An overview of heat stress in tomato (Solanum lycopersicum L.)

Saudi J Biol Sci Saudi J Biol Sci 2150 sjbs Saudi Journal of Biological Sciences 1319-562X 2213-7106 Elsevier PMC7938145 PMC7938145.1 7938145 7938145 33732051 10.1016/j.sjbs.2020.11.088 S1319-562X(20)30655-0 1 Review An overview of heat stress in tomato ( Solanum lycopersicum L.) Alsamir Muhammed alsamir.hameed@sydney.edu.au ⁎ Mahmood Tariq Trethowan Richard Ahmad Nabil Plant Breeding Institute, Faculty of Agriculture and Environment, University of Sydney, 107 Cobbitty Road, Cobbitty, NSW 2570, Australia ⁎ Corresponding author at: Plant Breeding Institute, Faculty of Agriculture and Environment, University of Sydney, 107 Cobbitty Road, Cobbitty, NSW 2570, Australia. alsamir.hameed@sydney.edu.au 3 2021 08 12 2020 28 3 376827 1654 1663 28 7 2020 29 11 2020 30 11 2020 08 12 2020 16 03 2021 15 08 2025 © 2020 The Author(s) 2020 https://creativecommons.org/licenses/by-nc-nd/4.0/ This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). Heat stress has been defined as the rise of temperature for a period of time higher than a threshold level, thereby permanently affecting the plant growth and development. Day or night temperature is considered as the major limiting factor for plant growth. Earlier studies reported that night temperature is an important factor in the heat reaction of the plants. Tomato cultivars capable of setting viable fruits under night temperatures above 21 °C are considered as heat-tolerant cultivars. The development of breeding objectives is generally summarized in four points: (a) cultivars with higher yield, (b) disease resistant varieties in the 1970s, (c) long shelf-life in 1980s, and (d) nutritive and taste quality during 1990s. Some unique varieties like the dwarf “Micro-Tom”, and the first transgenic tomato (FlavrSavr) were developed through breeding; they were distributed late in the 1980s. High temperature significantly affects seed, pollen viability and root expansion. Researchers have employed different parameters to evaluate the tolerance to heat stress, including membrane thermo stability, floral characteristics (Stigma exertion and antheridia cone splitting), flower number, and fruit yield per plant. Reports on pollen viability and fruit set/plant under heat stress by comparing the pollen growth and tube development in heat-treated and non-heat-stressed conditions are available in literature. The electrical conductivity (EC) have been used to evaluate the tolerance of some tomato cultivars in vitro under heat stress conditions as an indication of cell damage due to electrolyte leakage; they classified the cultivars into three groups: (a) heat tolerant, (b) moderately heat tolerant, and (c) heat sensitive. It is important to determine the range in genetic diversity for heat tolerance in tomatoes. Heat stress experiments under field conditions offer breeders information to identify the potentially heat tolerant germplasm. Keywords Tomato Heat stress High temperature Stress response Heat shock proteins Tolerance mechanism pmc-status-qastatus 0 pmc-status-live yes pmc-status-embargo no pmc-status-released yes pmc-prop-open-access yes pmc-prop-olf no pmc-prop-manuscript no pmc-prop-legally-suppressed no pmc-prop-has-pdf yes pmc-prop-has-supplement no pmc-prop-pdf-only no pmc-prop-suppress-copyright no pmc-prop-is-real-version no pmc-prop-is-scanned-article no pmc-prop-preprint no pmc-prop-in-epmc yes pmc-license-ref CC BY-NC-ND 1 Introduction Increasing the temperature 10–15 °C above the optimum temperature is generally termed as heat stress or heat shock ( Wahid et al., 2007 ). Heat stress is a multifaceted function that depends on the speed of rise in temperature and the total period ( Blum, 1988 ). The frequency of heat shocks and the duration of high day/night temperature mainly affect the intensity of heat stress in specific climatic zones. Thermotolerance indicates the capability of a plant to survive with extremely high or low temperature and produce economic yield. Cherry tomato ( Solanum lycopersicum var. cerasiforme ), a wild relative of cultivated species, was first found in South America and Mexico ( Bai and Lindhout, 2007 ). Reports show that the tomato crop frequently experiences high temperatures in some parts of the world. Tomato reproduction is extremely sensitive to heat stress. High temperature can cause abortion of the male gametophyte and lead to reduction in fruit set. The expected increase in atmospheric temperature (1.5–11 °C) by 2100 can severely affect crop productivity ( Reddy and Kakani, 2007 , Stainforth et al., 2005 ). Therefore, the reproductive behavior of crop plants under these extreme environments needs to be extensively studied ( Karapanos et al., 2010 ). A small increase in the average atmospheric temperature over the threshold may cause serious hazard to crop production in many parts of the world ( Hall, 2010 ). Tomato ( Solanum lycopersicum L.) belongs to the family Solanaceae, and it is a widely cultivated crop. Mexico, Brazil, Spain, and Italy are the major tomato producing countries where as Belgium and Netherlands lead in yield per hectare ( Tubiello et al., 2013 ). Despite its capability to grow under variable climates, tomato fruit production is affected by high temperature stress because the increase in day/night temperatures above 26/20 °C, respectively, can significantly affect fruit setting and yield ( Lohar and Peat, 1998 ). Rhodes and Hanson (1993) reported that many plant species have developed defense mechanisms to cope with stressful conditions because they have been exposed to various stresses during their evolutionary history and the accumulation of sugars, amino acids, and betaines is one of the strategies that help plants to survive under stressful environments ( Chen and Murata, 2002 ). Tomato was introduced to Europe during the 16th century and it later spread to the Mediterranean area ( Pék and Helyes, 2004 ). Through breeding programs a large number of cultivars have been developed since. With climate change, the priority is to develop heat-tolerant varieties that can survive high temperature and other abiotic stresses. Different from Solanum chilense, commercial tomatoes have limited heat tolerance potential. As a result of global warming, the main threat to crop production in many parts of the world is heat stress ( Sato et al., 2000 , Hedhly et al., 2009 ). Increasing the day temperature above 25 °C significantly decreases fruit numbers, the weight of the fruit, and seed number per fruit ( Peet et al., 1998 ). Short term exposure to extremely high temperature (45 °C) can lead to programmed cell death (PCD), release of cytochrome c , and induced production of caspase-like enzymes ( Qu et al., 2009 ). The reproductive stage in the plant is generally more susceptible to high temperature than the vegetative stage ( Ruan et al., 2010 , Zinn et al., 2010 ). Summer heat stress in many countries terminates tomato production ( Saeed et al., 2007 ). The deficiency of heat tolerance in most tomato cultivars presents a major restriction on growing them in regions where temperatures during part of the growing season, even for short duration, reach 38 °C or higher ( Dinar and Rudich, 1985b , Sung et al., 2003 ). High temperature affects physiological and biochemical development and thus leads to fruit yield reduction ( Singh et al., 2017 , Dinar and Rudich, 1985a ). Tomato plants are sensitive to high temperatures and heat stress can stimulate flower abscission ( Camejo et al., 2005 ) and limit the fruit yield ( Driedonks, 2018 ). Increase in temperature negatively affected the pollen grain, especially at the first stage, leading to poor pollen germination and impaired pollen tube development ( Raja et al., 2019 ). High temperature dose not just reduce the flowering and fruit set of the plant, but also affects the development and maturity of the fruit and consequently reduces the crop yield. High temperature also affects photosynthesis ( Nankishore and Farrell, 2016 , Salvucci and Crafts-Brandner, 2004 , Pareek et al., 2009 ), changes the membrane fluidity, disrupts the general stability of metabolic mechanism, and thus causes over-production of reactive oxygen species and oxidative stress ( Larkindale et al., 2005 ). 2 Tomato responses to heat stress Tomato heat tolerance is a quantitative trait ( Wen et al., 2019 ). A number of studies have evaluated heat tolerance in tomato using various parameters. The phenotypic index is a direct diagnostic tool that can directly reflect the degree of heat damage ( Wu and Zhang, 2013 ). Therefore, the heat injury index is a preferred and the most reliable index for the degree of heat damage to tomato seedlings under high-temperature stress ( Min et al., 2012 ). Membrane damage is a primary symptom of heat injury, and heat tolerance is positively correlated with the electrolytic leakage rate ( Xu et al., 2017 ). Physiological and biochemical indexes ( Siddiqui et al., 2017 , Zhou et al., 2018 ) are also reliable evaluation tools especially that these changes respond faster than morphological changes to high temperature stress. High-temperature stress leads to the inhibition of chlorophyll biosynthesis ( Berova et al., 2013 ); hence, chlorophyll content can also be used as an effective evaluation index for high-temperature stress. In other studies ( Srivastava et al., 2017 ), microscopic observation index has been used in heat tolerance evaluations. 2.1 Pollen development Many studies have focused on the effects of heat stress on pollen development ( Raja et al., 2019 , Pressman et al., 2002 , Firon et al., 2006 , Frank et al., 2009 ). Pressman et al. (2002) reported that heat stress in tomato caused male sterility but that the male sterile plants growing at 29 °C were able to bear fruits once they received pollen developed at 25 °C. In tomato, the pollen germination and pollen tube development are reduced at temperatures above 30 °C ( Vasil, 1987 ). Kakani et al. (2005) reported that the optimal temperature for pollen germination in vitro was 15–22 °C, whereas 25 °C was the best temperature for pollen germination in vivo ( Dempsey, 1970 ). The heat stress significantly affects the male reproductive organs ( Fig. 1 ) as it decreases the number of pollen grains developed and released in the anther, pollen viability, and germination ( Alsamir et al., 2017d , Rieu et al., 2017 ). Fig. 1 The effect of high-temperature on floral structure including the size and morphology of the floral constituents. A-B. LA3847 and LA4284, respectively, showing flowers under control (flower on the left) and heat conditions (flower on the right) without noticeable stigma exsertion under heat. C. LA4256 accession with stigma exsertion and deformation of the style as a sign of sensitivity to heat (flower on the right). D. LA0373 showing stigma exsertion above the anther cone similarly under control and heat conditions. E-G. LA1930 showing the mostly exserted stigmata among all accession. E. Flower with dissected anthredial cone showing the long style exserted above the level of anthers. F. Non-dissected flower showing the exserted stigma. G. Prolific production of self-incompatible flowers with exserted stigmata under control condition. H-I. LA0716 showing exserted stigmata under control and high temperature conditions, respectively ( Alsamir et al., 2017d ). Increasing temperature up to 35 °C damaged both the physiological and biochemical activities of the plant ( Singh et al., 2017 , Al-Khatib and Paulsen, 1999 , Rivero et al., 2001 ). Heat stress reduced flower pollination rate in tomato and thus lead to low fruit setting and low yield; this phenomenon also affected the lycopene content, causing high evaporation and low fruit quality. 2.2 Fruit development Sucrose cleavages enzymes are one of the main compounds found in tomato fruit and are an ideal system to study fruit development under heat stress. Mclaughlin and Boyer (2004) reported that sucrose and cell wall invertase are highly susceptible to abiotic stresses, causing ovary abortion under drought in maize. Li et al. (2011b) reported that high sucrose availability, and invertase activity at the reproductive stage in tomato contributed to heat tolerance in young fruit. 2.3 Fruit production High temperature affects the physiological functions of roots alongside the development of the aboveground plant parts such as fruits. However, plant responses to higher temperatures are difficult to assess by measuring the physiological processes of intact roots, especially when a minor change in root temperature (12 °C to 15 °C) can significantly reduce fruit yield ( Driedonks, 2018 , Bar Tsur et al., 1985 , , 2013 , Sato et al., 2000 ). The high temperature affected the morphology of the tomato flowers and its physiological metabolism, and altered the production of compounds, such as carbohydrates, polyamines, and proline ( Alsamir et al., 2017b , Pressman et al., 2002 , Sato et al., 2006 , Song et al., 2002 ). Changing the temperature to suboptimal temperature conditions significantly affected the reproductive growth of the tomato, causing comparatively higher damage to anthers than to female organs ( Peet et al., 1998 , Sato et al., 2000 , Xu et al., 2017 ). Failure in pollen development causes loss in fruit setting ( Sato et al., 2000 ). Giri et al. (2017) reported that increase in the temperature can decrease root growth, the concentration of nutrient-uptake, nutrient-assimilation proteins, and the rate of nutrient uptake by roots. Heat stress can also change the sink-source association among roots and shoots, which affects the vegetative and the reproductive growth in tomato plants leading to reduced yield and fruit quality ( Abdul-Baki and Stommel, 1995 , Zinn et al., 2010 , Wahid et al., 2007 ). Furthermore, high temperature has been reported to affect floral abortion causing 80% flower loss in tomato plants leading to reduced fruit set ( Ruan et al., 2010 , Rieu et al., 2017 ). Hanson et al. (2002) suggested that the flowering and fruit set are the most important parameters in the evaluation of different tomato cultivars under heat stress as they are very sensitive towards high temperature. Camejo et al. (2005) reported that high temperature affected photosynthetic activity and the subsequent development and maturity of the fruit thereby reducing the crop yield. High temperature significantly affected morpho-physiological parameters, such as plant height, number of branches, and total plant biomass ( Shaheen et al., 2016 ). 2.4 Respiration The relationship between respiration rates and growth rates can affect the balance of physiological activities in the plant and this can help define temperature effects on plant growth. Gary et al. (2003) explained the effects of high temperature on respiration and growth of the tomato plant and reported that the temperature affected both metabolic rates and metabolic efficiency. High and low temperatures not only affected the membrane integrity or enzyme denaturation but also caused loss of substrate carbon level efficiency ( Holladay et al., 2004 ). Loka and Oosterhuis (2010) reported that higher difference between day and night temperatures might increase the seed germination. Heat shock protein 70 is synthesized when the plants are exposed to environmental stresses ( Sung et al., 2001 ). Increasing the night temperature to 30 °C might stimulate mechanisms to fixing damage at 40 °C during the days. 2.5 Nutrient uptake Heat stress affected both the nutrient metabolism and ammonium assimilation in tomatoes ( Giri, 2013 , Hungria and Kaschuk, 2014 ). Bassirirad (2000) reported that many factors causing decrease in nutrient absorption under heat stress including the decrease in root growth or a reduction in nutrient absorption per unit root. 2.6 Cell wall invertase (CWIN) Liu et al. (2016) reported that reduced CWIN activity was observed to be related with poor seed and fruit set under high temperature. They found that the rise of CWIN activity led to automatic cell death in fruits. Firon et al., 2006 , Li et al., 2011b reported that higher CWIN activity in the anther and fruit of tomato plants decreased the fruit abortion under extreme high temperature compared to lower CWIN activity in other cultivars. Additionally, a rise in CWIN activity was noticed in ovary-to-fruit transition ( Palmer et al., 2015 ). 3 Mechanisms of heat tolerance in tomato Chen et al., (2007) reported that one of the basic strategies for the defense and survival of plants under heat stress was the accumulation of proline, sugars, and polyols. Environment changes can cause a significant change in the levels of phenolics and flavonoids contents in tomato ( Ilahy et al., 2016 ). 3.1 Sugar level Sugar level is affected by heat stress treatment in tomatoes ( Harsh et al., 2016 ). Significant variation between the studied genotypes was observed and sugar level reduced in affected pollen grains before anthesis resulting in decreased fruit set and lower accumulation of total sugar ( Raja et al., 2019 , Driedonks, 2018 , Mazzeo et al., 2018 ). Zhou et al., 2017a , Zhou et al., 2017b reported that soluble sugar content increased in the leaves of heat-tolerant tomato plants under heat stress compared with sensitive plants at the flowering and anthesis stages. This was largely because the sensitive genotypes could not regulate carbohydrate synthesis under heat stress. 3.2 Polyamine (PA) changes Polyamines (PAs) are small ubiquitous chemicals that play a key role in the regulation of physiological activities and a range of stress reactions in plants; they accumulate under abiotic stress (heat stress) ( Bouchereau et al., 1999 , Yang et al., 2007 ). Increased PA level significantly increased the protective reaction of plants to different abiotic stresses ( Kumar et al., 2006 ). PA played an important role in abiotic stress tolerance through osmotic modification, membrane stability, and balancing the stomatal movements ( Liu et al., 2007 ). The genetic control of PA metabolism is important to determine its role in drought and salt stress. Increased tolerance to abiotic stress was reported when PA biosynthetic genes were over expressed, including arginine decarboxylase ( Capell et al., 2004 , Masgrau et al., 1997 , Roy and Wu, 2001 ), ornithine decarboxylase ( Kumria and Rajam, 2002 ), S-adenosy-lmethionine decarboxylase ( Torrigiani et al., 2005 ), and spermidine synthase ( Kasukabe et al., 2004 , Kasukabe et al., 2006 ) in rice, tobacco, Arabidopsis , and sweet potato plants. S-Adenosyl- l -methionine decarboxylase (SAMDC) is an important enzyme regulating the biosynthesis of PAs. SAMDC over expression in plants led to improved tolerance to abiotic stresses, such as salt ( Roy and Wu, 2002 ), drought ( Waie and Rajam, 2003 ), acidic oxidative stress ( Wi et al., 2006 ) and heat stress ( Berberich et al., 2015 ). 3.3 Polyphenol oxidase activity Rivero et al. (2001) reported a significant change in metabolite content of phenolics, and enzymatic function under heat stress in tomato. They reported that decreased biomass weight increased the concentration of soluble phenolics, and decreased peroxidase and polyphenol oxidase function under heat stress at 35 °C. 3.4 Fatty acid and cellular membrane Membrane lipid composition changes under heat stress, helping to maintain membrane integrity ( Iba, 2002 ). Liu et al., 2006 , Murakami et al., 2000 reported a rise in concentration of saturated fatty acids in polar lipids involved in protection of membrane integrity in tomato plants. Fatty acids are affected under stress and a change is reflected in membrane-bound proteins, and photosynthetic function and mitochondrial respiration in Arabidopsis ( Kim and Portis, 2005 ). Membrane damage leads to starvation, decreasing the ion mutability, creation of toxic compounds, and rise in oxidative compounds ( Schöffl et al., 1999 , Howarth, 2005 ). Change in saturated fatty acids is one of the important mechanisms in the plant when exposed to heat stress ( Wakita et al., 2001 , Anai et al., 2003 , Orlova et al., 2003 , Sakurai et al., 2003 ). The change in membrane fatty acids help the plant maintain an environment appropriate for the activity of important proteins under heat stress ( Upchurch, 2008 ). High content of polyunsaturated fatty acids, 70% of the total, composed of dienoic and trienoic fatty acids (TAs) are available in the leaf cellular membrane lipids whereas the other fatty acid was found in diverse intracellular membrane systems ( Kodama et al., 1997 , McConn, 1996 , Ohlrogge and Browse, 1995 ). Several authors ( Anai et al., 2003 , Matos et al., 2007 , Orlova et al., 2003 , Zhang et al., 2005 , Kodama et al., 1995 ) reported that Accumulation of TAs in membrane lipids was associated with tolerance under chilling stress. Membrane lipid concentration is an important factor linked to many biological and physiological activities and plays a key role in recovering the chloroplast activity, pollen growth, temperature tolerance and hormone synthesis ( Gibson et al., 1994 , Xu et al., 2017 , Kodama et al., 1995 , McConn, 1996 , Routaboul and Fischer, 2000 ). The continued activity of cellular membranes under stress is necessary for physiological functions, like photosynthesis and respiration ( Blum, 1988 ). Photosystem II (PSII) is very sensitive to the change in temperature and its function significantly declines or stops under heat stress ( Camejo et al., 2005 ), because of the direct effect of heat stress on the thylakoid membranes where PSII is located ( McDonald and Paulsen, 1997 ). Electrolyte leakage has been used in many studies to measure the tolerance and sensitivity towards heat stress and distinguish between the plant genotypes. The thermo stability of the cell membrane affecting the electrolyte leakage has been studied in tomato ( Biswas et al., 2012 ), wheat and barley ( Wahid and Shabbir, 2005 ). The cellular membrane integrity gets decreased and cell electrolytes flow out under heat stress. Bajji et al., (2002) suggested electrolyte leakage as a useful parameter to discriminate between the genotypes under heat stress. Alsadon et al. (2006) used electrical conductivity as a method in detecting genetic variability in heat tolerance by measuring the amount of leakage from injured cells. Kumar et al., 2012 , Wahid et al., 2007 reported a decrease in membrane thermo stability under heat stress in tomato and recorded that the tolerant genotypes had higher membrane thermo stability. 3.5 Glycinebetaine (GB) level Characteristic compatible solutes, in different species, include polyols, sugars, amino acids, betaines, and associated compounds ( , 2013 , Rhodes and Hanson, 1993 ). Glycinebetaine is low-molecular-weight metabolite and plays an important role in tolerance against abiotic stress and helps the plant survive ( , 2013 , Bohnert et al., 1995 , Chen and Murata, 2002 ). McCue and Hanson, 1990 , Bohnert et al., 1995 , Rhodes and Hanson, 1993 reported that under biotic stress the glycinebetaine (GB) level increased rapidly. Accumulation of GB in vivo, in tobacco, led to improved tolerance to heat stress and improved growth and photosynthesis ( Shi et al., 2006 ). Bita and Gerats (2013) reported that maize and sugarcane lines tolerant to high temperature stress had high level of GB. Adcox et al., 2005 , Chen and Murata, 2008 , Park et al., 2006 , Yang and Lu, 2006 reported that exogenous application of GB increased tolerance in maize plants to different abiotic stresses due to heat, drought, salt and freezing. Rivero et al. (2013) found that GB accumulation increased under a combination of heat and salt stress in tomato plants. Einset et al. (2007) exogenously applied GB in Arabidopsis and reported that it improved the genes expression for transcription factors, membrane moving mechanisms, reactive oxygen, and plasma membrane functions. Hayashi et al., 1998 , Yang et al., 2005 , Yang et al., 2007 reported the importance of GB in increasing the heat stress tolerance. GB is important metabolite associated with the activation of HSPs under heat shock and increased the thermo tolerance of the plant, thus clarifying that GB and HSP70 had role in protecting and improving the Krebs cycle enzyme functions. Diamant et al. (2003) stated that GB activated ClpB (HSP100) which helped increase competence for disaggregation of proteins under heat shock ( Chou et al., 1989 , Lin et al., 1984 , Allakhverdiev et al., 2008 , Lui and Shono, 1999 , Sanmiya et al., 2004 ). 3.6 Salicylic acid (SA) Salicylic acid (SA) (2-hydroxybenzoic acid) plays an important role in systemic acquired resistance and hypersensitive response, and contributes to basal and acquired thermo tolerance ( Dat et al., 1998a , Dat et al., 2000 , Lopez-Delgado et al., 1998 ). Salicylic acid was important for plant growth, and resistance responses, and played important role in inducing specific enzymes ( Chen and Gallie, 2006 ). SA regulated the enzyme activity, like biosynthetic enzyme, catalyzed biosynthetic reactions for generating protective compounds ( Solecka and Kacperska, 2003 ). SA standardized the protective enzymes, like SOD and POD, that were important to increase plant’s tolerance to abiotic stresses ( Shim et al., 2003 ). Raskin, 1992 , Conrath et al., 1995 found that SA enhanced induced HSP accumulation in plants. Raskin, 1992 , Snyman and Cronjé, 2008 reported that SA influenced the heat shock response in tomato plant. The phenolic compounds and antioxidative enzymes’ function increased when SA was applied in the Salvia miltiorrhiza cell culture ( Dong et al., 2010 ). Shinwari, et al., (2018) reported increased tomato thermo tolerance when treated with SA. 3.7 Proline level Proline works as an osmolyte and a molecular chaperone regulating the structure of protein and protecting the cells from damage under stress conditions ( Verbruggen and Hermans, 2008 , Szabados and Savouré, 2010 ). Proline accumulated during heat stress in tolerant tomato plant to protect the cell wall from damage ( Mazzeo et al., 2018 ). Claussen, 2005 , Singh et al., 2017 found an increase in the proline level in tomato leaves under heat stress and it was positively associated with the pollen viability. Proline level increased in many plants in response to abiotic stresses, however, in tobacco and Arabidopsis plants, proline did not accumulate under heat stress ( Rizhsky et al., 2004 , Dobra et al., 2010 ).  Gholi-Tolouie et al. (2018) reported an increase in the proline level under biotic stress in tomato leaves. The proline level was controlled by the regulation of biosynthesis and catabolism ( Szabados and Savouré, 2010 ). 3.8 Myo-inositol Myo-inositol plays an important role as a junction position for abiotic and biotic stress responses and its accumulation under abiotic stresses has a positive correlation with plant tolerance to abiotic stress ( Tan et al., 2013 ). 3.9 Gamma-aminobutyric acid (GABA) Gamma-aminobutyric acid (GABA) increased in many plants under heat, osmotic and salt stress as it regulates effector proteins ( Pareek et al., 2009 , Kinnersley and Turano, 2000 ). GABA is mostly created by glutamate decarboxylase in the cytosol, and transferred to the mitochondria. GABA succinic semi-aldehyde dehydrogenase transfer GABA into succinate in the TCA phase ( Fait et al., 2008 , Shelp et al., 1999 ). GABA metabolism was linked with carbon–nitrogen constancy ( Bouche and Fromm, 2004 , Song et al., 2002 ). The role of GABA was important for salt stress tolerance in Arabidopsis thaliana ( Renault et al., 2010 ). 3.10 Abscisic acid (ABA) Abscisic acid (ABA) is an important controller of abiotic stress tolerance and is up-regulated rapidly under stress. ABA has a role in opening and closing of stomata to regulate water loss by transpiration ( Cutler et al., 2010 , Hubbard et al., 2010 , Raghavendra et al., 2010 ). 3.11 Ca 2+ and root uptake Calcium acts as a cellular messenger in plant physiological function, affects the integrity of cell walls, maintains the cell contact, and inhibits ion leakage caused by stress ( Fortes et al., 2017 ). Changing the amount of calcium in the plant tissue is affecting biochemical and physiological proceedings. Hepler (2005) mentioned that calcium looks to be the first transducer of hormonal and ecological indicators. Akula and Ravishankar (2011) reported the increased level of Ca 2+ in the cytoplasm under abiotic stress. They also suggested that induced variations in microsomal membrane role characteristic of enhanced senescence could happen under ecological stresses like physical damage, chilling wound, and heat shock. Heat stress affects negatively root nutrient uptake and nutritional quality which lead to reduced crop production ( Giri et al., 2017 ) The high temperature over a longer period caused lower oxygen availability and led to the root browning, thus affecting membrane integrity ( Fukuoka and Enomoto, 2001 , Wells and Eissenstat, 2002 ). Saidi et al. (2010) reported that high solution temperature in both short and long term treatment affected membrane transport (as it was affected by many environmental factors), and heat stress caused damage to membrane fluidity and permeability of cells. 3.12 Heat shock proteins (HSP) As discussed above, heat shock proteins play an important role in regulating plant thermo tolerance and enhancing the survival of the plant under extreme heat exposure ( Howarth and Ougham, 1993 , Lin et al., 1984 , Vierling, 1991 ). There are two types of thermotolerance; acquired thermotolerance and basal thermotolerance ( Suzuki et al., 2008 ). The capability for acquired thermotolerance can be increased by increasing the expression levels of protective genes before exposing to heat stress ( Larkindale and Vierling, 2008 ). Tomato thermo tolerance is controlled by 21 heat stress transcription factors (Hsfs) ( Scharf et al., 1998 ). Heat stress transcription factor A-2 (HsfA2) and Hsf B1are heat inducible ( Scharf et al., 1998 ), but the activity is organized by HsfA1 playing a role as main controller of the heat shock response ( Mishra et al., 2002 ). Scharf et al., (1998) reported the importance of the collaboration of HsfA2 and HsfA1for the co-localization of HsfA2 in the nucleus. HsfA2 plays a key role for controlling Hsfs under heat stress ( Mishra et al., 2002 ) . The heat stress induced creation of HSP70 and the gene expression of HSP70 in Arabidopsis improved at maturation and germination of seeds under controlled conditions ( Sung et al., 2001 ). HSP70 is important for thermo-tolerance in seed germination ( Su and Li, 2008 ). Li et al. (2011a) found that the increase in night temperatures increased the respiration rate, leading to decreased levels of ATP and carbohydrates. Heat shock proteins70 is created and accumulated in dry seeds of Arabidopsis when plants are under environmental stresses and at seed maturation but they are down-regulated quickly through seed germination ( Sung et al. 2001 ). Giorno et al., 2009 , Sun et al., 2002 reported that the activation of heat shock gene expression through plant growth is more associated with developmental programme than the reaction of the plant under stress conditions. Giorno et al., 2009 , Nover et al., 1989 , Scharf et al., 1998 , Heerklotz et al., 2001 , Heerklotz et al., 2001 , Port et al., 2004 explained the main role of HsfA2 in three phases: (1) a soluble nuclear phase, (2) a soluble cytoplasmic phase, and (3) a stored phase. The development of pollen grain is highly sensitive to heat shock and it is partially due to failure in increase of Hsf and Hsp mRNAs ( Frova et al., 1989 , Gagliardi et al., 1995 , Giorno et al., 2009 , Mascarenhas and Crone, 1996 , Paupière et al., 2017 ). 4 Breeding for high temperature stress Data on global temperatures show a rising trend in temperatures thus making heat stress on tomatoes a critical issue to address. High temperature negatively affects tomato growth resulting in lower yield and productivity ( Sato et al., 2006 ). For a sustainable crop system the understanding of the genetic and physiological responses in tomatoes is crucially important. Tomato being a major vegetable crop is important in terms of its food and economic value. Also the tomato is a suitable model plant species having a moderately compact genome (950 Mb) and genetic linkage map, wide germplasm resources ( http://tgrc.ucdavis.edu ), diploidy, and moderately short life cycle ( Pujar et al., 2013 ). Due to the diversity in germplasm resources and plant characters including photoperiod, flowering and the development of fruits, compound leaves and mycorrhizal roots, it offers itself as an alternative model plant to Arabidopsis thaliana ( Carvalho et al., 2011 ). The massive availability of mutants in tomato is also another beneficial characteristic of a model plant ( Emmanuel and Levy, 2002 ). The modern tomato cultivars may be employed for genomic studies ( Sun et al., 2006 ). The availability of genetic variation in fruit set under heat stress may help selection for heat tolerance. The capacity to tolerate heat stress can be enhanced through modifying the expression levels of “receptive” genes before the heat shock ( Frank et al., 2009 ). The genes conferring stress tolerance are available in germplasm collections, wild relatives, and materials surviving in extreme environments ( Krishna et al., 2019 ). Transgenic technology could be an important tool to improve the tolerance of tomato to heat stress, particularly if combined with conventional approaches. Transgenic technology including transformation and re development procedures and gene editing (CRISPR-CAS9) may play important role in developing the cultivars tolerant to heat stress ( Krishna et al., 2019 , Brooks et al., 2014 ). A limited number of studies to incorporate heat tolerance in tomato are available compared to many more studies aiming tolerance to drought, salt and cold ( Marco et al., 2015 ). Several proteins are reported to be related to enhanced tomato thermo-tolerance ( Cheng et al., 2009 ). The cultivated tomatoes can be enriched with desired traits from wild sources but it is often associated with agronomic inferiority in the offspring. The major complications arise due to the quantitative nature of the traits with many genes involved. Earlier reports ( Grandillo et al., 1999 , Saliba-Colombani et al., 2001 , Van der Knaap and Tanksley, 2003 ) highlighted that yield and yield contributing traits in tomato were the polygenic characters. These reports also indicated the existence of continuous selection pressure for yield related traits through the progression of domestication. The information gained on chromosomal segments related to intricate traits, the simultaneous effects of the chromosomal segments on other characters, or the genetic control of traits (dominance or over-dominance etc.) through conventional breeding is generally insufficient ( Semel et al., 2006 ). Researchers also agree that depending only on phenotypic criteria for selection was less precise under high G × E effects. Identification of genetic markers may improve the selection and breeding of polygenic traits of interest. DNA markers have enabled identification of quantitative trait loci (QTLs) to improve the traits of interest ( Gur and Zamir, 2004 ). Molecular mapping established on crosses between the cultivated tomato and the related wild species is valuable to make use of the variation existing in the available genetic resources. Data on tomato introgression lines assayed for fruit related traits is available ( Gur et al., 2004 ). However, limited molecular work on the effect of heat stress on tomato fruit has been reported. A suitably designed molecular genetics investigation may help identify genes for heat tolerance response in tomato. Ibrahim (2016) reported that the genotypes considered as heat tolerant can make important genetic resource for introgression of heat tolerance genes, and recommended breeding programs to improve the fruit quality using backcross hybridization. Declaration of Competing Interest The authors declared that there is no conflict of interest. References Abdul-Baki A.A. Stommel J.R. Pollen Viability and Fruit Set of Tomato Genotypes under Optimumand High-temperature Regimes HortScience 30 1 1995 115 117 Adcox K. Adler S.S. Afanasiev S. Aidala C. Ajitanand N.N. Akiba Y. Aphecetche L. Formation of dense partonic matter in relativistic nucleus–nucleus collisions at RHIC: experimental evaluation by the PHENIX collaboration Nucl. Phys. A 757 1–2 2005 184 283 Akula R. Ravishankar G.A. Influence of abiotic stress signals on secondary metabolites in plants Plant Signaling Behav. 6 11 2011 1720 1731 10.4161/psb.6.11.17613 PMC3329344 22041989 Al-Khatib K. Paulsen G.M. High-temperature effects on photosynthetic processes in temperate and tropical cereals Crop Sci. 39 1 1999 119 125 Allakhverdiev S.I. Kreslavski V.D. Klimov V.V. Los D.A. Carpentier R. Mohanty P. Heat stress: an overview of molecular responses in photosynthesis Photosynth. Res. 98 1–3 2008 541 18649006 10.1007/s11120-008-9331-0 Alsadon A. Wahb-allah M. Khalil S. In vitro evaluation of heat stress tolerance in some tomato cultivars Journal of King Saud University 2006 Alsamir M. Ahmad N.M. Mahmood T. Trethowan R. Morpho-Physiological Traits Linked to High Temperature Stress Tolerance in Tomato ( S. lycopersicum L.). American Journal of Plant Sciences 8 11 2017 2681 Alsamir M. Ahmad K. C, N.M., Mahmood, T. and Trethowan, R. Identification of High-Temperature Tolerant and Agronomically Viable Tomato (S. lycopersicum) Genotypes from a Diverse Germplasm Collection Advances in crop science and Technology 5 2017 299 Anai T. Koga M. Tanaka H. Kinoshita T. Rahman S.M. Takagi Y. Improvement of rice ( Oryza sativa L.) seed oil quality through introduction of a soybean microsomal omega-3 fatty acid desaturase gene Plant Cell Rep. 21 10 2003 988 992 12835909 10.1007/s00299-003-0609-6 Bai Y. Lindhout P. Domestication and breeding of tomatoes: what have we gained and what can we gain in the future? Ann. Bot. 100 5 2007 1085 1094 17717024 10.1093/aob/mcm150 PMC2759208 Bajji M. Kinet J.-M. Lutts S. The use of the electrolyte leakage method for assessing cell membrane stability as a water stress tolerance test in durum wheat Plant Growth Regul. 36 1 2002 61 70 Bar Tsur A. Rudich J. Bravdo B. High temperature effects on CO2 gas exchange in heat-tolerant and sensitive tomatoes J ournal of the American Society for Horticultural Science 1985 Bassirirad H. Kinetics of nutrient uptake by roots: responses to global change The New Phytologist 147 1 2000 155 169 Berberich T. Sagor G.H.M. Kusano T. Polyamines in plant stress response Polyamines 2015 Springer Tokyo 155 168 Berova M. Stoeva N. Zlatko Z. Ganeva D. Physiological response of some tomato genotypes (Lycopersicon esculentum L.) to high-temperature stress J Cent Eur Agric. 9 2013 723 732 Biswas P. East A. Hewett E. Heyes J. Increase in electrolyte leakage as a function of chilling stress and ripening of tomato Acta Hortic. 945 2012 283 290 Bita, C.E. and Gerats, T. (2013). Plant tolerance to high temperature in a changing environment: scientific fundamentals and production of heat stress-tolerant crops. Frontiers in plant science, 4. 10.3389/fpls.2013.00273 PMC3728475 23914193 Blum A. Plant breeding for stress envirnments/by Abraham Blum (No PA 581 24 1988 B5.) Bohnert H.J. Nelson D.E. Jensen R.G. Adaptations to environmental stresses The plant cell 7 7 1995 1099 12242400 10.1105/tpc.7.7.1099 PMC160917 Bouche N. Fromm H. GABA in plants: just a metabolite? Trends Plant Sci. 9 3 2004 110 115 15003233 10.1016/j.tplants.2004.01.006 Bouchereau A. Aziz A. Larher F. Martin-Tanguy J. Polyamines and environmental challenges: recent development Plant Sci. 140 2 1999 103 125 Brooks C. Nekrasov V. Lippman Z.B. Van Eck J. Efficient gene editing in tomato in the first generation using the clustered regularly interspaced short palindromic repeats/CRISPR-associated9 system Plant Physiol. 166 3 2014 1292 1297 25225186 10.1104/pp.114.247577 PMC4226363 Camejo D. Rodríguez P. Morales M.A. Dell’Amico J.M. Torrecillas A. Alarcón J.J. High temperature effects on photosynthetic activity of two tomato cultivars with different heat susceptibility J. Plant Physiol. 162 3 2005 281 289 15832680 10.1016/j.jplph.2004.07.014 Capell T. Bassie L. Christou P. Modulation of the polyamine biosynthetic pathway in transgenic rice confers tolerance to drought stress PNAS 101 26 2004 9909 9914 15197268 10.1073/pnas.0306974101 PMC470772 Carvalho R.F. Campos M.L. Pino L.E. Crestana S.L. Zsögön A. Lima J.E. Peres L.E. Convergence of developmental mutants into a single tomato model system:'Micro-Tom'as an effective toolkit for plant development research Plant Methods 7 1 2011 18 21714900 10.1186/1746-4811-7-18 PMC3146949 Chen T.H. Murata N. Enhancement of tolerance of abiotic stress by metabolic engineering of betaines and other compatible solutes Curr. Opin. Plant Biol. 5 3 2002 250 257 11960744 10.1016/s1369-5266(02)00255-8 Chen T.H. Murata N. Glycinebetaine: an effective protectant against abiotic stress in plants Trends Plant Sci. 13 9 2008 499 505 18703379 10.1016/j.tplants.2008.06.007 Chen Z. Cuin T.A. Zhou M. Twomey A. Naidu B.P. Shabala S. Compatible solute accumulation and stress-mitigating effects in barley genotypes contrasting in their salt tolerance J. Exp. Bot. 58 15–16 2007 4245 4255 18182428 10.1093/jxb/erm284 Chen Z. Gallie D.R. Dehydroascorbate reductase affects leaf growth, development, and function Plant Physiol. 142 2 2006 775 787 16891549 10.1104/pp.106.085506 PMC1586046 Cheng L. Zou Y. Ding S. Zhang J. Yu X. Cao J. Lu G. Polyamine accumulation in transgenic tomato enhances the tolerance to high temperature stress J. Integr. Plant Biol. 51 5 2009 489 499 19508360 10.1111/j.1744-7909.2009.00816.x Chou M. Chen Y.-M. Lin C.-Y. Thermotolerance of isolated mitochondria associated with heat shock proteins Plant Physiol. 89 2 1989 617 621 16666591 10.1104/pp.89.2.617 PMC1055890 Claussen W. Proline as a measure of stress in tomato plants Plant Sci. 168 1 2005 241 248 Conrath U. Chen Z. Ricigliano J.R. Klessig D.F. Two inducers of plant defense responses, 2, 6-dichloroisonicotinec acid and salicylic acid, inhibit catalase activity in tobacco Proc. Natl. Acad. Sci. 92 16 1995 7143 7147 11607566 10.1073/pnas.92.16.7143 PMC41295 Cutler S.R. Rodriguez P.L. Finkelstein R.R. Abrams S.R. Abscisic acid: emergence of a core signaling network Annu. Rev. Plant Biol. 61 2010 651 679 20192755 10.1146/annurev-arplant-042809-112122 Dat J.F. Foyer C.H. Scott I.M. Changes in salicylic acid and antioxidants during induced thermotolerance in mustard seedlings Plant Physiol. 118 4 1998 1455 1461 9847121 10.1104/pp.118.4.1455 PMC34763 Dat J.F. Lopez-Delgado H. Foyer C.H. Scott I.M. Effects of salicylic acid on oxidative stress and thermotolerance in tobacco J. Plant Physiol. 156 5 2000 659 665 Dempsey W. Effects of temperature on pollen germination and tube growth Rep. Tomato Genet. Coop 20 1970 15 16 Diamant S. Rosenthal D. Azem A. Eliahu N. Ben-Zvi A.P. Goloubinoff P. Dicarboxylic amino acids and glycine-betaine regulate chaperone-mediated protein-disaggregation under stress Mol. Microbiol. 49 2 2003 401 410 12828638 10.1046/j.1365-2958.2003.03553.x Dinar M. Rudich J. Effect of heat stress on assimilate metabolism in tomato flower buds Ann. Bot. 56 2 1985 249 257 Dinar M. Rudich J. Effect of heat stress on assimilate partitioning in tomato Ann. Bot. 56 2 1985 239 248 Dobra J. Motyka V. Dobrev P. Malbeck J. Prasil I.T. Haisel D. Vankova R. Comparison of hormonal responses to heat, drought and combined stress in tobacco plants with elevated proline content J. Plant Physiol. 167 16 2010 1360 1370 20619485 10.1016/j.jplph.2010.05.013 Dong J. Wan G. Liang Z. Accumulation of salicylic acid-induced phenolic compounds and raised activities of secondary metabolic and antioxidative enzymes in Salvia miltiorrhiza cell culture J. Biotechnol. 148 2 2010 99 104 20576504 10.1016/j.jbiotec.2010.05.009 Driedonks N.J.W. From flower to fruit in the heat-Reproductive thermotolerance in tomato and its wild relatives(Doctoral dissertation [Sl sn]) 2018 Einset J. Nielsen E. Connolly E.L. Bones A. Sparstad T. Winge P. Zhu J.K. Membrane-trafficking RabA4c involved in the effect of glycine betaine on recovery from chilling stress in Arabidopsis Physiol. Plant. 130 4 2007 511 518 Emmanuel E. Levy A.A. Tomato mutants as tools for functional genomics Curr. Opin. Plant Biol. 5 2 2002 112 117 11856605 10.1016/s1369-5266(02)00237-6 Fait A. Fromm H. Walter D. Galili G. Fernie A.R. Highway or byway: the metabolic role of the GABA shunt in plants Trends Plant Sci. 13 1 2008 14 19 18155636 10.1016/j.tplants.2007.10.005 Firon N. Shaked R. Peet M.M. Pharr D.M. Zamski E. Rosenfeld K. Pressman E. Pollen grains of heat tolerant tomato cultivars retain higher carbohydrate concentration under heat stress conditions Sci. Hortic. 109 3 2006 212 217 Fortes A.M. Granell A. Pezzotti M. Bouzayen M. Molecular and Metabolic Mechanisms Associated with Fleshy Fruit Quality Front. Plant Sci. 8 2017 1236 28751907 10.3389/fpls.2017.01236 PMC5507992 Frank G. Pressman E. Ophir R. Althan L. Shaked R. Freedman M. Firon N. Transcriptional profiling of maturing tomato ( Solanum lycopersicum L.) microspores reveals the involvement of heat shock proteins, ROS scavengers, hormones, and sugars in the heat stress response J. Exp. Bot. 60 13 2009 3891 3908 19628571 10.1093/jxb/erp234 PMC2736902 Frova C. Taramino G. Binelli G. Heat-shock proteins during pollen development in maize Dev. Genet. 10 4 1989 324 332 Fukuoka N. Enomoto T. The occurrence of internal browning induced by high soil temperature treatment and its physiological function in Raphanus root Plant Sci. 161 1 2001 117 124 Gagliardi D. Breton C. Chaboud A. Vergne P. Dumas C. Expression of heat shock factor and heat shock protein 70 genes during maize pollen development Plant Mol. Biol. 29 4 1995 841 856 8541509 10.1007/BF00041173 Gary C. Baldet P. Bertin N. Devaux C. Tchamitchian M. Raymond P. Time-course of tomato whole-plant respiration and fruit and stem growth during prolonged darkness in relation to carbohydrate reserves Ann. Bot. 91 4 2003 429 438 12588722 10.1093/aob/mcg037 PMC4241059 Gholi-Tolouie S. Davari M. Sokhandan-Bashir N. Sedghi M. Influence of salicylic and jasmonic acids on the antioxidant systems of tomato ( Solanum lycopersicum cv. Superchief ) plants under biotic stresses Plant Physiol. 8 2 2018 2345 2351 Gibson S. Arondel V. Iba K. Somerville C. Cloning of a Temperature-Regulated Gene Encoding a Chloroplast [omega]-3 Desaturase from Arabidopsis thaliana Plant Physiol. 106 4 1994 1615 1621 7846164 10.1104/pp.106.4.1615 PMC159705 Giorno F. Wolters-Arts M. Grillo S. Scharf K.D. Vriezen W.H. Mariani C. Developmental and heat stress-regulated expression of HsfA2 and small heat shock proteins in tomato anthers J. Exp. Bot. 61 2 2009 453 462 19854799 10.1093/jxb/erp316 PMC2803211 Giri A. Effect of acute heat stress on nutrient uptake by plant roots 2013 The University of Toledo Giri A. Heckathorn S. Mishra S. Krause C. Heat Stress Decreases Levels of Nutrient-Uptake and-Assimilation Proteins in Tomato Roots Plants 6 1 2017 6 10.3390/plants6010006 PMC5371765 28106834 Grandillo S. Ku H. Tanksley S. Identifying the loci responsible for natural variation in fruit size and shape in tomato Theor. Appl. Genet. 99 6 1999 978 987 Gur A. Semel Y. Cahaner A. Zamir D. Real time QTL of complex phenotypes in tomato interspecific introgression lines Trends Plant Sci. 9 3 2004 107 109 15058274 10.1016/j.tplants.2004.01.003 Gur A. Zamir D. Unused natural variation can lift yield barriers in plant breeding PLoS Biol. 2 10 2004 e245 15328532 10.1371/journal.pbio.0020245 PMC514488 Hall A.E. Crop responses to environment 2010 CRC Press Hanson P.M. Chen J.-T. Kuo G. Gene action and heritability of high-temperature fruit set in tomato line CL5915 HortScience 37 1 2002 172 175 Harsh A. Sharma Y.K. Joshi U. Rampuria S. Singh G. Kumar S. Sharma R. Effect of short-term heat stress on total sugars, proline and some antioxidant enzymes in moth bean ( Vigna aconitifolia ) Annals of Agricultural Sciences 61 1 2016 57 64 Hayashi H. Sakamoto A. Murata N. Enhancement of the tolerance of Arabidopsisto high temperatures by genetic engineering of the synthesis of glycinebetaine Plant J. 16 2 1998 155 161 9839462 10.1046/j.1365-313x.1998.00284.x Hedhly A. Hormaza J. Herrero M. Flower emasculation accelerates ovule degeneration and reduces fruit set in sweet cherry Sci. Hortic. 119 4 2009 455 457 Heerklotz D. Döring P. Bonzelius F. Winkelhaus S. Nover L. The balance of nuclear import and export determines the intracellular distribution and function of tomato heat stress transcription factor HsfA2 Mol. Cell. Biol. 21 5 2001 1759 1768 11238913 10.1128/MCB.21.5.1759-1768.2001 PMC86729 Hepler P.K. Calcium: a central regulator of plant growth and development Plant Cell 17 8 2005 2142 2155 16061961 10.1105/tpc.105.032508 PMC1182479 Holladay J.D. Jones E.O. Dagle R.A. Xia G.G. Cao C. Wang Y. High efficiency and low carbon monoxide micro-scale methanol processors J. Power Sources 131 1–2 2004 69 72 Howarth C. Genetic improvements of tolerance to high temperature Abiotic stresses: plant resistance through breeding and molecular approaches 2005 Howarth Press Inc. New York Howarth C.J. Ougham H.J. Gene expression under temperature stress New Phytol. 125 1 1993 1 26 10.1111/j.1469-8137.1993.tb03862.x 33874620 Hubbard K.E. Nishimura N. Hitomi K. Getzoff E.D. Schroeder J.I. Early abscisic acid signal transduction mechanisms: newly discovered components and newly emerging questions Genes Dev. 24 16 2010 1695 1708 20713515 10.1101/gad.1953910 PMC2922499 Hungria M. Kaschuk G. Regulation of N 2 fixation and NO 3−/NH 4+ assimilation in nodulated and N-fertilized Phaseolus vulgaris L. exposed to high temperature stress Environ. Exp. Bot. 98 2014 32 39 Iba K. Acclimative response to temperature stress in higher plants: approaches of gene engineering for temperature tolerance Annu. Rev. Plant Biol. 53 1 2002 225 245 12221974 10.1146/annurev.arplant.53.100201.160729 Ibrahim E. Tomato breeding for heat stress conditions European Journal of Academic Essays 3 2 2016 87 93 Ilahy R. Siddiqui M.W. Piro G. Lenucci M.S. Hdider C. Year-to-year variations in antioxidant components of high-lycopene tomato ( Solanum lycopersicum L.) breeding lines. Turkish Journal of Agriculture-Food Science and Technology 4 6 2016 486 492 Kakani V.G. Reddy K.R. Koti S. Wallace T.P. Prasad P.V.V. Reddy V.R. Zhao D. Differences in in vitro pollen germination and pollen tube growth of cotton cultivars in response to high temperature Ann. Bot. 96 1 2005 59 67 15851397 10.1093/aob/mci149 PMC4246808 Karapanos I. Akoumianakis K. Olympios C. Passam H.C. Tomato pollen respiration in relation to in vitro germination and pollen tube growth under favourable and stress-inducing temperatures Sex. Plant Reprod. 23 3 2010 219 224 20063191 10.1007/s00497-009-0132-1 Kasukabe Y. He L. Nada K. Misawa S. Ihara I. Tachibana S. Overexpression of spermidine synthase enhances tolerance to multiple environmental stresses and up-regulates the expression of various stress-regulated genes in transgenic Arabidopsis thaliana Plant Cell Physiol. 45 6 2004 712 722 15215506 10.1093/pcp/pch083 Kasukabe Y. He L. Watakabe Y. Otani M. Shimada T. Tachibana S. Improvement of environmental stress tolerance of sweet potato by introduction of genes for spermidine synthase Plant Biotechnology 23 1 2006 75 83 Kim K. Portis A.R. Temperature dependence of photosynthesis in Arabidopsis plants with modifications in Rubisco activase and membrane fluidity Plant Cell Physiol. 46 3 2005 522 530 15695447 10.1093/pcp/pci052 Kinnersley A.M. Turano F.J. Gamma aminobutyric acid (GABA) and plant responses to stress Crit. Rev. Plant Sci. 19 6 2000 479 509 Kodama H. Akagi H. Kusumi K. Fujimura T. Iba K. Structure, chromosomal location and expression of a rice gene encoding the microsome ω-3 fatty acid desaturase Plant Mol. Biol. 33 3 1997 493 502 9049269 10.1023/a:1005726210977 Kodama H. Horiguchi G. Nishiuchi T. Nishimura M. Iba K. Fatty acid desaturation during chilling acclimation is one of the factors involved in conferring low-temperature tolerance to young tobacco leaves Plant Physiol. 107 4 1995 1177 1185 12228424 10.1104/pp.107.4.1177 PMC157250 Krishna R. Karkute S.G. Ansari W.A. Jaiswal D.K. Verma J.P. Singh M. Transgenic tomatoes for abiotic stress tolerance: status and way ahead. 3 Biotech 9 4 2019 143 10.1007/s13205-019-1665-0 PMC6423223 30944790 Kumar R.R. Goswami S. Sharma S.K. Singh K. Gadpayle K.A. Kumar N. Rai R.D. Protection against heat stress in wheat involves change in cell membrane stability, antioxidant enzymes, osmolyte, H2O2 and transcript of heat shock protein International Journal of Plant Physiology and Biochemistry 4 4 2012 83 91 Kumar S.V. Sharma M. Rajam M. Polyamine biosynthetic pathway as a novel target for potential applications in plant biotechnology P hysiology and Molecular Biology of Plants 12 1 2006 13 Kumria R. Rajam M.V. Ornithine decarboxylase transgene in tobacco affects polyamines in vitro, morphogenesis and response to salt stress J ournal of plant physiology 159 9 2002 983 990 Larkindale J. Hall J.D. Knight M.R. Vierling E. Heat stress phenotypes of Arabidopsis mutants implicate multiple signaling pathways in the acquisition of thermotolerance Plant Physiol. 138 2 2005 882 897 15923322 10.1104/pp.105.062257 PMC1150405 Larkindale J. Vierling E. Core genome responses involved in acclimation to high temperature Plant Physiol. 146 2 2008 748 761 18055584 10.1104/pp.107.112060 PMC2245833 Li S. Li F. Wang J. Zhang W.E.N. Meng Q. Chen T.H. Yang X. Glycinebetaine enhances the tolerance of tomato plants to high temperature during germination of seeds and growth of seedlings Plant, Cell Environ. 34 11 2011 1931 1943 21711358 10.1111/j.1365-3040.2011.02389.x Li Z. Palmer W.M. Martin A.P. Wang R. Rainsford F. Jin Y. Ruan Y.L. High invertase activity in tomato reproductive organs correlates with enhanced sucrose import into, and heat tolerance of, young fruit J. Exp. Bot. 63 3 2011 1155 1166 22105847 10.1093/jxb/err329 PMC3276082 Lin C.-Y. Roberts J. Key J.L. Acquisition of thermotolerance in soybean seedlings synthesis and accumulation of heat shock proteins and their cellular localization Plant Physiol. 74 1 1984 152 160 16663370 10.1104/pp.74.1.152 PMC1066642 Liu J.-H. Kitashiba H. Wang J. Ban Y. Moriguchi T. Polyamines and their ability to provide environmental stress tolerance to plants Plant Biotechnology 24 1 2007 117 126 Liu X.Y. Yang J.H. Li B. Yang X.M. Meng Q.W. Antisense-Mediated Depletion of Tomato Chloroplast Omega-3 Fatty Acid Desaturase Enhances Thermal Tolerance J. Integr. Plant Biol. 48 9 2006 1096 1107 10.1111/j.1744-7909.2010.00957.x 20590987 Liu Y.-H. Offler C.E. Ruan Y.-L. Cell Wall Invertase Promotes Fruit Set under Heat Stress by Suppressing ROS-Independent Cell Death Plant Physiol. 172 1 2016 163 180 27462084 10.1104/pp.16.00959 PMC5074634 Lohar D. Peat W. Floral characteristics of heat-tolerant and heat-sensitive tomato ( Lycopersicon esculentum Mill.) cultivars at high temperature Sci. Hortic. 73 1 1998 53 60 Loka D. Oosterhuis D. Effect of high night temperatures on cotton respiration, ATP levels and carbohydrate content Environ. Exp. Bot. 68 3 2010 258 263 Lopez-Delgado H. Dat J.F. Foyer C.H. Scott I.M. Induction of thermotolerance in potato microplants by acetylsalicylic acid and H2O2 J. Exp. Bot. 49 321 1998 713 720 Lui J. Shono M. Characterization of mitochondria-located small heat shock protein from tomato ( Lycopersicon esculentum ) P lant and Cell Physiology 40 12 1999 1297 1304 10682350 10.1093/oxfordjournals.pcp.a029518 Marco F. Bitrián M. Carrasco P. Rajam M.V. Alcázar R. Tiburcio A.F. Genetic engineering strategies for abiotic stress tolerance in plants Plant biology and biotechnology 2015 Springer New Delhi 579 609 Mascarenhas J.P. Crone D.E. Pollen and the heat shock response Sex. Plant Reprod. 9 6 1996 370 374 Masgrau C. Altabella T. Farrás R. Flores D. Thompson A.J. Besford R.T. Tiburcio A.F. Inducible overexpression of oat arginine decarboxylase in transgenic tobacco plants Plant J. 11 3 1997 465 473 9107036 10.1046/j.1365-313x.1997.11030465.x Matos A.R. Hourton-Cabassa C. Ciçek D. Rezé N. Arrabaça J.D. Zachowski A. Moreau F. Alternative oxidase involvement in cold stress response of Arabidopsis thaliana fad2 and FAD3+ cell suspensions altered in membrane lipid composition plant and Cell Physiology 48 6 2007 856 865 June 2007 17507388 10.1093/pcp/pcm061 Mazzeo M.F. Cacace G. Iovieno P. Massarelli I. Grillo S. Siciliano R.A. Response mechanisms induced by exposure to high temperature in anthers from thermo-tolerant and thermo-sensitive tomato plants: A proteomic perspective PloS one 13 7 2018 e0201027 30024987 10.1371/journal.pone.0201027 PMC6053223 McConn M. The critical requirement for linolenic acid is pollen development, not photosynthesis, in an Arabidopsis mutant. The Plant Cell Online 8 3 1996 403 416 10.1105/tpc.8.3.403 PMC161109 12239389 McCue K.F. Hanson A.D. Drought and salt tolerance: towards understanding and application Trends Biotechnol. 8 1990 358 362 McDonald G.K. Paulsen G. High temperature effects on photosynthesis and water relations of grain legumes Plant Soil 196 1 1997 47 58 McLAUGHLIN J.E. Boyer J.S. Sugar-responsive gene expression, invertase activity, and senescence in aborting maize ovaries at low water potentials Ann. Bot. 94 5 2004 675 689 15355866 10.1093/aob/mch193 PMC4242214 Min L.S. Xiang Z.W. Ya L.L. Liu Y.Z. Han Y.P. Guang W. Heat tolerance identification of six tomato varieties Northern Hortic (Chinese). 21 2012 5 7 Mishra S.K. Tripp J. Winkelhaus S. Tschiersch B. Theres K. Nover L. Scharf K.D. In the complex family of heat stress transcription factors, HsfA1 has a unique role as master regulator of thermotolerance in tomato Genes Dev. 16 12 2002 1555 1567 12080093 10.1101/gad.228802 PMC186353 Murakami Y. Tsuyama M. Kobayashi Y. Kodama H. Iba K. Trienoic fatty acids and plant tolerance of high temperature Science 287 5452 2000 476 479 10642547 10.1126/science.287.5452.476 Nankishore A. Farrell A.D. The response of contrasting tomato genotypes to combined heat and drought stress J. Plant Physiol. 202 2016 75 82 27467552 10.1016/j.jplph.2016.07.006 Nover L. Scharf K.-D. Neumann D. Cytoplasmic heat shock granules are formed from precursor particles and are associated with a specific set of mRNAs Mol. Cell. Biol. 9 3 1989 1298 1308 2725500 10.1128/mcb.9.3.1298 PMC362722 Ohlrogge J. Browse J. Lipid biosynthesis Plant Cell 7 7 1995 957 7640528 10.1105/tpc.7.7.957 PMC160893 Orlova I.V. Serebriiskaya T.S. Popov V. Merkulova N. Nosov A.M. Trunova T.I. Los D.A. Transformation of tobacco with a gene for the thermophilic acyl-lipid desaturase enhances the chilling tolerance of plants Plant Cell Physiol. 44 4 2003 447 450 12721386 10.1093/pcp/pcg047 Palmer W.M. Ru L. Jin Y. Patrick J.W. Ruan Y.-L. Tomato ovary-to-fruit transition is characterized by a spatial shift of mRNAs for cell wall invertase and its inhibitor with the encoded proteins localized to sieve elements Molecular plant 8 2 2015 315 328 25680776 10.1016/j.molp.2014.12.019 Park E.-J. Jeknic Z. Chen T.H. Exogenous application of glycinebetaine increases chilling tolerance in tomato plants Plant Cell Physiol. 47 6 2006 706 714 16608869 10.1093/pcp/pcj041 Pareek A. Sopory S.K. Bohnert H.J. Abiotic stress adaptation in plants 2009 Springer University of Illinois at Urbana-USA Paupière M.J. Screening for pollen tolerance to high temperatures in tomato Euphytica 213 6 2017 130 Peet M. Sato S. Gardner R. Comparing heat stress effects on male-fertile and male-sterile tomatoes Plant, Cell Environ. 21 2 1998 225 231 Pék Z. Helyes L. The effect of daily temperature on truss flowering rate of tomato J. Sci. Food Agric. 84 13 2004 1671 1674 Port M. Tripp J. Zielinski D. Weber C. Heerklotz D. Winkelhaus S. Scharf K.D. Role of Hsp17. 4-CII as coregulator and cytoplasmic retention factor of tomato heat stress transcription factor HsfA2 Plant Physiol. 135 3 2004 1457 1470 15247379 10.1104/pp.104.042820 PMC519062 Pressman E. Peet M.M. Pharr D.M. The effect of heat stress on tomato pollen characteristics is associated with changes in carbohydrate concentration in the developing anthers Ann. Bot. 90 5 2002 631 636 12466104 10.1093/aob/mcf240 PMC4240456 Pujar, A., Menda, N., Bombarely, A., Edwards, J. D., Strickler, S. R., & Mueller, L. A. (2013). From manual curation to visualization of gene families and networks across Solanaceae plant species. Database, 2013. 10.1093/database/bat028 PMC3655285 23681907 Qu G.Q. Liu X. Zhang Y.L. Yao D. Ma Q.M. Yang M.Y. Luo Y.B. Evidence for programmed cell death and activation of specific caspa se-like enzymes in the tomato fruit heat stress response Planta 229 6 2009 1269 1279 19296126 10.1007/s00425-009-0908-4 Raghavendra A.S. Gonugunta V.K. Christmann A. Grill E. ABA perception and signalling T rends in plant science 15 7 2010 395 401 20493758 10.1016/j.tplants.2010.04.006 Raja M.M. Vijayalakshmi G. Naik M.L. Basha P.O. Sergeant K. Hausman J.F. Khan P.S.S.V. Pollen development and function under heat stress: from effects to responses Acta Physiologiae Plantarum 41 4 2019 47 Raskin I. Salicylate, a new plant hormone Plant Physiol. 99 3 1992 799 16669002 10.1104/pp.99.3.799 PMC1080546 Reddy K.R. Kakani V.G. Screening Capsicum species of different origins for high temperature tolerance by in vitro pollen germination and pollen tube length Sci. Hortic. 112 2 2007 130 135 Renault H. Roussel V. El Amrani A. Arzel M. Renault D. Bouchereau A. Deleu C. The Arabidopsis pop2-1 mutant reveals the involvement of GABA transaminase in salt stress tolerance BMC Plant Biol. 10 1 2010 20 20122158 10.1186/1471-2229-10-20 PMC2825238 Rhodes D. Hanson A. Quaternary ammonium and tertiary sulfonium compounds in higher plants Annu. Rev. Plant Biol. 44 1 1993 357 384 Rieu, I., Twell, D. and Firon, N.(2017). Pollen development at high temperature: From acclimation to collapse. Plant Physiology: pp. 01644.2016. 10.1104/pp.16.01644 PMC5373052 28246296 Rivero R.M. Ruiz J.M. Garcıa P.C. Lopez-Lefebre L.R. Sánchez E. Romero L. Resistance to cold and heat stress: accumulation of phenolic compounds in tomato and watermelon plants Plant Sci. 160 2 2001 315 321 11164603 10.1016/s0168-9452(00)00395-2 Rivero R.M. Mestre T.C. Mittler R. Rubio F. Garcia-Sanchez F. Martinez V. The combined effect of salinity and heat reveals a specific physiological, biochemical and molecular response in tomato plants Plant Cell Environ 37 2013 1059 1073 24028172 10.1111/pce.12199 Rizhsky L. Liang H. Shuman J. Shulaev V. Davletova S. Mittler R. When defense pathways collide. The response of Arabidopsis to a combination of drought and heat stress Plant Physiol. 134 4 2004 1683 1696 15047901 10.1104/pp.103.033431 PMC419842 Routaboul J.-M. Fischer S.F. Trienoic fatty acids are required to maintain chloroplast function at low temperatures Plant Physiol. 124 4 2000 1697 1705 11115886 10.1104/pp.124.4.1697 PMC59867 Roy M. Wu R. Arginine decarboxylase transgene expression and analysis of environmental stress tolerance in transgenic rice Plant Sci. 160 5 2001 869 875 11297783 10.1016/s0168-9452(01)00337-5 Roy M. Wu R. Overexpression of-adenosylmethionine decarboxylase gene in rice increases polyamine level and enhances sodium chloride-stress tolerance P lant Science 163 5 2002 987 992 Ruan Y.-L. Jin Y. Yang Y.-J. Li G.-J. Boyer J.S. Sugar input, metabolism, and signaling mediated by invertase: roles in development, yield potential, and response to drought and heat Molecular Plant 3 6 2010 942 955 20729475 10.1093/mp/ssq044 Saeed A. Hayat K. Khan A.A. Iqbal S. Heat tolerance studies in tomato ( Lycopersicon esculentum Mill.) Int. J. Agri. Biol 9 4 2007 649 652 Saidi Y. Peter M. Finka A. Cicekli C. Vigh L. Goloubinoff P. Membrane lipid composition affects plant heat sensing and modulates Ca2+-dependent heat shock response Plant Signaling Behav. 5 12 2010 1530 1533 10.4161/psb.5.12.13163 PMC3115095 21139423 Sakurai E. Taguchi H. Anand A. Ambati B.K. Gragoudas E.S. Miller J.W. Ambati J. Targeted disruption of the CD18 or ICAM-1 gene inhibits choroidal neovascularization Invest. Ophthalmol. Vis. Sci. 44 6 2003 2743 2749 12766082 10.1167/iovs.02-1246 Saliba-Colombani V. Causse M. Langlois D. Philouze J. Buret M. Genetic analysis of organoleptic quality in fresh market tomato. 1. Mapping QTLs for physical and chemical traits Theor. Appl. Genet. 102 2–3 2001 259 272 Salvucci M.E. Crafts-Brandner S.J. Relationship between the heat tolerance of photosynthesis and the thermal stability of Rubisco activase in plants from contrasting thermal environments Plant Physiol. 134 4 2004 1460 1470 15084731 10.1104/pp.103.038323 PMC419822 Sanmiya K. Suzuki K. Egawa Y. Shono M. Mitochondrial small heat-shock protein enhances thermotolerance in tobacco plants FEBS Lett. 557 1 2004 265 268 14741379 10.1016/s0014-5793(03)01494-7 Sato S. Kamiyama M. Iwata T. Makita N. Furukawa H. Ikeda H. Moderate increase of mean daily temperature adversely affects fruit set of Lycopersicon esculentum by disrupting specific physiological processes in male reproductive development Ann. Bot. 97 5 2006 731 738 16497700 10.1093/aob/mcl037 PMC2803419 Sato S. Peet M. Thomas J. Physiological factors limit fruit set of tomato ( Lycopersicon esculentum Mill.) under chronic, mild heat stress Plant, Cell Environ. 23 7 2000 719 726 Scharf K.-D. Höhfeld I. Nover L. Heat stress response and heat stress transcription factors J. Biosci. 23 4 1998 313 329 Schöffl, F., Prandl, R. and Reindl, A.(1999). Molecular responses to heat stress. Molecular responses to cold, drought, heat and salt stress in higher plants. RG Landes Co., Austin, Texas: 81-98. Semel Y. Nissenbaum J. Menda N. Zinder M. Krieger U. Issman N. Zamir D. Overdominant quantitative trait loci for yield and fitness in tomato Proc. Natl. Acad. Sci. 103 35 2006 12981 12986 16938842 10.1073/pnas.0604635103 PMC1552043 Shaheen M.R. Ayyub C.M. Amjad M. Waraich E.A. Morpho-physiological evaluation of tomato genotypes under high temperature stress conditions J. Sci. Food Agric. 96 8 2016 2698 2704 26304011 10.1002/jsfa.7388 Shelp B.J. Bown A.W. McLean M.D. Metabolism and functions of gamma-aminobutyric acid Trends Plant Sci. 4 11 1999 446 452 10529826 10.1016/s1360-1385(99)01486-7 Shi L. The MicroArray Quality Control (MAQC) project shows inter-and intraplatform reproducibility of gene expression measurements Nat. Biotechnol. 24 9 2006 1151 1161 16964229 10.1038/nbt1239 PMC3272078 Shim I.-S. Momose Y. Yamamoto A. Kim D.-W. Usui K. Inhibition of catalase activity by oxidative stress and its relationship to salicylic acid accumulation in plants Plant Growth Regul. 39 3 2003 285 292 Shinwari A. Ahmad I. Khan I. Thermo-Tolerance in Tomato: Acetyl Salicylic Acid Affects Growth and Yield of Tomato ( Solanum Lycopersicum L.) Under the Agro-Climatic Condition of Islamabad, Pakistan. Adv Agr Environ Sci 1 3 2018 102 107 Siddiqui M.H. Alamri S.A. Al-Khaishany M.Y.Y. Al-Qutami M.A. Ali H.M. Khan M.N. Nitric oxide and calcium induced physio-biochemical changes in tomato (Solanum lycopersicum L.) plant under high-temperature stress Fresen Environ Bull. 26 2017 1663 1672 Singh A.K. Singh M.K. Singh V. Singh R. Raghuvanshi T. Singh C. Debilitation in tomato ( Solanum lycopersicum L.) as result of heat stress J ournal of Pharmacognosy and Phytochemistry 6 6 2017 1917 1922 Snyman M. Cronjé M. Modulation of heat shock factors accompanies salicylic acid-mediated potentiation of Hsp70 in tomato seedlings J. Exp. Bot. 59 8 2008 2125 2132 18468986 10.1093/jxb/ern075 PMC2413278 Solecka D. Kacperska A. Phenylpropanoid deficiency affects the course of plant acclimation to cold Physiol. Plant. 119 2 2003 253 262 Song J. Nada K. Tachibana S. Suppression of S-adenosylmethionine decarboxylase activity is a major cause for high-temperature inhibition of pollen germination and tube growth in tomato ( Lycopersicon esculentum Mill.) Plant Cell Physiol. 43 6 2002 619 627 12091715 10.1093/pcp/pcf078 Srivastava K. Kumar S. Bhandari H.R. Vaishampayan A. Genetics of heat tolerance traits in tomato (Solanum lycopersicum L.) Int Plant Res. 30 2017 397 402 Stainforth D.A. Aina T. Christensen C. Collins M. Faull N. Frame D.J. Piani C. Uncertainty in predictions of the climate response to rising levels of greenhouse gases Nature 433 7024 2005 403 15674288 10.1038/nature03301 Su P.-H. Li H.-m. Arabidopsis stromal 70-kD heat shock proteins are essential for plant development and important for thermotolerance of germinating seeds Plant Physiol. 146 3 2008 1231 1241 18192441 10.1104/pp.107.114496 PMC2259073 Sun H.-J. Uchii S. Watanabe S. Ezura H. A highly efficient transformation protocol for Micro-Tom, a model cultivar for tomato functional genomics Plant Cell Physiol. 47 3 2006 426 431 16381658 10.1093/pcp/pci251 Sun W. Van Montagu M. Verbruggen N. Small heat shock proteins and stress tolerance in plants Biochimica et Biophysica Acta (BBA)-Gene Structure and Expression 1577 1 2002 1 9 12151089 10.1016/s0167-4781(02)00417-7 Sung D.-Y. Kaplan F. Lee K.-J. Guy C.L. Acquired tolerance to temperature extremes Trends Plant Sci. 8 4 2003 179 187 12711230 10.1016/S1360-1385(03)00047-5 Sung D.Y. Vierling E. Guy C.L. Comprehensive expression profile analysis of the Arabidopsis Hsp70 gene family Plant Physiol. 126 2 2001 789 800 11402207 10.1104/pp.126.2.789 PMC111169 Suzuki N. Bajad S. Shuman J. Shulaev V. Mittler R. The transcriptional co-activator MBF1c is a key regulator of thermotolerance in Arabidopsis thaliana J. Biol. Chem. 283 14 2008 9269 9275 18201973 10.1074/jbc.M709187200 Szabados L. Savouré A. Proline: a multifunctional amino acid Trends Plant Sci. 15 2 2010 89 97 20036181 10.1016/j.tplants.2009.11.009 Tan J. Wang C. Xiang B. Han R. Guo Z. Hydrogen peroxide and nitric oxide mediated cold-and dehydration-induced myo-inositol phosphate synthase that confers multiple resistances to abiotic stresses Plant, Cell Environ. 36 2 2013 288 299 22774933 10.1111/j.1365-3040.2012.02573.x Torrigiani P. Scaramagli S. Ziosi V. Mayer M. Biondi S. Expression of an antisense Datura stramonium S-adenosylmethionine decarboxylase cDNA in tobacco: changes in enzyme activity, putrescine-spermidine ratio, rhizogenic potential, and response to methyl jasmonate J. Plant Physiol. 162 5 2005 559 571 15940873 10.1016/j.jplph.2004.10.008 Tubiello F.N. Salvatore M. Rossi S. Ferrara A. Fitton N. Smith P. The FAOSTAT database of greenhouse gas emissions from agriculture Environ. Res. Lett. 8 1 2013 015009 Upchurch R.G. Fatty acid unsaturation, mobilization, and regulation in the response of plants to stress Biotechnol. Lett. 30 6 2008 967 977 18227974 10.1007/s10529-008-9639-z Van der Knaap E. Tanksley S. The making of a bell pepper-shaped tomato fruit: identification of loci controlling fruit morphology in Yellow Stuffer tomato Theor. Appl. Genet. 107 1 2003 139 147 12835939 10.1007/s00122-003-1224-1 Vasil I.K. Physiology and culture of pollen Int. Rev. Cytol. 107 1987 127 174 Verbruggen N. Hermans C. Proline accumulation in plants: a review Amino Acids 35 4 2008 753 759 18379856 10.1007/s00726-008-0061-6 Vierling E. The roles of heat shock proteins in plants Annu. Rev. Plant Biol. 42 1 1991 579 620 Wahid A. Gelani S. Ashraf M. Foolad M.R. Heat tolerance in plants: an overview Environ. Exp. Bot. 61 3 2007 199 223 Wahid A. Shabbir A. Induction of heat stress tolerance in barley seedlings by pre-sowing seed treatment with glycinebetaine Plant Growth Regul. 46 2 2005 133 141 Waie B. Rajam M.V. Effect of increased polyamine biosynthesis on stress responses in transgenic tobacco by introduction of human adenosylmethionine gene Plant Sci. 164 5 2003 727 734 Wakita Y. Otani M. Hamada T. Mori M. Iba K. Shimada T. A tobacco microsomal ω-3 fatty acid desaturase gene increases the linolenic acid content in transgenic sweet potato ( Ipomoea batatas ) Plant Cell Rep. 20 3 2001 244 249 Wells C.E. Eissenstat D.M. Beyond the roots of young seedlings: the influence of age and order on fine root physiology J ournal of Plant Growth Regulation 21 4 2002 324 334 Wen et al. Identification of heat-tolerance QTLs and high-temperature stress-responsive genes through conventional QTL mapping, QTLseq and RNA-seq in tomato 10.1186/s12870-019-2008-3 PMC6739936 31510927 Wi S.J. Kim W.T. Park K.Y. Overexpression of carnation S-adenosylmethionine decarboxylase gene generates a broad-spectrum tolerance to abiotic stresses in transgenic tobacco plants Plant Cell Rep. 25 10 2006 1111 1121 16642382 10.1007/s00299-006-0160-3 Wu L.J. Zhang J.F. Effect of high-temperature stress on growth and physiological indexes of tomato seedlings Northern Hortic (Chinese). 23 2013 19 22 Xu J. Wolters-Arts M. Mariani C. Huber H. Rieu I. Heat stress affects vegetative and reproductive performance and trait correlations in tomato ( Solanum lycopersicum ) Euphytica 213 7 2017 156 Yang X. Liang Z. Lu C. Genetic engineering of the biosynthesis of glycinebetaine enhances photosynthesis against high temperature stress in transgenic tobacco plants Plant Physiol. 138 4 2005 2299 2309 16024688 10.1104/pp.105.063164 PMC1183416 Yang X. Lu C. Effects of exogenous glycinebetaine on growth, CO2 assimilation, and photosystem II photochemistry of maize plants Physiol. Plant. 127 4 2006 593 602 Yang X. Wen X. Gong H. Lu Q. Yang Z. Tang Y. Lu C. Genetic engineering of the biosynthesis of glycinebetaine enhances thermotolerance of photosystem II in tobacco plants Planta 225 3 2007 719 733 16953431 10.1007/s00425-006-0380-3 Zhang M. Barg R. Yin M. Gueta-Dahan Y. Leikin-Frenkel A. Salts Y. Ben-Hayyim G. Modulated fatty acid desaturation via overexpression of two distinct ω-3 desaturases differentially alters tolerance to various abiotic stresses in transgenic tobacco cells and plants Plant J. 44 3 2005 361 371 16236147 10.1111/j.1365-313X.2005.02536.x Zhou R. Kong L. Wu Z. Rosenqvist E. Wang Y. Zhao L. Physiological response of tomatoes at drought, heat and their combination followed by recovery Physiol Plant. 165 2018 144 154 29774556 10.1111/ppl.12764 Zhou R. Kjær K.H. Rosenqvist E. Yu X. Wu Z. Ottosen C.O. Physiological response to heat stress during seedling and anthesis stage in tomato genotypes differing in heat tolerance J. Agron. Crop Sci. 203 1 2017 68 80 Zhou X.Y. Luo J.N. Li J.Y. Li W.H. Wu H.B. Thermo tolerance of Luffa Acutangula seedlings and their physiological response to high temperature stress J Trop Subtrop Bot (Chinese). 25 2017 357 369 Zinn K.E. Tunc-Ozdemir M. Harper J.F. Temperature stress and plant sexual reproduction: uncovering the weakest links J. Exp. Bot. erq053 2010 10.1093/jxb/erq053 PMC2917059 20351019 Further Reading Alsamir M. Ahmad N.M. Mahmood T. Trethowan R. Impact of heat stress on Fusarium wilt (' F. solani ') incidence in cultivated tomato and related species Aust. J. Crop Sci. 11 8 2017 997 Alsamir M. Mahmood T. Ahmad N. Trethowan R. Distribution of organic metabolites after Fusarium wilt incidence in tomato (' Solanum lycopersicum 'L.) Aust. J. Crop Sci. 11 9 2017 1123 Chengkun, H., 1996. Effects of drought stress on activated oxygen metabolism in tomato. Journal of Fujian Agricultural University (China). Dat J.F. Lopez-Delgado H. Foyer C.H. Scott I.M. Parallel changes in H2O2 and catalase during thermotolerance induced by salicylic acid or heat acclimation in mustard seedlings Plant Physiol. 116 4 1998 1351 1357 9536052 10.1104/pp.116.4.1351 PMC35042 De Guadalupe Moctezuma-Zárate M. Vargas-Morales J.M. Cárdenas-González J.F. Martínez-Juárez V.M. Acosta-Rodríguez I. Induction of Extracellular Lytic Enzymes by Fusarium solani Adv Microbiol 3 2013 24 30 Devasirvatham V. Tan D.K. Trethowan R.M. Breeding strategies for enhanced plant tolerance to heat stress Advances in plant breeding strategies: Agronomic, abiotic and biotic stress traits 2016 Springer Cham 447 469 Dresselhaus, T., & Hückelhoven, R., 2018. Biotic and Abiotic Stress Responses in Crop Plants. Fabro G. Kovács I. Pavet V. Szabados L. Alvarez M.E. Proline accumulation and AtP5CS2 gene activation are induced by plant-pathogen incompatible interactions in Arabidopsis Mol. Plant Microbe Interact. 17 4 2004 343 350 15077666 10.1094/MPMI.2004.17.4.343 Golam F. Prodhan Z.H. Nezhadahmadi A. Rahman M. Heat Toler- ance in Tomato Life Science Journal 9 2012 1936 1950 Kaplan F. Guy C.L. β-Amylase induction and the protective role of maltose during temperature shock Plant Physiol. 135 3 2004 1674 1684 15247404 10.1104/pp.104.040808 PMC519081 Lin K.H. Lo H.F. Lee S.P. Kuo C.G. Chen J.T. Yeh W.L. RAPD markers for the identification of yield traits in tomatoes under heat stress via bulked segregant analysis Hereditas 143 2006 142 154 17362348 10.1111/j.2006.0018-0661.01938.x Mattoo A. Handa A. Tomato plant responses to biotic and abiotic stress CA Avila, SC Irigoyen and KK Mandadi, Texas A&M AgriLife Research, USA. In Achieving sustainable cultivation of tomatoes 2017 Burleigh Dodds Science Publishing 191 208 Mehrotra R. Agarwal A. Plant Pathology 2nd edi. In. 2003 (Tata Mc Graw Hill Publishing com. Ltd) ' Mesihovic A. Iannacone R. Firon N. Fragkostefanakis S. Heat stress regimes for the investigation of pollen thermotolerance in crop plants Plant reproduction 29 1–2 2016 93 105 27016360 10.1007/s00497-016-0281-y Morkunas I. Ratajczak L. The role of sugar signaling in plant defense responses against fungal pathogens Acta Physiol Plant 36 2014 1607 1619 Poudyal D. Rosenqvist E. Ottosen C.O. Phenotyping from lab to field–tomato lines screened for heat stress using Fv/Fm maintain high fruit yield during thermal stress in the field Funct. Plant Biol. 46 1 2019 44 55 10.1071/FP17317 30939257 Rajam M.V. Dagar S. Waie B. Yadav J.S. Kumar P.A. Shoeb F. Kumria R. Genetic engineering of polyamine and carbohydrate metabolism for osmotic stress tolerance in higher plants J. Biosci. 23 4 1998 473 482 Tamietti G. Valentino D. Soil solarization as an ecological method for the control of Fusarium wilt of melon in Italy Crop Prot. 25 4 2006 389 397 Willits D. Peet M. The effect of night temperature on greenhouse grown tomato yields in warm climates Agric. For. Meteorol. 92 3 1998 191 202 Peer review under responsibility of King Saud University.