Leaves metabolomic profiling of Musa acuminata accessions using UPLC–QTOF–MS/MS and their antioxidant activity

Abstract

Musa acuminata (Musaceae) is a wild species native to South East Asia. In addition to its potential as a food crop, different non-food morphological parts of the plant have been investigated for various pharmacological activities, including anticholinesterase and antioxidant activity. This study aimed to characterize Musa leaf extracts based on their phenolic composition and their agro-morphological traits. A metabolomic approach was applied to discover biomarkers that can be used to separate eight accessions of the species originating from five different countries. Statistical analysis was employed for data analysis. The antioxidant activity and total phenolic content was measured by Ferric Reducing Antioxidant Power (FRAP) assay and Folin–Ciocalteu colorimetric method, respectively. Over 500 metabolites were observed. Thirty-one of them were important for defining variations among the accessions. The identities of some of these markers were confirmed based on their MS2 fragmentation. These include Quercetin O-rhamnoside-O hexoside (m/z 609), Kaempferol-3-O-rutinoside (m/z 593), Quercetin O hexoside (m/z 463), Hexadecanoic acid (m/z 255), Rhamnoside-O-rutinoside (m/z 623). Country of origin and methods of extraction did not play any significant role in the separation, although extraction of accessions by Soxhlet gave better yield (20.0–60.0%) than by sonication (18.4–23.0%). Accession TMp 24 from Nigeria gave the highest yield in both methods of extraction. The sonicated accession TMb 8 exhibited highest antioxidant activity having FRAP values of 49.14 mg GAE/g and 125.10 mg TROLOX/g. The next accession in FRAP activity was the sonicated leaf extract of TMb 116 with 31.69 mg GAE/g and 121.57 mg TROLOX/g. The PCA analysis allowed the separation of the accessions into two groups. The metabolomics approach was found to be informative as a screening tool of the Musa accessions. The extracts showed good antioxidant activity and can be a potential source of bioactive metabolites for industrial use.

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

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

References

  1. 1.

    I.A. Ross, Medicinal Plants of the World, vol. 3. (Humana Press, Totowa, 2005). https://doi.org/10.1007/978-1-59259-887-8

  2. 2.

    B. Suneetha, D. Sujatha, K.V. Prasad, Antidiabetic and antioxidant activities of stem juice of Musa paradisiaca on alloxan induced diabetic rats. Pharmanest Int. J. Adv. Pharm. Sci. 1, 167–176 (2010)

    Google Scholar 

  3. 3.

    P.K. Agarwal, A. Singh, K. Gaurav, S. Goel, H.D. Khanna, R.K. Goel, Evaluation of wound healing activity of extracts of plantain banana (Musa sapientum var. paradisiaca) in rats. Indian J. Exp. Biol. 47, 32–40 (2009)

    CAS  Google Scholar 

  4. 4.

    R.K. Goel, K. Sairam, Anti-ulcer drugs from indigenous sources with emphasis on Musa sapientum, tamrabhasma, Asparagus racemosus and Zingiber officinale. Indian J.Pharmacol. 34, 100–110 (2002)

    CAS  Google Scholar 

  5. 5.

    P. Prabha, T. Karpagam, B.A. Varalakshmi, A. Sohna, C. Packiavathy, Indigenous anti-ulcer activity of Musa Sapientum on peptic ulcer. Pharmacog. Res. 3, 232–238 (2011)

    CAS  Article  Google Scholar 

  6. 6.

    M. Singhal, P. Ratra, Investigation of immunomodulatory potential of methanolic and hexane extract of Musa acuminata peel (plantain) extracts. Global J. Pharmacol. 7, 69–74 (2013)

    Google Scholar 

  7. 7.

    S.P. Dhanabal, M. Sureshkumar, M. Ramanathan, B. Suresh, Hypoglycemic effect of ethanolic extract of Musa sapientum on alloxan induced diabetic mellitus in rats and its relation with antioxidant potential. J. Herbal Pharmacother. 5, 7–19 (2005)

    CAS  Article  Google Scholar 

  8. 8.

    S.C. Shanmuga, S. Subramanian, Musa paradisiaca flower extract improves carbohydrate metabolism in hepatic tissues of streptozotocin-induced experimental diabetes in rats. Asian Pac. J. Trop. Biomed. 2(Suppl 3), S1498–S1503 (2012). https://doi.org/10.1016/S2221-1691(12)60444-4

    Article  Google Scholar 

  9. 9.

    K. Mangathayaru, G. Umeshankar, G. Muralitharan, E. Cordairayen, J. Vasantha, Antimicrobial activity of some indigenous plants. Indian J. Pharm. Sci. 66, 123 (2004)

    Google Scholar 

  10. 10.

    C.S. Alisi, C.E. Nwanyanwu, C.O. Akujobi, C.O. Ibegbulem, Inhibition of dehydrogenase activity in pathogenic bacteria isolates by aqueous extracts of Musa paradisiaca (var sapientum). Afr. J. Biotechnol. 7(12), 1821–1825 (2008)

    Article  Google Scholar 

  11. 11.

    P.K. Rai, D. Jaiswal, N.k.. Rai, S. Pandhija, A.K. Rai, G. Watal, Role of glycemic elements of Cynodon dactylon and Musa paradisiaca in diabetes management. Lasers Med. Sci. 24(5), 761–768 (2009). https://doi.org/10.1007/s10103-008-0637-0

    Article  Google Scholar 

  12. 12.

    P.K. Agarwal, A. Singh, K. Gaurav, S. Goel, H.D. Khanna, R.K. Goel, Evaluation of wound healing activity of extracts of plantain banana (Musa sapientum var. paradisiaca) in rats. Indian J. Exp. Biol. 47(1), 32–40 (2009)

    CAS  Google Scholar 

  13. 13.

    S. Kumar, C.K. Mishra, A. Ahuja, A. Rani, R.K. Nema, Phytoconstituents and pharmacological activities of Musa paradisiaca Linn. Asian J. Biochem. Pharm. Res. 2(4), 15–20 (2012). Retrieved from http://www.ajbpr.com/issues/volume2/issue4/FINAL 18.pdf

  14. 14.

    G. Madhukar, E.T. Tamboli, P. Rabea, S.H. Ansari, M.Z. Abdin, A. Sayeed, Rapid, sensitive, and validated UPLC/Q-TOF-MS method for quantitative determination of vasicine in Adhatoda vasica and its in vitro culture. Pharmacog. Mag. 10, S198–S205 (2014)

    Article  Google Scholar 

  15. 15.

    R. Plumb, J. Castro-Perez, J. Granger, I. Beattie, K. Joncour, A. Wright, Ultra-performance liquid chromatography coupled to quadrupole-orthogonal time-of-flight mass spectrometry. Rapid Commun. Mass Spectrom. 18, 2331–2337 (2004). https://doi.org/10.1002/rcm.1627

    CAS  Article  Google Scholar 

  16. 16.

    L. Nováková, L. Matysová, P. Solich, Advantages of application of UPLC in pharmaceutical analysis. Talanta. 68, 908–918 (2006)

    Article  Google Scholar 

  17. 17.

    R. An, L. You, Y. Zhang, X. Wang, Y. Ma, A rapid UPLC method for simultaneous determination of eleven components in “Ge-Gen-Qin-Lian” decoction. Pharmacogn. Mag. 10, 464–469 (2014). https://doi.org/10.4103/0973-1296.141821

    Article  Google Scholar 

  18. 18.

    I.O. Ayoola, B. Gueye, M.A. Sonibare, M.T. Abberton, Antioxidant activity and acetylcholinesterase inhibition of field and in vitro grown Musa. L. species. J. Food Meas. Charact. 11(2), 488–499 (2017)

    Article  Google Scholar 

  19. 19.

    R. Jaiswal, S. Deshpande, N. Kuhnert, Profiling the chlorogenic acids of Rudbeckia hirta, Helianthus tuberosus, Carlina acaulis and Symphyotrichum novae-angliae leaves by LC-MS(n). Phytochem. Anal. 22, 432–441 (2011)

    CAS  Article  Google Scholar 

  20. 20.

    T. Pluskal, S. Castillo, A. Villar-Briones, M. Oresic, MZmine 2: modular framework for processing, visualizing, and analyzing mass spectrometry-based molecular profile data. BMC Bioinform. 11, 395 (2010). https://doi.org/10.1186/1471-2105-11-395

    Article  Google Scholar 

  21. 21.

    K. Thaipong, U. Boonprakoba, K. Crosbyb, L. Cisneros-Zevallosc, D.H. Byrnec, Comparison of ABTS, DPPH, FRAP, and ORAC assays for estimating antioxidant activity from guava fruit extracts. J. Food Comp. Anal. 19, 669–675 (2006). https://doi.org/10.1016/j.jfca.2006.01.003

    CAS  Article  Google Scholar 

  22. 22.

    N. Cicco, M.T. Lanorte, M. Paraggio, M. Viggiano, V. Lattanzio, A reproducible, rapid and inexpensive Folin-Ciocalteu micro-method in determining phenolics of plant methanol extracts. Microchem. J. 91, 107–110 (2009)

    CAS  Article  Google Scholar 

  23. 23.

    R. Sanghi, S.S. Kannamkumarath, Comparison of extraction methods by Soxhlet, sonicator and microwave in screening pesticides residues from solid matrices. J. Anal. Chem. 59, 1032–1036 (2004)

    Article  Google Scholar 

  24. 24.

    R. Jaiswal, L. Jayasinghe, N. Kuhnert, Identification and characterization of proanthocyanidins of 16 members of the Rhododendron genus (Ericaceae) by tandem LC-MS. J. Mass Spectrom. 47, 502–515 (2012). https://doi.org/10.1002/jms.2954

    CAS  Article  Google Scholar 

  25. 25.

    R. Jaiswal, H. Müller, A. Müller, M.G.E. Karar, N. Kuhnert, Identification and characterization of chlorogenic acids, chlorogenic acid glycosides and flavonoids from Lonicera henryi. L. (Caprifoliaceae) leaves by LC-MSn. Phytochemistry. 108, 252–263 (2014). https://doi.org/10.1016/j.phytochem.2014.08.023

    CAS  Article  Google Scholar 

  26. 26.

    M.A. Patras, B.P. Milev, G. Vrancken, N. Kuhnert, Identification of novel cocoa flavonoids from raw fermented cocoa beans by HPLC-MSn. Food Res. Int. 63, 353–359 (2014). https://doi.org/10.1016/j.foodres.2014.05.031

    CAS  Article  Google Scholar 

  27. 27.

    F. Sánchez-Rabaneda, O. Jáuregui, R.M. Lamuela-Raventós, F. Viladomat, J. Bastida, C. Codina, Qualitative analysis of phenolic compounds in apple pomace using liquid chromatography coupled to mass spectrometry in tandem mode. Rapid Commun. Mass Spectrom. 18, 553–563 (2004). https://doi.org/10.1002/rcm.1370

    Article  Google Scholar 

  28. 28.

    D. Callemien, S. Collin, Use of RP-HPLC-ESI (-)-MS/MS to differentiate various proanthocyanidin isomers in lager beer extracts. J. Am. Soc. Brew. Chem. 66, 109–115 (2008)

    CAS  Google Scholar 

  29. 29.

    Y. Sakanashi, K. Oyama, H. Matsui, T.B. Oyama, T.M. Oyama, Y. Nishimura, Y. Oyama, Possible use of quercetin, an antioxidant, for protection of cells suffering from overload of intracellular Ca2+: A model experiment. Life Sci. 83, 164–169 (2008). https://doi.org/10.1016/j.lfs.2008.05.009

    CAS  Article  Google Scholar 

  30. 30.

    A.N. Begum, J. Terao, Protective effect of quercetin against cigarette tar extract-induced impairment of erythrocyte deformability. J. Nutr. Biochem. 13, 265–272 (2002). https://doi.org/10.1016/S0955-2863(01)00219-4

    CAS  Article  Google Scholar 

  31. 31.

    P. Iacopini, M. Baldi, P. Storchi, L. Sebastiani, Catechin, epicatechin, quercetin, rutin, resveratrol in red grape: content, in vitro antioxidant activity and interactions. J. Food Comp. Anal. 21, 589–598 (2008)

    CAS  Article  Google Scholar 

  32. 32.

    A. Stalmach, W. Mullen, C. Nagai, A. Crozier, On-line HPLC analysis of the antioxidant activity of phenolic compounds in brewed, paper-filtered coffee. Braz. J. Plant Physiol. 18, 253–262 (2006). https://doi.org/10.1590/S1677-04202006000100018

    CAS  Article  Google Scholar 

  33. 33.

    M. Nardini, M. D’Aquino, G. Tomassi, V. Gentili, M. Di Felice, C. Scaccini, Inhibition of human low-density lipoprotein oxidation by caffeic acid and other hydroxycinnamic acid derivatives. Free Rad. Biol. Med. 19, 541–552 (1995). https://doi.org/10.1016/0891-5849(95)00052-Y

    CAS  Article  Google Scholar 

  34. 34.

    H. Fufa, P.S. Baenziger, B.S. Beecher, I. Dweikat, R.A. Graybosch, K.M. Eskridge, Comparison of phenotypic and molecular marker-based classifications of hard red winter wheat cultivars. Euphytica 145, 133–146 (2005)

    CAS  Article  Google Scholar 

  35. 35.

    M. West-Eberhard, Phenotypic plasticity and the origins of diversity. Annu. Rev. Ecol. Syst. 20, 249–278 (1989). https://doi.org/10.1146/annurev.es.20.110189.001341

    Article  Google Scholar 

  36. 36.

    R. Ortiz, Morphological variation in Musa germplasm. Genet. Resour. Crop Evol. 44, 393–404 (1997). https://doi.org/10.1023/A:1008606411971

    Article  Google Scholar 

  37. 37.

    K. Ghasemi, Y. Ghasemi, M.A. Ebrahimzadeh, Antioxidant activity, phenol and flavonoid contents of 13 Citrus species peels and tissues. Pak. J. Pharm. Sci. 22, 277–281 (2009)

    CAS  Google Scholar 

  38. 38.

    G. Oboh, Antioxidant properties of some commonly consumed and underutilized tropical legumes. Eup. Food Res. Technol. 224, 61–65 (2006). https://doi.org/10.1007/s00217-006-0289-x

    CAS  Article  Google Scholar 

  39. 39.

    D. Yiǧit, N. Yiǧit, A. Mavi, Antioxidant and antimicrobial activities of bitter and sweet apricot (Prunus armeniaca L.) kernels. Braz. J. Med. Biol. Res. 42, 346–352 (2009)

    Article  Google Scholar 

  40. 40.

    E.K. Akkol, F. Göger, M. Koşar, K.H.C. Başer, Phenolic composition and biological activities of Salvia halophila and Salvia virgata from Turkey. Food Chem. 108, 942–949 (2008). https://doi.org/10.1016/j.foodchem.2007.11.071

    CAS  Article  Google Scholar 

  41. 41.

    J. Kubola, S. Siriamornpun, Phenolic contents and antioxidant activities of bitter gourd (Momordica charantia L.) leaf, stem and fruit fraction extracts in vitro. Food Chem. 110, 881–890 (2008). https://doi.org/10.1016/j.foodchem.2008.02.076

    CAS  Article  Google Scholar 

  42. 42.

    C. Quettier-Deleu, B. Gressier, J. Vasseur, T. Dine, C. Brunet, M. Luyckx, F. Trotin, Phenolic compounds and antioxidant activities of buckwheat (Fagopyrum esculentum Moench) hulls and flour. J. Ethnopharmacol. 72, 35–42 (2000). https://doi.org/10.1016/S0378-8741(00)00196-3

    CAS  Article  Google Scholar 

Download references

Acknowledgements

The authors would like to thank Mrs. Anja Mueller for her technical assistance in the ion trap experiment. This research received financial support by Alexander von Humboldt foundation through the return fellowship awarded to MAS to Germany for part of the study.

Author information

Affiliations

Authors

Corresponding author

Correspondence to M. A. Sonibare.

Ethics declarations

Conflict of interest

The authors report no declarations of interest.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 871 KB)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Sonibare, M.A., Ayoola, I.O., Gueye, B. et al. Leaves metabolomic profiling of Musa acuminata accessions using UPLC–QTOF–MS/MS and their antioxidant activity. Food Measure 12, 1093–1106 (2018). https://doi.org/10.1007/s11694-018-9725-4

Download citation

Keywords

  • Polyphenolics
  • UPLC–QTOF–MS/MS
  • Morphological traits
  • Metabolomics
  • Antioxidant
  • Musa acuminata