Serotonin: Its Functional Role in Plants

Abstract

Serotonin, also known as 5-hydroxyamine, is an indoleamine that plays crucial roles as a neurotransmitter and hormone regulator in various physiological processes across the animal kingdom. This essential signaling molecule is synthesized from the aromatic amino acid tryptophan and is found in virtually all living organisms. Over the last few years, enormous research has been done on this biomolecule. In plants, they are found to be involved in several metabolic and developmental functions. Despite its widespread importance in plants still many things to understand about the mechanism of action of this biomolecule. Therefore, this chapter focuses on the current knowledge of the role of serotonin in plants.

1. Introduction

Serotonin is an important biochemical molecule found in both plants, as well as in animals. In plants, it is known as phytoserotonin. Initially, it was reported in the legume known as Macuna pruriens [1]. Later, it was found in almost 42 plant species from almost 20 different families [2]. A significant amount of the serotonin was reported in these plants. Chemically, it is known as 5-HT (5-hydroxytryptamine). It is actually a neurotransmitter recognized for its role in the mammalian central nervous system, now identified in all forms of the life from bacteria to higher eukaryotes [3]. In animal biology, especially in humans and vertebrates, numerous physiological roles of serotonin have been identified. In the beginning, it was known as enteramine as was discovered in the gut enterochromaffin cells [3], later named as serotonin and considered as one among the most ancient molecules originated first in prokaryotic life forms [4, 5, 6, 7]. Many useful functions of serotonin have been identified in animal science. It is involved to regulate the anxiety, sleep, and moods in the mammals [8] also, known for its hallucinogenic drug effect [9]. But in the case of plants less is known about its functional role despite been discovered in plants shortly after its discovery in the animals. Many biosynthetic products of serotonin in plants were identified in mid-1990s [10]. Serotonin is abundant in parenchyma of vascular bundle, companion cell and xylem cell, and vascular bundle of fruit wall of the banana [11]. The concentration of serotonin is found different in various parts of plant. For instance, in leguminous plant, Friffonia simplicifolia lower levels of serotonin are detected in its leaves, while significant amount of serotonin is present in its seeds [12]. Mostly, they are found in fruits vegetables, and seeds [13]. Even in fruits, the distribution of serotonin is not uniform [9, 14]. The amount of serotonin get increased as the fruit get ripen [15, 16, 17, 18].

2. Biosynthesis of serotonin

In animals, serotonin is produced by tryptophan in two-step processes by the two enzymes tryptophan hydroxylase and aromatic L-amino acid decarboxylase, (1) where tryptophan hydroxylase acts as rate-limiting step. Tryptophan is an essential amino acid, which is needed for synthesis of not only serotonin but also melatonin and auxin, [19, 20, 21]. Tryptophan first catalyzed into tryptamine by tryptophan decarboxylase. Tryptamine is catalyzed by tryptamine-5-hydroxylase to form serotonin (2). However, in certain plants, such as Hypericum perforatum serotonin is synthesized from the hydroxytryptophan as in mammals [22]. Hydroxylation of tryptophan leads to formation of 5-oxytryptophan in the presence of tryptophan-5-hydroxylase. Later, 5-oxytryptophan is decarboxylated by decarboxylase that gives serotonin (Figure 1).

Figure 1.

Biosynthesis of serotonin.

3. Physiological role of serotonin in plants

A lot of studies have been carried out to find out the role of serotonin in the vertebrates, whereas interest in phytoserotonin was prevented. It could be due to the less obvious role of serotonin in plants. In animals, it was first identified in 1868, whereas, in plants, it was discovered in mid-1990s. Now, serotonin is considered as an important phytohormone and stress defense compound [23, 24]. Along with melatonin, it has many roles in plant growth and survival processes [25]. A number of studies, which show its role in shoot branching [26], flowering [27], xylem sap exudation [9], ion permeability [28], morphogenesis [29], reproduction [30], germination [31], senescence [32], protection against stress [33], and root architecture (Figure 2) [34]. Different roles of serotonin are organized in Table 1. Few of them are:

Figure 2.

Different functions of the serotonin in the plants.

S. no	Functions	Plant	References
1.	Shoot branching	Arabidopsis	[35]
2.	Flowering	Datura	[27]
3.	Ion permeability	Pea Chloroplast	[36]
4.	Xylem sap exudation	Rice	[37]
5.	Morphogenesis & growth regulator	Mimosa pudica L Datura	[27, 38]
6.	Root architecture	Hypericum perforatum L, Arabidopsis	[34, 39]
7.	Reproduction	Datura	[27]
8.	Germination	Capsicum anuum L	[31]
9.	Senescence	Rice	[32]
10.	Protection against stress	Hazelnuts	[40]
14.	Coleoptile growth	Rice, plant tissue culture, Hypericum perforatum	[41, 42, 43]
16.	Stress defense compounds	Arabidopsis	[44]
17.	Photosynthesis	Chara australis	[45]
18.	Spikelet fertility & Increased stomata conductance	Rice	[9]
19.	Signaling	Arabidopsis	[46]
20.	Detoxification of ammonia	Walnut	[47]
21.	Fruit ripening	Tomato	[48]

Table 1.

Effect of serotonin on plant growth.

3.1 Growth regulation by serotonin

Extensive studies are carried out to investigate the role of serotonin on shoot branching. As we know that many of the factors involved in the regulation of plant morphogenesis. Auxin and melatonin are among the highly recognized metabolite of tryptophan along with serotonin. Various reports on signaling role of serotonin are connected with other phytohormones [26, 49]. Serotonin is now considered an important plant growth regulator [27, 38] as studies have shown its involvement in mediating vegetative growth and morphogenesis of the plants [26]. Exogenous application of serotonin in tissue culture leads to increase in shoot size and number, whereas using inhibitors revert its impact [41, 42, 50, 51, 52, 53]. In other studies in rice (Oryza sativa L) with deficiency of the enzyme serotonin N-acetyltransferase, which is involved in the conversion of serotonin to melatonin, serotonin concentration increased and resulted increased coleoptile growth [43]. An increase in endogenous serotonin level result in increased shoot production in H.perforatum [42], while application of serotonin inhibitors decrease shoot in culture [54, 55]. Similarly, inhibitors that prevent the conversion of serotonin to melatonin result in an increase in serotonin concentration, leading to the inhibition of auxin-induced rooting and the promotion of shoot growth [55]. In another study, application of serotonin in the presence of salt in sunflower seedlings increased primary root growth [39].

Serotonin along with melatonin is responsible for root elongation, formation and growth of lateral, and adventitious roots [56], thereby altering the root architecture. Many pathways are involved in their mode of action. They may act along with auxin or through independent pathways. As they are known for their role during stress, they interact with molecules like ROS, NO, and plant growth regulators. Examination of gene expression has shown that serotonin along with melatonin induced promotion of root induction and growth. Studies show that the accumulation of ROS in root tips regulates the formation of the primary growth. As melatonin and serotonin are also synthesized from tryptophan. Studies have shown that serotonin is responsible for root production in mimosa, walnut, sunflower, and Arabidopsis thaliana [56]. These have been explained by several theories. According to one theory in walnut culture, serotonin is converted into auxin, which has been known for apical dominance and root growth, which then induces rooting [57]. In another study, it was observed that serotonin in low concentration promotes lateral root primordial while in high conc. It has opposite effect on them [46]. Root growth and root hair development but adventurous root formation get enhanced. The authors, therefore, suggested that instead of enhancing auxin content, serotonin has an antagonistic effect. Serotonin treatment in sunflower increased primary root and hypocotyl length. Therefore, limited studies emphasize the need for further detailed studies on them. Serotonin elicits tissue-specific inhibitory effects on auxin-responsive genes at the site of primary and adventitious roots and also in lateral root primordial [9]. It seems that serotonin promotes root growth partially independent of auxin activity. Researchers of the Chinese Academy of Sciences compared the physiological response of Arabidopsis to exogenous melatonin and serotonin-mediated metabolism. The study has shown that moderate concentration of melatonin did not affect primary root growth but induce lateral root formation [35].

3.2 Role of serotonin in flowering

Flowers are associated with reproduction in the plants. Many factors influence its development. Rapid growth and development the oxidative environment in these tissues can lead to underdeveloped reproductive structure if anti-oxidative protection is absent [58, 59]. Along with melatonin serotonin gives protection for the growing flowers and seeds. This effect is noticed in various species such as Datura metal, Hypericum perforatum, Malus domestica, Vitis vinifera, and Prunus avium. These studies have shown that the serotonin concentration is higher in reproductive tissue than vegetative tissue [59, 60, 61, 62, 63]. Serotonin is predominantly distributed in reproductive structures. A study has revealed that Griffonia simplicifolia leaves have a minimal amount of serotonin, while the seeds have a high concentration [9, 64]. Serotonin gets accumulated in fruits [64, 65]. It may act as signal molecule in the reproductive development. Though the study on the activity of serotonin in plant reproduction is restricted, the existing literature suggests it has a strong impact on pollen germination in vivo, as well in vitro studies. During pollen growth in St. John’s wort the shift from tetrad to uninucleate phase results increase in serotonin concentration further suggesting its role in reproductive growth [63, 66]. In rice, wheat, and soybean. Each of small molecules enhanced the germination of seeds in the presence of abscisic acid, although potent inhibitor of ABA [67].

3.3 Antioxidative properties and anti-stress properties of serotonin

As serotonin is biochemically indolamine made up of indole backbone with the sidechain ethylamine derived from the tryptophan. In the last century, numerous physiological roles of serotonin were discovered in animal science. Several studies have proposed that serotonin acts as antioxidant in the animals [67]. It regulates abiotic stress-induced plant growth inhibition possibly by modification of hormone metabolism [68, 69, 70]. Structurally, auxin is more similar to serotonin and melatonin. Serotonin is also known for gene regulation with auxin-responsive related pathways [71]. Accumulation of serotonin has been observed in the leaves of rice plants in the response of biotic stress [72]. Genes of tryptophan biosynthetic pathway show coordination with genes of serotonin and auxin biosynthesis under abiotic and biotic stress [73]. The enormous production of serotonin in senescing rice leaves, which has been identified by chlorophyll loss, lipid peroxidation of membrane, increased reactive oxygen species (ROS), and induced senescence-related genes. Serotonin concentration get increased after salt stress. In another study, CdCl₂ treatment inhibited the serotonin N-acetyltransferase gene, thereby maintaining high levels of serotonin. When serotonin is provided exogenously, it gives protection to Brassica napus L against salt stress [74]. It can alleviate the growth inhibition in seedlings of the same plant under salt stress. Under mild drought conditions, serotonin improves the yield [32, 58]. Exogenous serotonin on tomato seedling during drought and salt stresses have shown that serotonin has strong antioxidative effect [75]. Serotonin also resulted increase in the biomass and isoflavones content, cell division, ethylene, and isoflavones biosynthesis under temperature stress in soybean cell culture [76].

3.4 Role of serotonin in senescence

Accumulation of serotonin is known to play a protective role against ROS, leading to a delay in senescence [77]. Serotonin prevents the accumulation of the toxic metabolite due to its powerful antioxidant activity in the senesced leaves. Because of its antioxidative activity, serotonin protects xylem parenchyma during senescence-induced oxidative damage. Serotonin overexpression in plants shows delay in senescence in rice leaves, whereas transgenic plants with low serotonin expression show fast senescence [73]. Serotonin relieves the accumulation of harmful biomolecules tryptamine by its antioxidant activity in the senescenced leaves. Further physiological analysis indicated that exogenous serotonin alleviates iron deficiency-induced leaf chlorosis [78] and improves drought and salt tolerance in tomato seedlings [79]. Serotonin shows the slow senescence in corn leaves, via calcium signal transduction, interacts with phosphatidylinositol, and maintains the chlorophyll content [80].

3.5 Contribution of serotonin in photosynthesis

Serotonin is believed to be localized in the chloroplast. There is a lot of evidence that shows its role in the maintenance of the photosynthetic tissues [36, 81, 82]. According to one study, isolated chloroplast of pea depicted that serotonin is capable of enhancing efflux of magnesium and calcium. Serotonin also helps in mediating light sensing in plants via phytochrome modification activity and helping in signaling networks [9]. The chlorophyll content gets decreased due to salinity was increased by exogenous serotonin [74]. Serotonin levels increased significantly under longer wavelength treatment and in dark conditions [9]. In rice plants, serotonin was found to improve stomatal conductance, spikelet fertility, and yield under mild drought stress conditions [9].

3.6 Interaction of serotonin with phytochrome

One of the most important roles of the serotonin is that it recognizes light and regulates circadian and seasonal rhythms. Phytochrome is used in this process through which serotonin interacts, therefore, induce diverse metabolic activities. Serotonin stimulates phosophoinositide turnover, therefore, modulates the red light effect, enhances the nitrate reductase transcription, and inhibits phy-I transcript accumulation [38, 83]. Many reports are indicating interaction of serotonin with phytochrome in an important signal cascade. First, it was reported in the eighties when external application of serotonin was capable of takeoff the effect of red light. It affects phytochrome either by activating it or by modifying the signal transduction pathway. In one study, it was observed that serotonin application could mimic the calcium uptake observed in light-grown culture of the protoplast [84, 85]. Besides stimulating the effects of red light exposure in plants, endogenous serotonin levels also get decreased in response to red light exposure to yellow or green light in Sedum morganianum E. Walther. Serotonin usually found in high concentration during the day time and lowered during the night [71]. Biosynthesis of indoleamine and role of serotonin along with melatonin has been well characterized in yeast, bacteria, and mammals [86, 87]. Many studies show serotonin treatment mimic the effects of red light exposure in other physiological processes such as fruit ripening, senescence, and leaf abscission. Interaction between serotonin with metabolite phenylpropanoid suggests its contribution in the maintance of chlorophyll pigments such as chlorophyll, as well as anthocyanin [88, 89].

3.7 Effect upon ammonia

However, serotonin is found during seed development, how exactly it functions out there is not known yet. Many studies indicate probably it is involved in the detoxification of the ammonia, hence prevent the embryo. In drying seed, serotonin assists to remove accumulating ammonia. Ammonia is metabolized in L-tryptophan. After decarboxylation, it gives tryptamine. Hydroxylation of tryptamine by cytochrome P450 monooxygenase forms serotonin [47]. Similar results of serotonin accumulation in cotyledon of walnut were observed. Here, serotonin is involved in the detoxification of ammonia reaction, thus prevent delicate plant tissue [90]. Serotonin was also detected in embryos of Juglans mandshurica histochemically [37, 91]. Further studies are needed to explore detail protective pathway of serotonin.

4. Conclusion and future perspectives

Though much new information is coming out about its regulatory role in plants, it is one of the most primitive biomolecules that evolved on Earth and is considered one of the most important molecules. From studies, it is now evident that it carries out diverse functions in plants. So, there is a growing interest among plant researchers to study the effect of serotonin on various plant systems. No doubt a new branch of phytoserotonin has emerged, where lots of things need to be worked out. In humans, it is involved in many vital roles. The discovery of serotonin in plants used in the treatment of human disorders provides a new route for the investigation of medicinally active compounds. Diverse roles of serotonin in plants are identified. As molecules regulate morphogenesis, they can be used as potential modulators in tissue culture regeneration techniques. The antistress and detoxification activities of serotonin further need to be investigated in detail. Moreover, auxin and serotonin biosynthesis are associated with tryptophan. Tryptophan is an important precursor for various metabolites. Thus, it is possible that both auxin and serotonin are related. So, it is important to find out the possibility of auxin-serotonin crosstalk or the crosstalk of serotonin with other hormones during different regulatory pathways.