant melatonin signaling system shares similarities with melatonin signal transduction in animals, where G-protein-coupled receptors (GPCRs) melatonin type 1 (MT1) and type 2 (MT2), activate a variety of signaling pathways, such as MAPK, protein kinase A, and calcium signaling. However, while animals possess two well-characterized GPCRs, studies indicate the existence of only one potential melatonin receptor in plants, which operates through a mechanism functionally similar to GPCRs (Hardeland 2009; Gao et al. 2022; Park 2024).
Melatonin mediates its effects through the Cand2 protein, believed to be the first identified phytomelatonin receptor (PMTR1) in A. thaliana (Wei et al. 2018; Khan et al. 2023a). Cand2 is proposed to function as an uncanonical G-protein-coupled receptor (GPCR) due to its interaction with the G-protein α subunit (Gα). However, the activation mechanism remains unclear, largely because traditional G-protein signaling in plants differs from that in animals; in plants, Gα is self-activated (Jones et al. 2011). Liu et al. (2021b) suggested a model for non-canonical GPCR action in plants, incorporating aspects of G-protein signaling from both animals and plants (Fig. 4). In animals, GPCR interacts with a G-protein composed of Gα and a Gβγ dimer, with Gα bound to guanosine diphosphate (GDP). Upon ligand binding, the GPCR promotes the exchange of GDP for guanosine triphosphate (GTP), triggering the dissociation of Gα from the Gβγ dimer and initiating signaling. Gα, with its intrinsic GTPase activity, hydrolyzes GTP to GDP, completing the signaling cycle (Jiang et al. 2022). In turn, in plants, Gα spontaneously exchanges GDP, resulting in self-activation without the need for GPCR induction. The regulator of G-protein signaling protein hydrolyzes GTP, returning Gα to its inactive state. In the proposed model, Cand2 serves as an uncanonical GPCR, acting as a signaling molecule that induces Gα self-activation. Upon receiving a signal, Gα exchanges GDP for GTP and activates itself. The dissociated Gα and Gβγ dimer then interact with various intracellular effectors, such as transcription factors and enzymes, to regulate plant growth and responses to environmental stimuli (Liu et al. 2021b; Maruta et al. 2021).
Fig. 4.
Proposed model for melatonin signaling via Cand2/PMTR1 in plants. Cand2/PMTR1, phytomelatonin receptor; Gα and Gβγ, G-protein subunits; GDP, guanosine diphosphate; GTP, guanosine triphosphate; MEL, melatonin; RGS, regulator of G-protein signaling protein (figure drafted on the base of Wei et al. 2018; Liu et al. 2021b, using BioRender tool at http://biorender.com)
In A. thaliana, Cand2 plays a critical role in melatonin-mediated stomatal closure, involving NADPH oxidase-dependent hydrogen peroxide production and the activation of Ca2+ channels (Wei et al. 2018). A. thaliana mutants lacking the CAND2 gene are insensitive to melatonin-induced stomatal closure and exhibit increased sensitivity to osmotic stress, along with heightened ROS accumulation (Wang et al. 2021a). In wild-type plants, melatonin induces the expression of antioxidant enzymes such as catalase and superoxide dismutase in response to stress; however, this induction is suppressed in CAND2 mutants. These findings underscore the essential role of Cand2 in melatonin-mediated gene expression and antioxidant responses. Bychkov et al. (2022) further demonstrated that melatonin, through Cand2, regulates mitochondrial gene expression during photooxidative stress. In A. thaliana, oxidative stress typically suppresses the expression of mitochondrial genes related to the respiratory chain, cytochrome c, ribosomal proteins, and transport proteins. Melatonin treatment during photooxidative stress contributed to maintain the expression of these genes in wild-type plants, but its effect on transcript accumulation in CAND2 knockout mutants was minimal. These receptor-dependent effects highlight melatonin’s broad regulatory roles, leading to suggestions that melatonin could be classified as a new phytohormone (Arnao and Hernández-Ruiz 2019). Although knowledge about the putative melatonin receptor Cand2/PMTR1 primarily comes from studies on A. thaliana, an ortholog of the CAND2 gene has been identified in several other plant species, including O. sativa (Barman et al. 2023), Medicago sativa (Yu et al. 2021), Zea mays (Wang et al. 2021b), G. hirsutum (Zhang et al. 2023b), and Manihot esculenta (Bai et al. 2022). However, no studies have yet been conducted on the role of Cand2/PMTR1 in cereal crops.
A known intracellular effector activated by melatonin receptor binding in both plants and animals is MAPK, which converts signals into physiological responses. In the MAPK cascade, at least three kinases are sequentially phosphorylated: MAPKKK, MAPKK, and MAPK. Upon activation, the final kinase translocates within the cell to phosphorylate various targets, including transcription factors (Back 2021; Nikolaev et al. 2022; Zhang and Zhang 2022). While MAPKs function downstream of GPCR signaling in animals, studies have shown that melatonin-induced MAPK activation is impaired in A. thaliana CAND2 mutants, but remains unaffected in both G-protein subunit α and β mutants. These findings suggest that melatonin signal transduction via MAPK may function independently of G-protein signaling (Chen et al. 2020; Lee and Back 2016; Yang et al. 2021b). Moreover, studies by Lee and Back (2016) have shown that melatonin-mediated MAPK activation in A. thaliana is not linked to calcium signaling. The independence of both calcium and G-protein signaling suggests that plants may have distinct melatonin signaling mechanisms compared to animals (Cecon et al. 2018). Liu et al. (2022b) proposed a model for melatonin signaling through the MAPK cascade, in which signaling remains inactive in the resting state due to a putative inhibitor that dephosphorylates MAPKKK (Fig. 5). Binding of melatonin to PMTR1 triggers the activation of the kinase responsible for inducing inhibitor ubiquitination. Following the degradation of the inhibitor, the MAPK cascade is activated, leading to the induction of various downstream effectors that allow melatonin to exert pleiotropic effects in plants. Further research on PMTR1 signaling via MAPK and the identification of new melatonin receptors will contribute to a better understanding of melatonin’s action in plants.
Fig. 5.
Proposed model of melatonin signal transduction through MAPK cascade. Cand2/PMTR1, phytomelatonin receptor; MAPKKK, mitogen-activated protein kinase; MEL, melatonin; TF, transcription factor (figure drafted on the base of Dzinyela et al. 2024; Liu et al. 2022a, b; Zhang and Zhang 2022, using BioRender tool at http://biorender.com)
Recently, Slominski et al. (2023) identified two nuclear melatonin receptors in human cells: the aryl hydrocarbon receptor (AHR) and the peroxisome proliferator-activated receptor gamma (PPARγ). Binding to these receptors may explain the cytoprotective actions of melatonin, as both AHR and PPARγ have been extensively studied for their roles in promoting barrier function and inflammatory signaling (Konger et al. 2021; Rothhammer and Quintana 2019). To date, no nuclear melatonin receptors have been found in plants.
Melatonin in antioxidant activity, redox homeostasis, and metabolic regulation
A primary function of melatonin, due to its chemical structure, is to act as a free radical scavenger. The antioxidant properties of melatonin derivatives prolong its effects in plants (Tan et al. 2014; Lee and Back 2022). The potential for an antioxidant cascade, where melatonin metabolites formed through interactions with free radicals continue to scavenge subsequent radicals, further enhances the antioxidative capacity of a single melatonin molecule (Reina and Martínez 2018). The stimulatory effect of melatonin on the activity of antioxidant enzymes, including superoxide dismutase, catalase, and peroxidase, has been documented in various crop species, such as Prunus persica (Gu et al. 2021), Brassica napus L. (Ali et al. 2023b), T. aestivum (Sun et al. 2023a), and O. sativa (Munir et al. 2024). Additionally, melatonin enhances the levels of ascorbic acid and glutathione, which are key antioxidants involved in the ascorbate–glutathione cycle, a major mechanism for hydrogen peroxide detoxification (Altaf et al. 2022a; Wang et al. 2012). Despite its antioxidant effects, melatonin stimulates respiratory burst oxidase homologs (RBOH), enzymes that transfer electrons from NADPH to oxygen, leading to the production of superoxide anions (Gu et al. 2022). While the excessive accumulation of ROS can cause oxidative damage and plant cell death, these molecules also function as signaling agents, enabling plants to adapt to dynamic environments (Khan et al. 2023b). The regulatory mechanism of melatonin-mediated ROS signaling has been experimentally validated in Solanum lycopersicum (Gong et al. 2017), A. thaliana (Li et al. 2020), and N. tabacum (Xiao et al. 2023). By acting as both a free radical scavenger and a mediator in antioxidant and pro-oxidant pathways, melatonin significantly contributes to maintaining redox homeostasis in plants. The interplay between ROS, reactive nitrogen species, and melatonin, including the induction of melatonin biosynthesis during stress conditions, forms a complex redox network essential for plant functioning (Arnao and Hernández-Ruiz 2019).
The action of melatonin in plants is linked with various components of the redox network, including nitric oxide (NO) (Zhu et al. 2019); however, studies in this area remain limited. Curiously, researches using human cell lines suggest that the interaction between melatonin and NO plays a role in regulating mitochondrial homeostasis. For instance, Sarti et al. (2013) proposed a model in which melatonin, at low concentrations, stimulates the expression of nitric oxide synthase (NOS), leading to an increase in NO levels and a reduction in oxidative phosphorylation efficiency. At higher concentrations, melatonin interacts with calmodulin, inhibiting NOS activity and reducing NO production in mitochondria. Moreover, melatonin inhibits mitochondrial permeability transition pores and induces uncoupling proteins, which helps maintain the optimal membrane potential and enhances oxidative phosphorylation (Slominski et al. 2017b; Tan et al. 2016b). Interestingly, studies in human cell lines indicate also that melatonin promotes DNA repair processes. Santoro et al. (2013) revealed that melatonin activates a p53-mediated DNA damage response, thereby influencing genome integrity. Subsequently, it was shown that melatonin induces activity of nucleotide excision repair factors, XPC and XPA, in a manner independent of MT1 and MT2 receptors (Janjetovic et al. 2017). Unfortunately, both the potential mechanism of melatonin-mediated DNA repair in plants and the role of the interactions between melatonin, NO, and calmodulin in mitochondrial regulation have yet to be clarified.
Melatonin regulates various metabolic processes in plants, including the accumulation of key metabolites in response to stress signals (Arnao and Hernández-Ruiz 2019). During drought stress, melatonin treatment enhances the levels of osmoprotectants such as polyamines, proline, and soluble sugars in various crop species (Tiwari et al. 2021). These osmoprotectants help stabilize cell membranes, maintain proper cell turgor, and prevent organelle damage, while also influencing stomatal arrangement, thereby affecting plant photosynthetic capacity (Ozturk et al. 2021). Through its regulation of polyamine metabolism, melatonin further boosts the antioxidant system, as polyamines possess direct antioxidant properties (Tiwari et al. 2023). Additionally, melatonin promotes the accumulation of flavonoids, anthocyanins, and carotenoids, which contribute to plant protection against abiotic stresses by absorbing UV light and scavenging ROS (Zhang et al. 2016; Liang et al. 2018; Sharma et al. 2020). Long-term UV radiation exposure can lead to cellular damage and elevated ROS levels, resulting in oxidative stress in plants. Melatonin-induced biosynthesis of flavonoids and anthocyanins serves as a protective mechanism, shielding cellular organelles from the effects of intense light (Ferreyra et al. 2021; Pan et al. 2023). Sun et al. (2023b) demonstrated that anthocyanin accumulation plays a crucial role in melatonin-mediated chromium stress tolerance in S. lycopersicum. Acting as metal chelators, anthocyanins reduce chromium toxicity by sequestering it into vacuoles. These findings suggest that by increasing the concentration of osmotic solutes and high-value metabolites, melatonin enables plants to effectively counteract stress signals.
Melatonin in regulation of photosynthesis and mitochondrial respiration
Numerous studies have shown that melatonin positively influences photosynthesis under adverse environmental conditions (Szafrańska et al. 2017; Yang et al. 2021c). The photosynthetic system is highly sensitive to abiotic stresses, which can damage thylakoid membranes, reduce photosynthetic rates, and inhibit plant growth (Muhammad et al. 2021). The concurrent occurrence of photosynthesis and melatonin production in chloroplasts is considered a complex defense mechanism that maintains photosynthetic performance during stress (Pan et al. 2023).
Jahan et al. (2020) reported that melatonin treatment in response to nickel-induced phytotoxicity increases the expression of chlorophyll synthesis genes, enhances gas exchange parameters, and improves the photochemical activity of Photosystem II (PSII) in S. lycopersicum. Similarly, Sharma et al. (2020) found that melatonin enhances photosynthesis in Carya cathayensis during drought stress by inducing metabolic pathways associated with chlorophyll synthesis and downregulating genes responsible for chlorophyll degradation. In C. sativus, melatonin upregulates proteins related to PSII and PSI, increases the activity of their reaction centers, and improves photosynthetic electron transfer (PET) efficiency in response to chilling stress. It has also been shown that melatonin increases the abundance of proteins involved in carbon fixation (Zhang et al. 2021). Altaf et al. (2022b) demonstrated that melatonin enhances photosynthesis under cold stress in C. annuum, improving gas exchange, increasing photosynthetic pigment content, and upregulating genes related to PSI and PSII. Moreover, melatonin increases the activity of photosynthetic enzymes in the Calvin-Benson cycle, enabling plants to maintain high carbon assimilation capacity. These findings clearly demonstrate melatonin’s critical role in maintaining photosynthetic efficiency during stress by promoting pigment recovery, improving gas exchange parameters, and regulating genes related to PSI, PSII, and PET.
In contrast to the extensive research on photosynthesis regulation, fewer studies have examined the effects of melatonin on mitochondrial respiration in plants. Samanta et al. (2020) reported that, under drought conditions in O. sativa, melatonin increases the activity and gene expression of key respiratory enzymes such as pyruvate dehydrogenase (PDH) and citrate synthase, indicating its role in regulating the Krebs cycle rate. Similarly, Turk and Genisel (2020) observed that melatonin has a comparable effect in Z. mays under cold stress, demonstrating that melatonin enhances the gene expression and protein levels of enzymes related to the mitochondrial electron transport chain (ETC). By increasing the activity of cytochrome oxidase, alternative oxidase, and adenosine triphosphate (ATP) synthase, melatonin increases ATP production, which is essential for maintaining cellular processes. These findings align with those of Bychkov et al. (2022), who revealed that during photooxidative stress in A. thaliana, melatonin induces the expression of genes related to various respiratory chain complexes and cytochrome c biosynthesis. Overall, melatonin influences mitochondrial respiration in plants in various environmental conditions by regulating the gene expression of PDH, enzymes associated with the Krebs cycle, and the mitochondrial ETC.
Melatonin in phytohormonal regulation
Early research on the interaction between melatonin and phytohormones focused on auxins due to the structural similarly between melatonin and indole-3-acetic acid (IAA), as well as melatonin’s auxin-like effects in promoting plant vegetative growth. Studies revealed that melatonin promotes auxin responses by regulating a wide range of genes involved in auxin biosynthesis and its signaling pathways (Khan et al. 2022). Wei et al. (2022) reported that melatonin enhances the expression of genes related to auxin biosynthesis (YUCCA), signal transduction (TIR1, AFB3), transport (AUX1, PIN), and various auxin-responsive genes in G. max (Table 2). Similarly, Liang et al. (2017) demonstrated that melatonin-induced root growth in O. sativa is associated with the activation of genes involved in the auxin signaling pathway. Therefore, melatonin regulates plant growth at least partially through an auxin-dependent manner.
Table 2.
The effect of melatonin on phytohormones in crops
| Hormone | Crop species | Melatonin interaction | Gene expressiona | References |
|---|---|---|---|---|
| Auxin | Oryza sativa | Synergistic | ↑Aux/IAA, ARF, SAUR, GH3 | Liang et al. (2017) |
| Malus prunifolia | Synergistic | ↑YUCCA1, YUCCA10, ARF7, ARF19, AUX1, PIN1, PIN3, GH3 | Mao et al. (2020) | |
| Glycine max | Synergistic | ↑YUCCA, AMI1, TIR1/AFB, Aux/IAA, ARFs, AUX1/LAX, PIN/PIL, SAUR-like, GH3 | Wei et al. (2022) | |
| Cytokinin | Lolium perenne | Synergistic | ↑IPT2, LOG1, ARR1, ARR10 | Zhang et al. (2017) |
| Agrostis stolonifera | Synergistic | ↑IPT, BRR2, ARR4, ARR9, BRR10, HK3, HK4, HP1, HP4 | Ma et al. (2018) | |
| Abscisic acid | Lolium perenne | Antagonistic | ↓ ZEP, NCED1, ABI3, ABI5 | Zhang et al. (2017) |
| Solanum lycopersicum | Antagonistic |
↓ NCED1, NCED2, AAO3, ABI3, ABI5 ↑CYP707A1, CYP707A2 |
Jahan et al. (2021) | |
| Oryza sativa | Antagonistic | ↓ NCED1, NCED2, AAO, ABI5 | Li et al. (2021b) | |
| Cucumis sativus | Antagonistic |
↓ NCED2 ↑CYP707A1, PYR/PYL/RCAR,, SnRK2, PP2C3, PP2C5 |
Zhang et al. (2023a) | |
| Gibberellin | Cucumis sativus | Synergistic | ↑GA20ox, GA3ox | Zhang et al. (2014) |
| Solanum lycopersicum | Synergistic |
↑GA20ox1, GA20ox2 ↓ GAI, GA2ox1, GA2ox2 |
Jahan et al. (2021) | |
| Oryza sativa | Synergistic |
↑GA1 ↓ GA2ox1, GA2ox2, GA2ox3, GA2ox4 |
Li et al. (2021b) | |
| Jasmonic acid | Solanum lycopersicum | Synergistic |
↑AOC, LoxD, PI II ↓ JAZ1 |
Liu et al. (2019) |
| Brassica napus | Antagonistic |
↑JAZ ↓ AOC |
Tan et al. (2019) | |
| Triticum aestivum | Synergistic | ↑LOX1.5, LOX2 | Luo et al. (2023) | |
| Salicylic acid | Solanum lycopersicum | Synergistic | ↑PR1, PR5 | Zhao et al. (2019a, b) |
| Actinidia deliciosa | Synergistic | ↑PAL, BA2H, PR1 | Guo et al. (2023) | |
| Ethylene | Musa acuminata | Antagonistic | ↓ ACO1, ACS1 | Hu et al. (2017) |
| Pyrus communis | Antagonistic | ↓ ACO1, ACS1 | Zhai et al. (2018) | |
| Solanum lycopersicum | Synergistic | ↑ACS2, ACS4, ACO1, ACO3, ETR1, ETR3, ETR4, ETR6 | Sun et al. (2020a, b) | |
| Vitis vinifera | Antagonistic | ↓ ACO2, ERF4, ERF5, ERF17, ERF26, ERF53, ERF71 | Liu et al. (2021a) | |
| Malus domestica | Synergistic | ↑ACS1, ACS3, ACO1, ACO2 | Verde et al. (2023) | |
| Triticum aestivum | Antagonistic | ↓ ACS | Sehar et al. (2023) | |
| Brassinosteroid | Oryza sativa | Synergistic |
↑DWF4, BRI1, RAVL1, D11, XTR3 ↓ BZR1 |
Hwang and Back (2018) |
| Brassica napus | Synergistic |
↑SQE, STE1 ↓ BSK |
Tan et al. (2019) |
aThe upward arrow represents an increase in gene expression caused by melatonin, whereas the downward arrow indicates a decrease
The effect of melatonin in plants has also been associated with transcriptional changes in genes related to cytokinins (CKs). Ma et al. (2018) demonstrated that melatonin increases the expression of CK biosynthesis genes (IPT) and elements of its signaling pathway in Agrostis stolonifera, delaying drought-induced leaf senescence and improving various physiological parameters. Similarly, Zhang et al. (2017) observed that melatonin, by modulating levels of CKs and abscisic acid (ABA), suppresses heat-induced leaf senescence in Lolium perenne L. During heat stress, melatonin induces the expression of genes involved in cytokinin biosynthesis (IPT2, OG1) and signaling pathways, while reducing the expression of genes associated with ABA biosynthesis (ZEP, NCED) and its transcription factors (ABI3, ABI5) (Table 2). The role of melatonin in mediating stress responses via ABA-dependent pathways has been extensively studied in plants (Ali et al. 2023a). Jahan et al. (2021) demonstrated that melatonin treatment affects ABA and gibberellin (GA) levels in S. lycopersicum during heat stress. In response to stress signals, melatonin decreased the expression of genes related to ABA biosynthesis and signaling while inducing ABA catabolism (Table 2). Melatonin-treated plants also exhibited increased expression of GA biosynthetic genes (GA20ox1, GA20ox2) and reduced expression of genes involved in GA catabolism (GA2ox1, GA2ox2) and signaling inhibition (GAI). Similar findings were reported by Li et al. (2021b), who showed that melatonin, in response to low-temperature stress (LT), induces GA biosynthesis and reduces ABA accumulation during O. sativa seed germination. Additionally, Zhang et al. (2023a) examined the effects of melatonin on C. sativus seed germination under LT stress, highlighting its influence on the expression of genes involved in ABA signaling. Zhang et al. (2014) also demonstrated that melatonin induces GA biosynthesis under salt stress in C. sativus seeds, promoting germination. In C. cathayensis, Sharma et al. (2020) revealed that melatonin reduces ABA accumulation while upregulating the levels of phytohormones such as GA, CK, and BR, contributing to enhanced drought tolerance.
Studies indicate that melatonin regulates both jasmonic acid (JA) and salicylic acid (SA) levels in plants. The regulation of JA and SA biosynthesis is critical for plant development, as many downstream effectors of their signaling pathways are involved in stress responses (Wang et al. 2020; Prakash et al. 2021). Guo et al. (2023) reported that melatonin induces the expression of enzymes involved in SA biosynthesis (PAL, BA2H) in Actinidia deliciosa, leading to the upregulation of SA-responsive genes (PR1) and enhancing plant resistance to chilling and oxidative stress. These findings align with Esmaeili et al. (2023), who observed increased SA levels and PAL activity in Linum album following melatonin treatment. Similarly, Zhang et al. (2019) demonstrated that melatonin induces the accumulation of SA and the expression of SA-responsive genes (PR1, PR5) in S. lycopersicum. Similarly, Luo et al. (2023) demonstrated that melatonin enhances the expression of JA biosynthetic genes (LOX1.5, LOX2) in T. aestivum during drought stress (Table 2). Additionally, melatonin treatment increased methyl jasmonate (MeJA) levels in C. lanatus in response to cold stress (Li et al. 2021a). Liu et al. (2019) demonstrated that melatonin stimulates MeJA accumulation in S. lycopersicum plants by upregulating key JA biosynthetic enzymes (LoxD, AOC) and repressing the negative regulator of JA signaling (JAZ). Conversely, in B. napus seedlings under high salinity conditions, melatonin reduced JA accumulation, alleviating stress-induced growth inhibition (Tan et al. 2019).
Ethylene (ET), like JA and SA, modulates plant defense mechanisms, enabling precise responses to environmental stressors. Additionally, ET plays a regulatory role in various physiological processes, including plant senescence (Chen et al. 2021). Studies on the ripening of Musa acuminata L. (Hu et al. 2017) and Pyrus communis L. fruits (Zhai et al. 2018) demonstrated that melatonin treatment represses ethylene biosynthesis by downregulating ACS1 and ACO1. In contrast, Verde et al. (2023) revealed that melatonin increases ET content during the ripening of Malus domestica fruits by enhancing the expression of its biosynthetic genes (Table 2). Moreover, Sun et al. (2020b) demonstrated that melatonin induces ET signaling in S. lycopersicum fruits, leading to increased carotenoid levels. Under abiotic stress, Liu et al. (2021a) found that melatonin mitigates the adverse effects of ozone stress in Vitis vinifera L. by inhibiting ET biosynthesis and signaling. Similarly, melatonin downregulates ET synthesis in T. aestivum, improving plant resistance to high temperatures (Sehar et al. 2023). These findings suggest that melatonin regulates ET accumulation and signaling, adjusting its levels based on physiological processes and environmental conditions.
Studies on the interaction between melatonin and strigolactones (SLs) or BRs in plants are limited. Zhang et al. (2019) suggested that SLs inhibit melatonin biosynthesis during floral transitions in A. thaliana, promoting flowering, though the exact mechanism remains unclear. Regarding BRs, Lee and Back (2019) demonstrated that suppressing melatonin biosynthesis genes (SNAT2, T5H, and COMT) in O. sativa led to a dwarf phenotype characterized by erect leaves and reduced expression of DWARF4, a key gene involved in BR biosynthesis. Moreover, Hwang and Back (2018) revealed that melatonin and BR interaction in O. sativa seedlings is associated with skotomorphogenesis. These findings suggest that melatonin coordinates plant development by regulating BR biosynthetic genes. Additionally, melatonin promotes the expression of genes involved in BR biosynthesis and signaling (Table 2). Tan et al. (2019) observed that melatonin treatment in B. napus upregulates genes involved in campesterol synthesis (SQE, STE1), a precursor of brassinolide, while downregulating one of the two BR receptor substrates (BSK). Moreover, Hwang and Back (2022) demonstrated that reducing melatonin levels in O. sativa, due to the suppression of RAVL1 and Gα genes, was partially alleviated by exogenous BR treatment, indicating mutual regulation between melatonin and BR synthesis, possibly mediated by a common signaling ligand involving Gα.
Melatonin-phytohormone crosstalk in root development
Abiotic stresses, such as drought, significantly affect root growth and structure, reducing the root’s ability to absorb water and nutrients from the soil. To cope with these environmental challenges, plants adapt by modifying their root system architecture, often directing root growth toward areas with greater water availability while avoiding dry surface soils where drought stress is most severe (Karlova et al. 2021). This adaptive response involves the activation of various signaling pathways in roots, many of which are associated with phytohormones. Understanding the molecular mechanisms behind these root adaptations is crucial for developing strategies to enhance crop resilience and productivity under stress conditions (Nziengui and Ditengou 2023). The role of melatonin in root development was first suggested in the early 2000s by Murch et al. (2001), who observed a correlation between endogenous melatonin levels and de novo root formation in Hypericum perforatum L. Since then, substantial evidence has demonstrated that melatonin regulates both the number and length of adventitious and lateral roots in various plant species (Arnao and Hernández-Ruiz 2017, 2021). Despite this emerging role, the precise molecular mechanisms and downstream targets of melatonin in root development remain unclear (Sun et al. 2021).
Melatonin-mediated root growth is often associated with its interaction with auxins. Liang et al. (2017) revealed that melatonin treatment promotes the number and length of lateral roots in O. sativa by activating auxin signaling. Ren et al. (2019) proposed a model illustrating the interaction between melatonin and auxin in lateral root formation in A. thaliana. According to this model, melatonin regulates the levels of the PIN5 protein, which mediates auxin transport from the endoplasmic reticulum to the nucleus. Both auxin and melatonin treatments downregulate PIN5 expression in roots, possibly through the WAG1 kinase, which reduces auxin transport into the nucleus and increases cytosolic auxin levels, thereby promoting lateral root growth. In another study, Yang et al. (2021a) demonstrated that melatonin stimulates primary root growth in A. thaliana through an IAA-dependent mechanism by modulating the expression of genes involved in auxin biosynthesis. Melatonin and IAA regulate a similar set of genes in A. thaliana roots, and the effect of melatonin on primary root growth diminished when auxin biosynthesis inhibitors were present. Moreover, in Malus prunifolia, melatonin influences adventitious root (AR) growth by increasing IAA levels and inducing the expression of WUSCHEL-related Homeobox 11 (WOX11) in the AR formation zone. The expression of WOX11 is also regulated by the auxin signaling pathway, suggesting that WOX11 may serve as a key mediator in the melatonin-auxin interaction during root primordia development (Mao et al. 2020; Zhang et al. 2018).
Melatonin regulates the levels of various phytohormones beyond auxins in plant root systems. Duan et al. (2022) revealed that melatonin increases the levels of IAA, BR, and GA while reducing ABA content in G. hirsutum seedling roots, alleviating the growth inhibition caused by salt stress. Similarly, Ma et al. (2023) reported that melatonin enhances hormone-mediated root growth in H. vulgare roots under low phosphorus stress, showing that melatonin treatment increases IAA and GA levels while decreasing ABA, thereby influencing root length. Similarly, melatonin elevates IAA and GA levels and lowers ABA concentration in M. prunifolia roots, promoting AR formation (Mao et al. 2020). Additionally, Hu et al. (2020) demonstrated that melatonin stimulates Cucumis melo L. root growth under copper stress by reducing JA biosynthesis. In addition to auxins, BRs are key regulators of lateral and AR formation. BRs influence root length by controlling cell elongation and meristem size (Jaillais and Vert 2016). Plants with BR deficiencies or impaired BR signaling exhibit significantly shortened root phenotypes (Fig. 6). While BRs interact with auxins and other compounds during root growth, many of these interactions remain poorly understood (Altamura et al. 2023). Further investigation is required to unravel the complexities of BR involvement in root development and their interplay with other phytohormones.
Fig. 6.
Differences in barley root length: BR-deficient mutant BW091, brh3.g (left), wild-type barley cv. Bowman (middle) and BR-insensitive plant BW885, uzu1.a (right) (photo by M. Michałek)
Recent studies highlight that both melatonin and BRs regulate plant root growth by influencing the expression of cell cycle genes. Moreover, melatonin influences lateral root growth in S. lycopersicum by stimulating enzymes such as polyamine oxidase (PAO) and RBOH, leading to the production of ROS, including hydrogen peroxide and superoxide radicals. These ROS influence the expression of cell cycle genes such as cyclin-dependent kinase A1 (CDKA1) and cyclin D3 (CYCD3) (Chen et al. 2019). The study correlated melatonin-induced lateral root formation to the upregulation of PAO and RBOH genes in the lateral root emerging zone, suggesting these genes act downstream of melatonin. Tian et al. (2024) further validated these findings in tomato roots, demonstrating that melatonin modulates root architecture by interacting with endogenous BRs. Similarly, Wen et al. (2023) showed that 24-epibrassinolide (EBL) induces AR formation in C. annuum via the PAO- and RBOH-dependent production of ROS. Through gene family screening and expression analysis, a correlation was observed between EBL-induced AR formation and the upregulation of various PAO and RBOH genes in the roots. Silencing these genes reduced ROS accumulation and suppressed EBL-induced root formation. Furthermore, EBL treatment influenced the expression of cell cycle-related genes, such as CYCD3 and CDKA1, in a ROS-dependent manner. These findings suggest that ROS signals generated by both EBL and melatonin activate signaling pathways that upregulate the expression of cell cycle genes, prompting root formation and elongation.
Auxins and brassinosteroids likely act as key co-regulators of root growth alongside melatonin (Fig. 7). However, the interaction between melatonin and other hormones, such as GA, CK, and ABA, in the root system remains unexplored. Further research is needed to elucidate the molecular mechanisms underlying melatonin crosstalk with phytohormones and its role in regulating cell cycle genes and WOX11 expression during root development.
Fig. 7.
Regulation of root growth by melatonin through various target pathways (figure drafted on the base of Chen et al. 2019, Hwang and Back 2018, Mao et al. 2020, Tan et al. 2019, Wei et al. 2022, using BioRender tool at http://biorender.com)
Conclusions and future directions
As evidenced, melatonin holds significant potential as a master regulator of various aspects of plant functioning, including its role in mitigating the harmful effects of stress. Its interactions with phytohormones hold significant promise for enhancing plant resilience to environmental stressors, as these phytohormones regulate various physiological and developmental processes. A viable strategy to support sustainable crop production under drought conditions involves leveraging melatonin’s interactions with phytohormones such as auxins and BRs to stimulate root growth and enhance water and nutrient absorption from the soil. The identification of ligands involved in melatonin-auxin crosstalk, such as PIN5 and WOX11, in root development offers new opportunities to optimize crop root systems. Additionally, genetic studies have identified potential ligands in melatonin-BR interactions, including SNAT2, DWF4, Gα, CDKA, and CYCD3 genes. However, the regulatory role of melatonin in shaping root architecture remains controversial, and the molecular mechanisms of its crosstalk with phytohormones are still not fully understood. The recent discovery of the receptor PMTR1/Cand2 could enhance understanding of melatonin’s involvement in hormonal signaling pathways. Additional research on crop plants using exogenous melatonin, as well as melatonin-deficient and -insensitive mutants, is essential to unravel the complex regulatory network of melatonin in plants.
Despite the surge in melatonin research, numerous aspects of its catabolism, signaling, phytohormone crosstalk, and its role in plant stress tolerance remain unclear. Further research should prioritize several key areas to advance understanding of melatonin’s role in plants. First, the role of Cand2/PMTR1 in other crop species, particularly in cereals, warrants investigation and investigating its involvement in the activation of G-protein signaling and the MAPK cascade could provide valuable insight. Another important area is the function of major melatonin metabolites in crop plants, as this remains poorly understood. Research should also aim to determine whether enzymatic or non-enzymatic melatonin transformation is more prevalent in plants. Another promising avenue is the interaction between melatonin and nanoparticles, as well as non-coding RNAs, including microRNAs. Finally, identifying new target genes for melatonin and potential ligands involved in its interaction with phytohormones will be critical for gaining a deeper insight into the regulatory functions of melatonin in plant biology. Given that research on melatonin in cereals is still in its infancy, significant efforts are needed, with barley emerging as a promising model species for advancing our understanding in this crop group.
Abbreviations
- AAO
Abscisic aldehyde oxidase
- ABI5
Abscisic acid-insensitive 5
- ACO
1-Aminocyclopropane-1-carboxylate oxidase
- ACS
1-Aminocyclopropane-1-carboxylate synthase
- AMI1
Amidase 1
- AOC
Allene oxide cyclase
- ARFs
Auxin response factors
- ARR
A-type response regulator
- Aux/IAA
Auxin/indole-3-acetic acid related genes
- AUX1
Auxin resistant 1
- BA2H
Benzoic acid-2-hydroxylase
- BRI1
Brassinosteroid insensitive 1
- BRR
B-type response regulator
- BSK
Brassinosteroid-signaling kinase
- BZR1
Brassinazole resistant 1
- CYP707A1
Abscisic acid 8′-hydroxylase 1
- CYP707A2
Abscisic acid 8′-hydroxylase 2
- D11
Dwarf 11
- DWF4
Dwarf 4
- ERF
Ethylene-responsive transcription factor
- ETR
Ethylene receptor
- GA20ox
Gibberellin 20-oxidase
- GA2ox
Gibberellin 2-oxidase
- GA3ox
Gibberellin 3-oxidase
- GA1
Gibberellin A1
- GAI
Gibberellic-acid insensitive
- GH3
Gretchen hagen 3
- HK
Histidine kinase
- HP
Histidine phosphotransfer
- IPT
Isopentenyl transferase
- JAZ
Jasmonate zim domain 1
- LOX
Lipoxygenase
- LoxD
Lipoxygenase D
- NCED1
9-Cis-epoxycarotenoid dioxygenase 1
- LOG1
Lonely guy 1
- PAL
Phenylalanine ammonia lyase
- PI II
Proteinase inhibitor II
- PILs
Pin-like genes
- PINs
Pin-formed genes
- PP2C
Protein phosphatase type 2C
- PR1
Pathogenesis-related gene 1
- PYR/PYL/RCAR
Pyrabactin resistance/pyrabactin resistance 1-like/regulatory component of ABA receptor
- RAVL1
Related to abi3/vp1-like 1
- SAUR
Small auxin up-regulated RNA genes
- SnRK
Snf1-related kinase
- SQE
Squalene epoxidase
- STE1
∆7-Sterol-c5-desaturase
- TIR1/AFB
Transport inhibitor response 1/auxin signaling f-box protein
- XTR3
Xyloglucan endotransglycosylase related 3
- YUCCA
Flavin-dependent monooxygenase
- ZEP
Zeaxanthin epoxidase
Author contribution
MM, AK, and KM conceived and drafted the manuscript. PO and MK critically revised the paper. All authors approved the final manuscript.
Funding
This work was funded by the National Centre of Science in Poland, project title: “Melatonin as a pivotal mediator for shaping root architecture and drought adaptation via modulation of phytohormones crosstalk in barley (Hordeum vulgare L.),” grant number 2019/35/B/NZ9/00208, and by the Doctoral School of the Institute of Plant Genetics, Polish Academy of Sciences.
Declarations
Ethics approval
Not applicable.
Consent to participate
Not applicable.
Consent for publication
Not applicable.
Competing interests
The authors declare no competing interests.
Footnotes
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Contributor Information
Anetta Kuczyńska, Email: akuc@igr.poznan.pl.
Krzysztof Mikołajczak, Email: kmik@igr.poznan.pl.
References
- Ahammed GJ, Xu W, Liu A, Chen S (2019) Endogenous melatonin deficiency aggravates high temperature-induced oxidative stress in Solanum lycopersicum L. Environ Exp Bot 161:303–311. 10.1016/j.envexpbot.2018.06.006 [Google Scholar]
- Ali M, Pan Y, Liu H, Cheng Z (2023) Melatonin interaction with abscisic acid in the regulation of abiotic stress in Solanaceae family plants. Front Plant Sci 14:1271137. 10.3389/fpls.2023.1271137 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ali S, Gill RA, Ulhassan Z, Zhang N, Hussain S, Zhang K, Huang Q, Sagir M, Tahir MB, Gill MB, Mwamba TM, Ali B, Zhou W (2023) Exogenously applied melatonin enhanced the tolerance of Brassica napus against cobalt toxicity by modulating antioxidant defense, osmotic adjustment, and expression of stress response genes. Ecotoxicol Environ Saf 1(252):114624. 10.1016/j.ecoenv.2023.114624 [DOI] [PubMed] [Google Scholar]
- Altaf MA, Shahid R, Ren MX, Naz S, Altaf MM, Khan LU, Tiwari RK, Lal MK, Shahid MA, Kumar R, Nawaz MA, Jahan MS, Jan BL, Ahmad P (2022a) Melatonin improves drought stress tolerance of tomato by modulating plant growth, root architecture, photosynthesis, and antioxidant defense system. Antioxidants 11(2):309. 10.3390/antiox11020309 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Altaf MA, Shu H, Hao Y, Mumtaz MA, Lu X, Wang Z (2022b) Melatonin affects the photosynthetic performance of pepper (Capsicum annuum L.) seedlings under cold stress. Antioxidants 11(12):2414. 10.3390/antiox11122414 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Altamura MM, Piacentini D, Della Rovere F, Fattorini L, Falasca G, Betti C (2023) New paradigms in brassinosteroids, strigolactones, sphingolipids, and nitric oxide interaction in the control of lateral and adventitious root formation. Plants 12(2):413. 10.3390/plants12020413 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Arnao MB, Giraldo-Acosta M, Castejón-Castillejo A, Losada-Lorán M, Sánchez-Herrerías P, El Mihyaoui A, Cano A, Hernández-Ruiz J (2023) Melatonin from microorganisms, algae, and plants as possible alternatives to synthetic melatonin. Metabolites 13:72. 10.3390/metabo13010072 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Arnao MB, Hernández-Ruiz J (2017) Growth activity, rooting capacity, and tropism: three auxinic precepts fulfilled by melatonin. Acta Physiol Plant 39:127. 10.1007/s11738-017-2428-3 [Google Scholar]
- Arnao MB, Hernández-Ruiz J (2019) Melatonin: a new plant hormone and/or a plant master regulator? Trends Plant Sci 24(1):38–48. 10.1016/j.tplants.2018.10.010 [DOI] [PubMed] [Google Scholar]
- Arnao MB, Hernández-Ruiz J (2021) Melatonin as a regulatory hub of plant hormone levels and action in stress situations. Plant Biol 1:7–19. 10.1111/plb.13202 [DOI] [PubMed] [Google Scholar]
- Back K (2021) Melatonin metabolism, signaling and possible roles in plants. Plant J 105:376–391. 10.1111/tpj.14915 [DOI] [PubMed] [Google Scholar]
- Back K, Tan DX, Reiter RJ (2016) Melatonin biosynthesis in plants: multiple pathways catalyze tryptophan to melatonin in the cytoplasm or chloroplasts. J Pineal Res 61:426–437. 10.1111/jpi.12364 [DOI] [PubMed] [Google Scholar]
- Bai Y, Wei Y, Yin H, Hu W, Cheng X, Guo J, Dong Y, Zheng L, Xie H, Zeng H, Reiter RJ, Shi H (2022) PP2C1 fine-tunes melatonin biosynthesis and phytomelatonin receptor PMTR1 binding to melatonin in cassava. J Pineal Res 73(1):e12804. 10.1111/jpi.12804 [DOI] [PubMed] [Google Scholar]
- Barman D, Kumar MN, Dalal M, Khan FN, Yadav J, Nagar S, Kumar VVS, Singh MP, Sathee L, Krishnan SG, Chinnusamy V (2023) Identification of rice melatonin receptor OsPMTR and its comparative in silico analysis with arabidopsis AtCAND2 receptor. S Afr J Bot 162:813–829. 10.1016/j.sajb.2023.09.054 [Google Scholar]
- Bellmaine S, Schnellbaecher A, Zimmer A (2020) Reactivity and degradation products of tryptophan in solution and proteins. Free Radic Biol Med 160:696–718. 10.1016/j.freeradbiomed.2020.09.002 [DOI] [PubMed] [Google Scholar]
- Bhowal B, Bhattacharjee A, Goswami K, Sanan-Mishra N, Singla-Pareek S, Kaur C, Sopory S (2021) Serotonin and melatonin biosynthesis in plants: genome-wide identification of the genes and their expression reveal a conserved role in stress and development. Int J Mol Sci 22:11034. 10.3390/ijms222011034 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bisquert R, Planells-Cárcel A, Alonso-Del-Real J, Muñiz-Calvo S, Guillamón JM (2023) The role of the PAA1 gene on melatonin biosynthesis in Saccharomyces cerevisiae: a search of new arylalkylamine N-acetyltransferases. Microorganisms 11(5):1115. 10.3390/microorganisms11051115 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bocheva G, Slominski RM, Janjetovic Z, Kim TK, Böhm M, Steinbrink K, Reiter RJ, Kleszczyński K, Slominski AT (2022) Protective role of melatonin and its metabolites in skin aging. Int J Mol Sci 23(3):1238. 10.3390/ijms23031238 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bychkov IA, Kudryakova NV, Shugaev AG, Kuznetsov VV, Kusnetsov VV (2022) The melatonin receptor CAND2/PMTR1 is involved in the regulation of mitochondrial gene expression under photooxidative stress. Dokl Biochem Biophys 502(1):15–20. 10.1134/S1607672922010021 [DOI] [PubMed] [Google Scholar]
- Byeon Y, Choi GH, Lee HY, Back K (2015) Melatonin biosynthesis requires N-acetylserotonin methyltransferase activity of caffeic acid O-methyltransferase in rice. J Exp Bot 66(21):6917–6925. 10.1093/jxb/erv396 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Byeon Y, Lee HY, Back K (2016) Cloning and characterization of the serotonin N-acetyltransferase-2 gene (SNAT2) in rice (Oryza sativa). J Pineal Res 61(2):198–207. 10.1111/jpi.12339 [DOI] [PubMed] [Google Scholar]
- Byeon Y, Lee HY, Lee K, Park S, Back K (2014) Cellular localization and kinetics of the rice melatonin biosynthetic enzymes SNAT and ASMT. J Pineal Res 56:107–114. 10.1111/jpi.12103 [DOI] [PubMed] [Google Scholar]
- Byeon Y, Lee K, Park YI, Park S, Back K (2013) Molecular cloning and functional analysis of serotonin N-acetyltransferase from the cyanobacterium Synechocystis sp. PCC 6803. J Pineal Res 55(4):371–376. 10.1111/jpi.12080 [DOI] [PubMed] [Google Scholar]
- Byeon Y, Tan DX, Reiter RJ, Back K (2015) Predominance of 2-hydroxymelatonin over melatonin in plants. J Pineal Res 59:448–454. 10.1111/jpi.12274 [DOI] [PubMed] [Google Scholar]
- Cecon E, Oishi A, Jockers R (2018) Melatonin receptors: molecular pharmacology and signalling in the context of system bias. Br J Pharmacol 175(16):3263–3280. 10.1111/bph.13950 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chang J, Guo Y, Yan J et al (2021) The role of watermelon caffeic acid O-methyltransferase (ClCOMT1) in melatonin biosynthesis and abiotic stress tolerance. Hortic Res 8:210. 10.1038/s41438-021-00645-5 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chen H, Bullock DA Jr, Alonso JM, Stepanova AN (2021) To fight or to grow: the balancing role of ethylene in plant abiotic stress responses. Plants 11(1):33. 10.3390/plants11010033 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chen J, Li H, Yang K, Wang Y, Yang L, Hu L, Liu R, Shi Z (2019) Melatonin facilitates lateral root development by coordinating PAO-derived hydrogen peroxide and Rboh-derived superoxide radical. Free Radic Biol Med 143:534–544. 10.1016/j.freeradbiomed.2019.09.011 [DOI] [PubMed] [Google Scholar]
- Chen M, Cecon E, Karamitri A, Gao W, Gerbier R, Ahmad R, Jockers R (2020) Melatonin MT1 and MT2 receptor ERK signaling is differentially dependent on Gi/o and Gq/11 proteins. J Pineal Res 68(4):e12641. 10.1111/jpi.12641 [DOI] [PubMed] [Google Scholar]
- Choi GH, Lee HY, Back K (2017) Chloroplast overexpression of rice caffeic acid O-methyltransferase increases melatonin production in chloroplasts via the 5-methoxytryptamine pathway in transgenic rice plants. J Pineal Res 63(1). 10.1111/jpi.12412 [DOI] [PubMed]
- Duan W, Lu B, Liu L, Meng Y, Ma X, Li J, Zhang K, Sun H, Zhang Y, Dong H, Bai Z, Li C (2022) Effects of exogenous melatonin on root physiology, transcriptome and metabolome of cotton seedlings under salt stress. Int J Mol Sci 23(16):9456. 10.3390/ijms23169456 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dzinyela R, Hwarari D, Opoku KN, Yang L, Movahedi A (2024) Enhancing drought stress tolerance in horticultural plants through melatonin-mediated phytohormonal crosstalk. Plant Cell Rep 43(11):272. 10.1007/s00299-024-03362-0 [DOI] [PubMed] [Google Scholar]
- Erland LAE (2024) Views and perspectives on the indoleamines serotonin and melatonin in plants: past, present and future. Plant Signal Behav 19(1):2366545. 10.1080/15592324.2024.2366545 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Esmaeili S, Sharifi M, Ghanati F, Soltani BM, Samari E, Sagharyan M (2023) Exogenous melatonin induces phenolic compounds production in Linum album cells by altering nitric oxide and salicylic acid. Sci Rep 13(1):4158. 10.1038/s41598-023-30954-9 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ferreyra MLF, Serra P, Casati P (2021) Recent advances on the roles of flavonoids as plant protective molecules after UV and high light exposure. Physiol Plant 173(3):736–749. 10.1111/ppl.13543 [DOI] [PubMed] [Google Scholar]
- Fischer TW, Sweatman TW, Semak I, Sayre RM, Wortsman J, Slominski A (2006) Constitutive and UV-induced metabolism of melatonin in keratinocytes and cell-free systems. FASEB J 20(9):1564–1566. 10.1096/fj.05-5227fje [DOI] [PubMed] [Google Scholar]
- Gao Y, Chen H, Chen D, Hao G (2023) Genetic and evolutionary dissection of melatonin response signaling facilitates the regulation of plant growth and stress responses. J Pineal Res 74(2):e12850. 10.1111/jpi.12850 [DOI] [PubMed] [Google Scholar]
- Gao Y, Zhao S, Zhang Y, Zhang Q (2022) Melatonin receptors: a key mediator in animal reproduction. Vet Sci 9:309. 10.3390/vetsci9070309 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gong B, Yan Y, Wen D, Shi Q (2017) Hydrogen peroxide produced by NADPH oxidase: a novel downstream signaling pathway in melatonin-induced stress tolerance in Solanum lycopersicum. Physiol Plant 160(4):396–409. 10.1111/ppl.12581 [DOI] [PubMed] [Google Scholar]
- Gu Q, Xiao Q, Chen Z, Han Y (2022) Crosstalk between melatonin and reactive oxygen species in plant abiotic stress responses: an update. Int J Mol Sci 23:5666. 10.3390/ijms23105666 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gu X, Xue L, Lu L, Xiao J, Song G, Xie M, Zhang H (2021) Melatonin enhances the waterlogging tolerance of Prunus persica by modulating antioxidant metabolism and anaerobic respiration. J Plant Growth Regul 40:2178–2190. 10.1007/s00344-020-10263-5 [Google Scholar]
- Guo W, Zhang C, Yang R, Zhao S, Han X, Wang Z, Li S, Gao H (2023) Endogenous salicylic acid mediates melatonin-induced chilling-and oxidative-stress tolerance in harvested kiwifruit. Postharvest Biol Technol 201:112341. 10.1016/j.postharvbio.2023.112341 [Google Scholar]
- Hardeland R (2009) Melatonin: signaling mechanisms of a pleiotropic agent. BioFactors 35(2):183–192. 10.1002/biof.23 [DOI] [PubMed] [Google Scholar]
- Hardeland R (2016) Melatonin in plants – diversity of levels and multiplicity of functions. Front Plant Sci 7:198. 10.3389/fpls.2016.00198 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hardeland R (2017) Taxon- and site-specific melatonin catabolism. Molecules 22:2015. 10.3390/molecules22112015 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hong Y, Zhang Y, Sinumporn S, Yu N, Zhan X, Shen X, Chen D, Yu P, Wu W, Liu Q, Cao Z, Zhao C, Cheng S, Cao L (2018) Premature leaf senescence 3, encoding a methyltransferase, is required for melatonin biosynthesis in rice. Plant J 14. 10.1111/tpj.13995 [DOI] [PubMed]
- Hu W, Yang H, Tie W, Yan Y, Ding Z, Liu Y, Wu C, Wang J, Reiter RJ, Tan DX, Shi H, Xu B, Jin Z (2017) Natural variation in banana varieties highlights the role of melatonin in postharvest ripening and quality. J Agric Food Chem 65(46):9987–9994. 10.1021/acs.jafc.7b03354 [DOI] [PubMed] [Google Scholar]
- Hu Z, Fu Q, Zheng J, Zhang A, Wang H (2020) Transcriptomic and metabolomic analyses reveal that melatonin promotes melon root development under copper stress by inhibiting jasmonic acid biosynthesis. Hortic Res. 7(1):79. 10.1038/s41438-020-0293-5 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Huang E, Tang J, Song S, Yan H, Yu X, Luo C, Chen Y, Ji H, Chen A, Zhou J, Liao H (2024) Caffeic acid O-methyltransferase from Ligusticum chuanxiong alleviates drought stress, and improves lignin and melatonin biosynthesis. Front Plant Sci 15:1458296. 10.3389/fpls.2024.1458296 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Huangfu L, Chen R, Lu Y, Zhang E, Miao J, Zuo Z, Zhao Y, Zhu M, Zhang Z, Li P, Xu Y, Yao Y, Liang G, Xu C, Zhou Y, Yang Z (2022) OsCOMT, encoding a caffeic acid O-methyltransferase in melatonin biosynthesis, increases rice grain yield through dual regulation of leaf senescence and vascular development. Plant Biotechnol J 20(6):1122–1139. 10.1111/pbi.13794 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hwang OJ, Back K (2018) Melatonin is involved in skotomorphogenesis by regulating brassinosteroid biosynthesis in rice plants. J Pineal Res 65(2):e12495. 10.1111/jpi.12495 [DOI] [PubMed] [Google Scholar]
- Hwang OJ, Back K (2022) Molecular regulation of antioxidant melatonin biosynthesis by brassinosteroid acting as an endogenous elicitor of melatonin induction in rice seedlings. Antioxidants 11(5):918. 10.3390/antiox11050918 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jahan MS, Guo S, Baloch AR, Sun J, Shu S, Wang Y, Ahammed GJ, Kabir K, Roy R (2020) Melatonin alleviates nickel phytotoxicity by improving photosynthesis, secondary metabolism and oxidative stress tolerance in tomato seedlings. Ecotoxicol Environ Saf 197:110593. 10.1016/j.ecoenv.2020.110593 [DOI] [PubMed] [Google Scholar]
- Jahan MS, Shu S, Wang Y, Hasan MM, El-Yazied AA, Alabdallah NM, Hajjar D, Altaf MA, Sun J, Guo S (2021) Melatonin pretreatment confers heat tolerance and repression of heat-induced senescence in tomato through the modulation of ABA- and GA-mediated pathways. Front Plant Sci 12:650955. 10.3389/fpls.2021.650955 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jaillais Y, Vert G (2016) Brassinosteroid signaling and BRI1 dynamics went underground. Curr Opin Plant Biol 33:92–100. 10.1016/j.pbi.2016.06.014 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Janjetovic Z, Nahmias ZP, Hanna S, Jarrett SG, Kim TK, Reiter RJ, Slominski AT (2014) Melatonin and its metabolites ameliorate ultraviolet B-induced damage in human epidermal keratinocytes. J Pineal Res 57(1):90–102. 10.1111/jpi.12146 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Janjetovic Z, Jarrett SG, Lee EF, Duprey C, Reiter RJ, Slominski AT (2017) Melatonin and its metabolites protect human melanocytes against UVB-induced damage: involvement of NRF2-mediated pathways. Sci Rep 7(1):1274. 10.1038/s41598-017-01305-2 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jiang H, Galtes D, Wang J, Rockman HA (2022) G protein-coupled receptor signaling: transducers and effectors. Am J Physiol Cell Physiol 323(3):C731–C748. 10.1152/ajpcell.00210.2022 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jones JC, Duffy JW, Machius M, Temple BR, Dohlman HG, Jones AM (2011) The crystal structure of a self-activating G protein alpha subunit reveals its distinct mechanism of signal initiation. Sci Signal 4(159):ra8. 10.1126/scisignal.2001446 [DOI] [PMC free article] [PubMed]
- Karlova R, Boer D, Hayes S, Testerink C (2021) Root plasticity under abiotic stress. Plant Physiol 187(3):1057–1070. 10.1093/plphys/kiab392 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Khan M, Ali S, Manghwar H, Saqib S, Ullah F, Ayaz A, Zaman W (2022) Melatonin function and crosstalk with other phytohormones under normal and stressful conditions. Genes 13:1699. 10.3390/genes13101699 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Khan D, Cai N, Zhu W, Li L, Guan M, Pu X, Chen Q (2023) The role of phytomelatonin receptor 1-mediated signaling in plant growth and stress response. Front Plant Sci 14:1142753. 10.3389/fpls.2023.1142753 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Khan MSS, Ahmed S, Ikram AU, Hannan F, Yasin MU, Wang J, Zhao B, Islam F, Chen J (2023) Phytomelatonin: A key regulator of redox and phytohormones signaling against biotic/abiotic stresses. Redox Biol 64:102805. 10.1016/j.redox.2023.102805 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kim TK, Slominski RM, Pyza E, Kleszczynski K, Tuckey RC, Reiter RJ, Holick MF, Slominski AT (2024) Evolutionary formation of melatonin and vitamin D in early life forms: insects take centre stage. Biol Rev Camb Philos Soc 99(5):1772–1790. 10.1111/brv.13091 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Konger RL, Derr-Yellin E, Zimmers TA, Katona T, Xuei X, Liu Y, Zhou HM, Simpson ER, Turner MJ (2021) Epidermal PPAR is a key homeostatic regulator of cutaneous inflammation and barrier function in mouse skin. Int J Mol Sci 22:8634. 10.3390/ijms22168634 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Korkmaz A, Sözeri E, Köklü AŞ, Havan A (2023) 2-hydroxymelatonin (2-OHM), a major melatonin metabolite, confers multiple stress tolerance in pepper at seed germination stage. South Afr J Bot 162:830–837. 10.1016/j.sajb.2023.09.056 [Google Scholar]
- Lee HY, Back K (2016) Mitogen-activated protein kinase pathways are required for melatonin-mediated defense responses in plants. J Pineal Res 60(3):327–335. 10.1111/jpi.12314 [DOI] [PubMed] [Google Scholar]
- Lee HY, Back K (2022) The antioxidant cyclic 3-hydroxymelatonin promotes the growth and flowering of Arabidopsis thaliana. Antioxidants 11(6):1157. 10.3390/antiox11061157 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lee HY, Byeon Y, Lee K, Lee HJ, Back K (2014) Cloning of Arabidopsis serotonin N-acetyltransferase and its role with caffeic acid O-methyltransferase in the biosynthesis of melatonin in vitro despite their different subcellular localizations. J Pineal Res 57(4):418–426. 10.1111/jpi.12181 [DOI] [PubMed] [Google Scholar]
- Lee K, Back K (2019) Melatonin-deficient rice plants show a common semidwarf phenotype either dependent or independent of brassinosteroid biosynthesis. J Pineal Res 66(2):e12537. 10.1111/jpi.12537 [DOI] [PubMed] [Google Scholar]
- Lee K, Zawadzka A, Czarnocki Z, Reiter RJ, Back K (2016) Molecular cloning of melatonin 3-hydroxylase and its production of cyclic 3-hydroxymelatonin in rice (Oryza sativa). J Pineal Res 61(4):470–478. 10.1111/jpi.12361 [DOI] [PubMed] [Google Scholar]
- Li D, Wei J, Peng Z, Ma W, Yang Q, Song Z, Sun W, Yang W, Yuan L, Xu X, Chang W, Rengel Z, Shen J, Reiter RJ, Cui X, Yu D, Chen Q (2020) Daily rhythms of phytomelatonin signaling modulate diurnal stomatal closure via regulating reactive oxygen species dynamics in Arabidopsis. J Pineal Res 68(3):e12640. 10.1111/jpi.12640 [DOI] [PubMed] [Google Scholar]
- Li H, Guo Y, Lan Z, Xu K, Chang J, Ahammed GJ, Ma J, Wei C, Zhang X (2021) Methyl jasmonate mediates melatonin-induced cold tolerance of grafted watermelon plants. Hortic Res 8(1):57. 10.1038/s41438-021-00496-0 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Li R, Jiang M, Song Y, Zhang H (2021) Melatonin alleviates low-temperature stress via abi5-mediated signals during seed germination in rice (Oryza sativa L.). Front Plant Sci 12:727596. 10.3389/fpls.2021.727596 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Liang C, Li A, Yu H, Li W, Liang C, Guo S, Zhang R, Chu C (2017) Melatonin regulates root architecture by modulating auxin response in rice. Front Plant Sci 8:134. 10.3389/fpls.2017.00134 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Liang D, Shen Y, Ni Z, Wang Q, Lei Z, Xu N, Deng Q, Lin L, Wang J, Lv X, Xia H (2018) Exogenous melatonin application delays senescence of kiwifruit leaves by regulating the antioxidant capacity and biosynthesis of flavonoids. Front Plant Sci 9:426. 10.3389/fpls.2018.00426 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Liu C, Chen L, Zhao R, Li R, Zhang S, Yu W, Sheng J, Shen L (2019) Melatonin induces disease resistance to Botrytis cinerea in tomato fruit by activating jasmonic acid signaling pathway. J Agric Food Chem 67(22):6116–6124. 10.1021/acs.jafc.9b00058 [DOI] [PubMed] [Google Scholar]
- Liu C, Kang H, Wang Y, Yao Y, Gao Z, Du Y (2021) Melatonin relieves ozone stress in grape leaves by inhibiting ethylene biosynthesis. Front Plant Sci 12:702874. 10.3389/fpls.2021.702874 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Liu G, Hu Q, Zhang X, Jiang J, Zhang Y, Zhang Z (2022) Melatonin biosynthesis and signal transduction in plants in response to environmental conditions. J Exp Bot 73(17):5818–5827. 10.1093/jxb/erac196 [DOI] [PubMed] [Google Scholar]
- Liu Y, Wang X, Dong D, Guo L, Dong X, Leng J, Zhao B, Guo YD, Zhang N (2021) Research advances in heterotrimeric G-Protein subunits and uncanonical G-Protein coupled receptors in plants. Int J Mol Sci 22:8678. 10.3390/ijms22168678 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Liu Y, Wang X, Lv H, Cao M, Li Y, Yuan X, Zhang X, Guo YD, Zhang N (2022) Anabolism and signaling pathways of phytomelatonin. J Exp Bot 73(17):5801–5817. 10.1093/jxb/erac158 [DOI] [PubMed] [Google Scholar]
- Luo M, Wang D, Delaplace P, Pan Y, Zhou Y, Tang W, Chen K, Chen J, Xu Z, Ma Y, Chen M (2023) Melatonin enhances drought tolerance by affecting jasmonic acid and lignin biosynthesis in wheat (Triticum aestivum L.). Plant Physiol Biochem 202:107974. 10.1016/j.plaphy.2023.107974 [DOI] [PubMed] [Google Scholar]
- Ma Y, Jiao J, Fan X, Sun H, Zhang Y, Jiang J, Liu C (2017) Endophytic bacterium Pseudomonas fluorescens RG11 may transform tryptophan to melatonin and promote endogenous melatonin levels in the roots of four grape cultivars. Front Plant Sci 7:2068. 10.3389/fpls.2016.02068 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ma X, Zhang J, Burgess P, Rossi S, Huang B (2018) Interactive effects of melatonin and cytokinin on alleviating drought-induced leaf senescence in creeping bentgrass (Agrostis stolonifera). Environ Exp Bot 145:1–11. 10.1016/j.envexpbot.2017.10.010 [Google Scholar]
- Ma Z, Yang K, Wang J, Ma J, Yao L, Si E, Li B, Ma X, Shang X, Meng Y, Wang H (2023) Exogenous melatonin enhances the low phosphorus tolerance of barley roots of different genotypes. Cells. 12(10):1397. 10.3390/cells12101397 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mannino G, Pernici C, Serio G, Gentile C, Bertea CM (2021) Melatonin and phytomelatonin: chemistry, biosynthesis, metabolism, distribution and bioactivity in plants and animals - an overview. Int J Mol Sci 22:9996. 10.3390/ijms22189996 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mao J, Niu C, Li K, Chen S, Tahir MM, Han M, Zhang D (2020) Melatonin promotes adventitious root formation in apple by promoting the function of MdWOX11. BMC Plant Biol. 20(1):536. 10.1186/s12870-020-02747-z [DOI] [PMC free article] [PubMed] [Google Scholar]
- Maruta N, Trusov Y, Jones AM, Botella JR (2021) Heterotrimeric G Proteins in plants: canonical and atypical G subunits. Int J Mol Sci 22:11841. 10.3390/ijms222111841 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Muhammad I, Shalmani A, Ali M, Yang QH, Ahmad H, Li FB (2021) Mechanisms regulating the dynamics of photosynthesis under abiotic stresses. Front Plant Sci 11:615942. 10.3389/fpls.2020.615942 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Munir R, Yasin MU, Afzal M, Jan M, Muhammad S, Jan N, Nana C, Munir F, Iqbal H, Tawab F, Gan Y (2024) Melatonin alleviated cadmium accumulation and toxicity by modulating phytohormonal balance and antioxidant metabolism in rice. Chemosphere 346:140590. 10.1016/j.chemosphere.2023.140590 [DOI] [PubMed] [Google Scholar]
- Muñiz-Calvo S, Bisquert R, Fernández-Cruz E, García-Parrilla MC, Guillamón JM (2019) Deciphering the melatonin metabolism in Saccharomyces cerevisiae by the bioconversion of related metabolites. J Pineal Res 66(3):e12554. 10.1111/jpi.12554 [DOI] [PubMed] [Google Scholar]
- Murch SJ, Campbell SSB, Saxena PK (2001) The role of serotonin and melatonin in plant morphogenesis: regulation of auxin-induced root organogenesis in in vitro-cultured explants of st. John’s Wort (Hypericum perforatum L.). In Vitro Cell Dev Biol-Plant 37:786–793. 10.1007/s11627-001-0130-y [Google Scholar]
- Nikolaev G, Robeva R, Konakchieva R (2022) Membrane melatonin receptors activated cell signaling in physiology and disease. Int J Mol Sci 23:471. 10.3390/ijms23010471 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nziengui H, Ditengou FA (2023) Editorial: in tune with their environment: how plant roots cope with environmental signals. Front Plant Sci 14:1234996. 10.3389/fpls.2023.1234996 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Okazaki M, Higuchi K, Aouini A, Ezura H (2010) Lowering intercellular melatonin levels by transgenic analysis of indoleamine 2,3-dioxygenase from rice in tomato plants. J Pineal Res 49(3):239–247. 10.1111/j.1600-079X.2010.00788.x [DOI] [PubMed] [Google Scholar]
- Ozturk M, Turkyilmaz Unal B, García-Caparrós P, Khursheed A, Gul A, Hasanuzzaman M (2021) Osmoregulation and its actions during the drought stress in plants. Physiol Plant 172(2):1321–1335. 10.1111/ppl.13297 [DOI] [PubMed] [Google Scholar]
- Pan Y, Xu X, Li L, Sun Q, Wang Q, Huang H, Tong Z, Zhang J (2023) Melatonin-mediated development and abiotic stress tolerance in plants. Front Plant Sci 14:1100827. 10.3389/fpls.2023.1100827 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Park M, Kang K, Park S, Back K (2008) Conversion of 5-hydroxytryptophan into serotonin by tryptophan decarboxylase in plants, Escherichia coli, and yeast. Biosci Biotechnol Biochem 72(9):2456–2458. 10.1271/bbb.80220 [DOI] [PubMed] [Google Scholar]
- Park S, Lee K, Kim YS, Back K (2012) Tryptamine 5-hydroxylase-deficient Sekiguchi rice induces synthesis of 5-hydroxytryptophan and N-acetyltryptamine but decreases melatonin biosynthesis during senescence process of detached leaves. J Pineal Res 52:211–216. 10.1111/j.1600-079X.2011.00930.x [DOI] [PubMed] [Google Scholar]
- Park WJ (2024) Have all of the phytohormonal properties of melatonin been verified? Int J Mol Sci 25:3550. 10.3390/ijms25063550 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pérez-González A, Galano A, Alvarez-Idaboy JR, Tan DX, Reiter RJ (2017) Radical-trapping and preventive antioxidant effects of 2-hydroxymelatonin and 4-hydroxymelatonin: contributions to the melatonin protection against oxidative stress. Biochim Biophys Acta Gen Subj 9:2206–2217. 10.1016/j.bbagen.2017.06.016 [DOI] [PubMed] [Google Scholar]
- Pham TH, Tian X, Zhao H, Li T, Lu L (2024) Genome-wide characterization of COMT family and regulatory role of CsCOMT19 in melatonin synthesis in Camellia sinensis. BMC Plant Biol 24(1):51. 10.1186/s12870-023-04702-0 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pospíšil P, Prasad A, Rác M (2019) Mechanism of the formation of electronically excited species by oxidative metabolic processes: role of reactive oxygen species. Biomolecules 9(7):258. 10.3390/biom9070258 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Prakash V, Singh VP, Tripathi DK, Sharma S, Corpas FJ (2021) Nitric oxide (NO) and salicylic acid (SA): a framework for their relationship in plant development under abiotic stress. Plant Biol 1:39–49. 10.1111/plb.13246 [DOI] [PubMed] [Google Scholar]
- Que Z, Ma T, Shang Y, Ge Q, Zhang Q, Xu P, Zhang J, Francoise U, Liu X, Sun X (2020) Microorganisms: producers of melatonin in fermented foods and beverages. J Agric Food Chem 68(17):4799–4811. 10.1021/acs.jafc.0c01082 [DOI] [PubMed] [Google Scholar]
- Reina M, Martínez A (2018) A new free radical scavenging cascade involving melatonin and three of its metabolites (3OHM, AFMK and AMK). Comput Theor Chem 1123:111–118. 10.1016/j.comptc.2017.11.017 [Google Scholar]
- Ren S, Rutto L, Katuuramu D (2019) Melatonin acts synergistically with auxin to promote lateral root development through fine tuning auxin transport in Arabidopsis thaliana. PLoS One 14(8):e0221687. 10.1371/journal.pone.0221687 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rothhammer V, Quintana FJ (2019) The aryl hydrocarbon receptor: an environmental sensor integrating immune responses in health and disease. Nat Rev Immunol 19(3):184–197. 10.1038/s41577-019-0125-8 [DOI] [PubMed] [Google Scholar]
- Samanta S, Singh A, Banerjee A, Roychoudhury A (2020) Exogenous supplementation of melatonin alters representative organic acids and enzymes of respiratory cycle as well as sugar metabolism during arsenic stress in two contrasting indica rice cultivars. J Biotechnol 324:220–232. 10.1016/j.jbiotec.2020.10.013 [DOI] [PubMed] [Google Scholar]
- Santoro R, Mori F, Marani M, Grasso G, Cambria MA, Blandino G, Muti P, Strano S (2013) Blockage of melatonin receptors impairs p53-mediated prevention of DNA damage accumulation. Carcinogenesis 34(5):1051–1061. 10.1093/carcin/bgt025 [DOI] [PubMed] [Google Scholar]
- Sarti P, Magnifico MC, Altieri F, Mastronicola D, Arese M (2013) New evidence for cross talk between melatonin and mitochondria mediated by a circadian-compatible interaction with nitric oxide. Int J Mol Sci 14(6):11259–11276. 10.3390/ijms140611259 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sehar Z, Fatma M, Khan S, Mir IR, Abdi G, Khan NA (2023) Melatonin influences methyl jasmonate-induced protection of photosynthetic activity in wheat plants against heat stress by regulating ethylene-synthesis genes and antioxidant metabolism. Sci Rep 13(1):7468. 10.1038/s41598-023-34682-y [DOI] [PMC free article] [PubMed] [Google Scholar]
- Shah AA, Ahmed S, Yasin NA (2019) 2-Hydroxymelatonin induced nutritional orchestration in Cucumis sativus under cadmium toxicity: modulation of non-enzymatic antioxidants and gene expression. Int J Phytoremediation 22(5):497–507. 10.1080/15226514.2019.1683715 [DOI] [PubMed] [Google Scholar]
- Sharma A, Wang J, Xu D, Tao S, Chong S, Yan D, Li Z, Yuan H, Zheng B (2020) Melatonin regulates the functional components of photosynthesis, antioxidant system, gene expression, and metabolic pathways to induce drought resistance in grafted Carya cathayensis plants. Sci Total Environ 713:136675. 10.1016/j.scitotenv.2020.136675 [DOI] [PubMed] [Google Scholar]
- Slominski AT, Kim TK, Slominski RM, Song Y, Qayyum S, Placha W, Janjetovic Z, Kleszczyński K, Atigadda V, Song Y, Raman C, Elferink CJ, Hobrath JV, Jetten AM, Reiter RJ (2023) Melatonin and its metabolites can serve as agonists on the aryl hydrocarbon receptor and peroxisome proliferator-activated receptor gamma. Int J Mol Sci 24(20):15496. 10.3390/ijms242015496 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Slominski AT, Semak I, Fischer TW, Kim TK, Kleszczyński K, Hardeland R, Reiter RJ (2017) Metabolism of melatonin in the skin: why is it important? Exp Dermatol 26(7):563–568. 10.1111/exd.13208 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Slominski AT, Zmijewski MA, Skobowiat C, Zbytek B, Slominski RM, Steketee JD (2012) Sensing the environment: regulation of local and global homeostasis by the skin’s neuroendocrine system. Adv Anat Embryol Cell Biol 212: vii:1–115. 10.1007/978-3-642-19683-6_1 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Slominski AT, Zmijewski MA, Semak I, Kim TK, Janjetovic Z, Slominski RM, Zmijewski JW (2017) Melatonin, mitochondria, and the skin. Cell Mol Life Sci 74(21):3913–3925. 10.1007/s00018-017-2617-7 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Slominski AT, Zmijewski MA, Plonka PM, Szaflarski JP, Paus R (2018) How UV light touches the brain and endocrine system through skin, and why. Endocrinology 159(5):1992–2007. 10.1210/en.2017-03230 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sun C, Gao L, Xu L, Zheng Q, Sun S, Liu X, Zhang Z, Tian Z, Dai T, Sun J (2023) Melatonin alleviates chromium toxicity by altering chromium subcellular distribution and enhancing antioxidant metabolism in wheat seedlings. Environ Sci Pollut Res Int 30(17):50743–50758. 10.1007/s11356-023-25903-y [DOI] [PubMed] [Google Scholar]
- Sun C, Liu L, Wang L, Li B, Jin C, Lin X (2021) Melatonin: a master regulator of plant development and stress responses. J Integr Plant Biol 63:126–145. 10.1111/jipb.12993 [DOI] [PubMed] [Google Scholar]
- Sun Q, Liu L, Zhang L, Lv H, He Q, Guo L, Zhang X, He H, Ren S, Zhang N, Zhao B, Guo YD (2020) Melatonin promotes carotenoid biosynthesis in an ethylene-dependent manner in tomato fruits. Plant Sci 298:110580. 10.1016/j.plantsci.2020.110580 [DOI] [PubMed] [Google Scholar]
- Sun S, Liu A, Li Z, Guo T, Chen S, Ahammed GJ (2023) Anthocyanin synthesis is critical for melatonin-induced chromium stress tolerance in tomato. J Hazard Mater 453:131456. 10.1016/j.jhazmat.2023.131456 [DOI] [PubMed] [Google Scholar]
- Sun S, Wen D, Yang W, Meng Q, Shi Q, Gong B (2020) Overexpression of caffeic acid O-methyltransferase 1 (COMT1) increases melatonin level and salt stress tolerance in tomato plant. J Plant Growth Regul 39:1221–1235. 10.1007/s00344-019-10058-3 [Google Scholar]
- Szafrańska K, Reiter RJ, Posmyk MM (2017) Melatonin improves the photosynthetic apparatus in pea leaves stressed by paraquat via chlorophyll breakdown regulation and its accelerated de novo synthesis. Front Plant Sci 29(8):878. 10.3389/fpls.2017.00878 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tan DX, Hardeland R, Back K, Manchester LC, Aatorre-Jimenez MA, Reiter RJ (2016) On the significance of an alternate pathway of melatonin synthesis via 5-methoxytryptamine: comparisons across species. J Pineal Res 61:27–40. 10.1111/jpi.12336 [DOI] [PubMed] [Google Scholar]
- Tan DX, Hardeland R, Manchester LC, Galano A, Reiter RJ (2014) Cyclic-3-hydroxymelatonin (C3HOM), a potent antioxidant, scavenges free radicals and suppresses oxidative reactions. Curr Med Chem 21(13):1557–1565. 10.2174/0929867321666131129113146 [DOI] [PubMed] [Google Scholar]
- Tan DX, Manchester LC, Di Mascio P, Martinez GR, Prado FM, Reiter RJ (2007) Novel rhythms of N1-acetyl-N2-formyl-5-methoxykynuramine and its precursor melatonin in water hyacinth: importance for phytoremediation. FASEB J 21(8):1724–1729. 10.1096/fj.06-7745com [DOI] [PubMed] [Google Scholar]
- Tan DX, Manchester LC, Esteban-Zubero E, Zhou Z, Reiter RJ (2015) Melatonin as a potent and inducible endogenous antioxidant: synthesis and metabolism. Molecules 20(10):18886–21906. 10.3390/molecules201018886 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tan DX, Manchester LC, Qin L, Reiter RJ (2016) Melatonin: a mitochondrial targeting molecule involving mitochondrial protection and dynamics. Int J Mol Sci 17(12):2124. 10.3390/ijms17122124 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tan DX, Reiter RJ (2020) An evolutionary view of melatonin synthesis and metabolism related to its biological functions in plants. J Exp Bot 71(16):4677–4689. 10.1093/jxb/eraa235 [DOI] [PubMed] [Google Scholar]
- Tan X, Long W, Zeng L, Ding X, Cheng Y, Zhang X, Zou X (2019) Melatonin-induced transcriptome variation of rapeseed seedlings under salt stress. Int J Mol Sci 20(21):5355. 10.3390/ijms20215355 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tian Q, Wang G, Dou J, Niu Y, Li R, An W, Tang Z, Yu J (2024) Melatonin modulates tomato root morphology by regulating key genes and endogenous hormones. Plants 13(3):383. 10.3390/plants13030383 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tiwari RK, Kumar R, Lal MK, Kumar A, Altaf MA, Devi R, Naz S, Altaf M, Dey A, Aftab T (2023) Melatonin-polyamine interplay in the regulation of stress responses in plants. J Plant Growth Regul 42:4834–4850. 10.1007/s00344-022-10717-y [Google Scholar]
- Tiwari RK, Lal MK, Kumar R, Chourasia KN, Naga KC, Kumar D, Das SK, Zinta G (2021) Mechanistic insights on melatonin-mediated drought stress mitigation in plants. Physiol Plant 172(2):1212–1226. 10.1111/ppl.13307 [DOI] [PubMed] [Google Scholar]
- Turk H, Genisel M (2020) Melatonin-related mitochondrial respiration responses are associated with growth promotion and cold tolerance in plants. Cryobiology 92:76–85. 10.1016/j.cryobiol.2019.11.006 [DOI] [PubMed] [Google Scholar]
- Verde A, Míguez JM, Gallardo M (2023) Melatonin stimulates postharvest ripening of apples by up-regulating gene expression of ethylene synthesis enzymes. Postharvest Biol Technol 195:112133. 10.1016/j.postharvbio.2022.112133 [Google Scholar]
- Wang J, Song L, Gong X, Xu J, Li M (2020) Functions of jasmonic acid in plant regulation and response to abiotic stress. Int J Mol Sci 21(4):1446. 10.3390/ijms21041446 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wang L, Feng C, Zheng X, Guo Y, Zhou F, Shan D, Liu X, Kong J (2017) Plant mitochondria synthesize melatonin and enhance the tolerance of plants to drought stress. J Pineal Res 63:e12429. 10.1111/jpi.12429 [DOI] [PubMed] [Google Scholar]
- Wang LF, Li TT, Zhang Y, Guo JX, Lu KK, Liu WC (2021) CAND2/PMTR1 is required for melatonin-conferred osmotic stress tolerance in Arabidopsis. Int J Mol Sci 22(8):4014. 10.3390/ijms22084014 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wang LF, Lu KK, Li TT, Zhang Y, Guo JX, Song RF, Liu WC (2021) Maize PHYTOMELATONIN RECEPTOR1 functions in plant tolerance to osmotic and drought stress. J Exp Bot 73(17):5961–5973. 10.1093/jxb/erab553 [DOI] [PubMed] [Google Scholar]
- Wang P, Yin L, Liang D, Li C, Ma F, Yue Z (2012) Delayed senescence of apple leaves by exogenous melatonin treatment: toward regulating the ascorbate–glutathione cycle. J Pineal Res 53:11–20. 10.1111/j.1600-079X.2011.00966.x [DOI] [PubMed] [Google Scholar]
- Wang W, Su S, Wang S, Ye L, Yu H (2019) Significantly improved catalytic efficiency of caffeic acid O-methyltransferase towards N-acetylserotonin by strengthening its interactions with the unnatural substrate’s terminal structure. Enzyme Microb Technol 125:1–5. 10.1016/j.enzmictec.2019.02.005 [DOI] [PubMed] [Google Scholar]
- Wei J, Li DX, Zhang JR, Shan C, Rengel Z, Song ZB, Chen Q (2018) Phytomelatonin receptor PMTR1-mediated signaling regulates stomatal closure in Arabidopsis thaliana. J Pineal Res 65(2):e12500. 10.1111/jpi.12500 [DOI] [PubMed] [Google Scholar]
- Wei W, Tao JJ, Yin CC, Chen SY, Zhang JS, Zhang WK (2022) Melatonin regulates gene expressions through activating auxin synthesis and signaling pathways. Front Plant Sci 13:1057993. 10.3389/fpls.2022.1057993 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wei Y, Zeng H, Hu W, Chen L, He C, Shi H (2016) Comparative transcriptional profiling of melatonin synthesis and catabolic genes indicates the possible role of melatonin in developmental and stress responses in rice. Front Plant Sci 7:676. 10.3389/fpls.2016.00676 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wei Z, Li J (2016) Brassinosteroids regulate root growth, development, and symbiosis. Mol Plant 9:86–100. 10.1016/j.molp.2015.12.003 [DOI] [PubMed] [Google Scholar]
- Wen Z, Chen Z, Liu X, Sun J, Zhang F, Zhang M, Dong C (2023) 24-Epibrassinolide facilitates adventitious root formation by coordinating cell-wall polyamine oxidase- and plasma membrane Respiratory Burst Oxidase Homologue-derived reactive oxygen species in Capsicum annuum L. Antioxidants 12:1451. 10.3390/antiox12071451 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Xiao L, Ma W, Zhang J, Pu X, Rengel Z, Song Z, Chen Q (2023) Phytomelatonin interferes with flavonols biosynthesis to regulate ROS production and stomatal closure in tobacco. J Plant Physiol 284:153977. 10.1016/j.jplph.2023.153977 [DOI] [PubMed] [Google Scholar]
- Xie X, Ding D, Bai D, Zhu Y, Sun W, Sun Y, Zhang D (2022) Melatonin biosynthesis pathways in nature and its production in engineered microorganisms. Synth Syst Biotechnol 7(1):544–553. 10.1016/j.synbio.2021.12.011 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Xu J, Li Y, Lv Y, Bian C, You X, Endoh D, Teraoka H, Shi Q (2019) Molecular evolution of tryptophan hydroxylases in vertebrates: a comparative genomic survey. Genes 10(3):203. 10.3390/genes10030203 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Yang L, You J, Li J, Wang Y, Chan Z (2021) Melatonin promotes Arabidopsis primary root growth in an IAA-dependent manner. J Exp Bot 72(15):5599–5611. 10.1093/jxb/erab196 [DOI] [PubMed] [Google Scholar]
- Yang Q, Peng Z, Ma W, Zhang S, Hou S, Wei J, Dong S, Yu X, Song Y, Gao W, Rengel Z, Huang L, Cui X, Chen Q (2021) Melatonin functions in priming of stomatal immunity in Panax notoginseng and Arabidopsis thaliana. Plant Physiol 187(4):2837–2851. 10.1093/plphys/kiab419 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Yang SJ, Huang B, Zhao YQ, Hu D, Chen T, Ding CB, Chen YE, Yuan S, Yuan M (2021) Melatonin enhanced the tolerance of Arabidopsis thaliana to high light through improving anti-oxidative system and photosynthesis. Front Plant Sci 7(12):752584. 10.3389/fpls.2021.752584 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Yang X, Chen J, Ma Y, Huang M, Qiu T, Bian H, Han N, Wang J (2022) Function, mechanism, and application of plant melatonin: an update with a focus on the cereal crop, barley (Hordeum vulgare L.). Antioxidants 11:634. 10.3390/antiox11040634 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Yao Z, Zhang X, Liang Y, Zhang J, Xu Y, Chen S, Zhao D (2022) NtCOMT1 responsible for phytomelatonin biosynthesis confers drought tolerance in Nicotiana tabacum. Phytochemistry 202:113306. 10.1016/j.phytochem.2022.113306 [DOI] [PubMed] [Google Scholar]
- Yu R, Zuo T, Diao P, Fu J, Fan Y, Wang Y, Zhao Q, Ma X, Lu W, Li A, Wang R, Yan F, Pu L, Niu Y, Wuriyanghan H (2021) Melatonin enhances seed germination and seedling growth of Medicago sativa under salinity via a putative melatonin receptor MsPMTR1. Front Plant Sci 12:702875. 10.3389/fpls.2021.702875 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Yu Y, Bian L, Jiao Z, Yu K, Wan Y, Zhang G, Guo D (2019) Molecular cloning and characterization of a grapevine (Vitis vinifera L.) serotonin N-acetyltransferase (VvSNAT2) gene involved in plant defense. BMC genomics 20:880. 10.1186/s12864-019-6085-3 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Yu Y, Lv Y, Shi Y, Li T, Chen Y, Zhao D, Zhao Z (2018) The role of phyto-melatonin and related metabolites in response to stress. Molecules 23(8):1887. 10.3390/molecules23081887 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zeng W, Mostafa S, Lu Z, Jin B (2022) Melatonin-mediated abiotic stress tolerance in plants. Front Plant Sci 13:847175. 10.3389/fpls.2022.847175 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zhai R, Liu J, Liu F, Zhao Y, Liu L, Fang C, Wang H, Li X, Wang Z, Ma F, Xu L (2018) Melatonin limited ethylene production, softening and reduced physiology disorder in pear (Pyrus communis L.) fruit during senescence. Postharvest Biol Technol 139:38–46. 10.1016/j.postharvbio.2018.01.017 [Google Scholar]
- Zhang H, Qiu Y, Ji Y, Wu X, Xu X, Wu P (2023) Melatonin promotes seed germination via regulation of aba signaling under low temperature stress in cucumber. J Plant Growth Regul 42:2232–2245. 10.1007/s00344-022-10698-y [Google Scholar]
- Zhang HJ, Zhang N, Yang RC, Wang L, Sun QQ, Li DB, Cao YY, Weeda S, Zhao B, Ren S, Guo YD (2014) Melatonin promotes seed germination under high salinity by regulating antioxidant systems, ABA and GA4 interaction in cucumber (Cucumis sativus L.). J Pineal Res 57(3):269–279. 10.1111/jpi.12167 [DOI] [PubMed] [Google Scholar]
- Zhang J, Shi Y, Zhang X, Du H, Xu B, Huang B (2017) Melatonin suppression of heat-induced leaf senescence involves changes in abscisic acid and cytokinin biosynthesis and signaling pathways in perennial ryegrass (Lolium perenne L.). Environ Exp Bot 138:36–45. 10.1016/j.envexpbot.2017.02.012 [Google Scholar]
- Zhang N, Sun Q, Li H, Li X, Cao Y, Zhang H, Li S, Zhang L, Qi Y, Ren S, Zhao B, Guo YD (2016) Melatonin improved anthocyanin accumulation by regulating gene expressions and resulted in high reactive oxygen species scavenging capacity in cabbage. Front Plant Sci 7:197. 10.3389/fpls.2016.00197 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zhang M, Chen X, Wang N, Guan L, Wang L, Chen X, Yang Z, Sun Y, Fan Y, Meng Y, Liu M, Chen W, Wu F, Song R, Wang S, Lu X, Wang J, Guo L, Zhao L, Nan H, Zhang K, Feng K, Ye W (2024) GhCOMT33D modulates melatonin synthesis, impacting plant response to Cd2⁺ in cotton via ROS. Physiol Plant 176(6):e14647. 10.1111/ppl.14647 [DOI] [PubMed] [Google Scholar]
- Zhang M, Zhang S (2022) Mitogen-activated protein kinase cascades in plant signaling. J Integr Plant Biol 64(2):301–341. 10.1111/jipb.13215 [DOI] [PubMed] [Google Scholar]
- Zhang T, Li R, Xing J, Yan L, Wang R, Zhao Y (2018) The YUCCA-Auxin-WOX11 module controls crown root Development in Rice. Front Plant Sci 9:523. 10.3389/fpls.2018.00523 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zhang X, Feng Y, Jing T, Liu X, Ai X, Bi H (2021) Melatonin promotes the chilling tolerance of cucumber seedlings by regulating antioxidant system and relieving photoinhibition. Front Plant Sci 9(12):789617. 10.3389/fpls.2021.789617 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zhang Y, Dai M, Wu Z, Wang S, Fan Y, Ni K, Lu X, Liu X, Liu M, Chen W, Chen X, Wang D, Wang J, Guo L, Zhao L, Wang X, Ye W (2023b) Melatonin receptor, GhCAND2-D5 motivated responding to NaCl signaling in cotton. Plant Physiol Bioch 203. 10.1016/j.plaphy.2023.108001 [DOI] [PubMed]
- Zhang Z, Hu Q, Liu Y, Cheng P, Cheng H, Liu W, Xing X, Guan Z, Fang W, Chen S, Jiang J, Chen F (2019) Strigolactone represses the synthesis of melatonin, thereby inducing floral transition in Arabidopsis thaliana in an FLC-dependent manner. J Pineal Res 67(2):e12582. 10.1111/jpi.12582 [DOI] [PubMed] [Google Scholar]
- Zhao D, Yu Y, Shen Y, Liu Q, Zhao Z, Sharma R, Reiter RJ (2019) Melatonin synthesis and function: evolutionary history in animals and plants. Front Endocrinol 10:249. 10.3389/fendo.2019.00249 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zhao L, Chen L, Gu P, Zhan X, Zhang Y, Hou C, Wu Z, Wu YF, Wang QC (2019) Exogenous application of melatonin improves plant resistance to virus infection. Plant Pathol 68(7):1287–1295. 10.1111/ppa.13057 [Google Scholar]
- Zhu Y, Gao H, Lu M, Hao C, Pu Z, Guo M, Hou D, Chen LY, Huang X (2019) Melatonin-nitric oxide crosstalk and their roles in the redox network in plants. Int J Mol Sci 20(24):6200. 10.3390/ijms20246200 [DOI] [PMC free article] [PubMed] [Google Scholar]