Skip to main content
SpringerLink
Log in

Investigation of Yacon Leaves (Smallanthus sonchifolius) for α-Glucosidase Inhibitors Using Metabolomics and In Silico Approach

  • Original Paper
  • Published:
Plant Foods for Human Nutrition Aims and scope Submit manuscript

Abstract

Yacon (Smallanthus sonchifolius (Poepp.) H. Robinson) leaves is traditionally consumed as herbal tea in many countries including Indonesia. This plant’s antidiabetic properties have been extensively researched, but studies on the responsible active compound identification are scarce. Information on the active compounds is critical for the consistency of Yacon herbal tea quality. The aim of this study was to identify α-glucosidase inhibitors in Indonesian Yacon leaves grown in two different locations using FTIR- and LC–MS/MS-based metabolomics in combination with in silico technique. Yacon leaves ethanol (50 and 95%) and water extracts were tested for α-glucosidase inhibitory activity, with the 95% ethanol extract being the most active. Geographical origins were found to have no major impact on the activity. In parallel, chemical profile of Yacon leaves extract was determined using FTIR and LC–MS/MS. Orthogonal Projection to Latent Structure (OPLS) was used to analyze both sets of data. OPLS analysis of FTIR data showed that compounds associated to α-glucosidase inhibitor activity included those with functional groups –OH, stretched CH, carbonyl, and alkene. It was consistent with the result of OPLS analysis of LC–MS/MS data, which revealed that based on their VIP and Y-related coefficient value, nystose, 1-kestose, luteolin-3′-7-di-O-glucoside, and 1,3-O-dicaffeoilquinic acid isomers, strongly linked to Yacon’s α-glucosidase inhibitor activity. In silico study supported these findings, revealing that the four compounds were potent α-glucosidase inhibitors with docking score in the range of − 100.216 to − 115.657 kcal/mol, which are similar to acarbose (− 115.774 kcal/mol) as a reference drug.

Graphical abstract

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

Similar content being viewed by others

Data Availability

All data and supplementary information are available as supplementary files and submitted together with the main manuscript.

Code Availability

Not Applicable.

References

  1. Kumar S, Narwal S, Kumar V, Prakash O (2011) α-glucosidase inhibitors from plants: a natural approach to treat diabetes. Pharmacogn Rev 5:19–29. https://doi.org/10.4103/0973-7847.79096

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Proença C, Freitas M, Ribeiro D et al (2017) α-glucosidase inhibition by flavonoids: an in vitro and in silico structure–activity relationship study. J Enzyme Inhib Med Chem 32:1216–1228. https://doi.org/10.1080/14756366.2017.1368503

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Ojansivu I, Ferreira CL, Salminen S (2011) Yacon, a new source of prebiotic oligosaccharides with a history of safe use. Trends Food Sci Technol 22:40–46. https://doi.org/10.1016/j.tifs.2010.11.005

    Article  CAS  Google Scholar 

  4. Valentová K, Ulrichová J (2003) Smallanthus sonchifolius and Lepidium meyenii - prospective Andean crops for the prevention of chronic diseases. Biomed Pap Med Fac Univ Palacky Olomouc Czech Repub 147:119–130. https://doi.org/10.5507/bp.2003.017

    Article  PubMed  Google Scholar 

  5. Kakuta H, Seki T, Hashidoko Y, Mizutani J (1992) Ent -kaurenic acid and its related compounds from glandular trichome exudate and leaf extracts of Polymnia sonchifolia. Biosci Biotechnol Biochem 56:1562–1564. https://doi.org/10.1271/bbb.56.1562

    Article  CAS  Google Scholar 

  6. Genta SB, Cabrera WM, Mercado MI et al (2010) Hypoglycemic activity of leaf organic extracts from Smallanthus sonchifolius: constituents of the most active fractions. Chem Biol Interact 185:143–152. https://doi.org/10.1016/j.cbi.2010.03.004

    Article  CAS  PubMed  Google Scholar 

  7. Zheng X, Fan H, Guo-Kang T et al (2010) Anti-diabetes constituents in leaves of Smallanthus sonchifolius. Nat Prod Commun 5:1–4. https://doi.org/10.1177/1934578X1000500123

    Article  Google Scholar 

  8. Serra-Barcellona C, Habib NC, Honoré SM et al (2017) Enhydrin regulates postprandial hyperglycemia in diabetic rats by inhibition of α-glucosidase activity. Plant Foods Hum Nutr 72:156–160. https://doi.org/10.1007/s11130-017-0600-y

    Article  CAS  PubMed  Google Scholar 

  9. Yuliana ND, Rosa D, Budijanto S et al (2014) Identification of adenosine A1 receptor ligands from Morus alba L. stem bark by NMR metabolomics approach. Int Food Res J 21:1067–1071

    Google Scholar 

  10. Aziz Z, Al Qisthi FH, Yuliana ND, Simanjuntak P (2019) Identification of α-glucosidase enzyme inhibitor compound from ethanol 96% extract of yakon leaves (Smallanthus sonchifolius [Poepp. & Endl.] H. Robinson). J Ilmu Kefarmasian Indones 17:21

    Article  Google Scholar 

  11. Sancheti S, Sancheti S, Seo SY (2009) Chaenomeles sinensis: a potent alpha-and beta-glucosidase inhibitor. Am J Pharmacol Toxicol 4:8–11. https://doi.org/10.3844/ajptsp.2009.8.11

    Article  Google Scholar 

  12. Naylor RL, Battisti DS, Vimont DJ et al (2007) Assessing risks of climate variability and climate change for Indonesian rice agriculture. Proc Natl Acad Sci USA 104:7752–7757. https://doi.org/10.1073/pnas.0701825104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Worley B, Powers R (2016) PCA as a practical indicator of OPLS-DA model reliability. Curr Metabolomics 4:97–103. https://doi.org/10.2174/2213235X04666160613122429

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Eriksson L, Trygg J, Wold S (2008) CV-ANOVA for significance testing of PLS and OPLS® models. J Chemom 22:594–600. https://doi.org/10.1002/cem.1187

    Article  CAS  Google Scholar 

  15. Lindgren F, Hansen B, Karcher W (1996) Model validation by permutation tests. J Chemom 10:521–532. https://doi.org/10.1002/(SICI)1099-128X(199609)10:5/6%3C521::AID-CEM448%3E3.0.CO;2-J

    Article  CAS  Google Scholar 

  16. Habib NC, Honoré SM, Genta SB, Sánchez SS (2011) Hypolipidemic effect of Smallanthus sonchifolius (yacon) roots on diabetic rats: biochemical approach. Chem Biol Interact 194:31–39. https://doi.org/10.1016/j.cbi.2011.08.009

    Article  CAS  PubMed  Google Scholar 

  17. Bharti SK, Krishnan S, Kumar A et al (2013) Antidiabetic activity and molecular docking of fructooligosaccharides produced by Aureobasidium pullulans in poloxamer-407-induced T2DM rats. Food Chem 136:813–821. https://doi.org/10.1016/j.foodchem.2012.08.083

    Article  CAS  PubMed  Google Scholar 

  18. Russo D, Valentão P, Andrade PB et al (2015) Evaluation of antioxidant, antidiabetic and anticholinesterase activities of Smallanthus sonchifolius landraces and correlation with their phytochemical profiles. Int J Mol Sci 16:17696–17718. https://doi.org/10.3390/ijms160817696

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Yin XL, Xu BQ, Zhang YQ (2018) Gynura divaricata rich in 3, 5-/4, 5-dicaffeoylquinic acid and chlorogenic acid reduces islet cell apoptosis and improves pancreatic function in type 2 diabetic mice. Nutr Metab 15:1–12. https://doi.org/10.1186/s12986-018-0310-y

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors would like to acknowledge Prof. Dr. Apt. Wahono Sumaryono for a fruitful discussion, and Prof. Dr. Apt. Siswandono M.Si for the Mollegro Virtual Dockers license.

Author information

Authors and Affiliations

  1. Faculty of Pharmacy, University of Pancasila, Srengseng Sawah Jagakarsa, South Jakarta, 12640, Indonesia

    Zuhelmi Aziz, Esti Mulatsari & Syamsudin Abdillah

  2. Department of Food Science and Technology, Faculty of Agricultural Technology, IPB University, IPB Dramaga Campus, Bogor, 16680, Indonesia

    Nancy Dewi Yuliana

  3. Research Center for Chemistry, National Research and Innovation Agency (BRIN), Puspitek Serpong, Tangerang Selatan, Banten, Indonesia

    Partomuan Simanjuntak

  4. Department of Chemistry, Faculty of Mathematics and Natural Sciences, IPB University, IPB Dramaga Campus, Bogor, 16680, Indonesia

    Mohamad Rafi

Authors
  1. Zuhelmi Aziz
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Nancy Dewi Yuliana
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Partomuan Simanjuntak
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mohamad Rafi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Esti Mulatsari
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Syamsudin Abdillah
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

ZA: conducted the experiment, wrote the first manuscript draft. NDY: finalized the manuscript, multivariate data analysis. PS: read and approved the manuscript, LC–MS data analysis. MR: FTIR data analysis, read and approved the manuscript. EM: in silico data analysis, read and approved the manuscript. SA: in vitro data analysis, read and approved the manuscript.

Corresponding author

Correspondence to Nancy Dewi Yuliana.

Ethics declarations

Ethics Approval

Not Applicable.

Consent for Participate

Not Applicable.

Consent for Publication

Not Applicable.

Conflict of Interest

The authors declare no competing financial interest.

Additional information

Publisher's Note

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

Supplementary Information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Aziz, Z., Yuliana, N.D., Simanjuntak, P. et al. Investigation of Yacon Leaves (Smallanthus sonchifolius) for α-Glucosidase Inhibitors Using Metabolomics and In Silico Approach. Plant Foods Hum Nutr 76, 487–493 (2021). https://doi.org/10.1007/s11130-021-00926-3

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11130-021-00926-3

Keywords

Search

Navigation