The Mediation of NO-Enhanced Chilling Tolerance by GSK-3 in Postharvest Peach Fruit

  • Caifeng Jiao
  • Yuquan DuanEmail author
Original Paper


The role of glycogen synthase kinase-3 (GSK-3) in nitric oxide (NO)-enhanced chilling tolerance in postharvest peach fruit was investigated. The fruits were immersed in sodium nitroprusside (SNP; exogenous NO donor) and bikinin (GSK-3 inhibitor). Results showed that the chilling injury (CI) index declined following the exposure of the peach fruit to exogenous SNP. SNP treatment also induced GSK-3 expression. Furthermore, SNP treatment reduced malondialdehyde (MDA) content and electrolyte leakage in the peach fruit. In addition, SNP treatment induced the increase in alternative oxidase (AOX) activity and the upregulation of the gene expression of 18.1-kDa class I heat shock protein (HSP), WRKY2, and C-repeat binding factor (CBF). The effects of SNP treatment were partly weakened by the addition of bikinin. These findings indicate that GSK-3 mediated the reduction of MDA content and electrolyte leakage and the activation of AOX, 18.1-kDa class I HSP, WRKY2, and CBF by NO, thereby inducing chilling tolerance in peach fruit.


SNP GSK-3 MDA and electrolyte leakage AOX HSP, WRKY and CBF Peach fruit 



Glycogen synthase kinase-3


Nitric oxide


Sodium nitroprusside


Chilling injury




Alternative oxidase


Heat shock protein


C-Repeat binding factor


Funding Information

This project was supported by the National Natural Science Foundation of China (31871862).


  1. Adachi, H., Nakano, T., Miyagawa, N., Ishihama, N., Yoshioka, M., Katou, Y., Yaeno, T., Shirasu, K., & Yoshioka, H. (2015). WRKY transcription factors phosphorylated by MAPK regulate a plant immune NADPH oxidase in Nicotiana benthamiana. Plant Cell, 27(9), 2645–2663.CrossRefGoogle Scholar
  2. Aghdam, M. S., & Mohammadkhani, N. (2014). Enhancement of chilling stress tolerance of tomato fruit by postharvest brassinolide treatment. Food and Bioprocess Technology, 7(3), 909–914.CrossRefGoogle Scholar
  3. Carranco, R., Almoguera, C., & Jordano, J. (1997). A plant small heat shock protein gene expressed during zygotic embryogenesis but noninducible by heat stress. Journal of Biological Chemistry, 272(43), 27470–27475.CrossRefGoogle Scholar
  4. Chen, G. P., Ma, W. S., Huang, Z. J., Xu, T., Xue, Y. B., & Shen, Y. Z. (2003). Isolation and characterization of TaGSK1 involved in wheat salt tolerance. Plant Science, 165(6), 1369–1375.CrossRefGoogle Scholar
  5. Cheng, M., Huang, Z., Hua, Q., Shan, W., Kuang, J., Lu, W., et al. (2017). The WRKY transcription factor HpWRKY44 regulates CytP450-like1 expression in red pitaya fruit (Hylocereus polyrhizus). Horticulture Research, 4, 17039.CrossRefGoogle Scholar
  6. Cvetkovska, M., & Vanlerberghe, G. C. (2012). Alternative oxidase modulates leaf mitochondrial concentrations of superoxide and nitric oxide. New Phytologist, 195(1), 32–39.CrossRefGoogle Scholar
  7. Ding, C., Wang, C., Gross, K., & Smith, D. (2001). Reduction of chilling injury and transcript accumulation of heat shock proteins in tomato fruit by methyl jasmonate and methyl salicylate. Plant Science, 161(6), 1153–1159.CrossRefGoogle Scholar
  8. Ding, Y., Sheng, J., Li, S., Nie, Y., Zhao, J., Zhu, Z., et al. (2015). The role of gibberellins in the mitigation of chilling injury in cherry tomato (Solanum lycopersicum L.) fruit. Postharvest Biology and Technology, 101(101), 88–95.CrossRefGoogle Scholar
  9. Ding, Y., Zhu, Z., Zhao, J., Nie, Y., Yu, Z., Sheng, J., et al. (2016). Effects of postharvest brassinolide treatment on the metabolism of white button mushroom (Agaricus bisporus) in relation to development of browning during storage. Food and Bioprocess Technology, 9(8), 1327–1334.CrossRefGoogle Scholar
  10. Dong, J., Qin, Y., Li, L., & Xua, M. (2012). Effect of yeast saccharide treatment on nitric oxide accumulation and chilling injury in cucumber fruit during cold storage. Postharvest Biology and Technology, 68(2), 1–7.CrossRefGoogle Scholar
  11. Hsieh, T., Lee, J., Yang, P., Chiu, L., Charng, Y., Wang, Y., et al. (2004). 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 Physiology, 135(2), 1145–1145.CrossRefGoogle Scholar
  12. Hu, X., Yang, J., & Li, C. (2015). Transcriptomic response to nitric oxide treatment in Larix olgensis Henry. International Journal of Molecular Sciences, 16(12), 28582–28597.CrossRefGoogle Scholar
  13. Jang, H. J., Pih, K. T., Kang, S. G., Lim, J. H., Jin, J. B., Hai, L. P., et al. (1998). Molecular cloning of a novel Ca2+-binding protein that is induced by NaCl stress. Plant Molecular Biology, 37(5), 839–847.CrossRefGoogle Scholar
  14. Jian, Z., Davis, L. C., & Verpoorte, R. (2005). Elicitor signal transduction leading to production of plant secondary metabolites. Biotechnology Advances, 23(4), 283–333.CrossRefGoogle Scholar
  15. Jiao, C., Zhu, L., & Gu, Z. (2017). GSK-3 mediates NO-cGMP-induced isoflavone production in soybean sprouts. Food Research International, 101, 203–208.CrossRefGoogle Scholar
  16. Jiao, C., Chai, Y., & Duan, Y. (2019). Inositol 1, 4, 5-trisphosphate mediates nitric-oxide-induced chilling tolerance and defense response in postharvest peach fruit. Journal of Agricultural and Food Chemistry, 67(17), 4764–4773.CrossRefGoogle Scholar
  17. Jin, P., Duan, Y., Wang, L., Wang, J., & Zheng, Y. (2014). Reducing chilling injury of loquat fruit by combined treatment with hot air and methyl jasmonate. Food and Bioprocess Technology, 7, 2259–2266.CrossRefGoogle Scholar
  18. Jonak, C., Beisteiner, D., Beyerly, J., & Hirt, H. (2000). Wound-induced expression and activation of WIG, a novel glycogen synthase kinase 3. Plant Cell, 12(8), 1467–1476.CrossRefGoogle Scholar
  19. Kudla, J., Xu, Q., Harter, K., Gruissem, W., & Luan, S. (1999). Genes for calcineurin B-like proteins in Arabidopsis are differentially regulated by stress signals. Proceedings of the National Academy of Sciences of the United States of America, 96(8), 4718–4723.CrossRefGoogle Scholar
  20. Leo, A. D. (2012). Involvement of hydrogen peroxide, calcium, and ethylene in the induction of the alternative pathway in chilling-stressed Arabidopsis callus. Planta, 235(1), 53–67.CrossRefGoogle Scholar
  21. Luisa, E., Roberta, M., Andrea, B., Claus, W., Otto, M., Lara, R., et al. (2006). Interaction between nitric oxide and ethylene in the induction of alternative oxidase in ozone-treated tobacco plants. Plant Physiology, 142(2), 595–608.CrossRefGoogle Scholar
  22. Luo, D. L., Ba, L. J., Shan, W., Kuang, J. F., Lu, W. J., & Chen, J. Y. (2017). Involvement of WRKY transcription factors in ABA-induced cold tolerance of banana fruit. Journal of Agricultural and Food Chemistry, 65(18), 3627–3635.CrossRefGoogle Scholar
  23. Lurie, S., & Crisosto, C. H. (2005). Chilling injury in peach and nectarine. Postharvest Biology and Technology, 37(3), 195–208.CrossRefGoogle Scholar
  24. Mao, G., Meng, X., Liu, Y., Zheng, Z., Chen, Z., & Zhang, S. (2011). Phosphorylation of a WRKY transcription factor by two pathogen-responsive MAPKs drives phytoalexin biosynthesis in Arabidopsis. Plant Cell, 23(4), 1639–1653.CrossRefGoogle Scholar
  25. Oakenfull, R. J., Robert, B., & Knight, M. R. (2013). A C-repeat binding factor transcriptional activator (CBF/DREB1) from European bilberry (Vaccinium myrtillus) induces freezing tolerance when expressed in Arabidopsis thaliana. PLoS One, 8(1), e54119.CrossRefGoogle Scholar
  26. Ruan, J., Li, M., Jin, H., Sun, L., Zhu, Y., Xu, M., & Dong, J. (2015). UV-B irradiation alleviates the deterioration of cold-stored mangoes by enhancing endogenous nitric oxide levels. Food Chemistry, 169, 417–423.CrossRefGoogle Scholar
  27. Sehrawat, A., Gupta, R., & Deswal, R. (2013). Nitric oxide-cold stress signalling cross-talk, evolution of a novel regulatory mechanism. Proteomics, 13(12-13), 1816–1835.CrossRefGoogle Scholar
  28. Shao, X., Zhu, Y., Cao, S., Wang, H., & Song, Y. (2013). Soluble sugar content and metabolism as related to the heat-induced chilling tolerance of loquat fruit during cold storage. Food and Bioprocess Technology, 6(12), 3490–3498.CrossRefGoogle Scholar
  29. Shi, J., Kim, K. N., Ritz, O., Albrecht, V., Gupta, R., Harter, K., Luan, S., & Kudla, J. (1999). Novel protein kinases associated with calcineurin B-like calcium sensors in Arabidopsis. The Plant Cell, 11(12), 2393–2405.PubMedPubMedCentralGoogle Scholar
  30. Vanlerberghe, G. C. (2013). Alternative oxidase: a mitochondrial respiratory pathway to maintain metabolic and signaling homeostasis during abiotic and biotic stress in plants. International Journal of Molecular Sciences, 14(4), 6805–6847.CrossRefGoogle Scholar
  31. Wang, C. Y., Fung, R. W. M., & Ding, C. K. (2005). Reducing chilling injury and enhancing transcript levels of heat shock proteins, PR-proteins and alternative oxidase by methyl jasmonate and methyl salicylate in tomatoes and peppers. V International Postharvest Symposium, 6821, 481–486.Google Scholar
  32. Wang, L., Chen, S., Kong, W., Li, S., & Archbold, D. (2006). Salicylic acid pretreatment alleviates chilling injury and affects the antioxidant system and heat shock proteins of peaches during cold storage. Postharvest Biology and Technology, 41(3), 244–251.CrossRefGoogle Scholar
  33. Xua, M., Zhang, M., Xu, X., & Sun, L. (2012). Cold-induced endogenous nitric oxide generation plays a role in chilling tolerance of loquat fruit during postharvest storage. Postharvest Biology and Technology, 65(3), 5–12.CrossRefGoogle Scholar
  34. Yan, C., Fan, M., Yang, M., Zhao, J., Zhang, W., Su, Y., Xiao, L., Deng, H., & Xie, D. (2018). Injury activates Ca2+/calmodulin-dependent phosphorylation of JAV1-JAZ8-WRKY51 complex for jasmonate biosynthesis. Molecular Cell, 70(1), 136–149.CrossRefGoogle Scholar
  35. Yang, G., Zhang, W., Liu, Z., Yi-Maer, A. Y., Zhai, M., & Xu, Z. (2017). Both JrWRKY2 and JrWRKY7 of Juglans regia mediate responses to abiotic stresses and abscisic acid through formation of homodimers and interaction. Plant Biology, 19(2), 268–278.CrossRefGoogle Scholar
  36. Yao, W., Xu, T., Farooq, S. U., Peng, J., & Zheng, Y. (2018). Glycine betaine treatment alleviates chilling injury in zucchini fruit (Cucurbita pepo L.) by modulating antioxidant enzymes and membrane fatty acid metabolism. Postharvest Biology and Technology, 144, 20–28.CrossRefGoogle Scholar
  37. Zahra, K., Hana, C., Sarah, H., Cathrine, M. K., & Zachara, N. E. (2010). O-linked β-N-acetylglucosamine (O-GlcNAc) regulates stress-induced heat shock protein expression in a GSK-3β-dependent manner. Journal of Biological Chemistry, 285(50), 39096–39107.CrossRefGoogle Scholar
  38. Zhu, Z., Ding, Y., Zhao, J., Nie, Y., Yu, Z., Sheng, J., et al. (2016). Effects of postharvest gibberellic acid treatment on chilling tolerance in cold-stored tomato (Solanum lycopersicum L.) fruit. Food and Bioprocess Technology, 9(7), 1202–1209.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Institute of Food Science and Technology, Chinese Academy of Agricultural Sciences/Key Laboratory of Agro-products Quality and Safety Control in Storage and Transport ProcessMinistry of Agriculture and Rural AffairsBeijingPeople’s Republic of China

Personalised recommendations