Abstract
The current study was devoted to assessing the impact of exogenous ascorbic acid (AsA) in inducing systemic thermotolerance against acute heat stress in tomato (Solanum lycopersicum) seedlings. There were four treatment groups including untreated control (CK), heat-stressed tomato (HS: exposure to 40 °C for 8 h), and treated with ascorbic acid (0.5 mM AsA), and the last group includes both the exogenous application of ascorbic acid and heat stress (AsA + HS). The HS led to leaf curling and mild wilting while plants treated with AsA displayed similar phenotype with control plants, approving that AsA eliminated the injurious effects of the heat stress. The oxidative damage to cell components was confirmed by higher levels of hydrogen peroxide, lipid peroxidation, electrolyte leakage, total oxidant status, and oxidative stress index. Moreover, acute heat stress significantly reduced the photosynthetic pigment contents, and nutrient contents in tomato seedling leaves. In contrast, ascorbic acid postulated a priming effect on tomato roots and, substantially, alleviated heat stress effects on seedlings through reducing the oxidative damage and increasing the contents of ascorbic acid, proline, photosynthetic pigments, and upregulation of heat shock proteins in leaves. Ascorbic acid seems to be a key signaling molecule which enhanced the thermotolerance of tomato plants.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abbas G, Chen Y, Khan F, Feng Y, Palta J, Siddique K (2018) Salinity and low phosphorus differentially affect shoot and root traits in two wheat cultivars with contrasting tolerance to salt. Agronomy 8:155. https://doi.org/10.3390/agronomy8080155
Abdel-Daim MM (2016) Synergistic protective role of ceftriaxone and ascorbic acid against subacute diazinon-induced nephrotoxicity in rats. Cytotechnology 68:279–289. https://doi.org/10.1007/s10616-014-9779-z
Abdel-Daim MM, El-Ghoneimy A (2015) Synergistic protective effects of ceftriaxone and ascorbic acid against subacute deltamethrin-induced nephrotoxicity in rats. Ren Fail 37:297–304. https://doi.org/10.3109/0886022X.2014.983017
Abdel-Daim MM, Abushouk AI, Donia T, Alarifi S, Alkahtani S, Aleya L, Bungau SG (2019a) The nephroprotective effects of allicin and ascorbic acid against cisplatin-induced toxicity in rats. Environ Sci Pollut Res 26:13502–13509. https://doi.org/10.1007/s11356-019-04780-4
Abdel-Daim MM, Ahmed A, Ijaz H, Abushouk AI, Ahmed H, Negida A, Aleya L, Bungau SG (2019b) Influence of Spirulina platensis and ascorbic acid on amikacin-induced nephrotoxicity in rabbits. Environ Sci Pollut Res 26:8080–8086. https://doi.org/10.1007/s11356-019-04249-4
Abdelgawad KF, El-Mogy MM, Mohamed MIA et al (2019) Increasing ascorbic acid content and salinity tolerance of cherry tomato plants by suppressed expression of the ascorbate oxidase gene. Agronomy 9:51. https://doi.org/10.3390/agronomy9020051
Abu-Elsaoud AM, Tuleukhanov ST (2013) Can He-Ne laser induce changes in oxidative stress and antioxidant activities of wheat cultivars from Kazakhstan and Egypt? J Ecol Health Environ 1:1–11. https://doi.org/10.12785/jehe/010101
Aghdam MS, Sevillano L, Flores FB, Bodbodak S (2013) Heat shock proteins as biochemical markers for postharvest chilling stress in fruits and vegetables. Sci Hortic 160:54–64. https://doi.org/10.1016/j.scienta.2013.05.020
Akram NA, Shafiq F, Ashraf M (2017) Ascorbic acid-a potential oxidant scavenger and its role in plant development and abiotic stress tolerance. Front Plant Sci 8. https://doi.org/10.3389/fpls.2017.00613
Allahveran A, Farokhzad A, Asghari M, Sarkhosh A (2018) Foliar application of ascorbic and citric acids enhanced ‘Red Spur’ apple fruit quality, bioactive compounds and antioxidant activity. Physiol Mol Biol Plants 24:433–440. https://doi.org/10.1007/s12298-018-0514-7
Al-Whaibi MH (2011) Plant heat-shock proteins: a mini review. J King Saud Univ Sci 23:139–150. https://doi.org/10.1016/j.jksus.2010.06.022
Asaduzzaman M, Saifullah M, Mollick AKMSR et al (2015) Influence of soilless culture substrate on improvement of yield and produce quality of horticultural crops. In: Asaduzzaman M (ed) Soilless culture - use of substrates for the production of quality horticultural crops. InTech
Ashrafuzzaman M, Oh SJ, Hong CB (2005) Low expression profiles of heat stress-related genes in Capsicum annuum. J Plant Biol 48:85–95. https://doi.org/10.1007/BF03030567
Athar H-R, Khan A, Ashraf M (2009) Inducing salt tolerance in wheat by exogenously applied ascorbic acid through different modes. J Plant Nutr 32:1799–1817. https://doi.org/10.1080/01904160903242334
Bandeh-hagh A, Toorchi M, Mohammadi A, et al. (2008) Growth and osmotic adjustment of canola genotypes in response to salinity
Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207. https://doi.org/10.1007/BF00018060
Ben Rejeb I, Pastor V, Mauch-Mani B (2014) Plant responses to simultaneous biotic and abiotic stress: molecular mechanisms. Plants (Basel) 3:458–475. https://doi.org/10.3390/plants3040458
Benke K, Tomkins B (2017) Future food-production systems: vertical farming and controlled-environment agriculture. Sustain Sci Pract Policy 13:13–26. https://doi.org/10.1080/15487733.2017.1394054
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. https://doi.org/10.3389/fpls.2013.00273
Caverzan A, Passaia G, Rosa SB, Ribeiro CW, Lazzarotto F, Margis-Pinheiro M (2012) Plant responses to stresses: role of ascorbate peroxidase in the antioxidant protection. Genet Mol Biol 35:1011–1019. https://doi.org/10.1590/S1415-47572012000600016
Chang H-C, Tang Y-C, Hayer-Hartl M, Hartl FU (2007) SnapShot: molecular chaperones, Part I. Cell 128:212
Chen K, Zhang M, Zhu H, Huang M, Zhu Q, Tang D, Han X, Li J, Sun J, Fu J (2017) Ascorbic acid alleviates damage from heat stress in the photosystem II of tall fescue in both the photochemical and thermal phases. Front Plant Sci 8. https://doi.org/10.3389/fpls.2017.01373
Choudhury FK, Rivero RM, Blumwald E, Mittler R (2017) Reactive oxygen species, abiotic stress and stress combination. Plant J 90:856–867. https://doi.org/10.1111/tpj.13299
Christou A, Filippou P, Manganaris GA, Fotopoulos V (2014) Sodium hydrosulfide induces systemic thermotolerance to strawberry plants through transcriptional regulation of heat shock proteins and aquaporin. BMC Plant Biol 14:42. https://doi.org/10.1186/1471-2229-14-42
Conklin PL, Barth C (2004) Ascorbic acid, a familiar small molecule intertwined in the response of plants to ozone, pathogens, and the onset of senescence. Plant Cell Environ 27:959–970. https://doi.org/10.1111/j.1365-3040.2004.01203.x
Cooper GM (2000) Protein folding and processing. The cell: a molecular approach 2nd edition
Dionisio-Sese ML, Tobita S (1998) Antioxidant responses of rice seedlings to salinity stress. Plant Sci 135:1–9. https://doi.org/10.1016/S0168-9452(98)00025-9
Duncan DB (1955) Multiple range and multiple F tests. Biometrics 11:1–42. https://doi.org/10.2307/3001478
El-Esawi MA, Elkelish A, Elansary HO et al (2017) Genetic transformation and hairy root induction enhance the antioxidant potential of Lactuca serriola L. In: Oxidative Medicine and Cellular Longevity. https://www.hindawi.com/journals/omcl/2017/5604746/. Accessed 9 Jan 2018
Elkelish AA, Soliman MH, Alhaithloul HA, El-Esawi MA (2019) Selenium protects wheat seedlings against salt stress-mediated oxidative damage by up-regulating antioxidants and osmolytes metabolism. Plant Physiol Biochem 137:144–153. https://doi.org/10.1016/j.plaphy.2019.02.004
Erel O (2004) A novel automated method to measure total antioxidant response against potent free radical reactions. Clin Biochem 37:112–119
Erel O (2005) A new automated colorimetric method for measuring total oxidant status. Clin Biochem 38:1103–1111
Fahad S, Bajwa AA, Nazir U, Anjum SA, Farooq A, Zohaib A, Sadia S, Nasim W, Adkins S, Saud S, Ihsan MZ, Alharby H, Wu C, Wang D, Huang J (2017) Crop production under drought and heat stress: plant responses and management options. Front Plant Sci 8. https://doi.org/10.3389/fpls.2017.01147
Fan Y, Tian Z, Yan Y et al (2017) Winter night-warming improves post-anthesis physiological activities and sink strength in relation to grain filling in winter wheat (Triticum aestivum L.). Front Plant Sci 8. https://doi.org/10.3389/fpls.2017.00992
FAO (ed) (2016) Climate change, agriculture and food security. FAO, Rome
Fenech M, Amaya I, Valpuesta V, Botella MA (2019) Vitamin C content in fruits: biosynthesis and regulation. Front Plant Sci 9. https://doi.org/10.3389/fpls.2018.02006
Feng B, Liu P, Li G, Dong ST, Wang FH, Kong LA, Zhang JW (2014) Effect of heat stress on the photosynthetic characteristics in flag leaves at the grain-filling stage of different heat-resistant winter wheat varieties. J Agron Crop Sci 200:143–155. https://doi.org/10.1111/jac.12045
Fogg DN, Wilkinson NT (1958) The colorimetric determination of phosphorus. Analyst 83:406–414. https://doi.org/10.1039/AN9588300406
Foyer CH, Noctor G (2011) Ascorbate and glutathione: the heart of the redox hub. Plant Physiol 155:2–18. https://doi.org/10.1104/pp.110.167569
Gallie DR (2013) L-ascorbic acid: a multifunctional molecule supporting plant growth and development. Scientifica (Cairo) 2013:795964–795924. https://doi.org/10.1155/2013/795964
Gest N, Gautier H, Stevens R (2013) Ascorbate as seen through plant evolution: the rise of a successful molecule? J Exp Bot 64:33–53. https://doi.org/10.1093/jxb/ers297
Gogoi N, Farooq M, Barthakur S, Baroowa B, Paul S, Bharadwaj N, Ramanjulu S (2018) Thermal stress impacts on reproductive development and grain yield in grain legumes. J Plant Biol 61:265–291. https://doi.org/10.1007/s12374-018-0130-7
Goo Y-M, Chun HJ, Kim T-W, Lee CH, Ahn MJ, Bae SC, Cho KJ, Chun JA, Chung CH, Lee SW (2008) Expressional characterization of dehydroascorbate reductase cDNA in transgenic potato plants. J Plant Biol 51:35–41. https://doi.org/10.1007/BF03030738
Grover A, Mittal D, Negi M, Lavania D (2013) Generating high temperature tolerant transgenic plants: achievements and challenges. Plant Sci 205–206:38–47. https://doi.org/10.1016/j.plantsci.2013.01.005
Hasanuzzaman M, Nahar K, Alam MM, Roychowdhury R, Fujita M (2013a) Physiological, biochemical, and molecular mechanisms of heat stress tolerance in plants. Int J Mol Sci 14:9643–9684. https://doi.org/10.3390/ijms14059643
Hasanuzzaman M, Nahar K, Alam MM, Roychowdhury R, Fujita M (2013b) Physiological, biochemical, and molecular mechanisms of heat stress tolerance in plants. Int J Mol Sci 14:9643–9684. https://doi.org/10.3390/ijms14059643
He M, He C-Q, Ding N-Z (2018) Abiotic stresses: general defenses of land plants and chances for engineering multistress tolerance. Front Plant Sci 9. https://doi.org/10.3389/fpls.2018.01771
Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198
Hoagland DR, Dennis R, Arnon DI, Daniel I (1950) The water-culture method for growing plants without soil. College of Agriculture, University of California, Berkeley
Holder M (1965) Chlorophylls: chemistry and biochemistry of plant pigments. In: Goodwin TW (ed) Chemistry and biochemistry of plant pigments.
Hu Y, Wu Q, Sprague SA, Park J, Oh M, Rajashekar CB, Koiwa H, Nakata PA, Cheng N, Hirschi KD, White FF, Park S (2015) Tomato expressing Arabidopsis glutaredoxin gene AtGRXS17 confers tolerance to chilling stress via modulating cold responsive components. Hortic Res 2:15051. https://doi.org/10.1038/hortres.2015.51
Hüve K, Bichele I, Rasulov B, Niinemets Ü (2011) When it is too hot for photosynthesis: heat-induced instability of photosynthesis in relation to respiratory burst, cell permeability changes and H2O2 formation. Plant Cell Environ 34:113–126. https://doi.org/10.1111/j.1365-3040.2010.02229.x
Jung K-H, Ko H-J, Nguyen MX, Kim SR, Ronald P, An G (2012) Genome-wide identification and analysis of early heat stress responsive genes in rice. J Plant Biol 55:458–468. https://doi.org/10.1007/s12374-012-0271-z
Karababa F, Yesilova Y, Turan E, Selek S, Altun H, Selek S (2013) Impact of depressive symptoms on oxidative stress in patients with psoriasis. Redox Rep 18:51–55. https://doi.org/10.1179/1351000213Y.0000000039
Khan A, Pan X, Najeeb U, Tan DKY, Fahad S, Zahoor R, Luo H (2018) Coping with drought: stress and adaptive mechanisms, and management through cultural and molecular alternatives in cotton as vital constituents for plant stress resilience and fitness. Biol Res 51. https://doi.org/10.1186/s40659-018-0198-z
Kikuchi A, Huynh HD, Endo T, Watanabe K (2015) Review of recent transgenic studies on abiotic stress tolerance and future molecular breeding in potato. Breed Sci 65:85–102. https://doi.org/10.1270/jsbbs.65.85
Kosová K, Vítámvás P, Urban MO, Prášil IT, Renaut J (2018) Plant abiotic stress proteomics: the major factors determining alterations in cellular proteome. Front Plant Sci 9. https://doi.org/10.3389/fpls.2018.00122
Krasensky J, Jonak C (2012) Drought, salt, and temperature stress-induced metabolic rearrangements and regulatory networks. J Exp Bot 63:1593–1608. https://doi.org/10.1093/jxb/err460
Kumar S, Kaur R, Kaur N et al (2011) Heat-stress induced inhibition in growth and chlorosis in mungbean (Phaseolus aureus Roxb.) is partly mitigated by ascorbic acid application and is related to reduction in oxidative stress. Acta Physiol Plant 33:2091. https://doi.org/10.1007/s11738-011-0748-2
Larkindale J, Huang B (2005) Effects of abscisic acid, salicylic acid, ethylene and hydrogen peroxide in thermotolerance and recovery for creeping bentgrass. Plant Growth Regul 47:17–28. https://doi.org/10.1007/s10725-005-1536-z
Lavania D, Dhingra A, Siddiqui MH, al-Whaibi MH, Grover A (2015) Current status of the production of high temperature tolerant transgenic crops for cultivation in warmer climates. Plant Physiol Biochem 86:100–108. https://doi.org/10.1016/j.plaphy.2014.11.019
Lee Y, Kim MW, Kim SH (2007) Cell type identity in Arabidopsis roots is altered by both ascorbic acid-induced changes in the redox environment and the resultant endogenous auxin response. J Plant Biol 50:484–489. https://doi.org/10.1007/BF03030687
Lennox LJ, Flanagan MJ (1982) An automated procedure for the determination of total Kjeldahl nitrogen. Water Res 16:1127–1133. https://doi.org/10.1016/0043-1354(82)90129-4
Liu Y, Huang W, Xian Z, Hu N, Lin D, Ren H, Chen J, Su D, Li Z (2017) Overexpression of SlGRAS40 in tomato enhances tolerance to abiotic stresses and influences auxin and gibberellin signaling. Front Plant Sci 8. https://doi.org/10.3389/fpls.2017.01659
Liu J, Wang R, Liu W, Zhang H, Guo Y, Wen R (2018) Genome-wide characterization of heat-shock protein 70s from Chenopodium quinoa and expression analyses of Cqhsp70s in response to drought stress. Genes 9:35. https://doi.org/10.3390/genes9020035
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25:402–408. https://doi.org/10.1006/meth.2001.1262
Los DA, Murata N (2004) Membrane fluidity and its roles in the perception of environmental signals. Biochim Biophys Acta Biomembr 1666:142–157. https://doi.org/10.1016/j.bbamem.2004.08.002
Mancinelli AL (1984) Photoregulation of anthocyanin synthesis : VIII. Effect of light pretreatments. Plant Physiol 75:447–453
Merewitz E (2016) Chemical priming-induced drought stress tolerance in plants. In: Hossain MA, Wani SH, Bhattacharjee S et al (eds) Drought stress tolerance in plants, vol 1. Springer International Publishing, Cham, pp 77–103
Mishra D, Shekhar S, Singh D, Chakraborty S, Chakraborty N (2018) Heat shock proteins and abiotic stress tolerance in plants. In: Asea AAA, Kaur P (eds) Regulation of heat shock protein responses. Springer International Publishing, Cham, pp 41–69
Niu Y, Xiang Y (2018) An overview of biomembrane functions in plant responses to high-temperature stress. Front Plant Sci 9. https://doi.org/10.3389/fpls.2018.00915
Nweze CC, Abdulganiyu MG, Erhabor OG (2015) Comparative analysis of vitamin C in fresh fruits juice of Malus domestica, Citrus sinensi, Ananas comosus and Citrullus lanatus by iodometric titration. Int J Sci Environ Technol 4:17–22
Palam LR, Mali RS, Ramdas B, Srivatsan SN, Visconte V, Tiu RV, Vanhaesebroeck B, Roers A, Gerbaulet A, Xu M, Janga SC, Takemoto CM, Paczesny S, Kapur R (2018) Loss of epigenetic regulator TET2 and oncogenic KIT regulate myeloid cell transformation via PI3K pathway. JCI Insight 3:e94679. https://doi.org/10.1172/jci.insight.94679
Pandey S, Muthamilarasan M, Sharma N, Chaudhry V, Dulani P, Shweta S, Jha S, Mathur S, Prasad M (2019) Characterization of DEAD-box family of RNA helicases in tomato provides insights into their roles in biotic and abiotic stresses. Environ Exp Bot 158:107–116. https://doi.org/10.1016/j.envexpbot.2018.11.018
Park C-J, Park JM (2019) Endoplasmic reticulum plays a critical role in integrating signals generated by both biotic and abiotic stress in plants. Front Plant Sci 10:10. https://doi.org/10.3389/fpls.2019.00399
Peet MM, Willits DH, Gardner R (1997) Response of ovule development and post-pollen production processes in male-sterile tomatoes to chronic, sub-acute high temperature stress. J Exp Bot 48:101–111. https://doi.org/10.1093/jxb/48.1.101
Peet MM, Sato S, Gardner RG (1998) Comparing heat stress effects on male-fertile and male-sterile tomatoes. Plant Cell Environ 21:225–231. https://doi.org/10.1046/j.1365-3040.1998.00281.x
Reddy PS, Chakradhar T, Reddy RA, Nitnavare RB, Mahanty S, Reddy MK (2016) Role of heat shock proteins in improving heat stress tolerance in crop plants. In: Asea AAA, Kaur P, Calderwood SK (eds) Heat shock proteins and plants. Springer International Publishing, Cham, pp 283–307
Riezman H (2004) Why do cells require heat shock proteins to survive heat stress? Cell Cycle 3:60–62. https://doi.org/10.4161/cc.3.1.625
Rowell DL (1994) Soil science: methods and applications. Longman Scientific & Technical
Saibil H (2013) Chaperone machines for protein folding, unfolding and disaggregation. Nat Rev Mol Cell Biol 14:630–642. https://doi.org/10.1038/nrm3658
Saidi Y, Peter M, Finka A, Cicekli C, Vigh L, Goloubinoff P (2010) Membrane lipid composition affects plant heat sensing and modulates Ca2+-dependent heat shock response. Plant Signal Behav 5:1530–1533. https://doi.org/10.4161/psb.5.12.13163
Saleh AAH, Abdel-Kader D, El Kelish A (2007) Role of heat shock and salicylic acid in antioxidant homeostasis in mungbean (Vigna radiata L.) plant subjected to heat stress. Am J Plant Physiol 2:344–355. https://doi.org/10.3923/ajpp.2007.344.355
Sanyal RP, Misra HS, Saini A (2018) Heat-stress priming and alternative splicing-linked memory. J Exp Bot 69:2431–2434. https://doi.org/10.1093/jxb/ery111
Sato S, Peet MM, Thomas JF (2000) Physiological factors limit fruit set of tomato (Lycopersicon esculentum Mill.) under chronic, mild heat stress. Plant Cell Environ 23:719–726. https://doi.org/10.1046/j.1365-3040.2000.00589.x
Seminario A, Song L, Zulet A, Nguyen HT, González EM, Larrainzar E (2017) Drought stress causes a reduction in the biosynthesis of ascorbic acid in soybean plants. Front Plant Sci 8. https://doi.org/10.3389/fpls.2017.01042
Sergiev I, Alexieva V, Yanev S, Karanov E (1997) Effect of atrazine and spermine on free proline content and some antioxidants in pea (Pisum sativum L.) plants. Comp Ren Del Academie Bul des Sci 51:121–124
Shamshiri RR, Jones JW, Thorp KR, Ahmad D, Man HC, Taheri S (2018) Review of optimum temperature, humidity, and vapour pressure deficit for microclimate evaluation and control in greenhouse cultivation of tomato: a review. Int Agrophys 32:287–302. https://doi.org/10.1515/intag-2017-0005
Sharma N, Acharya S, Kumar K et al (2018) Hydroponics as an advanced technique for vegetable production: an overview. J Soil Water Conserv 17:364. https://doi.org/10.5958/2455-7145.2018.00056.5
Siddiqui H, Ahmed KBM, Hayat S (2018) Comparative effect of 28-homobrassinolide and 24-epibrassinolide on the performance of different components influencing the photosynthetic machinery in Brassica juncea L. Plant Physiol Biochem 129:198–212. https://doi.org/10.1016/j.plaphy.2018.05.027
Silva HCCD, Asaeda T (2017) Effects of heat stress on growth, photosynthetic pigments, oxidative damage and competitive capacity of three submerged macrophytes. J Plant Interact 12:228–236. https://doi.org/10.1080/17429145.2017.1322153
Smirnoff N (2007) Ascorbate, tocopherol and carotenoids: metabolism, pathway engineering and functions. In: Antioxidants and reactive oxygen species in plants. Wiley-Blackwell, pp 53–86
Smirnoff N (2011) Chapter 4 - Vitamin C: the metabolism and functions of ascorbic acid in plants. In: Rébeillé F, Douce R (eds) Advances in botanical research. Academic Press, pp 107–177
Sofo A, Scopa A, Nuzzaci M, Vitti A (2015) Ascorbate peroxidase and catalase activities and their genetic regulation in plants subjected to drought and salinity stresses. Int J Mol Sci 16:13561–13578. https://doi.org/10.3390/ijms160613561
Soliman MH, Alayafi AAM, El Kelish AA, Abu-Elsaoud AM (2018) Acetylsalicylic acid enhance tolerance of Phaseolus vulgaris L. to chilling stress, improving photosynthesis, antioxidants and expression of cold stress responsive genes. Bot Stud 59. https://doi.org/10.1186/s40529-018-0222-1
Song Y, Chen Q, Ci D, Shao X, Zhang D (2014) Effects of high temperature on photosynthesis and related gene expression in poplar. BMC Plant Biol 14:111. https://doi.org/10.1186/1471-2229-14-111
Stetler RA, Gan Y, Zhang W, Liou AK, Gao Y, Cao G, Chen J (2010) Heat shock proteins: cellular and molecular mechanisms in the CNS. Prog Neurobiol 92:184–211. https://doi.org/10.1016/j.pneurobio.2010.05.002
Sukrong S, Yun K-Y, Stadler P, Kumar C, Facciuolo T, Moffatt BA, Falcone DL (2012) Improved growth and stress tolerance in the Arabidopsis oxt1 mutant triggered by altered adenine metabolism. Mol Plant 5:1310–1332. https://doi.org/10.1093/mp/sss065
Sung D-Y, Kaplan F, Lee K-J, Guy CL (2003) Acquired tolerance to temperature extremes. Trends Plant Sci 8:179–187. https://doi.org/10.1016/S1360-1385(03)00047-5
Tan W, Meng QW, Brestic M et al (2011) Photosynthesis is improved by exogenous calcium in heat-stressed tobacco plants. J Plant Physiol 168:2063–2071. https://doi.org/10.1016/j.jplph.2011.06.009
Tiwari YK, Yadav SK (2019) High temperature stress tolerance in maize (Zea mays L.): physiological and molecular mechanisms. J Plant Biol 62:93–102. https://doi.org/10.1007/s12374-018-0350-x
Uchida A, Jagendorf AT, Hibino T, Takabe T, Takabe T (2002) Effects of hydrogen peroxide and nitric oxide on both salt and heat stress tolerance in rice. Plant Sci 163:515–523. https://doi.org/10.1016/S0168-9452(02)00159-0
Veljović-Jovanović S, Vidović M, Morina F (2017) Ascorbate as a key player in plant abiotic stress response and tolerance. In: Ascorbic acid in plant growth, development and stress tolerance. Springer, Cham, pp 47–109
Wang H, Wang H, Shao H, Tang X (2016) Recent advances in utilizing transcription factors to improve plant abiotic stress tolerance by transgenic technology. Front Plant Sci 7. https://doi.org/10.3389/fpls.2016.00067
Wang Q-L, Chen J-H, He N-Y, Guo F-Q (2018) Metabolic reprogramming in chloroplasts under heat stress in plants. Int J Mol Sci 19. https://doi.org/10.3390/ijms19030849
Weids AJ, Ibstedt S, Tamás MJ, Grant CM (2016) Distinct stress conditions result in aggregation of proteins with similar properties. Sci Rep 6:24554. https://doi.org/10.1038/srep24554
Xiang J, Chen X, Hu W, Xiang Y, Yan M, Wang J (2018) Overexpressing heat-shock protein OsHSP50.2 improves drought tolerance in rice. Plant Cell Rep 37:1585–1595. https://doi.org/10.1007/s00299-018-2331-4
Xu Z, Jiang Y, Zhou G (2015) Response and adaptation of photosynthesis, respiration, and antioxidant systems to elevated CO2 with environmental stress in plants. Front Plant Sci 6. https://doi.org/10.3389/fpls.2015.00701
Yamamoto Y (2016) Quality control of photosystem II: the mechanisms for avoidance and tolerance of light and heat stresses are closely linked to membrane fluidity of the thylakoids. Front Plant Sci 7:7. https://doi.org/10.3389/fpls.2016.01136
Yamashita A, Nijo N, Pospísil P et al (2008) Quality control of photosystem II: reactive oxygen species are responsible for the damage to photosystem II under moderate heat stress. J Biol Chem 283:28380–28391. https://doi.org/10.1074/jbc.M710465200
Yeung AWK, Tzvetkov NT, El-Tawil OS et al (2019) Antioxidants: scientific literature landscape analysis. In: Oxidative Medicine and Cellular Longevity. https://www.hindawi.com/journals/omcl/2019/8278454/. Accessed 16 Jun 2019
Zahid KR, Ali F, Shah F, Younas M, Shah T, Shahwar D, Hassan W, Ahmad Z, Qi C, Lu Y, Iqbal A, Wu W (2016) Response and tolerance mechanism of cotton Gossypium hirsutum L to elevated temperature stress: a review. Front Plant Sci 7:7. https://doi.org/10.3389/fpls.2016.00937
Zhang Y, Jiang J, Yang YL (2013) Acetyl salicylic acid induces stress tolerance in tomato plants grown at a low night-time temperature. J Hortic Sci Biotechnol 88:490–496. https://doi.org/10.1080/14620316.2013.11512996
Zhang X, Xiong H, Liu A, Zhou X, Peng Y, Li Z, Luo G, Tian X, Chen X (2014) Microarray data uncover the genome-wide gene expression patterns in response to heat stress in rice post-meiosis panicle. J Plant Biol 57:327–336. https://doi.org/10.1007/s12374-014-0177-z
Zhang L, Hu T, Amombo E, Wang G, Xie Y, Fu J (2017) The alleviation of heat damage to photosystem II and enzymatic antioxidants by exogenous spermidine in tall fescue. Front Plant Sci 8. https://doi.org/10.3389/fpls.2017.01747
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible editor: Gangrong Shi
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Alayafi, A.A.M. Exogenous ascorbic acid induces systemic heat stress tolerance in tomato seedlings: transcriptional regulation mechanism. Environ Sci Pollut Res 27, 19186–19199 (2020). https://doi.org/10.1007/s11356-019-06195-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-019-06195-7