Exogenous application of melatonin mitigate the heat stress in different tomato (Solanum lycopersicum L.) cultivars

1 Introduction

Global warming is a serious cause of climate change owing to the increase in temperature of the universe. Thus, climate change involves in prompting various types of abiotic stresses including drought, salinity, heavy metal, and heat. Stress caused by heat is particularly a major threat for crop production including cereal crops and horticultural crops in a wide range of the world (Ohama et al., 2017) primarily in areas of low rainfall and high temperature. Heat stress disrupts the cellular and molecular mechanism of plants leading to plant wilt. Water scarcity faced by plants under heat stress leads to disorganized ion homeostasis mechanism, photosynthetic process, abated membrane stability index, increased malondialdehyde (MDA) contents and reactive oxygen species (ROS), misfolding of protein structure due to the hampered synthesis of protein and reduced cell division (Ahmad et al., 2019). The plant is known as a sessile organism, thus under stress conditions plant triggers defensive mechanisms against unfavorable environment by scavenging ROS species to reduce oxidative stress (Mittler et al., 2011). The antioxidant enzymes including SOD, POD, CAT, and APX, and non-enzymatic antioxidants such as glutathione (GHS), phenols, and carotenoids (Jahan et al., 2019) control a defensive system within plants for its protection against stressful environment. However, heat stress is a vital issue for growing horticultural crops and food security in the future for the increasing population around the world.

Tomato (Solanum lycopersicum L.) belongs to the Solanaceae family (Aldubai et al., 2022) and is native to Peru and Mexico (Guo et al., 2022). It has substantial importance in horticultural crops due to its significant role in economic and nutritional values. Tomato and its byproducts are full of nutrition including vitamins, proteins, and antioxidants which reduce health risks in human beings, especially for cancer and heart-related individuals (Siddiqui et al. 2019). The tolerance level of abiotic stresses varies from plant to plant and species to species. Thus, heat stress is also a key factor in stunted development and reduced productivity of tomato plants. Tomato plants induce numerous natural phytohormones as brassinosteroids (BRs), ethylene, auxins (Bouzroud et al., 2018), abscisic acid, and melatonin (Altaf et al., 2021) to cope with stressful environment (Altaf et al., 2022).

Melatonin is a hormone or molecule induced naturally in both animals and plants (Kaya et al., 2019; Siddiqui et al., 2020). It plays very significant biological functions in plants against several types of stress environments by prompting a strong defensive mechanism as a master regulator in plants (Kaya et al., 2020). Melatonin not only copes with heat stress but also ameliorates root architecture, seed germination, and vigorous plant growth. It is also capable of regulating nitrogen metabolism (Zhang et al., 2017) and gene expression linked with physiological traits of plants (Arnao and Hernández-Ruiz (2019)).

Melatonin is a multi-signaling plant molecule found as a bio-stimulant and master growth regulator to promote leaf area and photosynthesis process by scavenging ROS species. Reactive oxytocin is increased directly by the system. Reactive nitrogen strains (RNS) are also produced under abiotic and biotic stress environment. The foliar melatonin spray on plants promotes their growth by improving antioxidant activities, and photosynthetic pigment and ensures their heat, drought, salt, pathogenic, heavy metal, cold stress, and acidic rain tolerances (Debnath et al., 2019). Melatonin decreases reactive oxygen species (H2O2 and O2–) levels and improves PSII activity under NaCl stress in plants (Yin et al., 2019). Furthermore, Melatonin has also the ability to improve the growth of the plant under cold stress (Bajwa et al., 2014; Turk et al., 2014). It was hypothesized that the application of melatonin can induce stress tolerance in tomato plants. Hence the current investigation was aimed to evaluate the ameliorative effect of melatonin applied through foliar spray on different cultivars of tomato grown under heat-mediated stress.

2 Materials and methods

Seeds of selected heat tolerant (T60 F1 and Super cash F1) and heat sensitive (Naqeeb and Nagina) genotypes of tomato were sanitized with a solution of 5 % sodium hypochlorite followed by repetitive cleaning with water (double distilled). Seeds were grown in plastic pots (30 cm in height and 25 cm in diameter) containing 7 kg peat moss (Sia Pendstrup Ltd., Talsii, Latvia) as a growth medium. At a suitable distance in a pot three seeds were sown and after the emergence of seeds per pot density of the plant was adjusted to one and unhealthy or less vigorous 2 seedlings were eradicated. Half-strength Hoagland solution (Table 1.1) was used as a nutrition source for plants. Irrigation was done as per the requirement of the plant by detecting the moisture level of the media. Pots were placed under the field environmental conditions at the research area of the Department of Horticulture, University of Sargodha, Sargodha, Pakistan. The average climate of Sargodha has a maximum/ minimum temperature of 41/5 °C and precipitation of 114/4 mm over a year (Fig. 1).

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Fig. 1

Average maximum temperature (℃), minimum temperature (℃) and precipitation (mm) of Sargodha over a year.

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3 Results

3.5

3.5 Osmolytes and total soluble sugars

Results regarding osmolytes (proline and MDA contents) and TSS (Figs. 2 and 3) in all tomato cultivars reflected that foliar spray of melatonin improved proline contents, MDA contents, and total soluble sugars significantly (p ≤ 0.05) as compared to their respective control treatments in both heat tolerant (T60 F1 and Super cash F1) and heat sensitive cultivars (Naqeeb and Nagina) of tomato. The percentage of increase in proline contents was 54.24 % and 50.31 % in T60 F1 and Super cash F1 respectively and 39.17 % and 42.35 % in Naqeeb and Nagina respectively. Similarly, MDA contents were increased by 38.94 % and 35.31 % in T60 F1 and Super cash F1 respectively, and 30.27 % and 27.55 % in Naqeeb and Nagina respectively as compared to control. Similarly, total soluble sugars were increased with the percent values of 35.34 % and 39.74 % in T60 F1 and Super cash F1 respectively, and 26.67 % and 28.90 % in Naqeeb and Nagina respectively over control. However, it was noted that foliar application of melatonin enhanced the Proline contents, MDA, and TSS in heat-tolerant genotypes of tomato as compared to heat-sensitive.

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Fig. 2

Superoxide dismutase (A), peroxidase (B), catalase (C) and malondialdehyde (D) of different genotypes tomato (Solanum lycopersicum L.) subjected to foliar spray of melatonin under heat stress conditions (Mean ± S.E.).

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Fig. 3

Proline (A) and total soluble sugars (B) concentration of different genotypes tomato (Solanum lycopersicum L.) subjected to foliar spray of melatonin under heat stress conditions (Mean ± S.E.).

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3.7

3.7 Pearson association between growth parameters, antioxidants activity, osmolytes, TSS, and quality attributes of two different genotypes of tomato

The data revealed that the shoot fresh, shoot dry weight, shoot length, root fresh weight, root dry weight, root length, and dry weight, number of leaves plant-1, number of flowers plant-1, proline contents, MDA contents, quality attributes were significantly and positively associated with POD, SOD, and CAT an in all the tested genotypes of tomato (Fig. 4).

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Fig. 4

Correlation among growth attributes, antioxidant enzymes activity, proline contents, MDA contents, total soluble sugars (TSS) and quality attributes of different tomato cultivars.

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4 Discussion

Heat stress reduced growth attributes in both genotypes of tomatoes and this adverse impact of heat stress was mitigated by foliar application of melatonin. The plants treated with foliar spray of melatonin showed improvement in shoot and root length, shoot and root fresh biomass, shoot and root dry biomass, number of leaves, and number of flowers per plant as compared to control (without melatonin sprayed plants) (Martinez et al., 2018). This might be due to the role of melatonin in increased cell division (Zhang, et al., 2015; Li et al., 2017a) and cell elongation (Kocal et al., 2008) as well as in restricted production of reactive oxygen species (Martinez et al., 2016). Both these factors are linked with an increase in chlorophyll contents and the overall growth of tomatoes. Heat stress also reduced water contents in the leaf tissues causing necrosis, melatonin foliar spray enhanced the water absorbing capacity of the cell by modifying the permeability of the cell membrane and cell wall (Kumar et al., 2014) led to improved membrane stability index and subsequently the various growth attributes. Furthermore, melatonin also regulates the movement and transport of different hormones like gibberellins, auxins, and cytokinins, which are associated with the movement of nutrients and carbohydrates from above-ground portion to underground parts. Thus, it changes the cellular sensitivities of many growth promoters, resulting in the growth of plants getting increased (Martinez et al., 2018).

Heat stress consequences in the production of ROS species which actuate the various phototoxic reactions like protein degradation, lipid peroxidation (LPO), and alteration in DNA (Pospisil and Yamamoto, 2017). Plants sprayed with melatonin presented greater activities of SOD, POD, and CAT enzymes in both heat-tolerant and heat-sensitive genotypes of tomatoes. The increased activity of antioxidant enzymes was due to the role of melatonin in scavenging ROS species and the cellular redox homeostasis mechanism. Hence, melatonin significantly eliminated the drastic impact of heat stress by minimizing the ROS species and lipid peroxidation with the help of antioxidant enzymes (Martinez et al., 2018; Reiter et al., 2007; Kumar et al., 2012; Tan et al., 2015; Wang et al. 2016b; Zhao et al., 2019). Hence, melatonin also augmented antioxidant enzyme activity due to its quality of electron donor to ROS species leading to reduced oxidative damage.

A foliar spray of melatonin significantly raised the accumulation of osmolytes like proline, MDA and total soluble sugars, etc. The rise in production of osmolytes and TSS in this study was an indication of osmotic adjustment owing to increased leaf water contents after the application of melatonin. It indicates that melatonin indirectly accelerates plant growth by reducing the osmotic potential. Other than osmotic adjustments, osmolytes execute different other jobs like the uptake of water, the balance of nutrients, preservation of cell integrity, and regulation of the turgidity of cell (Rivero et al., 2014). Martinez et al. (2016) revealed that melatonin enhances osmolyte contents and soluble sugars in plants grown under abiotic stress, hence responsible for high osmotic adjustment.

Heat stress reduced the quality and yield of tomato plants by inducing ROS species, reducing water contents, and disrupting membrane stability, and photosynthetic apparatus. All these traits are responsible for improving the yield and quality of tomatoes (Hassan et al., 2022). These quality and yield attributes were improved by foliar spray of melatonin because melatonin is considered a master regulator and defensive player in stressful environment and plays its leading role in increasing water contents, protein contents, amino acids, and photosynthetic pigment. All these substances collectively improved the quality and yield of tomatoes in terms of fruit weight, fruit size, fruit diameter, fruit color, pH of tomato, number of fruits plant-1, and yield of fruit pot-1 (Jahan et al., 2019).

5 Conclusion

Heat stress increased the overproduction of ROS species leading to damage the plant defense system. This study demonstrated that the exogenous application of melatonin can mitigate the adverse effects of heat shock by providing a conducive environment for the growth of both types of tomato cultivars under heat stress. Melatonin governs the mechanisms linked with ion homeostasis and improved water absorption, photosynthetic pigment, osmotic adjustment, and nutrient assimilation particularly nitrogen which is the producer of protein and amino acids within the plant. It led to enhanced growth, quality, and defense mechanism by controlling activities of antioxidant enzymes such as SOD, POD, and CAT for the detoxification of ROS species within plants against heat stress. However, the response of heat-tolerant genotypes was promising as compared to heat-sensitive genotypes of tomato plants. Moreover, this research was limited to a pot experiment that provides baseline information about the melatonin-induced heat stress tolerance in tomatoes and will be further evaluated in the field environment of different ecological zones where the elevated temperature is a serious concern.

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