The content of melatonin in horticultural crops [16].
Abstract
Melatonin is an indoleamine, abundant in animals and plants, which has the functions of regulating circadian rhythm, improving immunity and anti-aging in animals, and is a good health care product beneficial to human health. Recent studies have shown that melatonin has physiological functions including regulating plant growth, promoting seed germination, controlling root development and delaying leaf senescence. The antioxidant properties of melatonin give it the ability to strengthen plants’ resistance to stress. The comprehensive researches in recent years, involving five aspects of \"the biosynthetic pathway of melatonin in plants, the melatonin in horticultural crops and its influencing factors, the roles of melatonin in the growth and development of horticultural crops, in the response to stress of horticultural crops, the signal transduction network of melatonin in regulating plant growth and the development and stress resistance,\" are reviewed in the present paper. The application of melatonin in horticulture production is also discussed, which can provide a theoretical reference for the application of melatonin in horticultural production.
Keywords
- development
- growth
- horticultural crops
- melatonin
- stress tolerance
1. Introduction
Melatonin,
2. The biosynthetic pathway of melatonin in plants
Melatonin is a small molecule, which can shuttle freely in and between cells due to its hydrophilic and lipophilic molecular structure [3]. Using St. John’s wort (
At present, key genes of melatonin synthesis,
3. Concentrations of melatonin in horticultural crops and its influential factors
Although policies regarding the free sale, universal use and food supplement of melatonin are still controversial, most developed countries have classified melatonin as an over-the-counter drug and allowed it to be sold freely in pharmacy stores. Currently, melatonin is regarded as an over-the-counter medicine and health care product to relieve sub-health and improve sleep [11]. Some studies indicated that regular consumption of melatonin-rich foods can significantly improve human health [12, 13, 14]. In view of the health benefits of melatonin, more and more nutritionists begin to pay attention to the amount of melatonin in food, hoping that people can get more natural melatonin from daily food.
Two research groups identified melatonin in some edible plants in 1995. Vantassel et al. [15] have identified the presence of plant-derived melatonin in higher plants of morning glory (
Common name | Specie name | Melatonin content (pg g−1) |
---|---|---|
Sweet cherries | 8000–120,000 (FW) | |
Tart cherries | 1000–19,500 (FW) | |
White radish | 657.2 (FW) | |
Ginger | 583.7 (FW) | |
Pomegranate | 540–5500 (FW) | |
Shungiku | 416.8 (FW) | |
Pineapple | 302 (FW) | |
Chinese cabbage | 112.5 (FW) | |
Cabbage | 107.4 (FW) | |
Carrot | 55.3 (FW) | |
Taro | 54.6 (FW) | |
Apple | 47.6 (FW) | |
Spinach | 38.7 (FW) | |
Onion | 31.5 (FW) | |
Cucumber | 24.6 (FW) | |
Kiwi fruit | 24.4 (FW) | |
Strawberry | 12.4 (FW) | |
Asparagus | 9.5 (FW) | |
Banana | 8.9 (FW) | |
Beet root | 2 (FW) | |
Tomato | 0.5–114,500 (FW) | |
Thyme | 38,000 (DW) | |
Chinese liquorice | 34,000 (DW) | |
Coffee beans | 5800–6800 (DW) | |
Feverfew | 1700 (DW) | |
Mulberry Morus | 1510 (DW) | |
Black pepper | 1092 (DW) | |
Kidney bean sprouts | 529 (DW) | |
Aloe | 516 (DW) | |
White radish Raphanus | 485 (DW) | |
Jujube | 256 (DW) | |
White mustard seed | Brassica hirta L. | 189 (DW) |
Qin Jiao | 180 (DW) | |
Mustard seed | 129 (DW) | |
Goji berry | 103–530 (DW) | |
Almond seed | 39 (DW) | |
Sunflower seed | 29 (DW) | |
Anise seed | 7 (DW) | |
Coriander seed | 7 (DW) | |
Celery seed | 7 (DW) | |
Walnut | 3.5 (DW) | |
Bell pepper | 0.179–0.581 (DW) |
The melatonin concentrations in horticultural crops are closely influenced by species, varieties, growing environment, cultivated methods, harvesting time and processing methods. As shown in Table 1, melatonin concentration in sweet cherry (13.46 ng g−1) is threefold higher than that in tomato. (4.1 ng g−1) [19]. In different varieties of tomato, the melatonin concentrations fluctuated greatly from 0.5 pg g−1 to 114.5 ng g−1. This difference is largely influenced by the genotype of the variety itself. Climate and environmental factors in different years have significant effects on the melatonin concentrations of horticultural crops. For example, the melatonin concentrations of ‘Marbone’ tomato harvested in 2010 were six times higher than those in 2009, while the melatonin concentrations of ‘Festival’ strawberries harvested in 2010 were three times lower than those in 2009 [20]. The concentrations of melatonin in field-cultivated tomato were significantly higher than those in the phytotron-cultivated tomato, and higher than those in the vitro-cultivated tomato [21]. Riga et al. [22] found that fruit bagging can significantly increase the melatonin concentrations in most tomato varieties but reduce the concentrations of melatonin in pepper (
4. Roles of melatonin in regulating growth and development of horticultural crops
4.1 Effects of melatonin on growth and yield formation of horticultural crops
Hernández-Ruiz et al. [18] were the first to propose that melatonin was a hormone-like growth regulator in plants. Because melatonin promotes the hypocotyl growth of albino lupine (
Byeon and Back [30] obtained transgenic rice with excessive melatonin accumulation via overexpression of sheep
Other studies have shown that 50 μmol L−1 of melatonin solution can significantly promote the growth of soybean seedlings and increase the yield of soybean [31]. Liu et al. [32] found that in the late stage of pear fruit development, spraying of 100 μmol L−1 of melatonin solution into the pear tree could promote the accumulation of endogenous melatonin in pear fruit. Melatonin increased the size of pear fruit by increasing the net photosynthetic rate and maximum quantum efficiency of photosystem II. During the ripening period, melatonin increased the concentrations of soluble sugar, especially sucrose and sorbitol, which may be the result of improving the accumulation of starch and promoting the expansion of pear fruit, which had a significant effect on increasing yield. In a study on grapes, Meng et al. [33] found that spraying of 100 mol L−1 of melatonin solution on young grape fruits could promote the accumulation of endogenous melatonin in grape fruits and promote the expansion of grape fruits, which had a significant effect on increasing production.
From these effects of melatonin on crop growth and yield, it becomes apparent that the promotion effect of melatonin on crop growth is a common feature. The difference was that the increase of endogenous melatonin concentrations reduced the rice yield, while the exogenous melatonin treatment increased the soybean and grape yield. The effect of melatonin on crop yield seems contradictory; however, we think that first, the soybean experiment adopted melatonin in treatment at seedling stage, but no melatonin was added at the yield formation stage. However, the melatonin level of transgenic rice was high in the whole growth period, so soybean showed an increase in yield, and rice showed a decreased yield. Second, according to the phenotypic difference, melatonin promoted plant growth in soybean more than it did in rice. The full growth of vegetative body provides more abundant photosynthetic products for reproductive growth. Third, the essence of melatonin inhibiting yield formation lies in inhibiting reproductive growth, that is, seed formation. The berry of grape is developed from ovary, which is similar to tomato and other berry crops. The expansion of ovary in the early stage of fruit development needs the stimulation of IAA to form a strong storage for nutrition. The effects of melatonin and IAA are similar, which may be the specific mechanism of melatonin in promoting the expansion of grape fruit. Fourth, Zhao et al. [34] showed that low concentrations of melatonin (10 μmol L−1) could promote the metabolism of sugars, photosynthesis, loading and transportation of sucrose in the maize phloem, thus promoting the growth of maize plants. However, high concentrations of melatonin (1 mmol L−1) could inhibit sucrose loading in phloem, resulting in the accumulation of excessive sucrose, hexose and starch in leaves. As a result, leaf photosynthesis and the growth of maize plants were inhibited. Zhang et al. [35] also obtained similar results on the effects of melatonin concentrations on flowering in apple tree. Overexpression of
4.2 Melatonin regulates the ripening, aging and preservation of horticultural crops
Ripening, aging and preservation are contradictory processes in the production of horticultural products. Interestingly, more and more studies have shown that melatonin can be used to flexibly regulate the ripening, aging and storage of horticultural crops under different concentrations and conditions. Sun et al. [36] found that pretreatment of tomato with 50 μmol L−1 and 100 μmol L−1 melatonin could promote tomato ripening. Its regulatory mechanism can be summarized as follows: melatonin activates the expression of
Shi et al. [40] showed that the concentrations of endogenous melatonin
4.3 Effects of melatonin on root development of horticultural crops
Endogenous melatonin has similar physiological functions with IAA, which promotes root development, elongation and lateral and adventitious root development. Chen et al. [43] found that 0.1 μmol L−1 melatonin promoted the elongation of mustard (
Although melatonin is closely related to IAA in the process of affecting plant root development, melatonin-induced root morphogenesis is independent of auxin signaling [44]. Melatonin promotes the elongation of the principal root and lateral root in
5. Role of melatonin in stress response of horticultural crops
Large numbers of studies have shown that the endogenous melatonin of plants often changes greatly under the stimulation of stress factors, including light intensity, light quality, temperature, water and oxygen, as well as the stimulation of salinity, ultraviolet (UV-B), paraquat, diseases and insect pests, etc. At the same time, exogenous addition of melatonin or enhancement of plant endogenous melatonin synthesis, through gene editing technology, can improve the plant’s resistance to adversity.
5.1 Regulation of melatonin resistance to abiotic stress
The efficient utilization of light energy for plant growth, development, yield and quality by light has always been the core of scientific research in horticulture production. Melatonin, on the other hand, has been shown to have a circadian rhythm in mammals, so it is inferred that there should also be a myriad of links between endogenous melatonin of plant and light environmental factors. Melatonin improved the growth performance of yeast under UV radiation and reduced the mortality [48]. The mechanism proposed suggests that melatonin increased the expression of antioxidant genes and DNA-repairing genes.
Kolar et al. [49] used 100 mmol L−1 and 500 mmol L−1 of melatonin solutions to treat the cotyledon and germ of the short-day plant
Temperature is a key environmental factor that affects horticultural crops, especially vegetable crops that are planted off season. Inappropriate temperature leads to substantial loss of yield and poor quality of horticultural crops. For this reason, horticultural researchers have been working on temperature adaptation mechanisms and efficient and safe plant growth regulators to cope with sudden temperature changes. Shi et al. [53] confirmed that melatonin was induced by high temperature in
Horticultural crops require lots of water in their cultivation. Water stress or physiological drought will affect the growth and development of crops and make a significant impact on the yield. Exogenous MT promoted the accumulation of soluble sugar and protein under stress, thereby alleviating the damage of rapeseed seedlings under drought stress [61]. Many orchards in arid/semi-arid areas (especially in mountainous areas) are in a state of long-term water shortage. Although fruit trees can grow, their productions are affected. Melatonin treatment significantly improved the drought resistance of wheat seedlings, including reduced membrane damage, more complete chloroplast grana lamella, higher photosynthetic rate, maximum efficiency of photosystem II, and higher cellular turgor and water-holding capacity [62]. Zuo et al. [45] cloned
There are about 831 million hectares of saline-alkali land in the world, including 397 million hectares of neutral saline soil and 434 million hectares of alkaline saline soil, accounting for 10% of the world’s arable land [65]. Salinity stress can lead to the reduction of water availability and nutrient imbalance, seriously restricting agricultural production. In addition, facility horticulture is also faced with the problem of soil secondary salinization due to the closed environment, lack of rain water leaching in the soil, excessive fertilization and other factors. Therefore, how to improve the salinity tolerance of horticultural crops becomes a key link in the development of characteristic horticulture industry in saline and alkaline areas. Ke et al. [66] demonstrated that melatonin pretreatment regulated polyamine metabolism in wheat and reduced the damage of salt stress. They also believed that melatonin induces enzyme activity that stimulates ROS to clear antioxidant defenses in response to salinity. In addition, exogenous melatonin can also prevent the accumulation of triacylglycerol and promote fatty acid β-oxidation and energy conversion under salt stress conditions. So it is helpful for improving PM H+-ATPase activity, activating gene expression of Na+-K+ reverse transporter, and maintaining K+/Na+ homeostasis of sweet potato (
5.2 The regulation of melatonin resistance to biological stress
Plants are often attacked by fungi, bacteria, viruses and pests during their growth and development. Under biological stress, plants produce endogenous hormone-regulated responses, such as salicylic acid (SA), jasmonic acid (JA), ethylene (Eth) and abscisic acid (ABA). Studies in recent years have shown that melatonin can interact with the signaling pathways of biological stress regulated by SA and JA, and negatively regulate plant resistance to biological stress.
The bacterial disease model strains
Application of exogenous melatonin to cotton could induce the expression of phenylpropanoid mevalonate (MVA), gossypol and other pathway-related genes, thus leading to increased lignin and gossypol concentrations in metabolites of this pathway and thus enhancing the resistance of cotton to Verticillium wilt [76]. Liu et al. [77] found that spraying of 50 mol L−1 of melatonin solution on tomato fruits can induce and enhance the activity of disease-resistant proteases CHI, GLU, PAL and PPO, and significantly enhance disease resistance to
In addition to the disease resistance mechanism mediated by SA signal, there is mechanical disease resistance that consists of epidermal tissue, cell wall, phenylalanine pathway-mediated disease resistance mechanism, etc. in plants. Zhao et al. [79] indicated that exogenous melatonin could downregulate the expression of invertase inhibitors of
6. Melatonin regulates the signal transduction network of plant growth and stress resistance
As mentioned above, melatonin is widely involved in the regulation of plant growth, development and resistance. Based on this, we sorted out the signal pathways involved in melatonin and summarized the schematic diagram of the signal transduction network regulated by melatonin (Figure 2). The main function of melatonin is to promote the biosynthesis of IAA and cooperate with IAA to promote the elongation and expansion of cells, which is manifested in the induction of root growth, lateral root occurrence, adventitious root occurrence and fruit expansion. Although both of them are indoleamine compounds, melatonin and IAA do not share a set of signal transduction networks [44]. Interestingly, melatonin inhibits the expression of auxin antagonistic transcription factor
Environmental stress and hormones can induce plant cells to produce polyamine (PAs) and NO. However, both PAs and NO are free radicals with strong reactivity. As two active small molecule signaling substances, they are easy to gain and lose electrons. Lei et al. [55] found that melatonin can induce the synthesis of polyamine, under low-temperature stress, and enhance cold resistance in carrot. However, NO is produced by melatonin during the induction of disease resistance [78], alkali resistance [71] and rooting [47], and NO is needed as the downstream signal. In recent years, we have found that NO is the downstream signal of PAs in tomato stress response, and it can activate several plant stress tolerance signaling pathways including antioxidant system [81]. Of course, the mechanical strengthening of melatonin on cell wall tissues [79] and the contact reaction between melatonin and ROS [82] also contributed to the acquisition of plant resilience traits. In addition, melatonin can directly regulate the expression of stress-related functional genes through transcription factor activation, such as senescence-associated genes (SAGs) [41], C-repeat binding factor (
7. Conclusion and prospect
Melatonin is widely found in plant tissues, but its concentration in plants is still very low and has obvious tissue specificity. The pan-frying, deep-frying, stir-frying, steaming and stewing techniques commonly used in Chinese food culture are not conducive to the preservation of melatonin in food. Therefore, the food sources mainly focusing on the acquisition of melatonin nutrition are mainly focused on gardening crops like fruits and vegetables suitable for fresh eating. However, melatonin is a substance with similar hormone activity in plants. The use of gene editing technology to comprehensively increase the melatonin concentrations in plants may destroy the balance of melatonin metabolism in plants and bring some adverse effects on the growth and development of plants. Based on this, we propose two suggestions for improving the concentrations of melatonin in horticultural crops: (1) inducing the expression of edible organs or specific developmental periods in horticultural crops by using tissue-specific or inducible promoters combined with melatonin synthesis of key genes. For example, tomato E8 promoter could be used to specifically express the key gene of melatonin synthesis in the fruit, and the effect of excessive melatonin accumulation on the plant was reduced on the basis of increasing the concentrations of melatonin in tomato fruit. Another example is that the chemical-induced expression system TetR combined with melatonin synthesis of key genes can be used to induce the expression of horticultural products in a time period prior to harvesting, which can improve the melatonin concentrations of the harvested products. (2) The
The study of melatonin can promote the improvement of global ecological environment. In the horticultural production system under great pressure in the natural environment and frequent outbreak of biological stress, the study on melatonin promoting growth and anti-stress regulation mechanism and the successful cases of exogenous melatonin promoting crop growth and enhancing resistance are expected to make great contributions to the high yield and high-quality production of horticultural crops. Based on the current research status, we make a prediction on the application of melatonin in horticulture production, hoping to attract more and more attention. (1) For cucumbers and others prone to premature aging, horticultural crops can be applied by exogenous melatonin to alleviate the aging process. (2) Leek, asparagus and most fruit trees show aging trend with the extension of cultivation year. The application of exogenous melatonin also plays a role in the rejuvenation of this kind of aging horticultural crops. (3) Taking advantage of the anti-aging and drought resistance properties of melatonin, it can be used for fresh cut flowers, fruits and leafy vegetables. (4) Melatonin can promote root growth and withstand low temperature in plants, alleviating the reduction in root growth and absorption of fertilizer and water that are caused by the excessive low ground temperature, thereby reducing heating costs, improving the utilization rate of CO2, and promoting the efficacy of fertilizer. (5) At present, shade means are often used in the over-summer cultivation of ginger and other light-tolerant and shade-tolerant horticultural crops to reduce leaf senescence and root loss caused by the damage of strong light to leaf photosynthetic organs. Melatonin is introduced into the cultivation technology of this type of crops by utilizing the mechanism of accumulation of melatonin in chloroplast and protection of photosynthetic organs and inhibition of leaf senescence. (6) In cucumber and pumpkin grafting, the technology of double broken root grafting is often adopted. Melatonin can promote the occurrence of adventitious root and prevent the infection of wound. At the same time, melatonin also has the function of promoting graft wound healing, which has great application potential in some fruit trees and flowers with low graft survival rate. (7) Taking advantage of the characteristics of melatonin in delaying senescence, MT is used as a flower-/fruit-preserving agent for vegetable crops in winter and summer to improve pollen vitality, increase fruit setting rate and reduce malformation fruit rate. (8) As a plant growth regulator, melatonin can be used in plant growth promotion and disease prevention to reduce the use of pesticides. Moreover, as a new type of growth regulation substance, it has the characteristics of high efficiency and environmental protection. Its development and utilization can greatly promote the healthy growth of horticultural crops, improve the fertilizer utilization ratio and reduce the occurrence of plant diseases and insect pests and pesticide dosage. It can play an important role in the process of using fewer chemical fertilizers and pesticides in China, and has a great development potential in promoting the healthy development of horticulture industry.
Acknowledgments
The authors would like to acknowledge the National Natural Science Foundation of China [U1903105 and 31872943] and the Natural Science Foundation of Shandong Province [ZR2019MC067] for their support.
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