Cell Stress and Chaperones

, Volume 24, Issue 1, pp 247–257 | Cite as

Exogenous trehalose confers high temperature stress tolerance to herbaceous peony by enhancing antioxidant systems, activating photosynthesis, and protecting cell structure

  • Da-Qiu Zhao
  • Ting-Ting Li
  • Zhao-Jun Hao
  • Meng-Lin Cheng
  • Jun TaoEmail author
Original Paper


Herbaceous peony (Paeonia lactiflora Pall.) is an excellent ornamental plant, which is usually stressed by summer high temperatures, but little is known about its relevant measures. In this study, the effects of trehalose on alleviating high temperature-induced damage in P. lactiflora were examined. High temperature stress in P. lactiflora increased production of reactive oxygen species (ROS), including superoxide anion free radical (O2·−) and hydrogen peroxide (H2O2), enhanced both malondialdehyde (MDA) content and relative electrical conductivity (REC), decreased superoxide dismutase (SOD) activity, increased catalase (CAT) activity, inhibited photosynthesis, and destroyed cell structure. However, exogenous trehalose effectively alleviated its high temperature-induced damage. Trehalose decreased O2·− and H2O2 accumulation, MDA content, and REC, increased the activities of antioxidant enzymes, enhanced photosynthesis, improved cell structure, and made chloroplasts rounder. Additionally, trehalose induced high temperature-tolerant-related gene expressions to different degrees. These results indicated that trehalose decreased the deleterious effect of high temperature stress on P. lactiflora growth by enhancing antioxidant systems, activating photosynthesis, and protecting cell structure. These findings indicate the potential application of trehalose for managing high temperatures in P. lactiflora cultivation.


High temperature Trehalose Lipid peroxidation Antioxidant Photosynthesis 



This work was supported by the Natural Science Foundation of China (31872141), the Young Talent Support Project of Jiangsu Provincial Association for Science and Technology, the Building Project of Combined and Major Innovation Carrier of Jiangsu Province (BM2016008), Agriculture Three New Project of Jiangsu Province (SXGC[2017]297), the Program of Key Members of Yangzhou University Outstanding Young Teacher, and the Priority Academic Program Development from Jiangsu Government.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Ali Q, Ashraf M, Anwar F, Al-Qurainy F (2012) Trehalose-induced changes in seed oil composition and antioxidant potential of maize grown under drought stress. J Am Oil Chem Soc 89:1485–1493Google Scholar
  2. An Y, Zhou P, Liang JF (2014) Effects of exogenous application of abscisic acid on membrane stability, osmotic adjustment, photosynthesis and hormonal status of two lucerne (Medicago sativa L.) genotypes under high temperature stress and drought stress. Crop Pasture Sci 65:274–286CrossRefGoogle Scholar
  3. Asada K (1999) The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annu Rev Plant Biol 50:601–639CrossRefGoogle Scholar
  4. Benaroudj N, Lee DH, Goldberg AL (2001) Trehalose accumulation during cellular stress protects cells and cellular proteins from damage by oxygen radicals. J Biol Chem 276:24261–24267CrossRefGoogle Scholar
  5. Benlloch-González M, Quintero JM, Suárez MP, Sánchez-Lucas R, Fernández-Escobar R, Benlloch M (2016) Effect of moderate high temperature on the vegetative growth and potassium allocation in olive plants. J Plant Physiol 207:22–29CrossRefGoogle Scholar
  6. Berlett BS, Stadtman ER (1997) Protein oxidation in aging, disease and oxidative stress. J Biol Chem 272:20313–20316CrossRefGoogle Scholar
  7. Brett W, Isaac N, Lalehvash M, Long H, Dickman MB, Zhang X, Mundree S (2015) Trehalose accumulation triggers autophagy during plant desiccation. PLoS Genet 11:e1005705CrossRefGoogle Scholar
  8. Chakraborty K, Bishi SK, Singh AL, Zala PV, Mahatma MK, Kalariya K, Jat R (2018) Rapid induction of small heat shock proteins improves physiological adaptation to high temperature stress in peanut. J Agron Crop Sci 204:285–297. CrossRefGoogle Scholar
  9. Chen WL, Yang WJ, Lo HF, Yeh DM (2014) Physiology, anatomy, and cell membrane thermostability selection of leafy radish (Raphanus sativus var. oleiformis Pers.) with different tolerance under heat stress. Sci Hortic 179:367–375CrossRefGoogle Scholar
  10. Eissa AE, Zaki MM (2011) The impact of global climatic changes on the aquatic environment. Procedia Environ Sci 4:251–259CrossRefGoogle Scholar
  11. Fan M, Sun X, Xu N, Liao Z, Li Y, Wang J, Fan Y, Cui D, Li P, Miao Z (2017) Integration of deep transcriptome and proteome analyses of salicylic acid regulation high temperature stress in Ulva prolifera. Sci Rep 7:11052CrossRefGoogle Scholar
  12. Fernandez O, Béthencourt L, Quero A, Sangwan RS, Clément C (2010) Trehalose and plant stress responses: friend or foe? Trends Plant Sci 15:409–417CrossRefGoogle Scholar
  13. Foyer CH, Lopez-Delgado H, Dat JF, Scott IM (1997) Hydrogen peroxide and glutathione-associated mechanisms of acclamatory stress tolerance and signaling. Physiol Plant 100:241–254CrossRefGoogle Scholar
  14. Giannopolitis CN, Ries SK (1977) Superoxide dismutase. I. Occurrence in higher plants. Plant Physiol 59:309–314CrossRefGoogle Scholar
  15. Goraya GK, Kaur B, Asthir B, Bala S, Kaur G, Farooq M (2017) Rapid injuries of high temperature in plants. J Plant Biol 60:298–305CrossRefGoogle Scholar
  16. Halliwell B, Gutteridge JM (1984) Oxygen toxicity, oxygen radicals, transition metals and disease. Biochem J 219:1–14CrossRefGoogle Scholar
  17. Hao ZJ, Wei MR, Gong SJ, Zhao D, Tao J (2016) Transcriptome and digital gene expression analysis of herbaceous peony (Paeonia lactiflora Pall.) to screen thermo-tolerant related differently expressed genes. Genes Genom 38:1201–1215CrossRefGoogle Scholar
  18. Hao ZJ, Zhou CH, Liu D, Wei MR, Tao J (2017) Effects of high temperature stress on photosynthesis, chlorophyll fluorescence and ultrastructure of herbaceous peony (Paeonia lactiflora Pall.). Mol Plant Breed 15:2359–2367 (in Chinese)Google Scholar
  19. Liu H, Shen G, Fang X, Fu Q, Huang K, Chen Y, Yu H, Zhao Y, Zhang L, Jin L, Ruan S (2013) Heat stress-induced response of the proteomes of leaves from Salvia splendens Vista and King. Proteome Sci 11:25CrossRefGoogle Scholar
  20. López-Gómez M, Lluch C (2012) Trehalose and abiotic stress tolerance. In: Ahmad P, Prasad M (eds) Abiotic stress responses in plants. Springer, New YorkGoogle Scholar
  21. Luo Y, Li WM, Wang W (2008) Trehalose: protector of antioxidant enzymes or reactive oxygen species scavenger under heat stress? Environ Exp Bot 63:378–384CrossRefGoogle Scholar
  22. Luo Y, Li F, Wang GP, Yang XH, Wang W (2010) Exogenously-supplied trehalose protects thylakoid membranes of winter wheat from heat-induced damage. Biol Plant 54:495–501CrossRefGoogle Scholar
  23. Luo Y, Gao YM, Wang W, Zou CJ (2014) Application of trehalose ameliorates heat stress and promotes recovery of winter wheat seedlings. Biol Plant 58:395–398CrossRefGoogle Scholar
  24. Mostofa MG, Hossain MA, Fujita M, Tran LS (2015) Physiological and biochemical mechanisms associated with trehalose-induced copper-stress tolerance in rice. Sci Rep 5:11433CrossRefGoogle Scholar
  25. Pang CP, Ye L, Ma J, Lu T, Yang ZY, Qi MF (2017) Regulation function of trehalose on tomato seedling leaf photosynthesis under high temperature. Jiangsu Agric Sci 45:143–146 (in Chinese)Google Scholar
  26. Putten M, Schneider S, Root T (2002) Wildlife responses to climate change: north American case studies. Island PressGoogle Scholar
  27. Rehman RNU, You Y, Zhang L, Goudia BD, Khan AR, Li P, Ma F (2017) High temperature induced anthocyanin inhibition and active degradation in Malus profusion. Front Plant Sci 8:1401CrossRefGoogle Scholar
  28. Rykaczewska K (2015) The effect of high temperature occurring in subsequent stages of plant development on potato yield and tuber physiological defects. Am J Potato Res 92:339–349CrossRefGoogle Scholar
  29. Sage TL, Bagha S, Lundsgaard-Nielsen V, Branch HA, Sultmanis S, Sage RF (2015) The effect of high temperature stress on male and female reproduction in plants. Field Crops Res 182:30–42CrossRefGoogle Scholar
  30. Sang Q, Shan X, An Y, Shu S, Sun J, Guo S (2017) Proteomic analysis reveals the positive effect of exogenous spermidine in tomato seedlings’ response to high-temperature stress. Front Plant Sci 8:120Google Scholar
  31. Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative CT method. Nat Protoc 36:1101–1108CrossRefGoogle Scholar
  32. Shahbaz M, Abid A, Masood A, Waraich EA (2017) Foliar-applied trehalose modulates growth, mineral nutrition, photosynthetic ability and oxidative defense system of rice (Oryza Sativa L.) under saline stress. J Plant Nutr 40:584–599CrossRefGoogle Scholar
  33. Sun SN, Wang Q, Sun CC, Liu FJ, Bi HG, Ai XZ (2017) Response and adaptation of photosynthesis of cucumber seedlings to high temperature stress. Chinese J Applied Ecol 28:1603–1610 (in Chinese)Google Scholar
  34. Tian F, Gong J, Zhang J, Zhang M, Wang G, Li A, Wang W (2013) Enhanced stability of thylakoid membrane proteins and antioxidant competence contribute to drought stress resistance in the tasg1 wheat stay-green mutant. J Exp Bot 64:1509–1520CrossRefGoogle Scholar
  35. Wahid A, Gelani S, Ashraf M (2007) Heat tolerance in plants: An overview. Environ Exp Bot 61: 199–223Google Scholar
  36. Wang D, Luo Y, Gao YM, Zhao YY, Zou CJ (2016) Effects of exogenous trehalose on the membrane lipid peroxidation in wheat seedlings under heat stress. J Triticeae Crops 36:925–932 (in Chinese)Google Scholar
  37. Wu HY, Shou SY, Zhu ZJ, Yang X (2001) Effects of high temperature stress on photosynthesis and chlorophyll fluorescence in sweet pepper (Capsicum fructescens L.). Acta Horticulturae Sinica 28:517–521 (in Chinese)Google Scholar
  38. Wu YQ, Zhao DQ, Han CX, Tao J (2016) Biochemical and molecular responses of herbaceous peony to high temperature stress. Can J Plant Sci 96:474–484CrossRefGoogle Scholar
  39. Yang XF, Guo FQ (2014) Research advances in mechanisms of plant leaf senescence under heat stress. Plant Physiol J 50:1285–1292 (in Chinese)Google Scholar
  40. Yang GP, Rhodes D, Joly RJ (1996) Effects of high temperature on membrane stability and chlorophyll fluorescence in glycinebetaine-deficient and glycinebetaine-containing maize lines. Funct Plant Biol 23:437–443CrossRefGoogle Scholar
  41. Zhang JP, Li DQ, Li K, Xia YP (2016) Reconsideration for the southward plantation of Paeonia lactiflora. Chinese Landscape Architecture 32:91–95 (in Chinese)Google Scholar
  42. Zhao DQ, Han CG, Zhou CH, Tao J (2015) Shade ameliorates high temperature-induced inhibition of growth in herbaceous peony (Paeonia lactiflora). Int J Agric Biol 17:911–919CrossRefGoogle Scholar
  43. Zou Q (2000) Plant physiology experimental guidance. China Agricultural Press, Beijing (in Chinese)Google Scholar

Copyright information

© Cell Stress Society International 2019

Authors and Affiliations

  • Da-Qiu Zhao
    • 1
    • 2
  • Ting-Ting Li
    • 1
    • 2
  • Zhao-Jun Hao
    • 1
    • 2
  • Meng-Lin Cheng
    • 1
    • 2
  • Jun Tao
    • 1
    • 2
    Email author
  1. 1.Jiangsu Key Laboratory of Crop Genetics and Physiology, College of Horticulture and Plant ProtectionYangzhou UniversityYangzhouPeople’s Republic of China
  2. 2.Institute of Flowers and Trees IndustryYangzhou University-Rugao CityRugaoPeople’s Republic of China

Personalised recommendations