Biologia Plantarum

, Volume 59, Issue 2, pp 382–388 | Cite as

Effects of acclimation and pretreatment with abscisic acid or salicylic acid on tolerance of Trigonobalanus doichangensis to extreme temperatures

  • Y. L. Zheng
  • W. Q. LiEmail author
  • W. B. Sun
Original Papers


The effects of acclimation to cold (4 °C) and heat (36/38/40 °C) on corresponding freezing and heat tolerances of one-year-old Trigonobalanus doichangensis seedlings were studied. In addition, the effects of abscisic acid (ABA) and salicylic acid (SA) pretreatments on the tolerance of this species to temperature extremes were tested. The results show that the content of soluble sugars increased with the duration of acclimation to cold (4 °C), and the relative electrical conductivity and malondialdehyde content increased significantly after 7 d; however, the content of proline did not vary significantly. After acclimation to cold for 3 and 7 d, the semilethal low temperature (LLT50) was 0.8 and 1.1 °C lower, respectively, compared with that of the control. The maximum quantum yield of photosystem II (measured as variable to maximum fluorescence ratio, Fv/Fm) decreased significantly after freezing treatments (−4 to −8 °C), however, less when the plants were pretreated with 1–100 mg dm−3 ABA. Acclimation to heat did not increase the semilethal high temperature (LHT50). A low concentration (1 mg dm−3) of SA increased LHT50, but medium and high concentrations (10 and 100 mg dm−3) decreased it. Fv/Fm decreased significantly after a heat shock (45–54 °C). The pretreatment with 1–50 mg dm−3 SA ameliorated a subsequent heat (48 °C) stress.

Additional key words

cold stress heat stress plant hormones semilethal temperature 



abscisic acid


electrical conductivity


heat shock protein


semilethal high temperature


semilethal low temperature


semilethal temperature


photosystem II


relative electrical conductivity


reactive oxygen species


salicylic acid


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  1. Aspinall, D., Paleg, L.G.: Proline accumulation: physiological aspects. — In Paleg, L.G., Aspinall, D. (ed.): The Physiology and Biochemistry of Drought Resistance in Plants. Pp. 205–241. Academic Press, Sydney 1981.Google Scholar
  2. Bohnert, H.J., Sheveleva, E.: Plant stress adaptations — making metabolism move. — Curr. Opin. Plant. Biol. 1: 267–274, 1998.PubMedCrossRefGoogle Scholar
  3. Crepet, W.L., Nixon, K.C.: Earliest megafossil evidence of Fagaceae: phylogenetic and biogeographic implications. — Amer. J. Bot. 76: 842–855, 1989.CrossRefGoogle Scholar
  4. Dat, J.F., Lopez-Delgado, H., Foyer, C.H., Scott, I.M.: Effects of salicylic acid on oxidative stress and thermotolerance in tobacco. — J. Plant Physiol. 156: 659–665, 2000.CrossRefGoogle Scholar
  5. Farhad, M.S., Babak, A.M., Reza, Z.M., Mir Hassan, R.S., Afshin, T.: Response of proline, soluble sugars, photosynthetic pigments and antioxidant enzymes in potato (Solanum tuberosum L.) to different irrigation regimes in greenhouse condition. — Aust. J. Crop Sci. 5: 55–60, 2011.Google Scholar
  6. Forman, L.: Trigonobalanus, a new genus of Fagaceae, with notes on the classification of the family. — Kew Bull. 17: 381–396, 1964.CrossRefGoogle Scholar
  7. Fracheboud, Y., Haldimann, P., Leipner, J., Stamp, P.: Chlorophyll fluorescence as a selection tool for cold tolerance of photosynthesis in maize (Zea mays L.). — J. exp. Bot. 50: 1533–1540, 1999.CrossRefGoogle Scholar
  8. Gusta, L.V., Trischuk, R., Weiser, C.J.: Plant cold acclimation: the role of abscisic acid. — J. Plant Growth Regul. 24: 308–318, 2005.CrossRefGoogle Scholar
  9. Guy, C.L.: Cold acclimation and freezing stress tolerance: role of protein metabolism. — Annu. Rev. Plant Physiol. Plant mol. Biol. 41: 187–223, 1990.CrossRefGoogle Scholar
  10. Heino, P., Palva, E.T.: Signal transduction in plant cold acclimation. — In Hirt, H., Shinozaki K. (ed.): Plant Responses to Abiotic Stress. Pp. 151–186. Springer-Verlag, Berlin — Heidelberg 2003.CrossRefGoogle Scholar
  11. Hsieh, T.H., Lee, J.T., Yang, P.T., Chiu, L.H., Charng, Y.Y., Wang, Y.C., Chan, M.T.: Heterology expression of the Arabidopsis C-repeat/dehydration response element binding factor 1 gene confers elevated tolerance to chilling and oxidative stresses in transgenic tomato. — Plant Physiol. 129:1086–1094, 2002.PubMedCentralPubMedCrossRefGoogle Scholar
  12. Horváth, E., Pál, M., Szalai, G., Páldi, E., Janda, T.: Exogenous 4-hydroxybenzoic acid and salicylic acid modulate the effect of short-term drought and freezing stress on wheat plants. — Biol. Plant. 51: 480–487, 2007a.CrossRefGoogle Scholar
  13. Horváth, E., Szalai, G., Janda, T.: Induction of abiotic stress tolerance by salicylic acid signaling. — J. Plant Growth Regul. 26: 290–300, 2007b.CrossRefGoogle Scholar
  14. Iba, K.: Acclimative response to temperature stress in higher plants: approaches of gene engineering for temperature tolerance. — Annu. Rev. Plant Biol. 53: 225–245, 2002.PubMedCrossRefGoogle Scholar
  15. Kaplan, F., Kopka, J., Haskell, D.W., Zhao, W., Schiller, K.C., Gatzke, N., Sung, D.Y., Guy, C.L.: Exploring the temperature-stress metabolome of Arabidopsis. — Plant Physiol. 136: 4159–4168, 2004.PubMedCentralPubMedCrossRefGoogle Scholar
  16. Kaplan, F., Kopka, J., Sung, D.Y., Zhao, W., Popp, M., Porat, R., Guy, C.L.: Transcript and metabolite profiling during cold acclimation of Arabidopsis reveals an intricate relationship of cold-regulated gene expression with modifications in metabolite content. — Plant J. 50: 967–981, 2007.PubMedCrossRefGoogle Scholar
  17. Kayihan, C., Eyidogan, F., Afsar, N., Oktem, H. A., Yucel M.: Cu/Zn superoxide dismutase activity and respective gene expression during cold acclimation and freezing stress in barley cultivars. — Biol. Plant. 56: 693–698, 2012.CrossRefGoogle Scholar
  18. Koster, K.L., Lynch, D.V.: Solute accumulation and compartmentation during the cold acclimation of Puma rye. — Plant Physiol. 98: 108–113, 1992.PubMedCentralPubMedCrossRefGoogle Scholar
  19. Krause, G.H., Weis, E.: Chlorophyll fluorescence and photosynthesis: the basics. — Annu. Rev. Plant Physiol. Plant mol. Biol. 42: 313–349, 1991.CrossRefGoogle Scholar
  20. Levitt, J.: Response of Plants to Environmental Stresses. Vol. 1: Chilling, Freezing and High Temperature Stresses. — Academic Press, New York 1980.Google Scholar
  21. Marmiroli, N., Restivo, F.M., Smith, C.J., Di Cola, G., Maestri, E., Tassi, F.: Induction of heat shock response and acquisition of thermotolerance in callus cultures of Gerbera jamesonii. — In Vitro cell. dev. Biol. Plant 33: 49–55, 1997.CrossRefGoogle Scholar
  22. Minami, A., Nagao, M., Ikegami, K., Koshiba, T., Arakawa, K., Fujikawa, S., Takezawa, D.: Cold acclimation in bryophytes: low-temperature-induced freezing tolerance in Physcomitrella patens is associated with increases in expression levels of stress-related genes but not with increase in level of endogenous abscisic acid. — Planta 220: 414–423, 2005.PubMedCrossRefGoogle Scholar
  23. Mutlu, S., Karadağoğlu, Ö., Atici, Ö., Nalbantoğlu, B.: Protective role of salicylic acid applied before cold stress on antioxidative system and protein patterns in barley apoplast. — Biol. Plant. 57: 507–513, 2013.CrossRefGoogle Scholar
  24. Naliwajski, M.R., Skłodowska, M.: The oxidative stress and antioxidant systems in cucumber cells during acclimation to salinity. — Biol. Plant. 58: 47–54, 2014.CrossRefGoogle Scholar
  25. Nautiyal, P.C., Rajgopal, K., Zala, P.V., Pujari, D.S., Basu, M., Dhadhal, B.A., Nandre, B.M.: Evaluation of wild Arachis species for abiotic stress tolerance: 1. Thermal stress and leaf water relations. — Euphytica 159: 43–57, 2008.CrossRefGoogle Scholar
  26. Nixon, K.C., Crepet, W.L.: Trigonobalanus (Fagaceae): taxonomic status and phylogenetic relationships. — Amer. J. Bot. 76: 828–841, 1989.CrossRefGoogle Scholar
  27. Roy, R., Mazumder, P.B., Sharma, G.D.: Proline, catalase and root traits as indices of drought resistance in bold grained rice (Oryza sativa) genotypes. — Afr. J. Biotechnol. 8: 6521–6528, 2009.Google Scholar
  28. Ruelland, E., Vaultier, M.N., Zachowski, A., Hurry, V.: Cold signaling and cold acclimation in plants. — Adv. Bot. Res. 49: 35–150, 2009.CrossRefGoogle Scholar
  29. Sakai, A., Larcher, W. ??: Frost Survival of Plants: Responses and Adaptation to Freezing Stress. — Springer-Verlag, New York 1987.CrossRefGoogle Scholar
  30. Samaras, Y., Bressan, R.A., Csonka, L.N., García-Ríos, M.G., Paino, D., Urzo, M., Rhodes, D.: Proline accumulation during drought and salinity. — In Smirnoff, N. (ed.): Environment and Plant Metabolism. Pp. 161–187. Bios Scientific Publishers, Oxford 1995.Google Scholar
  31. Shi, Q., Bao, Z., Zhu, Z., Ying, Q., Qian, Q.: Effects of different treatments of salicylic acid on heat tolerance, chlorophyll fluorescence, and antioxidant enzyme activity in seedlings of Cucumis sativa L.. — Plant Growth Regul. 48: 127–135, 2006.CrossRefGoogle Scholar
  32. Spoel, S.H., Dong, X.: Making sense of hormone crosstalk during plant immune responses. — Cell Host Microbe 3: 348–351, 2008.PubMedCrossRefGoogle Scholar
  33. Sridevi, V., Satyanarayana, N.V., Madhavarao, K.V.: Induction of heat shock proteins and acquisition of thermotolerance in germinating pigeonpea seeds. — Biol. Plant. 42: 589–597, 1999.CrossRefGoogle Scholar
  34. Theocharis, A., Clément, C., Ait Barka, E.: Physiological and molecular changes in plants grown at low temperatures. — Planta 235: 1091–1105, 2012.PubMedCrossRefGoogle Scholar
  35. Thomashow, M.F.: Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. — Annu. Rev. Plant Physiol. Plant mol. Biol. 50: 571–599, 1999.PubMedCrossRefGoogle Scholar
  36. Wahid, A., Gelani, S., Ashraf, M., Foolad, M.R.: Heat tolerance in plants: an overview. — Environ. exp. Bot. 61: 199–223, 2007.CrossRefGoogle Scholar
  37. Wang, X.K. (ed.): Principles and Techniques of Plant Physiological Biochemical Experiment. — Higher Education Press, Beijing 2006.Google Scholar
  38. Webb, M.S., Uemura, M., Steponkus, P.L.: A comparison of freezing injury in oat and rye: two cereals at the extremes of freezing tolerance. — Plant Physiol. 104: 467–478, 1994.PubMedCentralPubMedGoogle Scholar
  39. Welling, A., Palva, E.T.: Molecular control of cold acclimation in trees. — Physiol. Plant. 127: 167–181, 2006.CrossRefGoogle Scholar
  40. Xia, Y.Y., Ye, H., Ma, J.L., Jiang, Z.P., He, X.Y.: The study on semi-lethal high temperature and heat tolerance of four Camellia oleifera Abel clones. — Chin. Agr. Sci. Bull. 28: 58–61, 2012.Google Scholar
  41. Zhang, J., Wu, X., Niu, R., Liu, Y., Liu, N., Xu, W., Wang, Y.: Cold-resistence evaluation in 25 wild grape species. — Vitis 51: 153–160, 2012.Google Scholar
  42. Zhou, Z.K.: Origin, phylogeny and dispersal of Quercus from China. — Acta bot. yunnanica 14: 227–236, 1992.Google Scholar
  43. Zhu, J.H., Dong, C.H., Zhu, J.K.: Interplay between coldresponsive gene regulation, metabolism and RNA processing during plant cold acclimation. — Curr. Opin. Plant Biol. 10: 290–295, 2007.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  1. 1.Key Laboratory of Biodiversity Conservation in Southwest China, State Forestry AdministrationSouthwest Forestry UniversityKunmingP.R. China
  2. 2.The Germplasm Bank of Wild Species, Kunming Institute of BotanyChinese Academy of SciencesKunmingP.R. China
  3. 3.Kunming Botanical Garden, Kunming Institute of BotanyChinese Academy of SciencesKunmingP.R. China

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