The Role of Exogenously Applied Polyamines to Improve Heat Tolerance in Tomatoes: A Review

Abstract

Tomato (Solanum lycopersicum L.) is one of the most widely consumed vegetables globally and plays a crucial role in food security. However, rising temperatures due to climate change pose a significant threat to tomato cultivation by reducing yield and fruit quality. Among various abiotic stresses, heat stress (HS) can severely impair tomato growth, reproduction, and physiological functions. Polyamines (PAs), such as spermidine (Spd), putrescine (Put), and spermine (Spm), are natural compounds that play vital roles in plant stress tolerance by modulating growth and physiological responses. This review evaluates the effects of HS on tomatoes and examines the potential of exogenously applied PAs to mitigate HS. Through detailed analysis of agronomic, physiological, and biochemical responses, the review highlights how PAs can enhance heat tolerance by improving antioxidant activity, stabilizing cellular membranes, and maintaining photosynthetic efficiency. Understanding these mechanisms can aid in developing strategies to improve tomato resilience under climate stress and ensure sustainable production.

1. Introduction

Tomato (Solanum lycopersicum L.) is one of the most common and widely consumed vegetables and belongs to the family Solanaceae [1] with an estimated global production of over 189 million tons [1]. Based on the report of FAO, China, India, Turkey, America, Italy and Egypt are ranked first to sixth, respectively [2]. Tomatoes are a plentiful reservoir of vitamin A, C, and lycopene, and their increased utilization is found to reduce incidences of cardiovascular disease [3]. Tomato has remarkable nutritional value and is a source of health promoting antioxidants [4,5]. The lycopene of tomatoes also has anti-oxidative and anti-cancerous properties. Owing to these nutritional values, tomato production and consumption have been increasing continuously [6].

The Intergovernmental Panel on Climate Change (IPCC) announced that the average global temperature around the world would be 1.5 °C warmer between 2030 and 2052 and more than 3–4 °C warmer by 2100 at the present emission rate [7]. A temperature increase of 3–4 °C could cause crop yields to fall by 15–35% in Africa and Asia and by 25–35% in the Middle East [8]. Research indicates that Southern and Central Europe, particularly Spain, Portugal, and Italy, are expected to experience significant temperature increases in the future [9,10]. Pinke (2017) [11] observed a consistently increasing negative impact of temperature on crop yields in Hungary, with a 1 °C temperature rise reducing the yields of four main cereals by 9.6–14.8% Meanwhile, it is estimated that, by 2050, the global population will reach 9 billion, and food demand will increase by 100–110% compared with 2005 [12].

HS is often defined as the rise in temperature beyond a threshold level for a period sufficient to cause irreversible damage to plant growth and development. In general, HS refers to the condition in which the ambient temperature is 10–15 °C higher than the optimal temperature for crop growth [13]. The optimum temperature for tomato growth and development is 13–33 °C depending on species, and most varieties cannot grow well at temperatures above 38 °C [14]. Tomato cultivation is plagued by environmental stress, which can inhibit growth and development and ultimately lower yield and fruit quality [15]. Depending on the maximum day and night temperatures and the frequency and duration of exposure, fruit setting and yield are limited under high temperature stress due to flower abscission [16]. For this reason, maintaining crop yields under adverse environmental conditions is one of the major challenges facing modern agriculture, and PAs can play a crucial role in enhancing plant resilience to these stresses. Polyamines (PAs) are known as a group of natural compounds characterized by an aliphatic nitrogen structure. The most well-known PAs include spermidine (Spd), putrescine (Put), and spermine (Spm). PAs in plants could be present in free, soluble conjugated (phenolic compounds), and insoluble bound macromolecules, such as nucleic acids and proteins [17]. PAs are recognized for their role in regulating physiological and developmental processes [18,19]. The critical influence of PAs in protecting plant cells from several abiotic stresses has been extensively demonstrated in different plant species [20,21,22,23]. In tomato seedlings, the application of exogenous Put enhanced heat tolerance by increasing chlorophyll content, reducing the activity of chlorophyll catabolic enzymes, regulating endogenous free polyamines, boosting antioxidant defense capacity, and inducing the expression of heat-shock-related genes [24]. Karwa et al. (2022) [25] also reported that foliar-applied Spd enhanced antioxidant enzyme activities, boosting the antioxidant capacity, improved photosynthesis and spikelet fertility, and helped rice plants cope with heat stress. In citrus seedling, Chao et al. (2022) [26] reported that exogenous Spd improved heat tolerance by enhancing chlorophyll content, reducing lipid peroxidation, and increasing the activity of antioxidant enzymes, such as superoxide dismutase (SOD) and catalase (CAT). Similarly, in tomato, exogenous Spd application not only increased chlorophyll content and antioxidant enzyme activity but also reduced malondialdehyde (MDA) accumulation and modulated the expression of heat-shock proteins [27]. Luo et al. (2020) [28] showed that, in white clover, Spd treatment boosted the activity of peroxidase and polyphenol oxidase enzymes and heat-shock protein expression, and slowed leaf senescence under high temperatures. Likewise, Yang et al. (2022) [29] found that foliar application of exogenous Spd in lettuce seedlings under heat stress enhanced chlorophyll a and b content, increased net photosynthetic rate by 22.96%, and decreased stomatal density, preventing oxidative damage and resulting in preserved chloroplast and mitochondrial structure. Together, exogenous application of PAs plays a significant role in enhancing heat stress tolerance by modulating antioxidative mechanisms, maintaining cellular integrity, and improving metabolic functions across different plant species.

2. Tomato Responses to HS

Hot summers in many agricultural regions can negatively affect the vegetative and reproductive growth phases of crops [30,31]. Increasing the day temperature significantly restricts plant growth in many species, including tomato [32,33]. Exposure to elevated temperature can adversely influence various morphological, biochemical, and physiological traits, as well as the cellular and molecular functions of plants [34].

2.1. Agronomic Traits

Tomato plants will show many morphological changes when exposed to high temperatures, such as restricted growth of root and shoot, senescence and abscission of leaf, discoloration of fruit, number of leaves, and changes to total plant biomass and fresh weight [35,36,37].

Giri et al. (2017) [38] and Shorobi et al. (2023) [39] reported that an increase in temperature can decrease root growth, the concentration of nutrient uptake and the rate of nutrient uptake by roots. They also noted that HS causes more reduction in root growth compared to shoot growth, which decreases the rate of nutrient uptake in tomato. Furthermore, assessing plant response to high temperatures by intact roots is difficult, especially when a slight change in root temperature (12–15 °C) can significantly reduce fruit yield [40,41]. Bhattarai et al. (2021) [42] reported that the plant height and stem diameter of tomato reduced significantly under HS.

High temperature disrupts the morphology of the tomato flowers and its physiological metabolism, altering the production of compounds, such as carbohydrates, PAs, and proline [43,44,45]. This disruption contributes to floral abortion, which can result in up to 80% flower loss, thereby severely reducing fruit set [46,47]. Moreover, HS can change the sink–source association between roots and shoots, negatively influencing both vegetative and reproductive growth, which ultimately reduces yield and fruit quality [13,48]. Several researchers found that high temperature significantly decreased fruit set in tomato [49] (Table 1). For instance, Rajametov et al. (2021) [50] reported that temperature 40 °C Day/night for 7 days led to a decline in fruit weight (31.9%), fruit length (14.1%), fruit diameter (19.1%), and fruit hardness (19.1%) under HS in Dafnis cultivar while, in Minichal cultivar, fruit length (7.1%) and fruit diameter (12%) decreased but fruit weight (3.6%) and fruit hardness (8.3%) were enhanced.

Temperature affects not only fruit ripening time but also fruit growth rate [51]. The short term growth of fruit is strongly sensitive to temperature fluctuations [52,53]. One of the primary reasons for reduced fruit set under moderately elevated temperature is impaired pollen function, particularly reduced pollen release and viability, rather than pollen production itself [54,55]. Sato et al. (2000) [49] highlighted that high temperatures adversely impact pollen grain release and germination. Temperatures above 30 °C have been shown to reduce both pollen germination and pollen tube growth in tomato [56]. Pollen quality is often estimated based on carbohydrate content; moderate heat stress reduces starch and soluble sugar concentrations in mature pollen, thus diminishing pollen viability and subsequently lowering fruit set rate and yield [44,46,47,49,57,58].

As summarized in Table 1, many studies have reported that HS had a significantly harmful effect during the reproductive stage on pollen viability, quantity, and female fertility [44,49,59,60]. A significant correlation has been observed between reduced pollen viability and lower seeded fruit production [61], implicating this decline as a major limiting factor for flower pollination [54], fruit set, and lycopene accumulation in tomato under heat [44,49,62]. Furthermore, HS has a negative effect on male reproductive organ development, consistent with previous studies [43,47,59,60,63,64] (Figure 1). In addition, HS exacerbates physiological disorders, such as blossom end rot disease [65], cracked fruit appearance, and streaked ripening [65,66].

Table 1. Summary of High Temperature Impacts on Tomato Morphology and Productivity.

Name	Exposure Temperature	Effects
Tomato (Solanum lycopersicum)	(42/37 °C) Day/night	Reduction in roots more than shoots and slow to recover [38,39]
Tomato (Solanum lycopersicum) 43 varieties	(34/24 °C) Day/night	Reduction in plant height and stem diameter [42]
Tomato (Solanum lycopersicum) cultivars ‘Dafnis’ and ’Minichal	(40 °C) Daytime	Reduction in plant height, shoot fresh weight, root fresh weight, fruit yield, fruit length, fruit diameter [50]
Tomato (Solanum lycopersicum) cultivar Aromata	(36/28 °C) Day/night	Reduction in the shoot fresh weight [67]
(Solanum lycopersicum Mill.) cultivar (FL7156)	(32/28 °C) Day/night	Flower abortion [68]
Tomato (Solanum lycopersicum)	(37.8/26.7 °C) Day/night	Reduction in flower production [69]
Tomato (Solanum lycopersicum) genotypes (Binatomato-6, Binatomato-5, CLN-2413, D6 12 and D6 18)	(32 °C) Daytime	Significant reduction in the number of fruits, individual fruit weight and fruit yield/plant [66]
Tomato (Solanum lycopersicum) cultivars ’Minichal	(40 °C) Daytime	Decline in fruit length (7.1%) and fruit diameter (12%) [50]
Tomato (Solanum lycopersicum) cultivars ‘Dafnis’	(40 °C) Daytime	Decline in fruit weight (31.9%), fruit length (14.1%), fruit diameter (19.1%), and fruit hardness (19.1%) [50]
Tomato (Solanum lycopersicum) genotypes NC8288	(29 °C) Daytime	Reduction in fruit number, fruit weight per plant, and seed number per fruit [59]
Tomato (Solanum lycopersicum)	(32/28 °C) Day/night	Fruit abortion [49]
Tomato (Solanum lycopersicum)	(35/23 °C) Day/night	No fruit set [70]
Forty-four diverse tomatoes (Solanum lycopersicum) lines	(44/37 °C) Day/night	Reduction in fruit set [41,54,55,71,72]
Tomato (Solanum lycopersicum)	(above 30 °C) Daytime	Low pollen viability, slow pollen tube elongation, and fruit abortion [46,47]
Tomato (Solanum lycopersicum)	(35/23 °C) Day/night	Blossom end rot [65]
Tomato (Solanum lycopersicum) genotypes (Binatomato-6, Binatomato-5, CLN-2413, D6 12 and D6 18)	(32 °C) Daytime	Cracked and streaked ripening [66]

Table 1. Summary of High Temperature Impacts on Tomato Morphology and Productivity.

Name	Exposure Temperature	Effects
Tomato (Solanum lycopersicum)	(42/37 °C) Day/night	Reduction in roots more than shoots and slow to recover [38,39]
Tomato (Solanum lycopersicum) 43 varieties	(34/24 °C) Day/night	Reduction in plant height and stem diameter [42]
Tomato (Solanum lycopersicum) cultivars ‘Dafnis’ and ’Minichal	(40 °C) Daytime	Reduction in plant height, shoot fresh weight, root fresh weight, fruit yield, fruit length, fruit diameter [50]
Tomato (Solanum lycopersicum) cultivar Aromata	(36/28 °C) Day/night	Reduction in the shoot fresh weight [67]
(Solanum lycopersicum Mill.) cultivar (FL7156)	(32/28 °C) Day/night	Flower abortion [68]
Tomato (Solanum lycopersicum)	(37.8/26.7 °C) Day/night	Reduction in flower production [69]
Tomato (Solanum lycopersicum) genotypes (Binatomato-6, Binatomato-5, CLN-2413, D6 12 and D6 18)	(32 °C) Daytime	Significant reduction in the number of fruits, individual fruit weight and fruit yield/plant [66]
Tomato (Solanum lycopersicum) cultivars ’Minichal	(40 °C) Daytime	Decline in fruit length (7.1%) and fruit diameter (12%) [50]
Tomato (Solanum lycopersicum) cultivars ‘Dafnis’	(40 °C) Daytime	Decline in fruit weight (31.9%), fruit length (14.1%), fruit diameter (19.1%), and fruit hardness (19.1%) [50]
Tomato (Solanum lycopersicum) genotypes NC8288	(29 °C) Daytime	Reduction in fruit number, fruit weight per plant, and seed number per fruit [59]
Tomato (Solanum lycopersicum)	(32/28 °C) Day/night	Fruit abortion [49]
Tomato (Solanum lycopersicum)	(35/23 °C) Day/night	No fruit set [70]
Forty-four diverse tomatoes (Solanum lycopersicum) lines	(44/37 °C) Day/night	Reduction in fruit set [41,54,55,71,72]
Tomato (Solanum lycopersicum)	(above 30 °C) Daytime	Low pollen viability, slow pollen tube elongation, and fruit abortion [46,47]
Tomato (Solanum lycopersicum)	(35/23 °C) Day/night	Blossom end rot [65]
Tomato (Solanum lycopersicum) genotypes (Binatomato-6, Binatomato-5, CLN-2413, D6 12 and D6 18)	(32 °C) Daytime	Cracked and streaked ripening [66]

2.2. Physiological Traits

High temperatures adversely affect physiological and biochemical processes in tomato plants, significantly impairing growth, development, and yield [34]. Among the most heat sensitive processes is photosynthesis, primarily due to the vulnerability of chloroplast heat-sensitive organelles essential for energy capture and carbon assimilation [74].

Heat stress disrupts chlorophyll biosynthesis, reduces chlorophyll content, and compromises chloroplast structure and function. In thermotolerant tomato genotypes, a higher chlorophyll a:b ratio and a lower chlorophyll/carotenoid ratio has been associated with enhanced heat tolerance, while chlorophyll degradation, particularly in mature leaves, is exacerbated by the accumulation of reactive oxygen species (ROS) [16] Additionally, HS significantly decreases chlorophyll fluorescence, which reflects impaired photosystem function [42].

Photosynthetic efficiency is further reduced under HS due to a decline in net photosynthetic rate, increased stomatal conductance, intercellular CO₂ concentration, and transpiration rate [75]. One of the main enzymatic limitations under HS is the thermolability of Rubisco activase (RCA), which hinders the activation of Rubisco, thereby restricting carbon [76,77]. Key photosynthetic parameters, including chlorophyll content (CC), the efficiency of photosystem II (Fv/Fm), and net photosynthesis, are highly sensitive to elevated temperatures [78]. Heat-sensitive tomato varieties often exhibit rapid declines in CC and reduced Fv/Fm values [50,79], making these parameters useful indicators for screening heat-tolerant genotypes [32,42,80]. As a result, HS-induced impairment of photosynthesis can reduce carbohydrate availability, negatively affecting yield during reproductive stages [54].

In addition to photosynthetic limitations, membrane stability is significantly compromised under HS. Indicators such as electrolyte leakage (EL) and relative electrical conductivity (REC) are commonly used to assess membrane integrity [13,42,50,73,81,82,83]. Heat stress increases membrane permeability, often resulting in potassium ion leakage, which disrupts ion homeostasis and leads to oxidative damage [73]. Elevated EL levels in heat-sensitive cultivars reflect greater membrane injury and reduced solute retention capacity [61]. Rajametov et al. (2021) [50] reported increased EL in sensitive tomato plants compared to more tolerant lines, further emphasizing the role of membrane stability in thermotolerance.

Heat stress also impacts plant–water relations and metabolic rates. High daytime temperatures increase transpiration demand, inducing water deficits and reducing water potential [84]. Furthermore, reproductive development is particularly vulnerable to heat, with reduced cell wall invertase (CWIN) activity being linked to poor fruit and seed set. However, in thermotolerant cultivars, higher CWIN activity mitigates fruit abortion and supports reproductive success under elevated temperatures [85].

In summary, heat stress impairs multiple physiological and biochemical pathways in tomato, including photosynthetic performance, membrane stability, water relations, and reproductive function [75]. These disruptions, ranging from reduced chlorophyll biosynthesis and enzyme activity to altered membrane permeability, collectively lead to decreased growth, diminished yield, and increased susceptibility to oxidative stress [86].

2.3. Biochemical Traits

Environmental changes, particularly HS, profoundly affect the biochemical profile of tomato plants, influencing the accumulation of key compounds, such as phenols and flavonoids, which play important roles in stress adaptation [87]. One of the primary biochemical consequences of HS is the overproduction of ROS, often triggered by increased calcium uptake by mitochondria [61,88]. This oxidative burst leads to elevated levels of MDA, a marker of lipid peroxidation and membrane damage, indicating cellular oxidative stress. To mitigate oxidative damage, plants activate defense mechanisms. Hydrogen peroxide (H₂O₂) works as a second messenger and in the nucleus activates the expression of genes with heat shock elements in their promoters, such as heat shock proteins (HSPs) and other redox enzymes antioxidants (such as SOD and CAT), and ascorbate peroxidase (APX) and non-enzymatic antioxidants (such as ascorbic acid (ASA)) [13,89,90], to maintain appropriate ROS levels [91]. HS also promotes the accumulation of compatible osmolytes, such as proline [50,81] and soluble sugars [80], which protect proteins and maintain membrane stability [81]. Proline helps mitigate cellular damage and has been used to identify heat-tolerant tomato varieties [92,93].

3. The Biosynthetic Pathways of PAs and Their Role

The biosynthetic pathways of the main Pas, such as Put, Spd and Spm, are shown in Figure 2. S-adenosyl methionine decarboxylase (SAMDC) is a key enzyme involved in the biosynthesis of PAs. Cheng et al. (2009) [94] showed that transgenic tomato seedlings overexpressing the yeast S-adenosyl-l’methionine decarboxylase gene improved their tolerance to HS as compared to wild plants. Besides, another experiment studied the effect of salinity on plant growth, ethylene production and endogenous polyamine levels in spinach Spinacia oleracea, lettuce Lactuca sativa, melon Cucumis melo, pepper Capsicum annum, cabbage Brassica oleraceae, beetroot Beta vulgaris and tomato Solanum lycopersicum [95]. They found that PAs levels changed with salinity and, in most cases, Put decreased while Spd and/or Spm increased. The (Spd + Spm)/Put ratio increased with salinity in all species, increasing salinity tolerance. Endogenous PAs play pivotal roles in a wide range of growth and developmental processes, such as cell division, dormancy breaking of tubers and germination of seeds, leaf senescence, stimulation, support and development of flower buds, embryogenesis, fruit set and growth, fruit ripening, plant morphogenesis and response to biotic and abiotic stresses [96,97,98,99,100]. PAs also play a key role in stabilizing membranes, scavenging free radicals, DNA replication, transcription, and translation, affecting the activity of enzymes [101,102]. Recent studies further highlight the role of plant-derived PAs in improving stress tolerance under salinity [103], cold [104], drought [105], osmotic stress [106], high temperature [70], flooding [107,108] and enhancing abiotic stress tolerance [109]. Therefore, PAs are essential for plant development and other physiological processes [110,111,112] and it is essential to fill the knowledge gaps between climate change and food security by implementing mitigation and adaptation measures for a climate-smart food production system that ensures food security [113].

3.1. Improve Resistance to Abiotic Stresses by Exogenous Application of PAs

Numerous studies have indicated that exogenous PA application improved tolerance to different abiotic stress, as summarized in Table 2 [115,116,117,118,119]. For instance, under salinity stress conditions, Raziq et al. (2022) [120] reported that tomato seedlings treated with Spd performed noticeably better, exhibiting increased biomass and photosynthesis, improved ionic and osmotic homeostasis, and improved ROS scavenging ability. Rice plants treated with PAs also showed increased K⁺/Na⁺ ratios in their shoots, indicating better root-level discrimination between monovalent cations, particularly at xylem locations [121]. Applying exogenous Put decreased the net build-up of Na⁺ and Cl⁻ ions in response to salt stress. In another study, Put application mitigated the detrimental effect of NaCl on belladonna seed germination and the beginning stages of seedling growth [122]. Similarly, exogenous application of Put on rice cultivars (Oryza sativa L.) [123], soybean seedlings (Glycine max L.) [124], and mustard Brassica juncea seedlings [125] under salt stress increased ROS scavenging enzyme activity and reduced Superoxide radical (O₂⁻), H₂O₂ levels, MDA content, and EL. These results implied that Put improved the antioxidant system, which was then able to moderate the radical scavenging system and to lessen oxidative stress by increasing the antioxidant capacity. Similarly, applying exogenous Spd led to lower concentrations of Superoxide radical (O₂⁻) and H₂O₂, which in turn decreased oxidative stress in tomato plants [126]. Pascual et al. (2023) [127] noted, in response to salt and paraquat (S + PQ), that tomato plants treated with Spm increased their growth, photosynthesis, and PSII function. They also lessened the adverse impacts of S + PQ by lowering the stress-associated oxidative pressure. A study was conducted to assess the effects of supplementing Spm on cultivars of maize (Zea mays L.) that were subjected to drought stress. The results of the investigation showed that total phenols and flavonoids from both cultivars had higher concentrations of Spm and Spd after supplementation with Spm [128]. During drought stress, grafted tomato plants’ fruits had a high endogenous PA content, which had a beneficial effect on the accumulation of osmo-protectants and the activities of ROS scavenging enzymes [129]. The exogenous administration of Spm, Spd, and Put on sesame plants was investigated by Desoky et al. (2023) [130] for recovering tissue integrity, photosynthetic efficiency, and nutritional content balance. It also increased the amounts of osmo-protectants (i.e., proline and soluble sugars), as well as non-enzymatic and enzymatic antioxidants, all of which were linked to reducing ROS and the adverse effects on lipid peroxidation and EL. Drought-stressed sesame plants benefit from these beneficial effects, which raise production and quality of oil content. In wheat Triticum aestivum [131], cherry tomatoes [132], and onion Allium fstulosum [133], PAs activated the antioxidant system and alleviated the negative effects of drought stress and improved plant growth. All these results point to the role of PAs in withstanding drought stress.

Put and Spd could be applied exogenously to revitalize the adverse effect of chilling. Therefore, the enhanced EL and MDA content brought about by chilling were reduced by pretreatment with Put and Spd in cucumber [134,135]. This study showed that PAs are crucial to cucumber’s ability to withstand chilling stress, which is most likely accomplished by serving as oxidative defense against chilling damage. Moreover, another experiment found that inhibiting Put biosynthesis increased cold sensitivity, suggesting that PAs are crucial for cold adaptation in tomato plants [136].

Table 2. The effect of exogenous application of PAs on plants.

PAs (Type, Application Concentration, Durations)	Plant	Type of Stress	Effectiveness and Plant Response
Spd Foliar sprayed (0.1 mM) (3, 6, 12, 24, and 48 h)	Tomato (Solanum lycopersicum)	Salinity	Enhanced ion homeostasis (Na+/K+ ratio) Photosynthetic performance Enhanced expression of stress-responsive genes (RBOH1) Improved ROS scavenging [120]
Put, Spd, Spm Irrigation (1 mM) (5, 12, and 19 days)	Rice (Oryza sativa L.)	Salinity	Higher K+/Na+ ratio in the shoots Put induced a decrease in shoot water content [121]
Put Soaking seeds (0.01 mM) (8 h)	Belladonna (Atropa belladonna)	Salinity	Reduction of accumulation of (Na+/K+) ions Better germination Early seedling growth [122]
Put Foliar sprayed (0.1 mM) (Every 2 days)	Rice (Oryza sativa L.)	Salinity	Increased ROS scavenging enzyme activity Reduction of the EL [123]
Spd, Spm, Put Foliar sprayed (100 mg/L Spd, 150 mg/L Spm, and 150 mg/L Put)	Soybean (Glycine max L.)	Salinity	Spd enhanced the taproot Spm enhanced POD 39.66% and CAT 57.94% activity Put increased plant height, relative growth rate by 42.86% [124]
Put Irrigation (0.1 mM) (7 days)	Indian mustard (Brassica juncea)	Salinity	Induction of enzymes in leaf tissues APX > GR > CAT > SOD > POD Preventing membrane peroxidation Improving seedling growth [125]
Spd Soaking seeds (0.25 mM) (10 h)	Tomato (Solanum lycopersicum)	Salinity and Alkalinity	Enhanced root dry weights Enhance antioxidant capacity [126]
Spm Irrigation (0.5 mM) (Once a day)	Tomato (Solanum lycopersicum)	Salinity and Paraquat	Increased growth, photosynthesis, and PSII function, membrane stability Enhanced gene expression for stress tolerance Reduction of oxidative stress [127]
Put Foliar sprayed (0.20 and 40 mg/L) (Before flowering initiation phase, for three continuous weeks)	Thyme (Thymus vulgaris L.)	Drought	Improved leaf water content Upregulated antioxidant enzyme activities Increased essential oil content by 23.07% [137]
Put Soaking seed (0.1, 0.01, and 0.001 mM) (10 h)	Hybrid maize (Zea mays L.)	Drought	Improved plant biomass components, leaf water status, leaf area, germination rates, and antioxidant enzyme activities [138]
Spm Foliar sprayed (25 mg/L) (25 days)	Maize (Zea mays L.)	Drought	Increased total phenol and flavonoid concentration Improved water use efficiency, osmotic adjustment, and antioxidant enzyme activities [128]
Spd, Spm, Put Foliar sprayed (1 mM)	Grafted Tomato	Drought	Lower ROS and higher CAT, SOD activities Improve water use efficiency, osmotic adjustment, and antioxidant enzyme activities [129]
Spm, Spd Foliar sprayed (0.1 mM Spm, Put 0.2 mM) (15, 30, and 45 days after sowing)	Sesame (Sesamum indicum L.)	Drought	Enhancement in photosynthetic pigments stomatal conductance, water relations, relative water content, membrane stability index, excised leaf water retention, plant height, leaf area, number of capsules per plant, 1000-seed weight, seed yield, oil content, plant nutrient content (N, P, K) Highly significant amelioration in osmo-protectants (free proline, soluble sugars), and antioxidant enzyme activities (CAT, POD, SOD, APX) Highly significant reduction in oxidative stress markers (MDA, EL, O2−, H2O2) [130]
Put Prior flooding (2 mM)	Welsh onion (Allium fstulosum)	Drought	Alleviation of relative water content, plant growth and chlorophyll fluorescence Reduction of (O2−), (H2O2) contents [133]
Spd, Spm, Put Foliar sprayed (1 mM Spd, 1 mM Spm, and 2 mM Put) (Daily for 6 days)	Wheat (Triticum aestivum L.)	Drought	Improved grain weight, size, starch, and protein content in grains Activation of enzymes involved in starch and protein metabolism Improved physiological responses, water use efficiency, and osmotic adjustment. Enhanced antioxidant enzyme activities and oxidative stress markers. Improved impact on drought stress [131]
Spd Foliar sprayed before chilling (0.5 mM) (12 h before chilling)	Cucumber (Cucumis sativus L. cv Jinchun No. 3 and cv Suyo)	Chilling	Reduction of H2O2, ROS, and EL in leaves Alleviation of chilling injury Activities of antioxidant enzymes Improved membrane stability, plant growth [134]
Put, Spd Foliar sprayed (1 mM put, 0.5 mM Spd) (24 h before chilling)	Cucumber (Cucumis sativas L.)	Chilling	Reduction of EL and MDA content Activation of antioxidant enzymes [135]
Spd, Spm, Put Foliar sprayed before chilling (1 mM) (For 12 h daily)	Tomato (Solanum lycopersicum Mill.)	Chilling	Activation of antioxidant enzyme Gene expression (ornithine decarboxylase (ODC), arginine decarboxylase (ADC), and S-adenosylmethionine decarboxylase (SAMDC) Put plays an important role in tomato chilling tolerance [136]

Table 2. The effect of exogenous application of PAs on plants.

PAs (Type, Application Concentration, Durations)	Plant	Type of Stress	Effectiveness and Plant Response
Spd Foliar sprayed (0.1 mM) (3, 6, 12, 24, and 48 h)	Tomato (Solanum lycopersicum)	Salinity	Enhanced ion homeostasis (Na+/K+ ratio) Photosynthetic performance Enhanced expression of stress-responsive genes (RBOH1) Improved ROS scavenging [120]
Put, Spd, Spm Irrigation (1 mM) (5, 12, and 19 days)	Rice (Oryza sativa L.)	Salinity	Higher K+/Na+ ratio in the shoots Put induced a decrease in shoot water content [121]
Put Soaking seeds (0.01 mM) (8 h)	Belladonna (Atropa belladonna)	Salinity	Reduction of accumulation of (Na+/K+) ions Better germination Early seedling growth [122]
Put Foliar sprayed (0.1 mM) (Every 2 days)	Rice (Oryza sativa L.)	Salinity	Increased ROS scavenging enzyme activity Reduction of the EL [123]
Spd, Spm, Put Foliar sprayed (100 mg/L Spd, 150 mg/L Spm, and 150 mg/L Put)	Soybean (Glycine max L.)	Salinity	Spd enhanced the taproot Spm enhanced POD 39.66% and CAT 57.94% activity Put increased plant height, relative growth rate by 42.86% [124]
Put Irrigation (0.1 mM) (7 days)	Indian mustard (Brassica juncea)	Salinity	Induction of enzymes in leaf tissues APX > GR > CAT > SOD > POD Preventing membrane peroxidation Improving seedling growth [125]
Spd Soaking seeds (0.25 mM) (10 h)	Tomato (Solanum lycopersicum)	Salinity and Alkalinity	Enhanced root dry weights Enhance antioxidant capacity [126]
Spm Irrigation (0.5 mM) (Once a day)	Tomato (Solanum lycopersicum)	Salinity and Paraquat	Increased growth, photosynthesis, and PSII function, membrane stability Enhanced gene expression for stress tolerance Reduction of oxidative stress [127]
Put Foliar sprayed (0.20 and 40 mg/L) (Before flowering initiation phase, for three continuous weeks)	Thyme (Thymus vulgaris L.)	Drought	Improved leaf water content Upregulated antioxidant enzyme activities Increased essential oil content by 23.07% [137]
Put Soaking seed (0.1, 0.01, and 0.001 mM) (10 h)	Hybrid maize (Zea mays L.)	Drought	Improved plant biomass components, leaf water status, leaf area, germination rates, and antioxidant enzyme activities [138]
Spm Foliar sprayed (25 mg/L) (25 days)	Maize (Zea mays L.)	Drought	Increased total phenol and flavonoid concentration Improved water use efficiency, osmotic adjustment, and antioxidant enzyme activities [128]
Spd, Spm, Put Foliar sprayed (1 mM)	Grafted Tomato	Drought	Lower ROS and higher CAT, SOD activities Improve water use efficiency, osmotic adjustment, and antioxidant enzyme activities [129]
Spm, Spd Foliar sprayed (0.1 mM Spm, Put 0.2 mM) (15, 30, and 45 days after sowing)	Sesame (Sesamum indicum L.)	Drought	Enhancement in photosynthetic pigments stomatal conductance, water relations, relative water content, membrane stability index, excised leaf water retention, plant height, leaf area, number of capsules per plant, 1000-seed weight, seed yield, oil content, plant nutrient content (N, P, K) Highly significant amelioration in osmo-protectants (free proline, soluble sugars), and antioxidant enzyme activities (CAT, POD, SOD, APX) Highly significant reduction in oxidative stress markers (MDA, EL, O2−, H2O2) [130]
Put Prior flooding (2 mM)	Welsh onion (Allium fstulosum)	Drought	Alleviation of relative water content, plant growth and chlorophyll fluorescence Reduction of (O2−), (H2O2) contents [133]
Spd, Spm, Put Foliar sprayed (1 mM Spd, 1 mM Spm, and 2 mM Put) (Daily for 6 days)	Wheat (Triticum aestivum L.)	Drought	Improved grain weight, size, starch, and protein content in grains Activation of enzymes involved in starch and protein metabolism Improved physiological responses, water use efficiency, and osmotic adjustment. Enhanced antioxidant enzyme activities and oxidative stress markers. Improved impact on drought stress [131]
Spd Foliar sprayed before chilling (0.5 mM) (12 h before chilling)	Cucumber (Cucumis sativus L. cv Jinchun No. 3 and cv Suyo)	Chilling	Reduction of H2O2, ROS, and EL in leaves Alleviation of chilling injury Activities of antioxidant enzymes Improved membrane stability, plant growth [134]
Put, Spd Foliar sprayed (1 mM put, 0.5 mM Spd) (24 h before chilling)	Cucumber (Cucumis sativas L.)	Chilling	Reduction of EL and MDA content Activation of antioxidant enzymes [135]
Spd, Spm, Put Foliar sprayed before chilling (1 mM) (For 12 h daily)	Tomato (Solanum lycopersicum Mill.)	Chilling	Activation of antioxidant enzyme Gene expression (ornithine decarboxylase (ODC), arginine decarboxylase (ADC), and S-adenosylmethionine decarboxylase (SAMDC) Put plays an important role in tomato chilling tolerance [136]

3.2. PAs and Their Roles in Molecular Level

Proteomic and transcriptomic analyses have revealed novel and multifaceted roles for PAs in regulating plant growth, development, and responses to abiotic stress [139]. PAs contribute to ion homeostasis by modulating ion channels, for instance, by inhibiting non-selective cation channels in the tonoplast to limit cytoplasmic Na⁺ influx and stimulating Ca²⁺-ATPases to sustain calcium signaling crucial for stress responses [140]. Additionally, PAs stabilize macromolecules, such as proteins, DNA, and RNA, protect membrane integrity, and act as free radical scavengers under stress conditions [120,123,125,127,141]. A key function of PAs is enhancing antioxidant defense mechanisms. They upregulate enzymes like SOD, POD, and CAT, thereby mitigating oxidative damage caused by ROS [142]. Raziq et al. (2022) [120] demonstrated that exogenous application of Spd in tomato (Solanum lycopersicum) significantly improved heat stress tolerance by enhancing chlorophyll content, membrane stability, and antioxidant enzyme activities. Spd treatment reduced MDA and H₂O₂ levels in heat-stressed seedlings, increased antioxidant activity, and upregulated stress-related gene expression, suggesting a central role in oxidative stress tolerance [143,144].

Notably, Spd modulates gene expression at both transcriptional and post-transcriptional levels. While it generally enhances antioxidant defenses, it was also shown to downregulate CAT under high temperatures [143]. Spd appears to be the most influential agent for heat adaptation among polyamines, evidenced by its elevated concentration in heat-tolerant tomato seedlings [145]. Overexpression of PA biosynthetic genes further supports their critical role in stress responses. In European pear (Pyrus communis L.), transgenic lines exhibited improved osmotic stress tolerance through enhanced antioxidant activity and reduced oxidative markers [146]. Similarly, in Arabidopsis thaliana, overexpression of the ADC2 gene (encoding arginine decarboxylase) led to elevated putrescine levels and improved drought and heat stress tolerance via enhanced ROS scavenging and improved stomatal regulation [147]. In rice, overexpression of OsSAMDC2 increased Spd and Spm levels, which promoted the expression of heat shock proteins (HSPs) and conferred greater thermotolerance during reproductive development [148].

Spd has also been shown to modulate RBOH-dependent H₂O₂ signaling, a key mechanism in both salt and temperature stress responses [120,149]. Elevated PA levels are consistently associated with increased thermotolerance in various crops, making them promising biomarkers for stress resilience [150,151,152]. Beyond their antioxidant and signaling functions, PAs regulate amino acid metabolism and nitrogen flux, influencing stress-induced gene expression and protein biosynthesis [153]. In tomato fruits, Spd alleviated heat stress-induced metabolic disruptions and downregulated stress-responsive genes [154].

A crucial aspect of PA signaling lies in their catabolism. The degradation of PAs by polyamine oxidases and diamine oxidases generates hydrogen peroxide, which acts as a signaling molecule to activate stress-responsive gene networks or, under extreme stress, trigger programmed cell death [155]. Moreover, PAs interact with nitric oxide (NO), another key signaling molecule. This interaction forms a feedback loop that not only regulates PA biosynthesis but also enhances stress responses, further strengthening plant tolerance [23].

Spd also enhanced the expression of multiple stress-related genes, particularly associated with ethylene, hormone signaling (abscisic acid (ABA), jasmonic acid (JA), and gibberellins (GAs)), and polyamine biosynthesis [140,154]. While both PAs and ABA individually promote stomatal closure to mitigate water loss during drought stress, their combined effects can be antagonistic. Liu et al. (2023) [156] demonstrated that, in Vicia faba and Arabidopsis thaliana, polyamines partially inhibited ABA-induced stomatal closure by activating antioxidant enzymes, such as (SOD, POD, and CAT). These enzymes scavenge hydrogen peroxide (H₂O₂), a signaling molecule in ABA pathways, thereby modulating the stomatal response to ABA. Further, polyamines influence ABA biosynthesis by regulating the expression of 9-cis-epoxycarotenoid dioxygenase (NCED), a key enzyme in ABA production. They also modulate ABA-inducible genes, like RD29A and RD29B, enhancing plant tolerance to salt stress [140].

The interplay between polyamines and ethylene is complex and context dependent. In maize under salt stress, increased ethylene levels upregulate diamine oxidase (DAO), leading to the oxidation of Put and the production of H₂O₂. This H₂O₂ not only modulates ethylene production but also stimulates polyamine biosynthesis by upregulating arginine decarboxylase (ADC) expression, creating a feedback loop that fine-tunes stress responses [147]. In rice, water stress during meiosis elevated ethylene production and reduced Spd and Spm levels, contributing to spikelet degeneration. Application of Spd or ethylene synthesis inhibitors mitigated this effect, suggesting an antagonistic relationship between ethylene and polyamine biosynthesis [157].

Polyamines also interact with other hormones, such as jasmonic acid (JA), gibberellins (GAs), and cytokinins (CKs). Under drought stress, studies in cress (Lepidium sativum) revealed that, while levels of ABA, JA, and salicylic acid (SA) increased, polyamine levels decreased, indicating a complex hormonal adjustment to prolonged stress [158]. In Arabidopsis thaliana, inoculation with Bacillus endophyticus J13 under salt stress modulated polyamine and ethylene biosynthesis and enhanced brassinosteroid signaling. This microbial interaction adjusted the expression of key biosynthetic genes, contributing to improved salinity tolerance [159].

3.3. Effects of PAs in Mitigating HS in Tomatoes

PAs have been shown to play a crucial role in plant growth and development [160] especially in tomatoes, as summarized in Table 3. In another study, heat decreased plant height, stem diameter, shoot fresh weight, root fresh weight, and shoot dry weight of tomato by 36.7, 19.6, 31.9, 18.6, and 26.4%, respectively. However, application of exogenous 1 mM Spd remarkably increased plant biomass, and alleviated growth inhibition under the high temperature stress [143]. Some studies have shown that the exogenous application of PAs improved chlorophyll fluorescence properties, hardening, and the activity of PSII [161], photosynthetic rate [127,162,163], maintained Calvin cycle, and photosynthetic carbon assimilation under high-temperature stress [144] (Figure 3.) In a further study, exogenous Spd alleviated levels of Chl a, Chl b, and total Chl (a + b) [143]. The results of another study showed that exogenous Spd significantly alleviated the growth inhibition by regulating the metabolites involved in carbohydrate and N metabolism [164]. Additionally, treatments with Spm induced the opening of stomatal pores and enhanced transpiration in tomato plants [143,164]. This agrees with previous reports proposing Spm as a stomatal regulator [165,166].

Research has consistently shown that, under high temperature stress, ROS level increased significantly, causing a higher MDA level and EL, indicating severe oxidative stress and membrane lipid peroxidation damage. Therefore, under high-temperature stress, PAs can promote photosynthesis by increasing the antioxidant capacity and maintaining the osmotic balance of plants [114,127,143,145,164,167,168,169,170,171]. Nonenzymatic antioxidants, such as ASA and reduced Glutathione (GSH), are crucial for protection of cells from toxic ROS and for maintaining redox balance under environmental stress [143].

PAs could play a key role in tomato plant responses to combined stress and delayed ripening of fruits and HS tolerance [94,172,173]. Gao et al. (2021) [174] reported the role of PAs in fruit development and ripening. The presence of high quantities of PAs delayed ripening and prolonged shelf life in cherry tomato [175] and transgenic tomatoes [173]. PAs also increased the accumulation of lycopene in the tomato plant, since PAs have been described as anti-senescence agents [176], as summarized in Table 3. Generally, many studies have demonstrated that tomato plants treated with Spm improved survival, growth, leaf damage, photosynthesis and PSII function in response to stress [122,125,126,127,177]. Thus, the presence of PAs is a useful biomolecular marker that may be used to forecast sensitivity or tolerance to high temperatures.

Table 3. Effects of exogenous application of PAs on tomato (Lycopersicon esculentum) under HS.

Effectiveness and Plant Response	PAs (Type, Concentration, Application)
Increased plant biomass and growth Alleviated photosynthetic pigments, the levels of Chl a, Chl b, and total Chl (a + b) by 20.1, 21.8, and 20.6%, respectively	(Spd, 1 mM, foliar spray) [143]
Improved chlorophyll fluorescence properties, hardening and the activity of PSII	(Spd, 4 mM, foliar spray) [161]
Enhanced photosynthetic rate	(Put, 1 mM, foliar spray) [121] (Spd, 0.5 mM, root drench) [135] (Spm, 0.25 mM, foliar spray) [149] (Mixture of PAs, 0.5 mM) [150]
Improved the gene expression and activity of key enzymes for N metabolism	(Spd, 1 mM, foliar spray) [164]
Opening of stomatal pores and enhanced transpiration	(Spd, 1 mM, foliar spray) [134,151] (Spd, Put, Spm 1 mM, foliar spray) [152] (Spm, 0.5 mM, foliar spray) [177]
Reduced H2O2 and MDA accumulation, alleviated oxidative damage Increased antioxidant enzymes’ activities, protection of membrane lipid peroxidation ROS scavengers’ osmotic balance	(Spd, Put, Spm 1 mM, foliar spray) [101] (Spm, 1 mM, foliar spray) [121] (Spd, 1 mM, foliar spray) [134,151]
Improved the accumulation of lycopene as an anti-senescence agent in fruit ripening/senescence processes	(Increase polyamine levels by genetic modification) [176]
Increased fruit shelf-life and enhanced fruit juice quality Delayed ripening	(Increase polyamine levels by genetic modification) [94,172,173,174,175]

Table 3. Effects of exogenous application of PAs on tomato (Lycopersicon esculentum) under HS.

Effectiveness and Plant Response	PAs (Type, Concentration, Application)
Increased plant biomass and growth Alleviated photosynthetic pigments, the levels of Chl a, Chl b, and total Chl (a + b) by 20.1, 21.8, and 20.6%, respectively	(Spd, 1 mM, foliar spray) [143]
Improved chlorophyll fluorescence properties, hardening and the activity of PSII	(Spd, 4 mM, foliar spray) [161]
Enhanced photosynthetic rate	(Put, 1 mM, foliar spray) [121] (Spd, 0.5 mM, root drench) [135] (Spm, 0.25 mM, foliar spray) [149] (Mixture of PAs, 0.5 mM) [150]
Improved the gene expression and activity of key enzymes for N metabolism	(Spd, 1 mM, foliar spray) [164]
Opening of stomatal pores and enhanced transpiration	(Spd, 1 mM, foliar spray) [134,151] (Spd, Put, Spm 1 mM, foliar spray) [152] (Spm, 0.5 mM, foliar spray) [177]
Reduced H2O2 and MDA accumulation, alleviated oxidative damage Increased antioxidant enzymes’ activities, protection of membrane lipid peroxidation ROS scavengers’ osmotic balance	(Spd, Put, Spm 1 mM, foliar spray) [101] (Spm, 1 mM, foliar spray) [121] (Spd, 1 mM, foliar spray) [134,151]
Improved the accumulation of lycopene as an anti-senescence agent in fruit ripening/senescence processes	(Increase polyamine levels by genetic modification) [176]
Increased fruit shelf-life and enhanced fruit juice quality Delayed ripening	(Increase polyamine levels by genetic modification) [94,172,173,174,175]

4. Conclusions and Prospects

Tomatoes are particularly sensitive to HS, with flowering and fruit set being the most vulnerable developmental stages. Prolonged exposure to elevated temperatures often leads to significant reductions in yield and fruit quality. Polyamines have demonstrated potential in enhancing thermotolerance by mitigating heat-induced oxidative damage through the activation of antioxidant defense systems, stabilization of cellular membranes, and reduction of ROS accumulation. These protective mechanisms help preserve photosynthetic efficiency and overall plant vitality under HS conditions. Consequently, PAs-based treatments represent a promising strategy for improving plant resilience throughout the tomato life cycle.

However, despite these benefits, the specific developmental stages most responsive to exogenous PA application and the molecular mechanisms underlying PA-mediated thermotolerance remain insufficiently characterized. Future research should focus on evaluating PA effects across key growth stages by integrating gene expression analysis, physiological assessments, and morphological observations under controlled HS conditions. Moreover, recent advances in gene editing technologies, such as CRISPR/Cas9, provide powerful tools for precisely manipulating genes involved in PAs biosynthesis, catabolism, and signaling pathways. Combining these approaches with transcriptomic and physiological profiling could yield critical insights into the regulatory networks of PAs in heat stress adaptation and facilitate the development of tomato cultivars with enhanced heat tolerance.