Acta Physiologiae Plantarum

, 41:166 | Cite as

Coordinated regulation of three kinds of thermotolerance in tomato by antioxidant enzymes

  • Mintao Sun
  • Fangling Jiang
  • Rong Zhou
  • Benjian Cen
  • Zhen WuEmail author
Original Article


Although the relationship between basal (BT), acquired (AT) and maintenance of acquired thermotolerace (MT) has been illustrated in a heat resistant tomato genotype and sensitive tomato genotypes, whether more resistant and sensitive tomato genotypes are satisfied with the rule and the relationships of antioxidant enzymes (AE) activity in three kinds of thermotolerance are not known. Here, we have observed the intension of three kinds of tomato thermotolerance is associated with AE activities. The priming and enhancement of thermotolerance was temperature dependent with stronger thermotolerance priming by moderately high temperatures than warmer temperatures. Interestingly, AE activity also showed significantly higher in seedlings under moderately high temperature than ones at warmer temperatures. While after the first optimized priming of different high temperatures combined with secondary priming for a reasonable period, AE activity and its thermotolerance further enhanced. Surprisingly, these optimized acclimation treatments showed no difference in AE activity and MT intension, suggesting that secondary priming could supply gaps produced by the first priming of warmer high temperatures, through enhancing AE activity. Additionally, the basal heat resistant genotypes showed stronger AE activity and thermotolerance (AT and MT) than sensitive genotypes. Results from this study will provide insights into understanding mechanism behind regulating tomato thermotolerance and facilitate the development of heat tolerant cultivars.


Antioxidant enzyme Basal thermotolerance Acquired thermotolerance Maintenance of acquired thermotolerance Priming 



The authors acknowledge the National Natural Science Foundation of China Youth Fund (31701924), Fundamental Research Funds for the Central Universities (KYZZ201809, KJQN201814) and the Priority Academic Program Development of Jiangsu Higher Education Institutions.

Supplementary material

11738_2019_2951_MOESM1_ESM.doc (43 kb)
Supplementary material 1 (DOC 43 kb)


  1. Baxter A, Mittler R, Suzuki N (2014) ROS as key players in plant stress signalling. J Exp Bot 65:1229–1240. CrossRefPubMedGoogle Scholar
  2. Beyer WF, Fridovich I (1987) Assaying for superoxide dismutase activity: some large consequences of minor changes in conditions. Anal Biochem 161:559–566. CrossRefGoogle Scholar
  3. Charng YY, Liu HC, Liu NY et al (2006) Arabidopsis hsa32, a novel heat shock protein, is essential for acquired thermotolerance during long recovery after acclimation. Plant Physiol 140:1297–1305CrossRefGoogle Scholar
  4. Charng YY, Liu HC, Liu NY et al (2007) A heat-inducible transcription factor, HsfA2, is required for extension of acquired thermotolerance in Arabidopsis. Plant Physiol 143:251–262. CrossRefPubMedPubMedCentralGoogle Scholar
  5. Hong Z, Zhuoxiao C, Li Z et al (2007) Glutathione and glutathione-linked enzymes in normal human aortic smooth muscle cells: chemical inducibility and protection against reactive oxygen and nitrogen species-induced injury. Mol Cell Biochem 301:47–59. CrossRefGoogle Scholar
  6. Howarth CJ, Pollock CJ, Peacock JM (1997) Development of laboratory-based methods for assessing seedling thermotolerance in pearl millet. New Phytol 137:129–139. CrossRefGoogle Scholar
  7. Jenks MA, Hasegawa PM (2015) Plant abiotic stress. J Plant Physiol 183:30–31CrossRefGoogle Scholar
  8. Kapoor D, Sharma R, Handa N et al (2015) Redox homeostasis in plants under abiotic stress: role of electron carriers, energy metabolism mediators and proteinaceous thiols. Front Environ Sci 3:13. CrossRefGoogle Scholar
  9. Kumar G, Krishnaprasad BT, Savitha M et al (1999) Enhanced expression of heat-shock proteins in thermotolerant lines of sunflower and their progenies selected on the basis of temperature-induction response (TIR). Theor Appl Genet 99:359–367. CrossRefGoogle Scholar
  10. Lämke J, Brzezinka K, Altmann S et al (2016) A hit-and-run heat shock factor governs sustained histone methylation and transcriptional stress memory. Embo J 35:162–175. CrossRefPubMedGoogle Scholar
  11. Lin MY, Chai KH, Ko SS et al (2014) A positive feedback loop between HEAT SHOCK PROTEIN101 and HEAT STRESS-ASSOCIATED 32-KD PROTEIN modulates long-term acquired thermotolerance illustrating diverse heat stress responses in rice varieties. Plant Physiol 164:2045–2053. CrossRefPubMedPubMedCentralGoogle Scholar
  12. Meyer AS, Baker TA (2011) Proteolysis in the Escherichia coli heat shock response: a player at many levels. Curr Opin Microbiol 14:194–209. CrossRefPubMedPubMedCentralGoogle Scholar
  13. Mishra SK, Tripp J, Winkelhaus S et al (2002) In the complex family of heat stress transcription factors, HsfA1 has a unique role as master regulator of thermotolerance in tomato. Genes Dev 16:1555–1567. CrossRefPubMedPubMedCentralGoogle Scholar
  14. Muñoz-muñoz JL, Garcíamolina F, Garcíaruiz PA et al (2009) Enzymatic and chemical oxidation of trihydroxylated phenols. Food Chem 113:435–444. CrossRefGoogle Scholar
  15. Nakano Y, Asada K (1981) Hydrogen peroxide scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880. CrossRefGoogle Scholar
  16. Richter K, Haslbeck M, Buchner J (2010) The heat shock response: life on the verge of death. J Mol Cell 40:253–266. CrossRefGoogle Scholar
  17. 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. CrossRefGoogle Scholar
  18. Saxena I, Srikanth S, Chen Z (2016) Cross talk between H2O2 and interacting signal molecules under plant stress response. Front Plant Sci 7:570. CrossRefPubMedPubMedCentralGoogle Scholar
  19. Song L, Jiang Y, Zhao H et al (2012) Acquired thermotolerance in plants. Plant Cell Tissue Organ Cult 111:265–276. CrossRefGoogle Scholar
  20. Srikanthbabu V, Kumar G, Krishnaprasad BT et al (2002) Identification of pea genotypes with enhanced thermotolerance using temperature induction response (TIR) technique. J Plant Physiol 159:535–545. CrossRefGoogle Scholar
  21. Stief A, Altmann S, Hoffmann K et al (2014) Arabidopsis miR156 regulates tolerance to recurring environmental stress through SPL transcription factors. Plant Cell 26:1792–1807. CrossRefPubMedPubMedCentralGoogle Scholar
  22. Sun M, Jiang F, Zhang C et al (2016) A new comprehensive evaluation system for thermo-tolerance in tomato at different growth stage. J Agric Sci Tech B 6:152–168. CrossRefGoogle Scholar
  23. Sun M, Jiang F, Cen B et al (2018) Respiratory burst oxidase homologue-dependent H2O2 and chloroplast H2O2 are essential for the maintenance of acquired thermotolerance during recovery after acclimation. Plant Cell Environ 41:2373–2389. CrossRefPubMedGoogle Scholar
  24. Sun M, Jiang F, Cen B et al (2019) Antioxidant enzymes act as indicators predicting intension of acquired and maintenance of acquired thermotolerance and the relationships between basal, acquired and maintenance of acquired thermotolerance of tomato. Sci Hortic 247:130–137. CrossRefGoogle Scholar
  25. Suzuki N, Mittler R (2006) Reactive oxygen species and temperature stresses: a delicate balance between signaling and destruction. Physiol Plant 126:45–51. CrossRefGoogle Scholar
  26. Yang JY, Sun Y, Sun AQ et al (2006) The involvement of chloroplast hsp100/clpb in the acquired thermotolerance in tomato. Plant Mol Biol 62:385–395. CrossRefPubMedGoogle Scholar
  27. Yeh CH, Kaplinsky NJ, Hu C et al (2012) Some like it hot, some like it warm: phenotyping to explore thermotolerance diversity. Plant Sci 195:10–23. CrossRefPubMedPubMedCentralGoogle Scholar
  28. Yokotani N, Ichikawa T, Kondou Y et al (2008) Expression of rice heat stress transcription factor OsHsfA2e enhances tolerance to environmental stresses in transgenic Arabidopsis. Planta 227:957–967. CrossRefPubMedGoogle Scholar
  29. Zhang J, Jiang XD, Li TL et al (2014) Photosynthesis and ultrastructure of photosynthetic apparatus in tomato leaves under elevated temperature. Photosynthetica 52:430–436. CrossRefGoogle Scholar

Copyright information

© Franciszek Górski Institute of Plant Physiology, Polish Academy of Sciences, Kraków 2019

Authors and Affiliations

  • Mintao Sun
    • 1
    • 2
  • Fangling Jiang
    • 1
    • 2
  • Rong Zhou
    • 3
  • Benjian Cen
    • 1
    • 2
  • Zhen Wu
    • 1
    • 2
    Email author
  1. 1.College of HorticultureNanjing Agricultural UniversityNanjingChina
  2. 2.Key Laboratory of Horticultural Plant Biology and Germplasm Innovation in East ChinaMinistry of AgricultureNanjingChina
  3. 3.Department of Food ScienceAarhus UniversityÅrslevDenmark

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