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Enhancing thermotolerance of tomato plants (Lycopersieon esculentum mill) by heat hardening of seeds
Bulletin of the National Research Centre volume 43, Article number: 126 (2019)
High temperature is a crucial problem in growing good crops of high temperature-sensitive vegetables including tomato. Therefore, this study was carried out to investigate the effects of pre-sowing heat treatments of tomato seeds on germination, growth, and biochemical changes of the plants grown under high temperature stress.
Material and methods
The study included two experiments, experiment (I) dealt with the effect of pre-sowing heat hardening of tomato (Lycopersiecon esculentum Mill cv Marmand VF) for different periods of soaking at 25 °C for 5 min, 3 h and 6 h before exposing to 50 °C, 60 °C, and 70 °C for 0.5 h, 1 h, and 2 h.
Best results represented by germination parameters were obtained by soaking the seeds for 5 min before exposure to 50 °C, 60 °C, and 70 °C for 0.5 h, 1 h, and 2 h. According to the germination data, these treatments were chosen to study their effect on vegetative growth as well as some biochemical parameters (Experiment II). The study showed that seed hardening increased growth criteria expressed by stem length, number of branches, number and area of leaves, and fresh and dry weight of shoots. The same treatments increased photosynthetic pigments, i.e., (chlorophylls “a” and “b”) and carotenoids of tomato leaves as well as the studied chemical constituents of shoots (reducing sugars, sucrose, amino acids, proline and proteins, as well as nucleic acids and saturated fatty acids). Maximum response was attained by treatment with 60 °C for 1 h and 2 h.
Thus, these treatments can help the plant to cope with the adverse effects of high temperature prevailing during their growth stage.
Tomato (Lycopersicon esculentum mill) is one of the widely grown vegetable crops. It is an important crop for human consumption.
It is usually cultivated in the open field in Saudi Arabia during September as the prevailing temperature is suitable for growth and development of the plant. Tomato plants grow rapidly so extending the season and increasing continuity of supply can be achieved by sowing the seeds during spring. However, the plants exhibited to high temperature during their growth and development.
High temperature is a crucial problem in growing good crops of high temperature-sensitive vegetables including tomato. It impairs different morphological criteria (Khalil and Moursy 1983 and Warrag 1999). High temperature affects wide spectrum of both biochemical and physiological response within the plant cell. These results are expected and described by many researchers especially in the case of growing organs, since all the reaction in the plant already take place rapidly and further rise in temperature might easily disturb the balance (Fisher 1980). Other investigators reported that extreme and variation of high temperature can damage the intermolecular interactions needed for growth (Bita and Gerats 2013).
Protection of plants from high temperature stress can be achieved by several mechanisms; one of these mechanisms is seed hardening; it is a physiological seed enhancement method (Taylor et al. 1998). Seed hardening can be achieved by pre-sowing treatments in which the seeds are soaked in water, an osmotic solution or growth regulators, as well as exposing the seeds to elevated temperature above the maximum temperature prevailing during their growth. These treatments allow the seeds to go to the first stages of germination but not permit radicle protrusion through the seed coat (Heydeker, 1977). Planting hardened seeds in the field giving the plant a better start than the non-hardened plants. Thus, hardened plants might survive adverse environmental stresses like high temperature more easily because of the advanced state of development.
The present study is an additional contribution for understanding the effects of pre-sowing heat treatments of tomato seeds on germination, growth, and biochemical changes of the plant grown under high temperature stress (30–40 °C).
Material and methods
The study comprised of two experiments; the planning of the second experiment depended on the results of the first one according to the following order.
Experiment I: germination tests
Uniform seeds of tomato (Lycopersicon esculentum Mill cv. Marmand VF) were soaked in water at 25 °C for 5 min, 3 h, and 6 h; dried quickly within two layers of filter paper; and each group was divided to two sets. The first set from each group was weighed then dried at 105 °C till constant weight according to Hart and Neustadt (1957) to measure moisture content that reached 20.6%, 44.33%, and 63.52% respectively. The second set from each group was subjected to 50, 60, and 70 °C for 0.5 h, 1 h, and 2 h. The seeds were germinated at 25 °C in Petri dish each containing 20 seeds.
Ten replicates were allotted for each treatment as well as control treatment (seeds soaked for 0.5 h or 1 h or 3 h at room temperature (25 °C)). Germination was recorded for 8 days, then germination data were recorded as follows: germination capacity, radicle and hypocotyl length, as well as radicle fresh weight and seedling fresh weight.
The previous experiment results indicated that the best results were obtained in seeds soaked for 5 min (moisture content 20.6%) and exposed to 50 °C, 60 °C, and 70 °C for 0.5 h, 1 h, and 2 h as well as seeds soaked for 5 min only as (control). These treatments were chosen to study their effect on vegetative growth and some biochemical parameters.
Growing technique and sampling
Tomato seeds were sown on March in JV (seven) cubes; when the seeds attained 30 days, they were transferred to 30 cm in diameter pots filled with equal amounts of soil (consisted of clay + petmoss + perlite at the ratio of 1: 3: 5 (w/w)). Fertilization was applied as the recommended dose (5 g superphosphate, 10 g mixture of ammonium sulphate and potassium sulphate at the ratio of 3:2) for each pot.
The plants were supplied with water according to their requirements which was governed by climatic conditions. The experiment was carried out doors in the screen of Girls College of Science, Damman, Saudi Arabia for two successive seasons. The maximum and minimum temperature as well as relative humidity are shown in Table 1.
Samples were collected at random 30 days after transplanting (DAT). Each treatment is divided into three replicates for recording vegetative characters as well as chemical analysis.
Photosynthetic pigments [chlorophyll (a), chlorophyll (b), and carotenoids (car)] were determined in fresh leaves (Metzner et al. 1965).
The following parameters were estimated in dry shoots at 70 °C
Reducing sugars, sucrose, and polysaccharides were measured according to (Dubios et al. 1956). Total amino acids were analyzed according to Boulter and Barber (1963). Protein extraction followed Anderson and Beardal (1991) and estimated as described by Lowry et al. (1951).
Proline, nucleic acids, and fatty acids were determined in fresh shoots. Proline was measured according to Troll and Lidsley (1955). Nucleic acids were extracted according to Schmidt and Thaunhauser (1945), whereas ribonucleic acid (RNA) and deoxyribonucleic acid (DNA) were estimated according to the method of Winzler (1955) and Burton (1956), respectively.
Fatty acids were analyzed through four successive steps: (1) extraction by petroleum ether 60–40 °C, (2) saponification with NaOH (20%), (3) methylation by methyl alcohol, and (4) identification by GLC (Varian Model 6000 chromatography). The GLC condition was as follows: THE glass column filled with (15% DEGS). The column oven temperature was programmed at 6 °C/min from 80 to 130 °C and kept finally for 25 min. Injector and detector temperature were 220 °C and 260 °C, respectively. Gases flow rates were 30, 30, 300 cm/min for N2, H2, and air, respectively. The flow rate inside the column was adjusted to 1 ml/ min.
The data of the first experiment was subjected to statistical analysis according to analysis of variance with interaction. The values of least significant difference (LSD) were calculated at 5% level of probability.
The data of the second experiment was arranged in complete randomized design. The obtained data were statistically analyzed according to Duncan (1955) at probability 5%. Mean value followed by the same letter within each column are not significant.
By applying the Steel and Torrie (1960) test, the results showed the same trend. Therefore, the combined analysis of the two seasons was calculated. Combined analysis of the two seasons was calculated after Steel and Torrie (1960) as the results obtained showed the same trend.
Germination percentage (Table 2) showed the optimum values as the seeds soaked for 5 min, 3 h, and 6 h at room temperature compared to the other treatments at the different degrees (50, 60, and 70 °C). Moreover, these treatments decreased germination percentage by increasing degree of temperature from 50 → 60 → 70 °C as well as prolonging the period of soaking from 5 min → 3 h → 6 h. The lowest value of germination percentage was obtained by soaking the seeds for 3 h or 6 h before exposure for 70 °C for any period of exposure. Thus, the seeds did not tolerate the high percentage of moisture content concomitant to high temperature.
Results in Table 3 revealed the interaction of the soaking period of the seeds and period of exposure to different degrees of temperature on radicle length; their length significantly increased by exposing the seeds to 50 °C or 60 °C for all exposure periods after soaking the seeds for 5 min. However, soaking the seeds for 6 h before exposing to 70 °C at all used periods decreased significantly the length of radicle as compared to control. Hypocotyl length significantly increased by soaking tomato seeds for 5 min before exposing to the different used periods at 50 °C. On the other hand, increasing period of soaking to 3 h and 6 h accompanied with elevating the exposure temperature to 60 °C or 70 °C significantly decreased hypocotyl length. Maximum significant decrease was reached by soaking the seeds for 3 h or 6 h before exposing to different periods at 70 °C (Table 2).
Radicle fresh weight did not show any significant increase due for treatments. In addition, significant decrease was obtained by soaking the seeds for 3 h or 6 h before exposing to 60 °C or 70 °C for all exposure periods (Table 3).
Seedling fresh weight exhibited significant increase by soaking the seeds for 5 min before exposing to 50 °C or 60 °C for 0.5 h or 1 h. However, prolonging the period of soaking to 3 h and 6 h before exposing the seeds to different temperature degrees for all used periods of exposure (0.5 h, 1 h, and 2 h) showed opposite trend as all treatments decreased fresh weight of seedling (Table 3).
The studied parameters of growth were shown in Table 4. Stem length of tomato plants showed increase by exposing the seed for 60 °C or 70 °C. Significant increments were attained by treatment 60 °C for 2 h or 70 °C for 0.5 h.
Number of branches significantly increased by all treatments seeds for 50 °C for 0.5 h, and the highest number of branches was obtained by treatment 60 °C as well as treatment 70 °C for 0.5 h. Maximum significant increase was attained by exposing the seeds to 60 °C for 1 h or 2 h.
Number of leaves significantly increased by treatment 50 °C for 1 h or 2 h and 60 °C for all periods of exposure.
Area and fresh weight of leaves increased significantly by all treatments with the exception of seeds treatment 70 °C for 2 h. Maximum increase attained by treating the seeds for 2 h at 60 °C. Dry weight of leaves followed almost the same trend but increase with the treatment 50 °C for 0.5 was not significant (Table 4).
Shoot fresh weight showed significant increase with all treatments except treating the seeds at 70 °C for 2 h.
Shoot dry weight followed the same pattern of changes shown in case of fresh weight. Meanwhile, the increase with treatment 50 °C for 0.5 h was not significant (Table 4).
Results recorded in Table 5show the effect of hardening on photosynthetic pigments and the studied carbohydrate fractions. Chl (a) significantly increased with all treatments except those exposed to 50 °C for 0.5 h. The maximum increase was given by exposing the seeds to 60 °C for 2 h followed by treatments 60 °C or 70 °C for 1 h. Chl (b) content significantly increased with treatment 60 °C for 2 h and 70 °C for all used exposure periods. Total chlorophylls (a + b) showed significant increase by all hardening treatments except 50 °C or 60 °C for 0.5 h.
Carotenoids content showed significant increase with all treatments except 50 °C for 0.5 h. The highest value was obtained by exposing the seeds to 60 °C for 1 h or 2 h.
Carbohydrate fractions showed that direct reducing sugars were significantly increased for all treatments except the treatment 50 °C for 0.5 h and 60°°C for 1 h or 2 h.
Sucrose content followed more or less the same trend of reducing sugars with all treatments except the treatment 70 °C for 2 h; treatment 60 °C for 1 h or 2 h resulted in the highest significant increase.
Polysaccharides content clearly showed opposite trend to reducing sugars and sucrose. Significant decrease recorded for all treatments except for treatment 50 °C for 0.5 h. Maximum decrease was recorded by treatment 60 °C for 1 h followed by 2 h (Table 5).
Table 6 shows the changes of proline, amino acids, protein, as well as nucleic acids RNA and DNA. Proline content exhibited significant increment, the exception for all treatments except for the treatment 50 °C for 0.5. Maximum increase was obtained by the treatment 60 °C for 1 h followed by 2 h.
Amino acids significantly increased with all treatments 60 °C or 70 °C. Highest value of increase was obtained by 60 °C for 2 h as well as 70 °C for 1 h.
Protein content exhibited significant increments by all treatments with the exception of two treatments 50 °C or 60 °C for 0.5 h. The highest value of significance was obtained by the treatment 60 °C for 1 h. Followed by treatment for 2 h.
Nucleic acid (RNA) recorded significant increase for most treatments except 50 °C for 0.5 h as well as 70 °C for 1 h or 2 h. Meanwhile, maximum significant increase was recorded by treatment 60 °C for 1 h or 2 h. DNA content showed significant increase by the following treatments: 50 °C for 1 h, 60 °C for 1 h or 2 h, and 70 °C for 1 h (Table 6).
Table 7 shows the effect of heat hardening of tomato seeds on the percentage of fatty acids. Analysis shows increase of myristic acid percentage, while it shows decrease of palmitic oleic and palmitoleic percentage. Total saturated fatty acids percentage was increased obviously compared to untreated plants. Maximum increments were recorded by treatment 60 °C for 2 h.
High temperature is considered one of the most important environmental factors that affect plant growth. It is the most influential factor which induces an increase of plant evaporation demand and indirectly contributes to water deficiency or salt stress (Karim et al. 1998). Seed hardening modulate the physiological and biochemical nature of seeds that lead to induction of the ability of seeds to withstand higher temperature for prolonged period (Sujatha et al. 2013).
It is clear that exposure of seeds to suitable high temperature and period of soaking improved radicle and plumule length as well as seedling fresh weight. However, increase of temperature and period of exposure caused harmful effect (Tables 2 and 3). This results coincide with the findings of other investigators (Farooq et al. 2004; Farooq et al. 2005; Rehman et al. 2014).
Other researchers stated that seed hardening can modify physiological and biochemical characters that enable seeds to tolerate environmental stress and good stand more easily under unsuitable conditions (Matsushima and Sakagani 2013). Increase of radicle and plumule length as well as fresh weight of seedlings indicated many alterations, such as changes within the cytoplasm as hydration of colloids and increase the viscosity and elasticity (Sujatha et al. 2013). Metabolic activity was also suggested by other investigators as soaking of seeds enhancing metabolites (Barsa et al. 2005) and inducing carbohydrate to become ready to be used for cell elongation (Farooq et al. 2006 on rice). All these changes lead to better start and uniform of the seedling that can endure environmental stress (Farahani et al. 2011). Thus, seed hardening stimulates pregermination metabolic process without protrusion of the radicle through the seed coat (Heydeker 1977) and provides faster and synchronized germination (Nawaz et al. 2009).
Improvement of vegetative growth represented by enhancement of branching, increase of number and area of leaves, as well as fresh and dry weight of tomato leaves and shoots indicates generally positive effect. Pre-sowing heat hardening of tomato seeds with 50 °C and 60 °C for 1 h or 2 h showed the highest increments (Table 4). These results may be attributed to healthy germination of seed, which in turn gave the plant better start and induced further growth of tomato seedlings. These results were supported by the findings of other researchers (Khalil and Moursy 1983; Gamal El-Din 1999; El-Moursi et al. 2012) who proved that heat hardening of seeds promoted growth of different plants. In addition, Souza and Devaraj (2013) reported accumulation of biomass in heat acclimated Dilchos libalab under heat stress condition.
Photosynthetic pigments (chl a, chb, and carotenoids) were increased by hardening of tomato seeds. Maximum level was attained by seeds treatment with 60 °C for 2 h (Table 5). Lower level of the photosynthetic pigments in control plants reflects the effect of high temperature stress as the ambient temperature above the threshold (43-44). The impairment of chlorophylls accumulation is the first process occurring in the plastids due to high temperature. Anjum et al. (2011) reported that decrease of chlorophylls under drought stress may be a result of pigment photo-oxidation and chlorophyll degradation. Other researchers attributed decrease of chlorophylls to reduction of their synthesis or acceleration of degradation or combination of both. In support to these finding, Dutta et al. (2009) and Reda and Mandura (2011) showed destruction of numerous enzymes involved in the mechanism of chlorophylls synthesis under high temperature stress. High chlorophylls content due to hardening in the present study improved protection of tomato plants from heat stress as susceptible genotypes showed higher reduction of total chlorophylls than tolerant ones (Gosavi et al. 2014 and Zhou et al. 2017). Moreover, other researchers stated that the accumulation of chlorophylls have been used to characterize the variability of thermotolerance for many crop species (Selvaraj et al. 2011).
Increase of carotenoids accompanied with high level of chlorophylls in treated plants pointed clearly to the effective role of carotenoids in protecting chlorophylls from the damage of singlet oxygen. Carotenoids scavenge them through direct quenching the excited triplet state of chlorophylls molecule and dissipate as a heat (Pallet and Young 1993). Kuczyriska et al. (2012) reported that xanthophylls play a key role in minimizing the over oxidation in higher plants. Thus, tomato seed hardening increased photosynthetic pigments (ch1s and carotenoids of tomato plant), which in turn minimize the damage of light-absorbing efficiency of photosystems (PSI and PSII) (Murkowski 2001; Langium et al. 2006; Souza et al. 2004).
Reducing sugars as well as sucrose increased by hardening treatments in the present study especially by 60 °C for 1 h or 2 h treatments. On the other hand, the same treatments showed pronounced decrease of polysaccharides content (Table 5). Other researchers studied the correlation between soluble sugars and polysaccharides in tolerant and sensitive varieties of plants as the tolerant varieties contain high level of soluble sugars specially sucrose concomitant to high activity of sucrose–phosphate synthetase compared to sensitive ones (Kerr et al. 1987, Basu et al. 1991). Previously, Dinar and Rudich (1985) showed increase of sucrose accompanied by decrease of starch in tolerant variety of tomato (Robbin) compared to the sensitive one (Roma). Later, other investigators proved that sucrose has a crucial role in increasing the osmotic potential of stressed cells (Ruan et al. 2010). In addition, Greer and Weston (2010) reported accumulation of total soluble sugars in heat acclimated varieties of vitis venefera.
Proline is one of the most important amino acids which were accumulated under stress. The present investigation showed that proline content increased by most of the hardening treatments. Maximum increment was given by 60 °C for 1 h followed by exposure for 2 h. Several studies cleared a good relation between proline and increasing tolerance of plants under environmental stresses. These amino acids have different crucial roles and act as hydroxyl scavenger, stabilization of membranes and protein structure, as sink for carbon and nitrogen for stress recovery, and buffering cellular redox potential under stress (Hayat et al. 2012; Kavikishor and Speenivasulv 2014; Yaish 2015). Moreover, Li et al. (2013) reported inducing of tolerance of maize plants under high temperature stress concomitant to accumulation of proline through P5C5 (Δ′′ pyrrolidine -5-carbolate synthesis (188.8.131.52)) using hydrogen sulphide. Other researchers reported that accumulation of proline under high temperature stress allows the plants to cope with heat stress (Chakraborty and Tongden 2005; Rasheed et al. 2011).
Worth to mention that heat stress injury involves water deficit and cell turgor as high temperature cause increases in transpiration and in turn these changes lead to water deficit and increments of loss turgidity (Cansev 2012).
Protection against dehydration due to high temperature stress can occur via osmoprotectant (soluble sugars, amino acids, and proline as these metabolites act as stabilizer of cellular membranes and mentain turger) (Farooq et al. 2008). Many researchers proved that tolerant verities of different plants induced osmolytes as soluble sugars and proline under drought and high temperature (Arunkumar et al. 2012; Yingyan et al. 2013; Devi and Sujatha 2014; Solanki and Samangi 2014). Thus, accumulation of soluble sugars and proline are one of the potential biochemical indicators in selecting tolerant cultivars and allowing the plant to cope with heat stress.
Total protein showed significant increase due to heat hardening of tomato seeds treatment 60 °C for 2 h showed the highest level (Table 6). The same observation was recorded by other researchers (Gulen and Eris 2004; He et al. 2005). Worth to be mention that tomato plants in the present study exposed to high temperature during their growth as the ambient temperature reached (30–40°C) (Table 1).
Nucleic acid (DNA and RNA) contents of tomato shoots (Table 6) were increased due to hardening of seeds. Maximum increase was attained by treatment 60 °C for 1 h or 2 h. The promoting effect of heat hardening overcame the impairment of the prevailing high temperature on tomato plants. Other investigators reported decrease of DNA and RNA in wheat plants due to high temperature (Saduk and Orabi 2015). Heat stress injury involves water deficit and cell turgor. Other studies showed decrease of nucleic acid associated with rise of RNase activity under deficient water supply (Mukherjee and Mukherjee 2015).
High temperature stress induces changes of lipid membranes and it increases their fluidity via decreasing their lipid saturation (Horvath et al. 2012). Thus, it is important to increase the saturation of fatty acids for maintaining stability and enhancement of heat tolerance for membranes (Larkindale and Huany 2004).
The present study showed that heat hardening of seeds increased the percentage of saturated fatty acids treatment 50 °C for 2 h as well as treatment 60 °C for 1 h or 2 h increased the ratio of saturated fatty acids to 72.81%, 70.70%, and 79.60%, respectively compared to control.
Finally, it can be concluded that heat hardening of tomato seeds with 60 °C for 1 or 2 h could alleviate the harmful effect of high temperature prevailing during tomato plants growth, through the enhancement of their protective parameters such as carotenoids, proline, osmolytes, and saturated fatty acids. Thus, this protective mechanism helped the plants to induce their tolerance against high temperature stress, which in turn was reflected on their growth.
Anderson JW, Beardall J (1991) Molecular activities of plant cells: an introduction to plant biochemistry. Blackwell scientific publications, London, p 264
Anjum SA, Yie X, Wang L, Saleem MF, Man C, Lei W (2011) Morphological, physiological and biochemical responses of plant to drought stress. African J Agric Res 6:2026–2032
Arunkumar R, Sairam RK, Deshmukh PS, Pal M, Sangeeta K, Sunll KP, Kashwaha SR, Singh TP (2012) High temperature stress and accumulation of compatible solution in ckickpea (Cicer arietinum L.). Indian J Plant Physol 17:145–150
Barsa SMA, Farooq M, Tabassum R, Ahmed N (2005) Seed treatment in fine rice (Oryza sativa L.). Seed Sci Tech 33:623–628
Basu PS, Minhas JS (1991) Heat tolerance and assimilate transport in different potato genotypes. J Experim Bot 42:860–861
Bita CE, Gerats T (2013) Plant tolerance to high temperature in a changing environment: scientific fundamentals and production of heat stress –tolerant crops. Front Plant Sci 4:1–18
Boulter D, Barber T (1963) Amino acid metabolism in germinating seed of Vicia faba L. in relation to their biology. New phytologist 62:301–304
Burton K (1956) A study on the condition for the colorimetric estimation of deoxyribonucleic acid. Biochem J 62:315–317
Cansev A (2012) Physiological effect of high temperature treatment on leaves of olive Cv. Gemlik. Plant Archives 12:521–525
Chakraborty U. and Tongden, C. Evaluation of heat acctimation and salicylic acid treatments as potent inducers of thermotolerance in cicer arientum L.,2005, Curr. Sci. 89: 384-389
Devi SPS, Sujatha B (2014) Drought. Induced accumulation of soluble sugars and proline in two pigeon pea (Cajans Cajanus L. Mill sp.) Cultivars. Inter J Res Dev 3:302–306
Dinar M, Rudich J (1985) Effect of heat stress on assimilate partitioning in tomato. Ann Bot 56:239–248
Dubios M, Gilles KA, Hamelton JK, Robers PA (1956) Colourimetric method for determination of sugars and related substances. Anal Chem 28:350–356
Duncan DB (1955) multiple range and multiple F-test. Biometrics 11:1–4
Dutta A, Mohanty S, Tripathy BC (2009) Role of temperature stress on chloroplast biogenesis and protein important in pea. Plant Physiol 150:1050–1061
El-Moursi A, Gamal El-Din KA, Tarraf SA (2012) Physiological response of lupine plant (Lupinus temis L.) to heat hardening. Am Eurasian J Agric Environ 12:660–663
Farahani HA, Moaven P, Maroufi K (2011) Effect of thermopriming on germination of cowpea (Vigna seninsis L.). Adv Enivron Biol 5:1668–1675
Farooq M, Barsa SMA, Rehman H, Saleem BA (2008) Seed priming enhances the performance of late sown wheat (Triticum aestivum L.) by improving the chilling tolerance. J Agron Crop Sci 194:55–60
Farooq M, Basra SMA, Ahmed N, Hafeez K (2005) Thermal hardening: a new seed vigor enhancement tool in rice. J Integ Plant Biol 47:187–193
Farooq M, Basra SMA, Hafeez K, Warriach EA (2004) Influence of high and low temperature treatments on the seed germination and seedling vigor of coarse and fine rice. Int Rice Res Notes 29:69–71
Farooq M, Basra SMA, Khalid M, Tabassum R, Mahmood T (2006) Nutrient Homeostasis, metabolism of reserves, and seedling vigor as affected by seed priming in Coarse Rice. Cand J Bot 84:1196–1202
Fisher, R.A. Influences of water stress on crop yield in semiarid regions 323–339 “adaptation of plants to water and high Temerature stress edit. Turner, N.C. and Kramer P.J. Willey Inter. Pub. 1980
Gamal El-Din KM (1999) Vegetative growth, amino acids and alkaloids changes by heat hardening treatments of Hyoscyamus muticus L. Egypt J Appl Sci 14:216–227
Gosavi GU, Jadhav AA, Kale AA, Godakh SR, Pawar BD, Chimoto VP (2014) Effect of heat stress on proline, cholorophyll content, heat shock proteins and antioxidant activity in sorghum (Sorghum bicolor) at seedling stage. Indian J Biotechnol 13:356–363
Greer DH, Weston C (2010) Heat stress affect growth, sugar accumulation and photosynthesis of Vitis vinifera c.v Semillon grapevines grown in controlled environment. Funct Plant Biol 37:206–214
Gulen H, Eris A (2004) Effect of heat, stress on peroxidase activity and total protein content in strawberry plants. Plant Sci 186:739–744
Hart JR, Neustadt MH (1957) Application of the Karl Fisher method to gain moisture determination. Cereal Chem 34:26–30
Hayat S, Hagat Q, Ahmed A (2012) Role of proline under changing environments. Plant Signal Behav 1:1456–1466
He Y, Lin X, Huang B (2005) Protein changes in acclimated and non-aclimated creeping bentgrass Agostis Palustris, Hads. J Amer Soc Hort Sci 130:521–526
Heydeker W, Joshua A (1977) Alleviation the thermodormancy of lettuce seeds. J Hortic Sci 52:87–98
Horvath I, Glatz A, Nakamoto H, Mishkind ML, Munnk T, Saidi Y (2012) Heat shock response in photosynthetic organisms: membranes and lipid connections. Prog Lipid Res 51:208–220
Ibrahim SK, El-Moqadam L (2015) Improving tolerance of tomato plants (Lycopersicon esculentum Mill) by foliar application of benzyl adenine. Middle East J Appl Sci 5:848–854
Karim MA, Fracheboud Y, Stamp P (1998) Heat tolerance of maize with reference to some physiological characteristics. Ann Bangladesh Agric 1:27–35
Kavikishor PB, Speenivasulv N (2014) Is Proline accumulation per se correlated with stress tolerance or is proline homeostatis are more critical tissue. Plant Cell Environ 37:300–311
Kerr JL, Kimpel J, Nagao RT (1987) Heat shock gene families of soybean and the regulation of their expression. In: Alan R (ed) Plant Gene system and their Biology. Alan R. Liss, Inc., New York, pp 87–97
Khalil S, Moursy HA (1983) Changes in some germination morphological and reproductive characters of tomato plant as influenced by heat treatments of seeds. Annals Agric. Sci Fac. Agric. Ain Shams Uni. Cairo Egypt 28:1099–1121
Kuczyriska P, Latowski D, Niczyporuk S (2012) Zeanthin epoxidation-an in vitro approach. Acta Biochem. Polonica 59:105–107
Langium CUI, Jianlong LI, Yamin FAN, Sheng XU, Zang Z (2006) High temperature effects on photosynthesis, PS II functionality and antioxidant activity of two Festuca arundinacea cultivars with different heat susceptibility. Botanical Studies 47:61–69
Larkindale J, Huany BR (2004) Thermotolerance and antioxidant systems in Agrostis stolonifera Involvment of salicylic acid, abscisic acid, calcium hydrogen peroxide and ethylene. J Plant Phystol 161:405–413
Li ZG, Ding XJ, Du PF (2013) Hydrogen sulphide donor sodium hydro-sulfide improved heat tolerance in maize and involvement of proline. J Plant Physiol 170:741–747
Lowry OH, Rosebrogh NJ, Farr AL, Randall RJ (1951) Protein measurement with folin phenol reagent. J Biol Chem 193:265–275
Matsushima KI, Sakagani JI (2013) Effects of seed hydropriming on germination and seedling vigor during emergence of rice under different soil moisture conditions. Amer J Plant Sci 4:1584–1593
Metzner H, Ran H, Senger H (1965) Untresuchugen zur synchronisier barkit ein zeiner pigment Mangol Mutanten von chloreila. Planta 65:186
Mukherjee S, Mukherjee D (2015) Growth responses and changes in protein and nucleic acids of Cajanus cajan L. under normal, excess and deficient water supply. Inter J Agric Innov Res 3:1574–1578
Murkowski A (2001) Heat stress and spermidene affect chlorophyll fluorescence in tomato plants. Biol Plant 44:53–57
Nawaz A, Amjad M, Iqbal J (2009) Effect of thermal hardening on germination and seedling vigour of tomato. J Res (Science) 10:39–49
Pallet, K. E and Young, A. J Carotenoids In: Antioxidants In Higher Plants. ed. By R.G. Alscher and John L. Hess. CRC Press Boca Raton Ann. Arbor London, Tokyo pp. 60–89, 1993
Rasheed R, Wahid A, Forooq M, Hussain I, Basra SMA (2011) Role of proline and glycinbetadine in improving heat tolerance of sprouting sugarcane (Saccharum sp.) buds. Plant Growth Regul 65:35–45
Reda F, Mandura HMH (2011) Response of enzymes activities, photosynthetic pigments, proline to low or high temperature stressed wheat plant (Triticum aestivum L. ) in the presence or absence of exogenous proline or cysteine. Int J Acad Res 3:108–116
Rehman AU, Farooq M, Ali H, Sarwar N, Qamar R (2014) Thermal hardening improves germination and early seedling growth of chickpea. Asian J Agri Biol 2:51–58
Ruan YL, Jin Y, Yang YJ, Li GT, Boyer JS (2010) Sugar input, metabolism and signaling mediated by invertase: roles in development yield potential and response to drought and heat. Mol Plants 3:942–955
Saduk MS, Orabi SA (2015) Improving thermotolerance of wheat plant by foliar application of citric acid and oxalic acid, 2015. Int J Chem Tech Res 8:111–123
Schmidt G, Thaunhauser SJ (1945) A method for determination of deoxyribonucleic acid, ribonucleic acid and phosphoproteins in animal tissues. J Biol Chem 161:83–89
Selvaraj MG, Burow G, Burke JJ, Belankar V, Puppala N, Burow MD (2011) Heat stress secreening of peanut (Archis hypoguea L.) seedling for acquired thermotolerance. Plant Growth Regul 65:83–91
Shao HB, Chuc LY, Zang JH, Lua ZH, Hug YC (2007) Change of some anti-oxidative physiological induces under soil water difficit among 10 wheat (Triticum aestivum L.) genotypes at tillering stage. Colloids Surf B Bioint 54:143–149
Solanki JK, Samangi SK (2014) Effect of drought stress on proline accumulation in peanut genotypes. Int J Adv Res 2:301–309
Souza MR, Devaraj VR (2013) Induction of thermotolerance through heat acclimation in lablab bean (Dilichos lablab). Afr J Biotechnol 12:5695–5704
Souza RP, Machadoa EC, Silva JABA, Lagoa M, Silveira JAG (2004) Photosynthetic gas exchange chlorophyll fluorescence and some associated metabolic changes in cowpea (Vigna anguiculata) during water stress and recovery. Environ Exp Bot 51:45–56
Steel RG, Torrie JH (1960) Principles and procedures of statistics with special References to Biological Sciences. Mc.Craw- Hill Book Company- Inc, New York. Toronto- London, p 481
Sujatha K, Sivasubramaniam J, Padma J, Selvarani K (2013) Seed hardening. Inter J Agric Sci 9:392–412
Taylor AG, Allen PS, Bonnett MA, Bradford KJ, Burris JS, Misra MK (1998) Seed Enhancment. Seed Sci Res 8:245–256
Troll W, Lidsley J (1955) Photometric methods for determination of proline. J Biol Chem 215:655–660
Warrag MOA (1999) Flowering and fruiting of tomato (Lycopersicum esculentum Mill) in Qassin Saudi Arabia during summer. J King Saud Univ Agric Sci 3:241–250
Winzler RJ (1955) Methods in Biochemical Analysis. Interscience, New York, p 270
Yaish MW (2015) Proline accumulation is a general response to abiotic stress in the data palm tree (Phoenix dactylifera L.). Genet Mol Res 14:9943–9950
Yingyan H, Shuangxi F, Qiao Z, Wang Y (2013) Effect of heat stress ton the MDA, proline and soluble sugars content in leaf lettuce seedlings. Agric Sci 4:112–115
Zhou R, Kjaer KH, Rosenqvist E, Yu X, Wu Z, Ottosen CO (2017) Physiological response to heat stress during seedling and anthesis stage in tomato genotypes differing in heat tolerance. J Agron Crop Sci 203:68–80
The authors are thankful to the National Research Centre for provision of laboratory facilities to carry out this research.
There are currently no funding sources in the design of the study and collection, analysis, and interpretation of data and in writing the manuscript.
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Sohair K. Ibrahim Prof of plant Physiology at National Research Centre, Egypt and Lulwa A. El- Muqadam Prof of plant physiology at Damam University, Saudi Arabia.
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Ibrahim, S.K., El-Muqadam, L.A. Enhancing thermotolerance of tomato plants (Lycopersieon esculentum mill) by heat hardening of seeds. Bull Natl Res Cent 43, 126 (2019). https://doi.org/10.1186/s42269-019-0106-x
- Seed hardening
- High temperature stress