Abstract
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.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Baxter A, Mittler R, Suzuki N (2014) ROS as key players in plant stress signalling. J Exp Bot 65:1229–1240. https://doi.org/10.1093/jxb/ert375
Beyer WF, Fridovich I (1987) Assaying for superoxide dismutase activity: some large consequences of minor changes in conditions. Anal Biochem 161:559–566. https://doi.org/10.1016/0003-2697(87)90489-1
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 140:1297–1305
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. https://doi.org/10.1104/pp.106.091322
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. https://doi.org/10.1007/s11010-006-9396-z
Howarth CJ, Pollock CJ, Peacock JM (1997) Development of laboratory-based methods for assessing seedling thermotolerance in pearl millet. New Phytol 137:129–139. https://doi.org/10.1046/j.1469-8137.1997.00827.x
Jenks MA, Hasegawa PM (2015) Plant abiotic stress. J Plant Physiol 183:30–31
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. https://doi.org/10.3389/fenvs.2015.00013
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. https://doi.org/10.1007/s001220051
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. https://doi.org/10.15252/embj.201592593
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. https://doi.org/10.1104/pp.113.229609
Meyer AS, Baker TA (2011) Proteolysis in the Escherichia coli heat shock response: a player at many levels. Curr Opin Microbiol 14:194–209. https://doi.org/10.1016/j.mib.2011.02.001
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. https://doi.org/10.1101/gad.228802
Muñoz-muñoz JL, Garcíamolina F, Garcíaruiz PA et al (2009) Enzymatic and chemical oxidation of trihydroxylated phenols. Food Chem 113:435–444. https://doi.org/10.1016/j.foodchem.2008.07.076
Nakano Y, Asada K (1981) Hydrogen peroxide scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880. https://doi.org/10.1093/oxfordjournals.pcp.a076232
Richter K, Haslbeck M, Buchner J (2010) The heat shock response: life on the verge of death. J Mol Cell 40:253–266. https://doi.org/10.1016/j.molcel.2010.10.006
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
Saxena I, Srikanth S, Chen Z (2016) Cross talk between H2O2 and interacting signal molecules under plant stress response. Front Plant Sci 7:570. https://doi.org/10.3389/fpls.2016.00570
Song L, Jiang Y, Zhao H et al (2012) Acquired thermotolerance in plants. Plant Cell Tissue Organ Cult 111:265–276. https://doi.org/10.1007/s11240-012-0198-6
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. https://doi.org/10.1078/0176-1617-00650
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. https://doi.org/10.1105/tpc.114.123851
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. https://doi.org/10.17265/2161-6264/2016.03.002
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. https://doi.org/10.1111/pce.13351
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. https://doi.org/10.1016/j.scienta.2018.12.015
Suzuki N, Mittler R (2006) Reactive oxygen species and temperature stresses: a delicate balance between signaling and destruction. Physiol Plant 126:45–51. https://doi.org/10.1111/j.0031-9317.2005.00582.x
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. https://doi.org/10.1007/s11103-006-9027-9
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. https://doi.org/10.1016/j.plantsci.2012.06.004
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. https://doi.org/10.1007/s00425-007-0670-4
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. https://doi.org/10.1016/j.plantsci.2012.06.004
Acknowledgements
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.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by U. Feller.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Sun, M., Jiang, F., Zhou, R. et al. Coordinated regulation of three kinds of thermotolerance in tomato by antioxidant enzymes. Acta Physiol Plant 41, 166 (2019). https://doi.org/10.1007/s11738-019-2951-5
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11738-019-2951-5