Abstract
Postharvest yellowing is accompanied by the rapid nutrition deterioration of broccoli. Here, we investigated the effect of 24-epibrassinolide (EBR) treatment on the change of glucosinolates content during the yellowing of broccoli. EBR treatment maintained the content of glucosinolates, as indicated by higher levels of glucoraphanin, glucobrassicin, and neoglucobrassicin. Meanwhile, the transcript levels of BoCYP83A1 and BoCYP83B1 as well as BoMYB28, BoMYB34, and BoMYB122 involved in the glucosinolates biosynthesis pathway were upregulated in the treatment sample. Furthermore, the expressions of BoBRI1 gene and crucial transcription factors BoBZR1 and BoBES1 that participated in the brassinosteroids signal transduction pathway were activated under EBR treatment, which indirectly alleviated the decrease of glucosinolates content. Orthogonal partial least square model and pathway analysis further demonstrated that the improvement of glucosinolate biosynthetic ability and the enhancement of brassinosteroids signal transduction might be the mechanism responsible for the conservation of glucosinolates by EBR treatment.
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Data Availability
The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
Aghdam, M. S., & Mohammadkhani, N. (2014). Enhancement of chilling stress tolerance of tomato fruit by postharvest brassinolide treatment. Food and Bioprocess Technology, 7, 909–914. https://doi.org/10.1007/s11947-013-1165-x
Alvarez-Jubete, L., Valverde, J., Kehoe, K., Reilly, K., Rai, K. D., & Barry-Ryan, C. (2014). Development of a novel functional soup rich in bioactive sulforaphane using broccoli (Brassica oleracea L. ssp. italica) florets and byproducts. Food and Bioprocess Technology, 7, 1310–1321. https://doi.org/10.1007/s11947-013-1113-9
An, J. P., Wang, X. F., Zhang, X. W., You, C. X., & Hao, Y. J. (2021). Apple b-box protein bbx37 regulates jasmonic acid mediated cold tolerance through the jaz-bbx37-ice1-cbf pathway and undergoes miel1-mediated ubiquitination and degradation. New Phytologist, 229, 2707–2729. https://doi.org/10.1111/nph.17050
Bak, S., & Feyereisen, R. (2001). The involvement of two P450 enzymes, CYP83B1 and CYP83A1, in auxin homeostasis and glucosinolate biosynthesis. Plant Physiology, 127, 108–118. https://doi.org/10.1104/pp.127.1.108
Barickman, T., Kopsell, D., & Sams, C. (2013). Selenium influences glucosinolate and isothiocyanates and increases sulfur uptake in Arabidopsis thaliana and rapid-cycling Brassica oleracea. Journal of Agricultural and Food Chemistry, 61, 202–209. https://doi.org/10.1021/jf3037227
Ben-Fadhel, Y., Ziane, N., Salmieri, S., & Lacroix, M. (2018). Combined post-harvest treatments for improving quality and extending shelf-life of minimally processed broccoli florets (Brassica oleracea var. italica). Food and Bioprocess Technology, 11, 84–95. https://doi.org/10.1007/s11947-017-1992-2
Brown, P. D., Tokuhisa, J. G., Reichelt, M., & Gershenzon, J. (2003). Variation of glucosinolate accumulation among different organs and developmental stages of Arabidopsis thaliana. Phytochemistry, 62(3), 471–481. https://doi.org/10.1016/S0031-9422(02)00549-6
Cai, J. H., Luo, F., Zhao, Y. B., Zhou, Q., & Ji, S. J. (2019a). 24-Epibrassinolide treatment regulates broccoli yellowing during shelf life. Postharvest Biology and Technology, 154, 87–95. https://doi.org/10.1016/j.postharvbio.2019.04.019
Cai, J. H., Cheng, S. C., Luo, F., Zhao, Y. B., Wei, B. D., Zhou, Q., Zhou, X., & Ji, S. J. (2019b). Influence of ethylene on morphology and pigment changes in harvested broccoli. Food and Bioprocess Technology, 12, 883–897. https://doi.org/10.1007/s11947-019-02267-1
Cai, L. Y., Cao, M. J., Cao, A. L., & Zhang, W. D. (2019c). The effect of magnetic nanoparticles plus microwave thawing on the volatile flavor characteristics of largemouth bass (Micropterus salmoides) fillets. Food and Bioprocess Technology, 12, 1340–1351. https://doi.org/10.1007/s11947-019-02299-7
Chai, Y. M., Zhang, Q., Tian, L., Li, C. L., Xing, Y., Qin, L., & Shen, Y. Y. (2013). Brassinosteroid is involved in strawberry fruit ripening. Plant Growth Regulation, 69, 63–69. https://doi.org/10.1007/s10725-012-9747-6
Chen, L. G., Gao, Z. H., Zhao, Z. Y., Liu, X. Y., Li, Y. P., Zhang, Y. X., Liu, X. G., Sun, Y., & Tang, W. Q. (2019). BZR1 family transcription factors function redundantly and indispensably in BR signaling but exhibit bri1-independent function in regulating anther development in Arabidopsis. Molecular Plant, 12(10), 1408–1415. https://doi.org/10.1016/j.molp.2019.06.006
Chen, J. N., Nolan, T. M., Ye, H. X., Zhang, M. C., Tong, H. N., Xin, P. Y., Chu, J. F., Chu, C. C., Li, Z. H., & Yin, Y. H. (2017). Arabidopsis WRKY46, WRKY54, and WRKY70 transcription factors are involved in Brassinosteroid-Regulated plant growth and drought responses. The Plant Cell, 29(6), 1425–1439. https://doi.org/10.1105/tpc.17.00364
Ding, Y., Zhu, Z., Zhao, J. H., Nie, Y., Zhang, Y., Sheng, J. P., Meng, D. M., Mao, H. M., & Tang, X. M. (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, 1327–1334. https://doi.org/10.1007/s11947-016-1722-1
Dinkova-Kostova, A. T., & Kostov, R. V. (2012). Glucosinolates and isothiocyanates in health and disease. Trends in Molecular Medicine, 18, 337–347. https://doi.org/10.1016/j.molmed.2012.04.003
Fang, H. X., Luo, F., Li, P. X., Zhou, Q., Zhou, X., Wei, B. D., Cheng, S. C., Zhou, H. S., & Ji, S. J. (2020). Potential of jasmonic acid (JA) in accelerating postharvest yellowing of broccoli by promoting its chlorophyll degradation. Food Chemistry, 309, 125737. https://doi.org/10.1016/j.foodchem.2019.125737
Fang, H. X., Zhou, Q., Yang, Q. X., Zhou, X., Cheng, S. C., Wei, B. D., Li, J. K., & Ji, S. J. (2022). Influence of combined edible coating with chitosan and tea polyphenol on the quality deterioration and health-promoting compounds in harvested broccoli. Food and Bioprocess Technology, 15, 407–420. https://doi.org/10.1007/s11947-021-02751-7
Gao, H., Chai, H. K., Cheng, N., & Cao, W. (2017). Effects of 24-epibrassinolide on enzymatic browning and antioxidant activity of fresh-cut lotus root slices. Food Chemistry., 217, 45–51. https://doi.org/10.1016/j.foodchem.2016.08.063
Gigolashvili, T., Berger, B., & Flügge, U.-I. (2009). Specific and coordinated control of indolic and aliphatic glucosinolate biosynthesis by R2R3-myb transcription factors in Arabidopsis thaliana. Phytochemistry Reviews, 8(1), 3–13. https://doi.org/10.1007/s11101-008-9112-6
Groenbaek, M., Tybirk, E., & Kristensen, H. L. (2018). Glucosinolate and carotenoid content of white- and yellow-flowering rapeseed grown for human consumption as sprouts and seedlings under light emitting diodes. European Food Research and Technology, 244, 1121–1131. https://doi.org/10.1007/s00217-017-3027-7
Gu, Y. J., Guo, Q. H., Zhang, L., Chen, Z., Han, Y., & Gu, Z. (2012). Physiological and biochemical metabolism of germinating broccoli seeds and sprouts. Journal of Agricultural and Food Chemistry, 60, 209–213. https://doi.org/10.1021/jf203599v
Guo, R. F., Qian, H. M., Shen, W. S., Liu, L. H., Zhang, M., Cai C. X., Zhao, Y. T., Qiao, J. J., & Wang, Q. M. (2013). BZR1 and BES1 participate in regulation of glucosinolate biosynthesis by brassinosteroids in Arabidopsis. Journal of Experimental Botany, 64(8). https://doi.org/10.1093/jxb/ert094.
Guo, R. F., Hou, Q. M., Yuan, G. F., Zhao, Y. T., & Wang, Q. M. (2014). Effect of 2, 4-epibrassinolide on main health-promoting compounds in broccoli sprouts. LWT - Food Science and Technology, 58(1), 287–292. https://doi.org/10.1016/j.lwt.2014.02.047
Guo, L., Yang, R., & Gu, Z. (2016). Cloning of genes related to aliphatic glucosinolate metabolism and the mechanism of sulforaphane accumulation in broccoli sprouts under jasmonic acid treatment. Journal of the Science of Food and Agriculture, 96(13), 4329–4336. https://doi.org/10.1002/jsfa.7629
Guo, Y. F., Shan, W., Liang, S. M., Wu, C. J., Wei, W., Chen, J. Y., Lu, W. J., & Kuang, J. F. (2018). MaBZR1/2 act as transcriptional repressors of ethylene biosynthetic genes in banana fruit. Physiologia Plantarum, 165(3), 555–568. https://doi.org/10.1111/ppl.12750
Jannatizadeh, A., Aghdam, M. S., Luo, Z. S., & Razavi, F. (2019). Impact of exogenous melatonin application on chilling injury in tomato fruits during cold storage. Food and Bioprocess Technology, 12, 741–750. https://doi.org/10.1007/s11947-019-2247-1
Ji, Y. L., Qu, Y., Jiang, Z. Y., Yan, J. J., Chu, J. F., Xu, M. Y., Su, X., Yuan, H., & Wang, A. D. (2021). The mechanism for brassinosteroids suppressing climacteric fruit ripening. Plant Physiology, 185(4), 1875–1893. https://doi.org/10.1093/plphys/kiab013
Kang, M. K., Choi, J. H., Kim, H. S., Kushad, M. M., Jeffery, E. H., & Juvik, J. A. (2013). Methyl jasmonate and 1-methylcyclopropene treatment effects on quinone reductase inducing activity and post-harvest quality of broccoli. PLoS ONE, 8(10), e77127. https://doi.org/10.1371/journal.pone.0077127
Kim, H., Seomun, S., Yoon, Y., & Jang, G. (2021). Jasmonic acid in plant abiotic stress tolerance and interaction with abscisic acid. Agronomy, 11, 1886. https://doi.org/10.3390/agronomy11091886
Klug, T. V., Martínez-Hernández, G. B., Collado, E., Artés, F., & Artés-Hernández, F. (2018). Effect of microwave and high-pressure processing on quality of an innovative broccoli hummus. Food and Bioprocess Technology, 11, 1464–1477. https://doi.org/10.1007/s11947-018-2111-8
Lee, J. H., Lee, J., Kim, H. R., Chae, W. B., Kim, S., Lim, Y. P., & Oh, M. H. (2018). Brassinosteroids regulate glucosinolate biosynthesis in Arabidopsis thaliana. Physiologia Plantarum, 163, 450–458. https://doi.org/10.1111/ppl.12691
Lee, Y. R., Chen, M., Lee, J. D., Zhang, J., Lin, S. Y., Fu, T. M., Chen, H., Ishikawa, T., Chiang, S. Y., Katon, J., Shulga, Y. V., Bester, A. C., Fung, J., Monteleone, E., Wan, L, Shen, C., Hsu, C. H., Papa, A., Clohessy, J. G., Teruya-Feldstein, J., Jain, S., Wu, H., Matesic, L., Chen, R. H., Wei, W., & Pandolfi P. P. (2019). Reactivation of PTEN tumor suppressor for cancer treatment through inhibition of a MYC-WWP1 inhibitory pathway. Science, 364(6441), eaau0159. https://doi.org/10.1126/science.aau0159.
Li, G., & Quiros, C. F. (2002). Genetic analysis, expression and molecular characterization of BoGSL-ELONG, a major gene involved in the aliphatic glucosinolate pathway of brassica species. Genetics, 162(4), 1937–1943. https://doi.org/10.1093/genetics/162.4.1937
Li, Y., Palliyaguru, D. L., & Kensler, T. W. (2016). Frugal chemoprevention: Targeting Nrf2 with foods rich in sulforaphane. Seminars in Oncology, 43, 146–153. https://doi.org/10.1053/j.seminoncol.2015.09.013
Li, Z. S., Zheng, S. N., Liu, Y. M., Fang, Z. Y., Yang, L. M., Zhuang, M., Zhang, Y. Y., Lv, H. H., Wang, Y., & Xu, D. H. (2020). Characterization of glucosinolates in 80 broccoli genotypes and different organs using UHPLC-Triple-Tof-MS method. Food Chemistry, 334, 127519. https://doi.org/10.1016/j.foodchem.2020.127519
Lu, Z. M., Wang, X. L., Cao, M. M., Li, Y. Y., Su, J. L., & Gao, H. (2019). Effect of 24-epibrassinolide on sugar metabolism and delaying postharvest senescence of kiwifruit during ambient storage. Scientia Horticulturae, 253, 1–7. https://doi.org/10.1016/j.scienta.2019.04.028
Luo, F., Cai, J. H., Zhang, X., Tao, D. B., Zhou, X., Zhou, Q., Zhao, Y. B., Wei, B. D., Cheng, S. C., & Ji, S. J. (2018). Effects of methyl jasmonate and melatonin treatments on the sensory quality and bioactive compounds of harvested broccoli. Rsc Advances, 8(72), 41422–41431. https://doi.org/10.1039/C8RA07982J
Luo, F., Cheng, S. C., Cai, J. H., Wei, B. D., Zhou, X., Zhou, Q., Zhao, Y. B., & Ji, S. J. (2019a). Chlorophyll degradation and carotenoid biosynthetic pathways: Gene expression and pigment content in broccoli during yellowing. Food Chemistry, 297, 124964.1–124964.9. https://doi.org/10.1016/j.foodchem.2019a.124964.
Luo, F., Cai, J. H., Kong, X. M., Zhou, X., Zhou, Q., Zhao, Y. B., & Ji, S. J. (2019b). Transcriptome profiling reveals the roles of pigment mechanisms in postharvest broccoli yellowing. Horticulture Research, 6, 74. https://doi.org/10.1038/s41438-019-0155-1
Lv, B. S., Tian, H. Y., Zhang, F., Liu, J. J., Lu, S. C., Bai, M. Y., Li, C. Y., & Ding, Z. J. (2018). Brassinosteroids regulate root growth by controlling reactive oxygen species homeostasis and dual effect on ethylene synthesis in Arabidopsis. PLoS Genetics, 14, e1007144. https://doi.org/10.1371/journal.pgen.1007144
Major, I., Yoshida, Y., Campos, M., Kapali, G., Xin, X. F., Sugimoto, K., & Howe, G. A. (2017). Regulation of growth-defense balance by the JASMONATE ZIM-DOMAIN (JAZ)-MYC transcriptional module. New Phytologist, 215(4), 1533–1547. https://doi.org/10.1111/nph.14638
Meng, X. Y., Zhang, M., Zhan, Z. G., & Adhikari, B. (2014). Changes in quality characteristics of fresh-cut cucumbers as affected by pressurized argon treatment. Food and Bioprocess Technology, 7, 693–701. https://doi.org/10.1007/s11947-013-1092-x
Miao, H., Zeng, W., Zhao, M., Wang, J., & Wang, Q. (2020). Effect of melatonin treatment on visual quality and health-promoting properties of broccoli florets under room temperature. Food Chemistry, 319, 126498. https://doi.org/10.1016/j.foodchem.2020.126498
Nassarawa, S. S., Abdelshafy, A. M., Xu, Y., Li, L., & Luo, Z. (2021). Effect of light-emitting diodes (LEDs) on the quality of fruits and vegetables during postharvest period: A review. Food and Bioprocess Technology, 14, 388–414. https://doi.org/10.1007/s11947-020-02534-6
Pan, G., Liu, Y. Q., Ji, L. S., Zhang, X., He, J., Huang, J., & Wan, J. M. (2018). Brassinosteroids mediate susceptibility to brown planthopper by integrating with the salicylic acid and jasmonic acid pathways in rice. Journal of Experimental Botany, 69(18), 4433–4442. https://doi.org/10.1093/jxb/ery223
Pathak, N., Caleb, O. J., Geyer, M., Herppich, W. B., Rauh, C., & Mahajan, P. V. (2017). Photocatalytic and photochemical oxidation of ethylene: Potential for storage of fresh produce—A review. Food and Bioprocess Technology, 10, 982–1001. https://doi.org/10.1007/s11947-017-1889-0
Sønderby, I. E., Geu-Flores, F., & Halkier, B. A. (2010). Biosynthesis of glucosinolates—Gene discovery and beyond. Trends in Plant Science, 15(5), 283–290. https://doi.org/10.1016/j.tplants.2010.02.005
Soares, A., Carrascosa, C., & Raposo, A. (2017). Influence of different cooking methods on the concentration of glucosinolates and vitamin C in broccoli. Food and Bioprocess Technology, 10, 1387–1411. https://doi.org/10.1007/s11947-017-1930-3
Sreeramulu, S., Mostizky, Y., Sunitha, S., Shani, E., Nahum, H., Salomon, D., Hayun, L. B., Gruetter, C., Rauh, D., Ori, N., & Sessa, G. (2013). BSKs are partially redundant positive regulators of brassinosteroid signaling in Arabidopsis. Plant Journal, 74(6), 905–919. https://doi.org/10.1111/tpj.12175
Sun, H. J., Luo, M. L., Zhou, X., Zhou, Q., & Ji, S. J. (2020a). Influence of melatonin treatment on peel browning of cold-stored “Nanguo” Pears. Food and Bioprocess Technology, 13, 1478–1490. https://doi.org/10.1007/s11947-020-02489-8
Sun-Waterhouse, D., & Wadhwa, S. S. (2013). Industry-relevant approaches for minimising the bitterness of bioactive compounds in functional foods: A review. Food and Bioprocess Technology, 6, 607–627. https://doi.org/10.1007/s11947-012-0829-2
Sun, Y. K., Zhou, S. S., Guo, H., Zhang, J., Ma, T. J., Zheng, Y., Zhang, Z. G., & Cai, L. (2020b). Protective effects of sulforaphane on type 2 diabetes-induced cardiomyopathy via AMPK-mediated activation of lipid metabolic pathways and NRF2 function. Metabolism, 102, 154002. https://doi.org/10.1016/j.metabol.2019.154002
Traw, M., Kim, J., Enright, S., Cipollini, D., & Bergelson, J. (2003). Negative crosstalk between salicylate- and jasmonate-mediated pathways in the Wassilewskija ecotype of Arabidopsis thaliana. Molecular Ecology, 12, 1125–1135. https://doi.org/10.1046/j.1365-294X.2003.01815.x
Wang, M. Y., Cai, C. X., Lin, J. Y., Tao, H., Zeng, W., Zhang, F., Miao, H. Y., Sun, B., & Wang, Q. M. (2020). Combined treatment of epi-brassinolide and NaCl enhances the main phytochemicals in Chinese kale sprouts. Food Chemistry, 315(2), 126275. https://doi.org/10.1016/j.foodchem.2020.126275
Wasternack, C., & Strnad, M. (2019). Jasmonates are signals in the biosynthesis ofsecondary metabolites - Pathways, transcription factors and applied aspects A brief review. New Biotechnology, 48, 1–11. https://doi.org/10.1016/j.nbt.2017.09.007
Wei, L. Y., Liu, C. H., Zheng, H. H., & Zheng, L. (2019). Melatonin treatment affects the glucoraphanin-sulforaphane system in postharvest fresh-cut broccoli (brassica oleracea L.). Food Chemistry, 307, 125562. https://doi.org/10.1016/j.foodchem.2019.125562.
Yang, C. J., Zhang, C., Lu, Y. N., Jin, J. Q., & Wang, X. L. (2011). The mechanisms of brassinosteroids’ action: From signal transduction to plant development. Molecular Plant, 4, 588–600. https://doi.org/10.1093/mp/ssr020
Yang, Q. X., Zhou, Q., Zhou, X., Fang, H. X., Zhao, Y. B., Wei, B. D., & Ji, S, J. (2022). Insights into profiling of glucosinolates and genes involved in its metabolic pathway accompanying post-harvest yellowing of broccoli. Postharvest Biology and Technology, 185, 111780. https://doi.org/10.1016/j.postharvbio.2021.111780
Zhu, Z., Zhang, Z. Q., Qin, G. Z., & Tian, S. P. (2010). Effects of brassinosteroids on postharvest disease and senescence of jujube fruit in storage. Postharvest Biology & Technology, 56(1), 50–55. https://doi.org/10.1016/j.postharvbio.2009.11.014
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This work was supported by the National Key R&D Program of China [grant number 2016YFD0400103].
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Qingxi Yang: investigation, data curation, formal analysis, writing—original draft. Manli Luo: conceptualization, supervision, visualization. Qian Zhou: conceptualization, resources. Xin Zhou: investigation, conceptualization. Yingbo Zhao: resources, validation. Jianye Chen: conceptualization, resources. Shujuan Ji: project administration, funding acquisition, writing—review and editing.
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Yang, Q., Luo, M., Zhou, Q. et al. Insights into Profiling of 24-Epibrassinolide Treatment Alleviating the Loss of Glucosinolates in Harvested Broccoli. Food Bioprocess Technol 15, 2697–2711 (2022). https://doi.org/10.1007/s11947-022-02909-x
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DOI: https://doi.org/10.1007/s11947-022-02909-x