Abstract
Bioactive gibberellic acid (GA3) has been reported to mediate chilling stress responses in tomato. In this study, tomato (Solanum lycopersicum L. cv. Zhefen No. 702) fruit harvested at the mature green stage were pre-treated with 0- and 0.5-mM GA3 solution for 15 min and then stored at 4 ± 1 °C for 28 days to investigate the molecular mechanism underlying gibberellin (GA)-induced fruit tolerance to chilling stress. Results showed that GA3 treatment effectively reduced chilling injury (CI) index in mature green tomato fruit during long-term cold storage. Compared with the control, fruit treated with GA3 exhibited higher tissue GA3 levels and lower expression of the gene encoding a crucial GA signaling component and growth repressor known as DELLA protein (GAI). The expression of key GA biosynthetic genes (GA20ox1 and GA3ox1) was down-regulated, whereas the expression of GA catabolic gene (GA2ox1) was up-regulated. C-repeat/dehydration-responsive element-binding factors (CBFs) are key regulators of cold response. Transcriptional levels of CBF1 gene in GA3-treated fruit were higher than those of the control fruit. The elevated CBF1 expression was correlated with GA2ox1 up-regulation. Furthermore, exogenous GA3 treatment stimulated salicylic acid (SA) biosynthesis via isochorismate synthase (ICS) pathway. The study findings suggest new opportunities for investigation into the functional role of GA signaling network in fruit tolerance to chilling stress.
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References
Achard, P., & Genschik, P. (2009). Releasing the brakes of plant growth: how GAs shut down DELLA proteins. Journal of Experimental Botany, 60(4), 1085–1092.
Achard, P., Cheng, H., De Grauwe, L., Decat, J., Schoutteten, H., Moritz, T., et al. (2006). Integration of plant responses to environmentally activated phytohormonal signals. Science, 311(5757), 91–94.
Achard, P., Gong, F., Cheminant, S., Alioua, M., Hedden, P., & Genschik, P. (2008a). The cold-inducible CBF1 factor-dependent signaling pathway modulates the accumulation of the growth-repressing DELLA proteins via its effect on gibberellin metabolism. The Plant Cell, 20, 2117–2129.
Achard, P., Renou, J. P., Berthome, R., Harberd, N. P., & Genschik, P. (2008b). Plant DELLAs restrain growth and promote survival of adversity by reducing the levels of reactive oxygen species. Current Biology, 18(9), 656–660.
Alonso-Ramírez, A., Rodríguez, D., Reyes, D., Jiménez, J. A., Nicolás, G., López-Climent, M., et al. (2009). Evidence for a role of gibberellins in salicylic acid modulated early plant responses to abiotic stress in Arabidopsis thaliana seeds. Plant Physiology, 150(3), 1335–1344.
Bourne, M. C. (2006). Selection and use of postharvest technologies as a component of the food chain. Journal of Food Science, 69(2), 43–46.
Cruz-Mendívil, A., López-Valenzuela, J. A., Calderón-Vázquez, C. L., Vega-García, M. O., Reyes-Moreno, C., & Valdez-Ortiz, A. (2015). Transcriptional changes associated with chilling tolerance and susceptibility in ‘Micro-Tom’ tomato fruit using RNA-Seq. Postharvest Biology and Technology, 99(2015), 141–151.
Ding, Y., Wei, W., Wu, W., Davis, R. E., Jiang, Y., Lee, I.-M., et al. (2013a). Role of gibberellic acid in tomato defence against potato purple top phytoplasma infection. Annals of Applied Biology, 162(2), 191–199.
Ding, Y., Wu, W., Wei, W., Davis, R. E., Lee, I.-M., Hammond, R. W., et al. (2013b). Potato purple top phytoplasma-induced disruption of gibberellin homeostasis in tomato plants. Annals of Applied Biology, 162(1), 131–139.
Ding, Y., Sheng, J. P., Li, S. Y., Nie, Y., Zhao, J. H., 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(2015), 88–95.
Elliott, R. C., Ross, J. J., Smith, J. L., Lester, D. R., & Reid, J. B. (2001). Feed-forward regulation of gibberellin deactivation in pea. Journal of Plant Growth Regulation, 20(1), 87–94.
Harberd, N. P. (2003). Relieving DELLA restraint. Science, 299(5614), 1853–1854.
Hedden, P., & Phillips, A. L. (2000). Gibberellin metabolism: new insights revealed by the genes. Trends in Plant Science, 5(12), 523–530.
Hedden, P., & Thomas, S. G. (2012). Gibberellin biosynthesis and its regulation. Biochemical Journal, 444(1), 11–25.
Hsieh, T. H., Lee, J. T., Yang, P. T., Chiu, L. H., Charng, Y. Y., Wang, Y. C., et al. (2002). 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, 129(3), 1086–1094.
Jiang, C. F., & Fu, X. D. (2007). GA action: turning on de-DELLA repressing signaling. Current Opinion in Plant Biology, 10(5), 461–465.
Kendall, S. L., Hellwege, A., Marriot, P., Whalley, C., Graham, I. A., & Penfield, S. (2011). Induction of dormancy in Arabidopsis summer annuals requires parallel regulation of DOG1 and hormone metabolism by low temperature and CBF transcription factors. The Plant Cell, 23(7), 2568–2580.
Kim, Y., Park, S., Gilmour, S. J., & Thomashow, M. F. (2013). Roles of CAMTA transcription factors and salicylic acid in configuring the low-temperature transcriptome and freezing tolerance of Arabidopsis. The Plant Journal, 75(3), 364–376.
Lee, S. M., & Park, C.-M. (2010). Modulation of reactive oxygen species by salicylic acid in Arabidopsis seed germination under high salinity. Plant Signaling and Behavior, 5(12), 1534–1536.
Liang, L., Zhang, B., Yin, X. R., Xu, C. J., Sun, C. D., & Chen, K. S. (2013). Differential expression of the CBF gene family during postharvest cold storage and subsequent shelf-life of peach fruit. Plant Molecular Biology Reporter, 31(6), 1358–1367.
Luengwilai, K., Beckles, D. M., & Saltveit, M. E. (2012). Chilling-injury of harvested tomato (Solanum lycopersicum L.) cv. Micro-Tom fruit is reduced by temperature pre-treatments. Postharvest Biology and Technology, 63(1), 123–128.
Niu, S. H., Gao, Q., Li, Z. X., Chen, X. Y., & Li, W. (2014). The role of gibberellin in the CBF1-mediated stress-response pathway. Plant Molecular Biology Reporter, 32(4), 852–863.
Oakenfull, R. J., Baxter, R., & 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.
Sakamoto, T., Morinaka, Y., Ishiyama, K., Kobayashi, M., Itoh, H., Kayano, T., et al. (2003). Genetic manipulation of gibberellin metabolism in transgenic rice. Nature Biotechnology, 21(8), 909–913.
Schmittgen, T. D., & Livak, K. J. (2008). Analyzing real-time PCR data by the comparative CT method. Nature Protocols, 3(6), 1101–1108.
Shi, X. M., Jin, F., Huang, Y. T., Du, X. W., Li, C. M., Wang, M., et al. (2012). Simultaneous determination of five plant growth regulators in fruit by modified quick, easy, cheap, effective, rugged, and safe (QuEChERS) extraction and liquid chromatography-tandem mass spectrometry. Journal of Agricultural and Food Chemistry, 60(1), 60–65.
Sun, T. P., & Gubler, F. (2004). Molecular mechanism of gibberellin signaling in plants. Annual Review of Plant Biology, 55, 197–223.
Suo, H., Ma, Q., Ye, K., Yang, C., Tang, Y., Hao, J., et al. (2012). Overexpression of AtDREB1A causes a severe dwarf phenotype by decreasing endogenous gibberellin levels in soybean [Glycine max (L.) Merr]. PLOS ONE, 7(9), e45568.
Thomas, S. G., Phillips, A. L., & Hedden, P. (1999). Molecular cloning and functional expression of gibberellin 2-oxidases, multifunctional enzymes involved in gibberellins deactivation. Proceedings of the National Academy of Sciences of the United States of America, 96(8), 4698–4703.
Toyomasu, T., Kawaide, H., Mitsuhashi, W., Inoue, Y., & Kamiya, Y. (1998). Phytochrome regulates gibberellin biosynthesis during germination of photoblastic lettuce seeds. Plant Physiology, 118(4), 1517–1523.
Vega-García, M. O., López-Espinoza, G., Chávez Ontiveros, J., Caro-Corrales, J. J., Delgado Vargas, F., & López-Valenzuela, J. A. (2010). Changes in protein expression associated with chilling injury in tomato fruit. Journal of the American Society of Horticultural Science, 135(1), 83–89.
Vidal, A. M., Ben-Cheikh, W., Talón, M., & García-Martínez, J. L. (2003). Regulation of gibberellin 20-oxidase gene expression and gibberellin content in citrus by temperature and Citrus exocortis viroid. Planta, 217(3), 442–448.
Wang, F., Zhu, D. M., Huang, X., Li, S., Gong, Y. N., Yao, Q. F., et al. (2009). Biochemical insights on degradation of Arabidopsis DELLA proteins gained from a cell-free assay system. The Plant Cell, 21(8), 2378–2390.
Xu, Y. L., Li, L., Gage, D. A., & Zeevaart, J. A. (1999). Feedback regulation of GA5 expression and metabolic engineering of gibberellin levels in Arabidopsis. The Plant Cell, 11(5), 927–935.
Yamaguchi, S., & Kamiya, Y. (2000). Gibberellin biosynthesis: its regulation by endogenous and environmental signals. Plant and Cell Physiology, 41(3), 251–257.
Zawaski, C., & Busov, V. B. (2014). Roles of gibberellin catabolism and signaling in growth and physiological response to drought and short-day photoperiods in populous trees. PLoS ONE, 9(1), e86217.
Zentella, R., Zhang, Z. L., Park, M., Thomas, S. G., Endo, A., Murase, K., et al. (2007). Global analysis of DELLA direct targets in early gibberellin signaling in Arabidopsis. The Plant Cell, 19(10), 3037–3057.
Zhang, X., Fowler, S. G., Cheng, H. M., Lou, Y. G., Rhee, S. Y., Stockinger, E. J., et al. (2004). Freezing-sensitive tomato has a functional CBF cold response pathway, but a CBF regulon that differs from that of freezing-tolerant Arabidopsis. The Plant Journal, 39(6), 905–919.
Zhao, D. Y., Shen, L., Fan, B., Liu, K. L., Yu, M. M., Zheng, Y., et al. (2009). Physiological and genetic properties of tomato fruits from 2 cultivars differing in chilling tolerance at cold storage. Journal of Food Science, 74(5), C348–C352.
Zhao, R. R., Sheng, J. P., Lv, S. N., Zheng, Y., Zhang, J., Yu, M. M., et al. (2011). Nitric oxide participates in the regulation of LeCBF1 gene expression and improves cold tolerance in harvested tomato fruit. Postharvest Biology and Technology, 62(2011), 121–126.
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This work was supported by the National Natural Science Foundation of China (No. 31401551), the Fundamental Research Funds for the Central Research Institutes (No. 0032015017), and the Agricultural Science and Technology Innovation Program (ASTIP) from the Chinese Central Government.
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Zhen Zhu and Yang Ding contributed equally to this work.
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Zhu, Z., Ding, Y., Zhao, J. et al. Effects of Postharvest Gibberellic Acid Treatment on Chilling Tolerance in Cold-Stored Tomato (Solanum lycopersicum L.) Fruit. Food Bioprocess Technol 9, 1202–1209 (2016). https://doi.org/10.1007/s11947-016-1712-3
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DOI: https://doi.org/10.1007/s11947-016-1712-3