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

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Abstract

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.

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Abbreviations

GSK-3:

Glycogen synthase kinase-3

NO:

Nitric oxide

SNP:

Sodium nitroprusside

CI:

Chilling injury

MDA:

Malondialdehyde

AOX:

Alternative oxidase

HSP:

Heat shock protein

CBF:

C-Repeat binding factor

References

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Cvetkovska, M., & Vanlerberghe, G. C. (2012). Alternative oxidase modulates leaf mitochondrial concentrations of superoxide and nitric oxide. New Phytologist, 195(1), 32–39.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Jian, Z., Davis, L. C., & Verpoorte, R. (2005). Elicitor signal transduction leading to production of plant secondary metabolites. Biotechnology Advances, 23(4), 283–333.

    Article  Google Scholar 

  • Jiao, C., Zhu, L., & Gu, Z. (2017). GSK-3 mediates NO-cGMP-induced isoflavone production in soybean sprouts. Food Research International, 101, 203–208.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Lurie, S., & Crisosto, C. H. (2005). Chilling injury in peach and nectarine. Postharvest Biology and Technology, 37(3), 195–208.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

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Funding

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

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Authors and Affiliations

  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 Process, Ministry of Agriculture and Rural Affairs, Beijing, 100193, People’s Republic of China

    Caifeng Jiao & Yuquan Duan

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  1. Caifeng Jiao
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  2. Yuquan Duan
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Correspondence to Yuquan Duan.

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Highlights

• GSK-3 mediated NO-alleviated CI in peach fruit.

• GSK-3 mediated NO-reduced MDA content and electrolyte leakage.

• GSK-3 mediated NO-activated AOX.

• GSK-3 mediated NO-enhanced gene expression of 18.1 kDa classIHSP.

• GSK-3 mediated NO-enhanced gene expression of WRKY2 and CBF.

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Jiao, C., Duan, Y. The Mediation of NO-Enhanced Chilling Tolerance by GSK-3 in Postharvest Peach Fruit. Food Bioprocess Technol 12, 2028–2035 (2019). https://doi.org/10.1007/s11947-019-02367-y

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  • DOI: https://doi.org/10.1007/s11947-019-02367-y

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