Melatonin enhanced the disease resistance by regulating reactive oxygen species metabolism in postharvest jujube fruit
Lele Zhang
College of Food Science, Shanxi Normal University, Linfen, China
Contribution: Writing - review & editing
Search for more papers by this authorYouwei Yu
College of Food Science, Shanxi Normal University, Linfen, China
Contribution: Investigation, Resources
Search for more papers by this authorLulu Chang
College of Food Science, Shanxi Normal University, Linfen, China
Contribution: Conceptualization, Methodology
Search for more papers by this authorXiaojia Wang
College of Food Science, Shanxi Normal University, Linfen, China
Contribution: Data curation
Search for more papers by this authorCorresponding Author
Shaoying Zhang
College of Food Science, Shanxi Normal University, Linfen, China
Correspondence
Shaoying Zhang, College of Food Science, Shanxi Normal University, Linfen 041001, China.
Email: [email protected]
Contribution: Formal analysis, Funding acquisition
Search for more papers by this authorLele Zhang
College of Food Science, Shanxi Normal University, Linfen, China
Contribution: Writing - review & editing
Search for more papers by this authorYouwei Yu
College of Food Science, Shanxi Normal University, Linfen, China
Contribution: Investigation, Resources
Search for more papers by this authorLulu Chang
College of Food Science, Shanxi Normal University, Linfen, China
Contribution: Conceptualization, Methodology
Search for more papers by this authorXiaojia Wang
College of Food Science, Shanxi Normal University, Linfen, China
Contribution: Data curation
Search for more papers by this authorCorresponding Author
Shaoying Zhang
College of Food Science, Shanxi Normal University, Linfen, China
Correspondence
Shaoying Zhang, College of Food Science, Shanxi Normal University, Linfen 041001, China.
Email: [email protected]
Contribution: Formal analysis, Funding acquisition
Search for more papers by this authorAbstract
Melatonin (MT), as a putative pleiotropic signal molecule, could participate in inducing postharvest disease resistance and inhibiting postharvest pathogen infection in fruit. In this study, we investigate the mechanism of induced resistance by MT treatment against Alternaria rot of jujube. The results showed that 2 and 20 μmol/L MT did not have direct antimicrobial activity, 200 μmol/L MT had little influence on antifungal activity against Alternaria alternata in vitro. MT significantly reduced the lesion area of fruit inoculated with A. alternata. MT decreased the relative electrolytic leakage, malondialdehyde content, hydrogen peroxide, and the rate of superoxide anion production, while enhanced the ascorbic acid and reduced glutathione contents. Furthermore, MT observably increased the defensive enzyme activities of superoxide dismutase, the catalase, ascorbate peroxidase, peroxidase. Accordingly, these results indicated that MT treatment increased the disease resistance of jujube fruit by regulating reactive oxygen species metabolism.
Novelty impact statement
The results showed that MT treatment could inhibit the expansion of lesion diameter, reduce the decay rate of winter jujube, and reduce the accumulation of reactive oxygen species by activating the oxidase system, thus enhancing the resistance of winter Jujube fruit to Alternaria alternata infection by adjusting the ROS mechanism.
CONFLICT OF INTEREST
The authors have declared no conflicts of interest for this article.
Open Research
DATA AVAILABILITY STATEMENT
The raw/processed data required to reproduce these findings cannot be shared at this time as the data also forms part of an ongoing study.
REFERENCES
- Bao, G., Bi, Y., Li, Y., Kou, Z., Hu, L., Ge, Y., & Wang, D. (2014). Overproduction of reactive oxygen species involved in the pathogenicity of Fusarium in potato tubers. Physiological and Molecular Plant Pathology, 86, 35–42. https://doi.org/10.1016/j.pmpp.2014.01.004
- Bisquert, R., Muniz-Calvo, S., & Guillamon, J. (2018). Protective role of intracellular melatonin against oxidative stress and UV radiation in Saccharomyces cerevisiae. Frontiers in Microbiology, 9, 318. https://doi.org/10.3389/fmicb.2018.00318
- Bradley, D. J., Kjellbom, P., & Lamb, C. J. (1992). Elicitor- and wound-induced oxidative cross-linking of a proline-rich plant cell wall protein: A novel, rapid defense response. Cell, 70(1), 21–30. https://doi.org/10.1016/0092-8674(92)90530-P
- Camejo, D., Guzmán-Cedeño, A., Vera-Macias, L., & Jiménez, A. (2019). Oxidative post-translational modifications controlling plant-pathogen interaction. Plant Physiology and Biochemistry, 144, 110–117. https://doi.org/10.1016/j.plaphy.2019.09.020
- Fan, M., Li, W., Hu, X., Nehela, Y., Yu, G., & Zhang, X. (2016). Effect of micro-vacuum storage on active oxygen metabolism, internal browning and related enzyme activities in Laiyang pear (Pyrus bretschneideri Reld). LWT-Food Science and Technology, 72, 467–474. https://doi.org/10.1016/j.lwt.2016.05.015
- Gao, H., Lu, Z., Yang, Y., Wang, D., Yang, T., Cao, M., & Cao, W. (2018). Melatonin treatment reduces chilling injury in peach fruit through its regulation of membrane fatty acid contents and phenolic metabolism. Food Chemistry, 245, 659–666. https://doi.org/10.1016/j.foodchem.2017.10.008
- Gao, H., Zhang, Z. K., Chai, H. K., Cheng, N., Yang, Y., Wang, D. N., & Cao, W. (2016). Melatonin treatment delays postharvest senescence and regulates reactive oxygen species metabolism in peach fruit. Postharvest Biology and Technology, 118, 103–110. https://doi.org/10.1016/j.postharvbio.2016.03.006
- Garcia, J. J., Lopez-Pingarron, L., Almeida-Souza, P., Tres, A., Escudero, P., Garcia-Gil, F. A., & Bernal-Perez, M. (2014). Protective effects of melatonin in reducing oxidative stress and in preserving the fluidity of biological membranes: A review. Journal of Pineal Research, 56(3), 225–237. https://doi.org/10.1111/jpi.12128
- Ge, Y., Bi, Y., & Guest, D. I. (2013). Defence responses in leaves of resistant and susceptible melon (Cucumis melo L.) cultivars infected with Colletotrichum lagenarium. Physiological and Molecular Plant Pathology, 81, 13–21. https://doi.org/10.1016/j.pmpp.2012.09.002
- Hu, W., Yang, H., Tie, W., Yan, Y., Ding, Z., Liu, Y., & Jin, Z. (2017). Natural variation in banana varieties highlights the role of melatonin in postharvest ripening and quality. Journal of Agricultural and Food Chemistry, 65(46), 9987–9994. https://doi.org/10.1021/acs.jafc.7b03354
- Jiang, X., Lin, H., Lin, M., Chen, Y., Wang, H., Lin, Y., Shi, J., & Lin, Y. (2018). A novel chitosan formulation treatment induces disease resistance of harvested litchi fruit to Peronophythora litchii in association with ROS metabolism. Food Chemistry, 266(2018), 299–308. https://doi.org/10.1016/j.foodchem.2018.06.010
- Lee, H. Y., Byeon, Y., & Back, K. (2014). Melatonin as a signal molecule triggering defense responses against pathogen attack in Arabidopsis and tobacco. Journal of Pineal Research, 57(3), 262–268. https://doi.org/10.1111/jpi.12165
- Li, S., Xu, Y., Bi, Y., Zhang, B., Shen, S., Jiang, T., & Zheng, X. (2019). Melatonin treatment inhibits gray mold and induces disease resistance in cherry tomato fruit during postharvest. Postharvest Biology and Technology, 157, 110962. https://doi.org/10.1016/j.postharvbio.2019.110962
- Liu, C., Chen, L., Zhao, R., Li, R., & Shen, L. (2019). Melatonin induces disease resistance to botrytis cinerea in tomato fruit by activating jasmonic acid signaling pathway. Journal of Agricultural and Food Chemistry, 67, 6116–6124. https://doi.org/10.1021/acs.jafc.9b00058
- Mandal, M. K., Suren, H., Ward, B., Boroujerdi, A., & Kousik, C. (2018). Differential roles of melatonin in plant-host resistance and pathogen suppression in cucurbits. Journal of Pineal Research, 65(3), 12505. https://doi.org/10.1111/jpi.12505
- Onik, J. C., Wai, S. C., Li, A., Lin, Q., Sun, Q., Wang, Z., & Duan, Y. (2021). Melatonin treatment reduces ethylene production and maintains fruit quality in apple during postharvest storage. Food Chemistry, 337, 127753. https://doi.org/10.1016/j.foodchem.2020.127753
- Prochazkova, D., Sairam, R. K., Srivastava, G. C., & Singh, D. V. (2001). Oxidative stress and antioxidant activity as the basis of senescence in maize leaves. Plant Science, 161(4), 765–771. https://doi.org/10.1016/S0168-9452(01)00462-9
- Quiroga, M., de Forchetti, S. M., Taleisnik, E., & Tigier, H. A. (2001). Tomato root peroxidase isoenzymes: Kinetic studies of the coniferyl alcohol peroxidase activity, immunological properties and role in response to salt stress. Journal of Plant Physiology, 158(8), 1007–1013. https://doi.org/10.1078/0176-1617-00304
- Reiter, R., Tan, D., & Galano, A. (2014). Melatonin reduces lipid peroxidation and membrane viscosity. Frontiers in Physiology, 5, 377. https://doi.org/10.3389/fphys.2014.00377
- Ren, Y., Wang, Y., Bi, Y., Ge, Y., Wang, Y., Fan, C., & Deng, H. (2012). Postharvest BTH treatment induced disease resistance and enhanced reactive oxygen species metabolism in muskmelon (Cucumis melo L.) fruit. European Food Research and Technology, 234(6), 963–971. https://doi.org/10.1007/s00217-012-1715-x
- Sun, Y., Liu, Z., Lan, G., Jiao, C., & Sun, Y. (2019). Effect ofexogenous melatonin on resistance of cucumber to downy mildew. Scientia Horticulturae, 255, 231–241. https://doi.org/10.1016/j.scienta.2019.04.057
- Sun, J., Lin, H., Zhang, S., Lin, Y., Wang, H., Lin, M., Hung, Y. C., & Chen, Y. (2018). The roles of ros production-scavenging system in lasiodiplodia theobromae (pat.) griff. & maubl.-induced pericarp browning and disease development of harvested longan fruit. Food Chemistry, 247, 16–22. https://doi.org/10.1016/j.foodchem.2017.12.017
- Tai, F. (1979). Sylloge fungorum sinicorum (pp. 1–1527). Science Press.
- Wang, F., Zhang, X., Yang, Q., & Zhao, Q. (2019). Exogenous melatonin delays postharvest fruit senescence and maintains the quality of sweet cherries. Food Chemistry, 301, 125311. https://doi.org/10.1016/j.foodchem.2019.125311
- Wang, S. Y., Shi, X. C., Wang, R., Wang, H. L., Liu, F., & Laborda, P. (2020). Melatonin in fruit production and postharvest preservation: A review. Food Chemistry, 320, 126642. https://doi.org/10.1016/j.foodchem.2020.126642
- Wang, Y., Yu, T., Li, Y., Cai, D., Liu, X., Lu, H., & Zheng, X. D. (2009). Postharvest biocontrol of Alternaria alternata in Chinese winter jujube by Rhodosporidium paludigenum. Journal of Applied Microbiology, 107(5), 1492–1498.
- Wei, J., Li, D., Zhang, J., Shan, C., Rengel, Z., Song, Z., & Chen, Q. (2018). Phytomelatonin receptor PMTR1-mediated signaling regulates stomatal closure in Arabidopsis thaliana. Journal of Pineal Research, 65(2), e12500. https://doi.org/10.1111/jpi.12500
- Wei, Y., Hu, W., Wang, Q., Zeng, H., Li, X., Yan, Y., & Shi, H. (2016). Identification, transcriptional and functional analysis of heat-shock protein 90s in banana (Musa acuminata L.) highlight their novel role in melatonin-mediated plant response to Fusarium wilt. Journal of Pineal Research, 62(1), e12367. https://doi.org/10.1111/jpi.12367
- Xu, M., Pan, Y., Leng, J., Li, H., & Li, X. (2020). Effect of different high oxygen treatments on preservation of seedless long jujube in low temperature storage. Journal of Food Processing and Preservation, 44(1), e14314. https://doi.org/10.1111/jfpp.14314
- Xu, X., Yan, S., Bo, S., Jian, Z., & Guo, X. (2010). Effects of exogenous melatonin on active oxygen metabolism of cucumber seedlings under high temperature stress. Chinese Journal of Applied Ecology, 21(5), 1295. https://doi.org/10.3724/SP.J.1142.2010.40521
- Yan, J., Cao, J., Jiang, W., & Zhao, Y. (2012). Effects of preharvest oligochitosan sprays on postharvest fungal diseases, storage quality, and defense responses in jujube (Zizyphus jujuba mill. cv. Dongzao) fruit. Scientia Horticulturae, 142, 196–204. https://doi.org/10.1016/j.scienta.2012.05.025
- Yan, J., Yuan, S., Wang, C., Ding, X., Cao, J., & Jiang, W. (2015). Enhanced resistance of jujube (Zizyphus jujuba mill. cv. Dongzao) fruit against postharvest Alternaria rot by β-aminobutyric acid dipping. Scientia Horticulturae, 186, 108–114. https://doi.org/10.1016/j.scienta.2012.05.025
- Yin, L., Wang, P., Li, M., Ke, X., Li, C., Liang, D., & Ma, F. (2013). Exogenous melatonin improves Malus resistance to Marssonina apple blotch. Journal of Pineal Research, 54(4), 426–434. https://doi.org/10.1111/jpi.12038
- Zhang, S., Yu, Y., Xiao, C., Wang, X., & Lei, Y. (2014). Effect of ultraviolet irradiation combined with chitosan coating on preservation of jujube under ambient temperature. LWT - Food Science and Technology, 57(2), 749–754. https://doi.org/10.1016/j.lwt.2014.02.046
- Zhang, T., Shi, Z., Zhang, X., Zheng, S., Wang, J., & Mo, J. (2020). Alleviating effects of exogenous melatonin on salt stress in cucumber. Scientia Horticulturae, 262, 109070. https://doi.org/10.1016/j.scienta.2019.109070
- Zhang, W., Cao, J., Fan, X., & Jiang, W. (2020). Applications of nitric oxide and melatonin in improving postharvest fruit quality and the separate and crosstalk biochemical mechanisms. Trends in Food Science & Technology, 99, 531–541. https://doi.org/10.1016/j.tifs.2020.03.024
- Zhao, H., Zhang, K., Zhou, X., Xi, L., Wang, Y., Xu, H., & Zou, Z. (2017). Melatonin alleviates chilling stress in cucumber seedlings by up-regulation of CsZat12 and modulation of polyamine and abscisic acid metabolism. Science Report, 7, 4998. https://doi.org/10.1038/s41598-017-05267-3
- Zhao, Y., Tu, K., Su, J., Tu, S., Hou, Y., Liu, F., & Zou, X. (2009). Heat treatment in combination with antagonistic yeast reduces diseases and elicits the active defense responses in harvested cherry tomato fruit. Journal of Agricultural and Food Chemistry, 57(16), 7565–7570. https://doi.org/10.1021/jf901437q
- Zheng, H., Liu, W., Liu, S., Liu, C., & Zheng, L. (2019). Effects of melatonin treatment on the enzymatic browning and nutritional quality of fresh-cut pear fruit. Food Chemistry, 299, 125116.1–125116.8. https://doi.org/10.1016/j.foodchem.2019.125116