Characterization of bioactive compounds of Annona cherimola L. leaves using a combined approach based on HPLC-ESI-TOF-MS and NMR

  • Elixabet Díaz-de-Cerio
  • Luis Manuel Aguilera-Saez
  • Ana María Gómez-Caravaca
  • Vito Verardo
  • Alberto Fernández-Gutiérrez
  • Ignacio Fernández
  • David Arráez-Román
Research Paper
Part of the following topical collections:
  1. Discovery of Bioactive Compounds

Abstract

Annona cherimola Mill. (cherimoya) has widely been used as food crop. The leaves of this tree possess several health benefits, which are, in general, attributed mainly to its bioactive composition. However, literature concerning a comprehensive characterization based on a combined approach, which consists of nuclear magnetic resonance (NMR) and high-performance liquid chromatography coupled with time-of-flight mass spectrometry (HPLC-TOF-MS), from these leaves is scarce. Thus, the aim of this work was to study the polar profile of full extracts of cherimoya leaves by using these tools. Thus, a total of 77 compounds have been characterized, 12 of which were identified by both techniques. Briefly, 23 compounds were classified as amino acids, organic acids, carbohydrates, cholines, phenolic acid derivatives, and flavonoids by NMR, while 66 metabolites were divided into sugars, amino acids, phenolic acids and derivatives, flavonoids, phenylpropanoids, and other polar compounds by HPLC-TOF-MS. It is worth mentioning that different solvent mixtures were tested and the total phenolic content in the extracts quantified (TPC via HPLC-TOF-MS). The tendency observed was EtOH/water 80/20 (v/v) (17.0 ± 0.2 mg TPC/g leaf dry weight (d.w.)) ≥ acetone/water 70/30 (v/v) (16.1 ± 0.7 mg TPC/g leaf d.w.) > EtOH/water 70/30 (v/v) (14.0 ± 0.3 mg TPC/g leaf d.w.) > acetone/water 80/20 (v/v) (13.5 ± 0.4 mg TPC/g leaf d.w.). Importantly, flavonoids derivatives were between 63 and 76% of the TPC in those extracts. Major compounds were sucrose, glucose (α and β), and proline, and chlorogenic acid and rutin for NMR and HPLC-TOF-MS, respectively.

Graphical abstract

The combined use of LC-HRMS and NMR is a potential synergic combination for a comprehensive metabolite composition of cherimoya leaves

Keywords

Annona cherimola leaves HPLC-TOF-MS Nuclear magnetic resonance Phenolic compounds Natural compounds 

Notes

Acknowledgments

Vito Verardo thanks the MINECO for his “Ramon y Cajal” contract.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human or animal subjects.

Informed consent

Informed consent was not applicable.

Supplementary material

216_2018_1051_MOESM1_ESM.pdf (219 kb)
ESM 1 (PDF 218 kb)

References

  1. 1.
    González Vega ME. Chirimoya (Annona cherimola Miller), frutal tropical y sub-tropical de valores promisorios. Cultiv Trop. 2013;34(3):52–63.Google Scholar
  2. 2.
    Morton JF. Cherimoya. In: Curtis F. Dowling editors fruits of warm climates. Miami: J.F. Morton; 1987. p. 65–69.Google Scholar
  3. 3.
    Arun Jyothi B, Venkatesh K, Chakrapani P, Roja Rani A. Phytochemical and pharmacological potential of Annona cherimola-a review. Int J Phytomedicine. 2011;3(4):439–47.Google Scholar
  4. 4.
    Ribeiro da Silva LM, Teixeira de Figueiredo EA, Silva Ricardo NMP, Pinto Vieira IG, Wilane de Figueiredo R, Brasil IM, et al. Quantification of bioactive compounds in pulps and by-products of tropical fruits from Brazil. Food Chem. 2014;143:398–404.CrossRefGoogle Scholar
  5. 5.
    Seger C, Sturm S, Stuppner H. Mass spectrometry and NMR spectroscopy: modern high-end detectors for high resolution separation techniques—state of the art in natural product HPLC-MS, HPLC-NMR, and CE-MS hyphenations. Nat Prod Rep. 2013;30(7):970.CrossRefGoogle Scholar
  6. 6.
    Rizzuti A, Aguilera-Sáez LM, Gallo V, Cafagna I, Mastrorilli P, Latronico M, et al. On the use of Ethephon as abscising agent in cv. Crimson seedless table grape production: combination of fruit detachment force, fruit drop and metabolomics. Food Chem. 2015;171:341–50.CrossRefGoogle Scholar
  7. 7.
    Theodoridis GA, Gika HG, Want EJ, Wilson ID. Liquid chromatography-mass spectrometry based global metabolite profiling: a review. Anal Chim Acta. 2012;711:7–16.CrossRefGoogle Scholar
  8. 8.
    Milman BL. General principles of identification by mass spectrometry. TrAC - Trends Anal Chem. 2015;69:24–33.CrossRefGoogle Scholar
  9. 9.
    Van Der Hooft JJJ, Mihaleva V, De Vos RCH, Bino RJ, Vervoort J. A Strategy for fast structural elucidation of metabolites in small volume plant extracts using automated MS-guided LC-MS-SPE-NMR. Magn Reson Chem. 2011;49:S55–60.Google Scholar
  10. 10.
    Schymanski EL, Jeon J, Gulde R, Fenner K, Ruff M, Singer HP, et al. Identifying small molecules via high resolution mass spectrometry: communicating confidence. Environ Sci Technol. 2014;48(4):2097–8.CrossRefGoogle Scholar
  11. 11.
    Moco S, Vervoort J, Moco S, Bino RJ, De Vos RCH, Bino R. Metabolomics technologies and metabolite identification. TrAC - Trends Anal Chem. 2007;26(9):855–66.CrossRefGoogle Scholar
  12. 12.
    López-Ruiz R, Ruiz-Muelle AB, Romero-González R, Fernández I, Martínez Vidal JL, Garrido Frenich A. The metabolic pathway of flonicamid in oranges using an orthogonal approach based on high-resolution mass spectrometry and nuclear magnetic resonance. Anal Methods. 2017;9(11):1718–26.CrossRefGoogle Scholar
  13. 13.
    Nagana Gowda GA, Raftery D. Can NMR solve some significant challenges in metabolomics? J Magn Reson. 2015;260:144–60.CrossRefGoogle Scholar
  14. 14.
    Farag MA, Otify A, Porzel A, Michel CG, Elsayed A, Wessjohann LA. Comparative metabolite profiling and fingerprinting of genus Passiflora leaves using a multiplex approach of UPLC-MS and NMR analyzed by chemometric tools. Anal Bioanal Chem. 2016;408(12):3125–43.CrossRefGoogle Scholar
  15. 15.
    Coutinho ID, Baker JM, Ward JL, Beale MH, Creste S, Cavalheiro AJ. Metabolite profiling of sugarcane genotypes and identification of flavonoid glycosides and phenolic acids. J Agric Food Chem. 2016;64(21):4198–206.CrossRefGoogle Scholar
  16. 16.
    Hakeem Said I, Rezk A, Hussain I, Grimbs A, Shrestha A, Schepker H, et al. Metabolome comparison of bioactive and inactive Rhododendron extracts and identification of an antibacterial cannabinoid(s) from Rhododendron collettianum. Phytochem Anal. 2017;2017(June):454–64.CrossRefGoogle Scholar
  17. 17.
    García-Salas P, Gómez-Caravaca AM, Morales-Soto A, Segura-Carretero A, Fernández-Gutiérrez A. Identification and quantification of phenolic and other polar compounds in the edible part of Annona cherimola and its by-products by HPLC-DAD-ESI-QTOF-MS. Food Res Int. 2015;78(2015):246–57.CrossRefGoogle Scholar
  18. 18.
    Benatti Justino A, Carnevalli Miranda N, Rodrigues Franco R, Machado Martins M, da Silva NM, Salmen Espindola F. Annona muricata Linn. Leaf as a source of antioxidant compounds with in vitro antidiabetic and inhibitory potential against α-amylase, α-glucosidase, lipase, non-enzymatic glycation and lipid peroxidation. Biomed Pharmacother. 2018;100:83–92.CrossRefGoogle Scholar
  19. 19.
    Díaz-de-Cerio E, Rodríguez-Nogales A, Algieri F, Romero M, Verardo V, Segura-Carretero A, et al. The hypoglycemic effects of guava leaf (Psidium guajava L.) extract are associated with improving endothelial dysfunction in mice with diet-induced obesity. Food Res Int. 2017;96:64–71.CrossRefGoogle Scholar
  20. 20.
    Durand S, Sancelme M, Besse-Hoggan P, Combourieu B. Biodegradation pathway of mesotrione: complementarities of NMR, LC-NMR and LC-MS for qualitative and quantitative metabolic profiling. Chemosphere. 2010;81(3):372–80.CrossRefGoogle Scholar
  21. 21.
    Kim HK, Choi YH, Verpoorte R. NMR-based metabolomic analysis of plants. Nat Protoc. 2010;5(3):536–49.CrossRefGoogle Scholar
  22. 22.
    Nicholson JK, Lindon JC. Systems Biology: Metabonomics. Nature. 2007;274(5):1140–51.Google Scholar
  23. 23.
    Vendramin ME, Costa EV, Pereira dos Santos É, Belém Pinheiro ML, Barison A, Campos FR. Chemical constituents from the leaves of Annona rugulosa (Annonaceae). Biochem Syst Ecol. 2013;49(2009):152–5.CrossRefGoogle Scholar
  24. 24.
    Rabêlo SV, Costa EV, Barison A, Dutra LM, Nunes XP, Tomaz JC, et al. Alkaloids isolated from the leaves of atemoya (Annona cherimola × Annona squamosa). Brazilian J Pharmacogn. 2015;25(4):419–21.CrossRefGoogle Scholar
  25. 25.
    Thang TD, Kuo P-C, Huang G-J, Hung NH, Huang B-S, Yang M-L, et al. Chemical constituents from the leaves of Annona reticulata and their inhibitory effects on NO production. Molecules. 2013;18(4):4477–86.CrossRefGoogle Scholar
  26. 26.
    Pinto DCGA, Santos CMM, Silva AMS. Advanced NMR techniques for structural characterization of heterocyclic structures. In: TMVD Pinho e Melo editor. Recent research developments in heterocyclic chemistry. Kerala: Research Signpost; 2007. p. 397–475.Google Scholar
  27. 27.
    Manach C, Scalbert A, Morand C, Rémésy C, Jiménez L. Polyphenols: food sources and bioavailability. Am J Clin Nutr. 2004;79:727–47.CrossRefGoogle Scholar
  28. 28.
    Nijveldt RJ, van Nood E, van Hoorn DE, Boelens PG, van Norren K, van Leeuwen PA. Flavonoids: a review of probable mechanisms of action and potential applications. Am J Clin Nutr. 2001;74:418–25.CrossRefGoogle Scholar
  29. 29.
    George VC, Dellaire G, Rupasinghe HPV. Plant flavonoids in cancer chemoprevention: role in genome stability. J Nutr Biochem. 2017;45:1–14.CrossRefGoogle Scholar
  30. 30.
    Chan EW, Wong S, Lim Y, Ling S. Caffeoylquinic acids in leaves of selected Apocynaceae species: their isolation and content. Pharm Res. 2014;6(1):67.Google Scholar
  31. 31.
    Leiss KA, Maltese F, Choi YH, Verpoorte R, Klinkhamer PGL. Identification of Chlorogenic acid as a resistance factor for Thrips in chrysanthemum. Plant Physiol. 2009;150(3):1567–75.CrossRefGoogle Scholar
  32. 32.
    Chávez-Servín JL, Castellote AI, López-Sabater MC. Analysis of mono- and disaccharides in milk-based formulae by high-performance liquid chromatography with refractive index detection. J Chromatogr A. 2004;1043(2):211–5.CrossRefGoogle Scholar
  33. 33.
    Spínola V, Pinto J, Castilho PC. Identification and quantification of phenolic compounds of selected fruits from Madeira Island by HPLC-DAD-ESI-MSn and screening for their antioxidant activity. Food Chem. 2015;173:14–30.CrossRefGoogle Scholar
  34. 34.
    Steingass CB, Glock MP, Schweiggert RM, Carle R. Studies into the phenolic patterns of different tissues of pineapple (Ananas comosus [L.] Merr.) infructescence by HPLC-DAD-ESI-MSn and GC-MS analysis. Anal Bioanal Chem. 2015;407(21):6463–79.CrossRefGoogle Scholar
  35. 35.
    Fu Q, Zhang C, Lin Z, Sun H, Liang Y, Jiang H, et al. Rapid screening and identification of compounds with DNA-binding activity from folium Citri Reticulatae using on-line HPLC-DAD-MSn coupled with a post column fluorescence detection system. Food Chem. 2016;192:250–9.CrossRefGoogle Scholar
  36. 36.
    Wilson A. Flavonoid pigments in swallowtail butterflies. Phytochemistry. 1986;25:1309–13.Google Scholar
  37. 37.
    Vega MRG, Esteves-Souza A, Vieira IJC, Mathias L, Braz-Filho R, Echevarria A. Flavonoids from Annona dioica leaves and their effects in Ehrlich carcinoma cells, DNA-topoisomerase I and II. J Braz Chem Soc. 2007;18(8):1554–9.CrossRefGoogle Scholar
  38. 38.
    Rodríguez-Pérez C, Quirantes-Piné R, Amessis-Ouchemoukh N, Khodir M, Segura-Carretero A, Fernández-Gutierrez A. A metabolite-profiling approach allows the identification of new compounds from Pistacia lentiscus leaves. J Pharm Biomed Anal. 2013;77:167–74.CrossRefGoogle Scholar
  39. 39.
    Schügerl K. Extraction of primary and secondary metabolites. In: Kragl U, editor. Technology transfer in biotechnology advances in biochemical engineering. Berlin: Springer; 2005. p. 1–48.Google Scholar
  40. 40.
    Dai J, Mumper RJ. Plant phenolics: extraction, analysis and their antioxidant and anticancer properties. Molecules. 2010 Jan;15(10):7313–52.CrossRefGoogle Scholar
  41. 41.
    Schuelter Boeing J, Oliveira Barizão É, Costa e Silva B, Fernandes Montanher P, de Cinque Almeida V, Vergilio Visentainer J. Evaluation of solvent effect on the extraction of phenolic compounds and antioxidant capacities from the berries: application of principal component analysis. Chem Cent J. 2014;8(1):48.CrossRefGoogle Scholar
  42. 42.
    Díaz-de-Cerio E, Gómez-Caravaca AM, Verardo V, Fernández-Gutiérrez A, Segura-Carretero A. Determination of guava (Psidium guajava L.) leaf phenolic compounds using HPLC-DAD-QTOF-MS. J Funct Foods. 2016;22:376–88.CrossRefGoogle Scholar
  43. 43.
    Benmeziane F, Djamai R, Cadot Y, Seridi R. Optimization of extraction parameters of phenolic compounds from Algerian fresh table grapes, (Vitis Vinifera). Int Food Res J. 2014;21(3):1025–9.Google Scholar
  44. 44.
    Rohr GE, Meier B, Sticher O. Analysis of procyanidins. Stud Nat Prod Chem. 2000;21(PART B):497–570.CrossRefGoogle Scholar
  45. 45.
    Santos-Buelga C, Scalbert A. Proanthocyanidins and tannin like compounds nature, occurrence, dietary intake and effects on nutrition and health. J Sci Food Agric. 2000;80:1094–117.CrossRefGoogle Scholar
  46. 46.
    Dhaouadi K, Meliti W, Dallali S, Belkhir M, Ouerghemmi S, Sebei H, et al. Commercial Lawsonia inermis L. dried leaves and processed powder: phytochemical composition, antioxidant, antibacterial, and allelopathic activities. Ind Crop Prod. 2015;77:544–52.CrossRefGoogle Scholar
  47. 47.
    Wong Paz JE, Muñiz Márquez DB, Martínez Ávila GCG, Belmares Cerda RE, Aguilar CN. Ultrasound-assisted extraction of polyphenols from native plants in the Mexican desert. Ultrason Sonochem. 2014;22:1–8.Google Scholar
  48. 48.
    Zhen J, Villani TS, Guo Y, Qi Y, Chin K, Pan M-H, et al. Phytochemistry, antioxidant capacity, total phenolic content and anti-inflammatory activity of Hibiscus sabdariffa leaves. Food Chem. 2016;190:673–80.CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Elixabet Díaz-de-Cerio
    • 1
  • Luis Manuel Aguilera-Saez
    • 2
  • Ana María Gómez-Caravaca
    • 1
  • Vito Verardo
    • 3
    • 4
  • Alberto Fernández-Gutiérrez
    • 1
  • Ignacio Fernández
    • 2
  • David Arráez-Román
    • 1
    • 5
  1. 1.Department of Analytical Chemistry, Faculty of SciencesUniversity of GranadaGranadaSpain
  2. 2.Department of Chemistry and Physics, Research Centre for Agricultural and Food Biotechnology (CIAIMBITAL)University of AlmeriaAlmeriaSpain
  3. 3.Department of Nutrition and Food ScienceUniversity of Granada, Campus Universitario de CartujaGranadaSpain
  4. 4.Institute of Nutrition and Food Technology ‘José Mataix’, Biomedical Research CentreUniversity of GranadaGranadaSpain
  5. 5.Health Science Technological ParkResearch and Development Functional Food CentreGranadaSpain

Personalised recommendations