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Glucosinolates are important phytochemicals in Brassicaceae. We investigated the effect of CaCl2-HCl electrolyzed water (CHEW) on glucosinolates biosynthesis in broccoli sprouts. The results showed that CHEW treatment significantly decreased reactive oxygen species (ROS) and malondialdeh yde (MDA) contents in broccoli sprouts. On the the 8th day, compared to tap water treatment, the the total glucosinolate content of broccoli sprouts with CHEW treatment increased by 10.6% and calcium content was dramatically enhanced from 14.4 mg/g DW to 22.7 mg/g DW. Comparative transcriptome and metabolome analyses revealed that CHEW treatment activated ROS and calcium signaling transduction pathways in broccoli sprouts and they interacted through MAPK cascades. Besides, CHEW treatment not only promoted the biosynthesis of amino acids, but also enhanced the expression of structural genes in glucosinolate synthesis through transcription factors (MYBs, bHLHs, WRKYs, etc.). The results of this study provided new insights into the regulatory network of glucosinolates biosynthesis in broccoli sprouts under CHEW treatment.


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Transcriptomics integrated with metabolomics reveals the mechanism of CaCl2-HCl electrolyzed water-induced glucosinolate biosynthesis in broccoli sprouts

Show Author's information Cui Lia,Shuhui SongbYanan HeaHaijie Liua( )
College of Food Science and Nutritional Engineering, China Agricultural University, Beijing 100083, China
Institute of Agri-food Processing and Nutrition, Beijing Academy of Agriculture and Forestry Sciences, Beijing 100097, China

Peer review under responsibility of Tsinghua University Press.

Abstract

Glucosinolates are important phytochemicals in Brassicaceae. We investigated the effect of CaCl2-HCl electrolyzed water (CHEW) on glucosinolates biosynthesis in broccoli sprouts. The results showed that CHEW treatment significantly decreased reactive oxygen species (ROS) and malondialdeh yde (MDA) contents in broccoli sprouts. On the the 8th day, compared to tap water treatment, the the total glucosinolate content of broccoli sprouts with CHEW treatment increased by 10.6% and calcium content was dramatically enhanced from 14.4 mg/g DW to 22.7 mg/g DW. Comparative transcriptome and metabolome analyses revealed that CHEW treatment activated ROS and calcium signaling transduction pathways in broccoli sprouts and they interacted through MAPK cascades. Besides, CHEW treatment not only promoted the biosynthesis of amino acids, but also enhanced the expression of structural genes in glucosinolate synthesis through transcription factors (MYBs, bHLHs, WRKYs, etc.). The results of this study provided new insights into the regulatory network of glucosinolates biosynthesis in broccoli sprouts under CHEW treatment.

Keywords: Metabolomics, Transcriptomics, Glucosinolates, Broccoli sprouts, CaCl2-HCl electrolyzed water

References(38)

[1]

L. Subedi, J.H. Lee, S. Yumnam, et al., Anti-inflammatory effect of sulforaphane on LPS-activated microglia potentially through JNK/AP-1/NF-κB inhibition and Nrf2/HO-1 activation, Cells 8 (2019) 194. http://doi.org/10.3390/cells8020194.

[2]

R.Q. Yang, Q.R. Hui, Z.X. Gu, et al., Effects of CaCl2 on the metabolism of glucosinolates and the formation of isothiocyanates as well as the antioxidant capacity of broccoli sprouts, J. Funct. Foods 24 (2016) 156-163. http://doi.org/10.1016/j.jff.2016.04.007.

[3]

N. Nagata, L. Xu, S. Kohno, et al., Glucoraphanin ameliorates obesity and insulin resistance through adipose tissue browning and reduction of metabolic endotoxemia in mice, Diabetes 66 (2017) 1222-1236. http://doi.org/10.2337/db16-0662.

[4]

T. Martins, B. Colao, C. Venancio, et al., Potential effects of sulforaphane to fight obesity, J. Sci. Food Agric. (2018) 98. http://doi.org/10.1002/jsfa.8898.

[5]

S. Liu, H.B. Huang, X.Q. Yi, et al., Dissection of genetic architecture for glucosinolate accumulations in leaves and seeds of Brassica napus by genome-wide association study, Plant Biotechnol. J. 18 (2020) 1472-1484. http://doi.org/10.1111/pbi.13314.

[6]

I. Blaevi, S. Montaut, F. Burul, et al., Glucosinolate structural diversity, identification, chemical synthesis and metabolism in plants, Phytochemistry 169 (2019) 112100. http://doi.org/10.1016/j.phytochem.2019.112100.

[7]

J.W. Fahey, A.T. Zalcmann, P. Talalay, The chemical diversity and distribution of glucosinolates and isothiocyanates among plants, Phytochemistry 56 (2001) 5-51. http://doi.org/10.1016/S0031-9422(00)00316-2.

[8]

N. Agerbirk, C.E. Olsen, Glucosinolate structures in evolution, Phytochemistry 77 (2012)16-45. http://doi.org/10.1016/j.phytochem.2012.02.005.

[9]

M. Piotrowski, A. Schemenewitz, A. Lopukhina, et al., Desulfoglucosinolate sulfotransferases from arabidopsis thaliana catalyze the final step in the biosynthesis of the glucosinolate core structure, J. Biol. Chem. 279 (2004) 50717-50725. http://doi.org/10.1074/jbc.M407681200.

[10]

J.W. Fahey, Y.S. Zhang, P. Talalay, Broccoli sprouts: an exceptionally rich source of inducers of enzymes that protect against chemical carcinogens, PNAS 94 (1997) 10367-10372. http://doi.org/10.1073/pnas.94.19.10367.

[11]

M. Ouassou, M. Mukhaimar, A.E. Amrani, et al., Biosynthè se des glucosinolates indoliques et rle é cologique de leurs modifications secondaires biosynthesis of indole glucosinolates and ecological role of secondary modification pathways, C. R. Biol. 342 (2019) 58-80. http://doi.org/10.1016/j.crvi.2019.03.005.

[12]

I.E. Sønderby, F. Geu-Flores, B.-A. Halkier, Biosynthesis of glucosinolates--gene discovery and beyond, Trends Plant Sci. 15 (2010) 283-290. http://doi.org/10.1016/j.tplants.2010.02.005.

[13]

L.P. Guo, Y.L. Zhu, F.W. Wang, Calcium sulfate treatment enhances bioactive compounds and antioxidant capacity in broccoli sprouts during growth and storage, Postharvest Biol. Tec. 139 (2018) 12-19. http://doi.org/10.1016/j.postharvbio.2018.01.010.

[14]

J.H. Sun, L.P. Kou, P. Geng, et al., Metabolomic assessment reveals an elevated level of glucosinolate content in CaCl2 treated broccoli microgreens, J. Agric. Food Chem. 63 (2015) 1863-1868. http://doi.org/10.1021/jf504710r.

[15]

L.Z. Li, J. X. Hao, S.H. Song, et al., Effect of slightly acidic electrolyzed water on bioactive compounds and morphology of broccoli sprouts, Food Res. Int. 105 (2018) 102-109. https://doi.org/10.1016/j.foodres.2017.10.052.

[16]

L. Zhuang, K.X. Xu, Y.L. Zhu, et al., Calcium affects glucoraphanin metabolism in broccoli sprouts under ZnSO4 stress, Food Chem. 334 (2021) 127520. http://doi.org/10.1016/j.foodchem.2020.127520.

[17]

J.W. Wang, K. Huang, Y.J. Huang, et al., The research progress of transcription factors regulating glucosinolates biosynthesis in cruciferous vegetables, Yuan Yi Xue Bao 46 (2019) 1752-1764. http://doi.org/10.16420/j.issn.0513-353x.2019-0462.

[18]

T.T. Dong, R.P. Han, J.W. Yu, et al., Anthocyanins accumulation and molecular analysis of correlated genes by metabolome and transcriptome in green and purple asparaguses (Asparagus officinalis L.), Food Chem. 271 (2019) 18-28. http://doi.org/10.1016/j.foodchem.2018.07.120.

[19]

C. Li, S.H. Song, Y.N. He, et al., CaCl2-HCl electrolyzed water affects glucosinolate metabolism and improves the quality of broccoli sprouts, Food Res. Int. 150 (2021) 110807. http://doi.org/10.1016/j.foodres.2021.110807.

[20]

S. Nasser, K. Kemal, P. M. Schenk, Global plant stress signaling: reactive oxygen species at the cross-road, Front. Plant Sci. 7 (2016) 1-21. http://doi.org/10.3389/fpls.2016.00187.

[21]

L.Z. Li, S.H. Song, S. Nirasawa, et al., Slightly acidic electrolyzed water treatment enhances the main bioactive phytochemicals content in broccoli sprouts via changing metabolism, J. Agric. Food Chem. 67 (2019) 606-614. http://doi.org/10.1021/acs.jafc.8b04958.

[22]

E. Katz, D.A. Chamovitz, Wounding of Arabidopsis leaves induces indole-3-carbinol-dependent autophagy in roots of Arabidopsis thaliana, Plant J. 91 (2017) 779-787. http://doi.org/10.1111/tpj.13610.

[23]

E. Katz, R. Bagchi, V. Jeschke, et al., Diverse allyl glucosinolate catabolites independently influence root growth and development. Plant Physiol. 183 (2020) 1376-1390. http://doi.org/10.1104/pp.20.00170.

[24]

Y. Takahashi, J. Zhang, P.K. Hsu, et al., MAP3Kinase-dependent SnRK2-kinase activation is required for abscisic acid signal transduction and rapid osmotic stress response, Nat. Commun. 11 (2020) 12. http://doi.org/10.1038/s41467-019-13875-y.

[25]

N.N. Wang, L.L. Zhao, R. Lu, et al., Cotton mitogen-activated protein kinase4(GhMPK4) confers the transgenic Arabidopsis hypersensitivity to salt and osmotic stresses, Plant Cell Tiss. Org. 123 (2015) 619-632. http://doi.org/10.1007/s11240-015-0865-5.

[26]

C.Z. Zhao, P.C. Wang, T. Si, et al., MAP kinase cascades regulate the cold response by modulating ICE1 protein stability, Dev. Cell 43 (2017) 618-629. http://doi.org/10.1016/j.devcel.2017.09.024.

[27]

D. Marino, C. Dunand, A. Puppo, et al., A burst of plant NADPH oxidases, Trends Plant Sci. 17 (2012) 9-15. http://doi.org/10.1016/j.tplants.2011.10.001.

[28]

M.C. Rentel, D. Lecourieux, F. Ouaked, et al., Oxi1 kinase is necessary for oxidative burst-mediated signalling in arabidopsis, Nature 427 (2004) 858-861. http://doi.org/10.1038/nature02353.

[29]

I.M. Hwang, B. Park, Y.M. Dang, et al., Simultaneous direct determination of 15 glucosinolates in eight Brassica species by UHPLC-Q-Orbitrap-MS, Food Chem. 282 (2019) 127-133. http://doi.org/10.1016/j.foodchem.2018.12.036.

[30]

Y. Yagishita, J.W. Fahey, A.T. Dinkova-Kostova, et al., Broccoli or sulforaphane: is it the source or dose that matters, Molecules 24 (2019) 3593. http://doi.org/10.3390/molecules24193593.

[31]

M. Pfalz, H. Vogel, J. Kroymann, The gene controlling the indole glucosinolate modifier1 quantitative trait locus alters indole glucosinolate structures and aphid resistance in arabidopsis, Plant Cell 21 (2009) 985-999. http://doi.org/10.1105/tpc.108.063115.

[32]

M. Pfalz, M.D. Mikkelsen, P. Bednarek, et al., Metabolic engineering in nicotiana benthamiana reveals key enzyme functions in arabidopsis indole glucosinolate modification, Plant Cell 23 (2011) 716-729. http://doi.org/10.2307/41434503.

[33]

P.J. Sánchez-Pujante, M. Borja-Martínez, M.N. Pedreo, et al., Biosynthesis and bioactivity of glucosinolates and their production in plant in vitro cultures, Planta 246 (2017) 1-14. http://doi.org/10.1007/s00425-017-2705-9.

[34]

S. Ambawat, P. Sharma, N.R. Yadav, et al., MYB transcription factor genes as regulators for plant responses: an overview, Physiol. Mol. Biol. Plants 19 (2013) 307-321. http://doi.org/10.1007/s12298-013-0179-1.

[35]

E. Butelli, L. Titta, M. Giorgio, et al., Enrichment of tomato fruit with health-promoting anthocyanins by expression of select transcription factors, Nat. Biotechnol. 26 (2008) 1301-1308. http://doi.org/10.1038/nbt.1506.

[36]

M. Schön, A. Töller, C. Diezel, et al., Analyses of wrky18 wrky40 plants reveal critical roles of sa/eds1 signaling and indole-glucosinolate biosynthesis for golovinomyces orontii resistance and a loss-of resistance towards pseudomonas syringae pv. tomato avrrps4, Mol. Plant Microbe. Interact. 26 (2013) 758-767. http://doi.org/10.1094/MPMI-11-12-0265-R.

[37]

I. Gadjev, S. Vanderauwera, T.S. Gechev, et al., Transcriptomic footprints disclose specificity of reactive oxygen species signaling in arabidopsis, Plant Physiol. 141 (2006) 436-445. http://doi.org/10.1104/pp.106.078717.

[38]

A. Singh, A. Kumar, S. Yadav, et al., Reactive oxygen species-mediated signaling during abiotic stress, Plant Gene 18 (2019) 100173. http://doi.org/10.1016/j.plgene.2019.100173.

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Publication history

Received: 16 June 2022
Revised: 17 July 2022
Accepted: 10 August 2022
Published: 25 September 2023
Issue date: March 2024

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© 2024 Beijing Academy of Food Sciences. Publishing services by Tsinghua University Press.

Acknowledgements

This work was supported by the National Natural Science Foundation of China (31972091).

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This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

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