Skip to main content
SpringerLink
Log in

Effects of Sulfur and Selenium on Glucosinolate Biosynthesis in Cabbage

  • Original Paper
  • Published:
Plant Molecular Biology Reporter Aims and scope Submit manuscript

Abstract

The effects of S and Se treatment on cabbage, especially the interactions of S and Se metabolism with the biosynthesis of glucosinolate (GSL), including glucoraphanin, which is a major aliphatic GSL in cruciferous vegetables and the precursor of the anticancer compound sulforaphane, were examined. Cabbage plants were treated with sulfate and selenite (SeO32−), and the total S, Se, and GSL contents of cabbage head and outer foliage leaves were measured. Results showed that selenite treatment was beneficial to GSL biosynthesis and Se accumulation in cabbage head and outer foliage leaves. GSL synthesis was induced by exogenous selenite-elevated sulfate treatment at certain concentration ratios, i.e., 50-μΜ selenite + 1-mΜ sulfate or 100-μΜ selenite + 4-mΜ sulfate. A high exogenous sulfate concentration was more favorable to GSL accumulation than a low sulfate concentration. According to the relative expression of genes on GSL synthesis, an increase in the GSL content was attributed to the upregulation of gene expression and possible transportation from the outer foliage leaf to the head of cabbage. These results might be helpful for increasing the health benefits of cabbage by supplying exogenous S and Se. Further research should explore the effects of sulfate and selenite on GSL precursor substances to reveal the reason why total GSL contents increased.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Anderson J (1993) Selenium interactions in sulfur metabolism. In: Kock D et al (eds) Sulfur nutrition and assimilation in higher plants: regulatory agricultural and environmental aspects. SPB Academic, The Hague

    Google Scholar 

  • Barickman TC, Kopsell DA, Sams CE (2013) Selenium influences glucosinolate and isothiocyanates and increases sulfur uptake in Arabidopsis thaliana and rapid-cycling Brassica oleracea. J Agric Food Chem 61(1):202–209

    Article  CAS  PubMed  Google Scholar 

  • Birringer M, Pilawa S, Flohé L (2002) Trends in selenium biochemistry. Nat Prod Rep 19(6):693–718

    Article  CAS  PubMed  Google Scholar 

  • Cartea ME, Velasco P (2008) Glucosinolates in brassica foods: bioavailability in food and significance for human health. Phytochem Rev 7(2):213–229

    Article  CAS  Google Scholar 

  • Chen YC, Prabhu KS, Das A, Mastro AM (2013) Dietary selenium supplementation modifies breast tumor growth and metastasis. Int J Cancer 133(9):2054–2064

    Article  CAS  PubMed  Google Scholar 

  • Clarke DB (2010) Glucosinolates, structures and analysis in food. Anal Methods 2(4):310–325

    Article  CAS  Google Scholar 

  • Clarke JD, Dashwood RH, Ho E (2008) Multi-targeted prevention of cancer by sulforaphane. Cancer Letters 269(2):291–304

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gandin V, Khalkar P, Braude J, Fernandes AP (2018) Organic selenium compounds as potential chemotherapeutic agents for improved cancer treatment. Free Radical Biology & Medicine (on line)

  • Geuflores F, Nielsen MT, Nafisi M, Møldrup ME, Olsen CE, Motawia MS, Halkier BA (2009) Glucosinolate engineering identifies a gamma-glutamyl peptidase. Nat Chem Biol 5(8):575–577

    Article  CAS  Google Scholar 

  • Gigolashvili T, Yatusevich R, Berger B, Müller C, Flügge UI (2010) The R2R3-MYB transcription factor HAG1/MYB28 is a regulator of methionine-derived glucosinolate biosynthesis in Arabidopsis thaliana. Plant J 51(2):247–261

    Article  CAS  Google Scholar 

  • Hirai MY, Sugiyama K, Sawada Y, Tohge T, Obayashi T, Suzuki A, Araki R, Sakurai N, Suzuki H, Aoki K (2007) Omics-based identification of Arabidopsis Myb transcription factors regulating aliphatic glucosinolate biosynthesis. Proc Natl Acad Sci U S A 104(15):6478–6483

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hsu FC, Wirtz M, Heppel SC, Bogs J, Krämer U, Khan MS, Bub A, Hell R, Rausch T (2011) Generation of Se-fortified broccoli as functional food: impact of Se fertilization on S metabolism. Plant Cell Environ 34(2):192–207

    Article  CAS  PubMed  Google Scholar 

  • Huang K, Lin JC, Wu QY, Yan JY, Liu MY, Zhang S, Xiao WJ (2016) Changes in sulforaphane and selenocysteine methyltransferase transcript levels in broccoli treated with sodium selenite. Plant Molecular Biology Reporter 34:807–814

    Article  CAS  Google Scholar 

  • Khan MS, Hell R (2014) Applied cell biology of sulphur and selenium in plants. Springer, Berlin Heidelberg

    Book  Google Scholar 

  • Kim SJ, Ishii G (2010) Glucosinolate profiles in the seeds, leaves and roots of rocket salad (Eruca sativa Mill.) and anti-oxidative activities of intact plant powder and purified 4-methoxyglucobrassicin. Soil Sci Plant Nutr 52(3):394–400

    Article  CAS  Google Scholar 

  • Kim SJ, Kawaharada C, Jin S, Hashimoto M, Ishii G, Yamauchi H (2007) Structural elucidation of 4-(cystein-S-yl)butyl glucosinolate from the leaves of Eruca sativa. Journal of the Agricultural Chemical Society of Japan 71(1):114–121

    CAS  Google Scholar 

  • Kim YB, Li XH, Kim SJ, Kim HH, Lee J, Kim H, Park SU (2013) MYB transcription factors Regulate glucosinolate biosynthesis in different organs of Chinese cabbage (Brassica rapa ssp. pekinensis). Molecules 18:8682–8695

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kraker JWD, Gershenzon J (2011) From amino acid to glucosinolate biosynthesis: protein sequence changes in the evolution of methylthioalkylmalate synthase in Arabidopsis. Plant Cell 23(1):38–53

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Lv J, Wu J, Zuo J, Fan L, Shi J, Gao L, Li M, Wang Q (2017) Effect of Se treatment on the volatile compounds in broccoli. Food Chemistry 216:225–233

    Article  CAS  PubMed  Google Scholar 

  • Lyi SM, Heller LI, Rutzke M, Welch RM, Kochian LV, Li L (2005) Molecular and biochemical characterization of the selenocysteine Se-methyltransferase gene and Se-methylselenocysteine synthesis in broccoli. Plant Physiology 138(1):409–420

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mahn A (2017) Modelling of the effect of selenium fertilization on the content of bioactive compounds in broccoli heads. Food Chemistry 233:492–499

    Article  CAS  PubMed  Google Scholar 

  • Malagoli M, Schiavon M, Dall’Acqua S, Pilonsmits EAH (2015) Effects of selenium biofortification on crop nutritional quality. Front Plant Sci 6(280):1–5

    Google Scholar 

  • Matich AJ, Mckenzie MJ, Lill RE, Brummell DA, Mcghie TK, Chen KY, Rowan DD (2012) Selenoglucosinolates and their metabolites produced in Brassica spp. fertilised with sodium selenate. Phytochemistry 75(3):140–152

    Article  CAS  PubMed  Google Scholar 

  • Matusheski NV, Juvik JA, Jeffery EH (2004) Heating decreases epithiospecifier protein activity and increases sulforaphane formation in broccoli. Phytochemistry 65(9):1273–1281

    Article  CAS  PubMed  Google Scholar 

  • Mullineaux PM, Rausch T (2005) Glutathione, photosynthesis and the redox regulation of stress-responsive gene expression. Photosynthesis Research 86(3):459–474

    Article  CAS  PubMed  Google Scholar 

  • Pérez C, Barrientos H, Román J, Mahn A (2014) Optimization of a blanching step to maximize sulforaphane synthesis in broccoli florets. Food Chem 145(7):264–271

    Article  PubMed  CAS  Google Scholar 

  • Pu Q, Shi S, Zhang L, Gao Q, Ren X, Xiang C, Yang P, Lin B, Geng M (2017) Cloning and expression analysis of BoIAA2 and BoIAA19 genes of AUX/IAA family in cabbage. J Agric Sci Technol 19(9):24–33

    CAS  Google Scholar 

  • Pyrzynska K (2009) Selenium speciation in enriched vegetables. Food Chem 114:1183–1191

    Article  CAS  Google Scholar 

  • Rausch T, Wachter A (2005) Sulfur metabolism: a versatile platform for launching defence operations. Trends in Plant Science 10(10):503–509

    Article  CAS  PubMed  Google Scholar 

  • Rosen CJ, Fritz VA, Gardner GM, Hecht SS, Carmella SG, Kenney PM (2005) Cabbage yield and glucosinolate concentrations as affected by nitrogen and sulfur fertility. HortScience 40:1493–1498

    Article  CAS  Google Scholar 

  • Sams CE, Panthee DR, Charron CS, Kopsell DA, Yuan JS (2011) Selenium regulates gene expression for glucosinolate and carotenoid biosynthesis in arabidopsis. Journal of the American Society for Horticultural Science American Society for Horticultural Science 136(1):23–34

    Article  CAS  Google Scholar 

  • Sang JP, Minchinton IR, Johnstone PK, Rjw T (1984) Glucosinolate profiles in the seed, root and leaf tissue of cabbage, mustard, rapeseed, radish and swede. Can J Plant Sci 64(1):77–93

    Article  CAS  Google Scholar 

  • Sepúlveda I, Barrientos H, Mahn A, Moenne A (2013) Changes in SeMSC, glucosinolates and sulforaphane levels, and in proteome profile in broccoli (Brassica oleracea var. Italica) fertilized with sodium selenate. Molecules 18(5):5221–5234

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sønderby IE, Geu-Flores F, Halkier BA (2010) Biosynthesis of glucosinolates--gene discovery and beyond. Trends in Plant Science 15(5):283–290

    Article  PubMed  CAS  Google Scholar 

  • Sors TG, Ellis DR, Salt DE (2005) Selenium uptake, translocation, assimilation and metabolic fate in plants. Photosynthesis Research 86(3):373–389

    Article  CAS  PubMed  Google Scholar 

  • Sors TG, Ellis DR, Na GN, Lahner B, Lee S, Leustek T, Pickering IJ, Salt DE (2010) Analysis of sulfur and selenium assimilation in Astragalus plants with varying capacities to accumulate selenium. Plant Journal for Cell & Molecular Biology 42(6):785–797

    Article  CAS  Google Scholar 

  • Sun J, Zhang M, Chen P (2016) GLS-Finder: a platform for fast profiling of glucosinolates in brassica Vegetables. J Agric Food Chem 64(21):4407–4415

    Article  CAS  PubMed  Google Scholar 

  • Tarun AS, Böck A, Caruso J, Terry N (2004) Overexpression of selenocysteine methyltransferase in Arabidopsis and Indian mustard increases selenium tolerance and accumulation. Plant Physiology 135(1):377–383

    Article  PubMed  PubMed Central  Google Scholar 

  • Tian M, Xu X, Liu Y, Xie L, Pan S (2016) Effect of Se treatment on glucosinolate metabolism and health-promoting compounds in the broccoli sprouts of three cultivars. Food Chemistry 190:374–380

    Article  CAS  PubMed  Google Scholar 

  • Tian M, Yang Y, Avila FW, Fish T, Yuan H, Hui M, Pan S, Thanhauser T, Li L (2018) Effects of selenium supplementation on glucosinolate biosynthesis in broccoli. Journal of Agricultural & Food Chemistry 66(30):8036–8044

    Article  CAS  Google Scholar 

  • Valdez-Barilla JR, Quinn CF, Pilon-Smits EAH (2011) Selenium accumulation in plants – phytotechnological applications and ecological implications. International journal of phytoremediation 13:166–178

    Article  Google Scholar 

  • Zhao FJ (2010) Selenium uptake, translocation and speciation in wheat supplied with selenate or selenite. New Phytologist 178(1):92–102

    Google Scholar 

Download references

Acknowledgments

This research was funded by National Natural Science Foundation of China (No. 31772325, 31902023), Hunan Provincial Natural Science Foundation of China (2018JJ3217), Hunan Provincial Sci-Tech Project (2018NK2022), Open Foundation of Key laboratory of Biology and Genetic Improvement of Horticultural Crops, Ministry of Agriculture (IVF201702), and Foundation for Young Scholars of Hunan Agricultural University(17QN33).

Author information

Authors and Affiliations

  1. College of Horticulture & Landscape, Hunan Agricultural University, Changsha, 410128, China

    Junwei Wang, Shuxiang Mao, Haoran Xu, Qi Wu, Mantian Liang, Yiming Yuan, Mingyue Liu, Ke Huang & Qiuyun Wu

Authors
  1. Junwei Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shuxiang Mao
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Haoran Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Qi Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mantian Liang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yiming Yuan
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Mingyue Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Ke Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Qiuyun Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Qiuyun Wu.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Key message

Selenite treatment was beneficial to glucosinolate (GSL) biosynthesis and Se accumulation in cabbage head and outer foliage leaf. GSLs synthesis was induced by exogenous selenite-elevated sulfate treatment of 50 mΜ selenite +1 mΜ sulfate or 100 mM selenite +4 mΜ sulfate.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, J., Mao, S., Xu, H. et al. Effects of Sulfur and Selenium on Glucosinolate Biosynthesis in Cabbage. Plant Mol Biol Rep 38, 62–74 (2020). https://doi.org/10.1007/s11105-019-01178-x

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11105-019-01178-x

Keywords

Search

Navigation