Journal of Food Science and Technology

, Volume 55, Issue 7, pp 2702–2711 | Cite as

Effect of pomegranate peel extract on shelf life of strawberries: computational chemistry approaches to assess antifungal mechanisms involved

  • D. RongaiEmail author
  • N. Sabatini
  • P. Pulcini
  • C. Di Marco
  • L. Storchi
  • A. Marrone
Original Article


In Italy Botrytis cinerea represents the most significant disease in strawberry crops and causes major quality and quantity losses in postharvest storage. An alternative strategy to the synthetic fungicides in crop defence could be the use of bioactive compounds with high antifungal activity. This research regards the use of Punica granatum peel extract to extend the shelf life of strawberry and the proposal of a possible mechanism for its antifungal activity. In vitro and in vivo tests showed the ability of pomegranate peel extract to control strawberry gray mould. Fourier transform near infrared spectroscopy showed a high correlation between spectra and disease severity then, a putative molecular mechanism for the interaction of punicalagin on ergosterol of fungal membrane was described by means of computational chemistry approaches. Molecular dynamics simulations were performed by using Gromacs to gain multiconformational representations of either punicalagin and an antifungal compound of clinical relevance, i.e. amphotericin B. The use of grid-based procedures, allowed to shed some light on the molecular mechanism featuring the antifungal activity of punicalagin.


Gray mould Punicalagin Postharvest diseases Ergosterol Computational chemistry 



This work was supported by the projects “Difesa delle colture con prodotti naturali nella Regione Lazio (DI.CO.PRO.NA.L) financed by the Lazio region.

Supplementary material

13197_2018_3192_MOESM1_ESM.doc (576 kb)
Supplementary material 1 (DOC 575 kb)


  1. Anderson TM, Clay MC, Cioffi AG, Diaz KA, Hisao GS, Tuttle MD, Nieuwkoop AJ, Comellas G, Maryum N, Wang S, Uno BE, Wildeman EL, Gonen T, Rienstra CM, Burke MD (2014) Amphotericin forms an extramembranous and fungicidal sterol sponge. Nat Chem Biol 10(5):400–406CrossRefPubMedPubMedCentralGoogle Scholar
  2. Baginski M, Resat H, Borowski E (2002) Comparative molecular dynamics simulations of amphotericin B-cholesterol/ergosterol membrane channels. Biochim Biophys Acta 1567:63–78CrossRefPubMedGoogle Scholar
  3. Bendini A, Cerretani L, Di Virgilio F, Belloni P, Bonoli-Carbognin M, Lercker G (2007) Preliminary evaluation of the application of the FT-IR Spectroscopy to control the geographic origin and quality of virgin olive oils. J Food Qual 30:424–437CrossRefGoogle Scholar
  4. Berendsen HJC, Postma JPM, van Gunsteren WF, Di Nola A, Haak JR (1984) Molecular dynamics with coupling to an external bath. J Chem Phys 81:3684–3690CrossRefGoogle Scholar
  5. Cross S, Cruciani G (2010) Molecular fields in drug discovery: getting old or reaching maturity? Drug Discov Today 15:23–32CrossRefPubMedGoogle Scholar
  6. Darden TA, York DM, Pedersen LG (1993) Particle mesh Ewald: an Nlog(N) method for Ewald sums in large systems. J Chem Phys 98:10089–10092CrossRefGoogle Scholar
  7. Daura X, Gademann K, Jaun B, Seebach D, van Gunsteren WF, Mark AE (1999) Peptide folding: when simulation meets experiment. Angew Chem Int Ed 38:236–240CrossRefGoogle Scholar
  8. Di Qiu M, Shenkin P, Hollinger F, Still W (1997) Continuum model for solvation. A fast analytical method for the calculation of approximate Born radii. J Phys Chem A 101:3005–3014CrossRefGoogle Scholar
  9. Fischer UA, Carle R, Kammerer DR (2011) Identification and quantification of phenolic compounds from pomegranate (Punica granatum L.) peel, mesocarp, aril and differently produced juices by HPLC-DAD–ESI/MSn. Food Chem 127:807–821CrossRefPubMedGoogle Scholar
  10. Foss SR, Nakamura CV, Ueda-Nakamura T, Cortez DA, Endo EH, Dias Filho BP (2014) Antifungal activity of pomegranate peel extract and isolated compound punicalagin against dermatophytes. Ann Clin Microbiol Antimicrob 5:13–32Google Scholar
  11. Ghannoum MA, Rice LB (1999) Antifungal agents: mode of action, mechanisms of resistance, and correlation of these mechanisms with bacterial resistance. Clin Microbiol Rev 12(4):501–517PubMedPubMedCentralGoogle Scholar
  12. Hartsel S, Bolard J (1996) Amphotericin B: new life for an old drug. Trends Pharmacol Sci 17:445–449CrossRefPubMedGoogle Scholar
  13. Helbig J (2002) Ability of the antagonistic yeast Cryptococcus albidus to control Botrytis cinerea in strawberry. Biocontrol 47:85–99CrossRefGoogle Scholar
  14. Hess B, Bekker H, Berendsen HJC, Frajie JCEM (1997) LINCS: a linear constraint solver for molecular simulations. J Comput Chem 18:1463–1472CrossRefGoogle Scholar
  15. Johnson L (2003) Dermatophytes—the skin eaters. Mycologist 17:147–149CrossRefGoogle Scholar
  16. Jones E, Oliphant T, Peterson P (2001) SciPy: open source scientific tools for Python.
  17. Kaminski GA, Friesner RA, Tirado-Rives J, Jorgensen WL (2001) Evaluation and reparameterization of the OPLS-AA force field for proteins via comparison with accurate quantum chemical calculations on peptides. J Phys Chem B 105:6474–6487CrossRefGoogle Scholar
  18. Landi L, Feliziani E, Romanazzi G (2014) Expression of defense genes in strawberry fruits treated with different resistance inducers. J Agric Food Chem 62:3047–3056CrossRefPubMedGoogle Scholar
  19. Lopez-Reyes JG, Spadaro D, Gullinoa ML, Garibaldi A (2010) Efficacy of plant essential oils on postharvest control of rot caused by fungi on four cultivars of apples in vivo. Flavour Fragr J 25:171–177CrossRefGoogle Scholar
  20. Marrone A, Re N, Storchi L (2016) The effects of Ca2+ concentration and E200K mutation on the aggregation propensity of PrPC: a computational study. PLoS ONE 11(12):e0168039. CrossRefPubMedPubMedCentralGoogle Scholar
  21. Mlikota Gablera F, Smilanickb JL, Mansourb MF, Karaca H (2010) Influence of fumigation with high concentrations of ozone gas on postharvest gray mold and fungicide residues on table grapes. Postharvest Biol Technol 55(2):85–90CrossRefGoogle Scholar
  22. Nabigol A, Morshedi H (2011) Evaluation of the antifungal activity of the Iranian thyme essential oils on the postharvest pathogens of strawberry fruits. Afr J Biotechnol 10(48):9864–9869Google Scholar
  23. O’Boyle NM, Morley C, Hutchison GR (2008) Pybel: a Python wrapper for the OpenBabel cheminformatics toolkit. Chem Cent J 2:5–10CrossRefPubMedPubMedCentralGoogle Scholar
  24. Romanazzi G, Lichter A, Mlikota Gabler F, Smilanick JL (2012) Recent advances on the use of natural and safe alternatives to conventional methods to control postharvest gray mold of table grapes. Postharvest Biol Technol 63:141–147CrossRefGoogle Scholar
  25. Romanazzi G, Feliziani E, Santini M, Landi L (2013) Effectiveness of postharvest treatment with chitosan and other resistance inducers in the control of storage decay of strawberry. Postharvest Biol Technol 75:24–27CrossRefGoogle Scholar
  26. Romanazzi G, Smilanick JL, Feliziani E, Droby S (2016) Integrated management of postharvest gray mold on fruits crops. Postharvest Biol Technol 113:69–76CrossRefGoogle Scholar
  27. Rongai D, Pulcini P, Pesce B, Milano F (2015) Antifungal activity of some botanical extracts on Fusarium oxysporum. Open Life Sci (previously Cent Eur J Biol) 10:409–416Google Scholar
  28. Rongai D, Pulcini P, Pesce B, Milano F (2017) Antifungal activity of pomegranate peel extract against fusarium wilt of tomato. Eur J Plant Pathol 147:229–238CrossRefGoogle Scholar
  29. Storchi L, Paciotti R, Re N, Marrone A (2015) Investigation of the molecular similarity in closely related protein systems: the PrP case study. Prot Struct Funct Bioinform 83:1751–1765CrossRefGoogle Scholar
  30. Van Der Spoel D, Lindahl E, Hess B, Groenhof G, Mark AE, Berendsen HJ (2005) GROMACS: fast, flexible, and free. J Comput Chem 26:1701–1718CrossRefGoogle Scholar

Copyright information

© Association of Food Scientists & Technologists (India) 2018

Authors and Affiliations

  1. 1.CREA Research Centre for Plant Protection and CertificationRomeItaly
  2. 2.CREA Research Centre for Engineering and Agro-Food ProcessingCittà Sant’AngeloItaly
  3. 3.(UNI-CH) Università degli Studi G. D’Annunzio Chieti-PescaraChietiItaly
  4. 4.Molecular Discovery LimitedMiddlesex, LondonUK

Personalised recommendations