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Valorization of Algerian Saffron: Stigmas and Flowers as Source of Bioactive Compounds

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Abstract

Purpose

Saffron is widely used for its medicinal and culinary properties. Its stigmas are the most expensive part comparing with the flowers that are discarded during production. For that, the objective of this work was to determine the phytocomplex of stigma and flower material (except stigma) of saffron from Algeria. Crocin, picrocrocin and safranal contents were quantified to classify its quality according to ISO/TS 3632 standards. The antioxidant and antimicrobial properties of extracts were also investigated.

Methods

Crocins, total phenolic content, flavonoids, phenolic acids, and anthocyanins were detected and quantified by HPLC-DAD and spectrophotometric analyses. The antioxidant potential was evaluated by 4 in vitro assays. The antimicrobial activity against seven bacteria and two strains of Candida albicans was also evaluated.

Results

The results revealed that the chromatographic analysis showed the presence of 20 phenolic acids and flavonoids in the plant samples, with the highest concentrations in stigmas. Crocin derivatives were found only in stigmas, except that trans-crocetin (β-D-gentiobiosyl) which was present also in flower material. The highest total phenolic, total flavonoid and total flavonol contents were observed in stigmas and the highest level of anthocyanins and hydrolysable and condensed tannins in flowers. This extract showed a stronger protection effect from β-carotene bleaching and a higher TAC. The both extracts had some antimicrobial effect.

Conclusions

These results point out that flower material could be considered as natural bioresource of polyphenolic compounds, with higher biological activities which remain to be exploited.

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References

  1. Kamalipour, M., Akhondzadeh, S.: Cardiovascular effects of saffron: an evidence- based review. J. Tehran Heart Cent. 6(2), 59–61 (2011)

    Google Scholar 

  2. Dar, R.A., Shahnawaz, M., Malik, S.B., Sangale, M.K., Ade, A.B., Qazi, P.H.: Cultivation, distribution, taxonomy, chemical composition and medical importance of Crocus sativus. J. Phytopharmacol. 6(6), 356–358 (2017)

    Article  Google Scholar 

  3. Ahmad Tantry, M., Ahmad Dar, B., Singh, S.: An economic analysis of production and marketing of saffron in Jammu and Kashmir. Int. J. Soc. Relev. Concern. 5(10), 12–19 (2017)

    Google Scholar 

  4. Abdullaev, F.: Biological properties and medicinal use of saffron (Crocus sativus L.). Acta Hort. (ISHS) 739, 339–345 (2007). https://doi.org/10.17660/ActaHortic.2007.739.44

    Article  Google Scholar 

  5. Hosseini, A., Razavi, B.M., Hosseinzadeh, H.: Saffron (Crocus sativus) petal as a new pharmacological target: a review. Iran. J. Basic Med. Sci. 21(11), 1091–1099 (2018). https://doi.org/10.22038/IJBMS.2018.31243.7529

    Article  Google Scholar 

  6. Pitsikas, N.: Constituents of saffron (Crocus sativus L.) as potential candidates for the treatment of anxiety disorders and schizophrenia. Molecules. 21(3), 303 (2016). https://doi.org/10.3390/molecules21030303

    Article  Google Scholar 

  7. Rios, J., Recio, M., Giner, R., Manez, S.: An update review of saffron and its active constituents. Phytother. Res. 10(3), 189–193 (1996)

    Article  Google Scholar 

  8. Xi, L., Qian, Z.: Pharmacological properties of crocetin and crocin (digentiobiosyl ester of crocetin) from saffron. Nat. Prod. Commun. 1(1), 65–75 (2006)

    Article  Google Scholar 

  9. Caser, M., Demasi, S., Stelluti, S., Donno, D., Scariot, V.: Crocus sativus L. cultivation in alpine environments: stigmas and tepals as source of bioactive compounds. Agronomy 10, 1473 (2020). https://doi.org/10.3390/agronomy10101473

    Article  Google Scholar 

  10. Soil Science Division Staff: Soil Survey Manual. In: Ditzler, C., Scheffe, K., Monger, H.C. (eds.) USDA Handbook 18. Government Printing Office, Washington, DC (2017)

    Google Scholar 

  11. Walkley, A., Black, I.A.: An examination of the Degtjareff method for determining soil organic matter, and a proposed modification of the chromic acid titration method. Soil Sci. 37, 29–38 (1934)

    Article  Google Scholar 

  12. Bremner, J.: Determination of nitrogen in soil by the Kjeldahl method. J. Agric. Sci. 55, 11–33 (1960)

    Article  Google Scholar 

  13. ISO 3632-2:2010: Spices—Saffron (Crocus sativus L.). In: Part 2: Test Methods, 1st edn. International Organization for Standardization, Genève (2010)

    Google Scholar 

  14. Gismondi, A., Serio, M., Canuti, L., Canini, A.: Biochemical, antioxidant and antineoplastic properties of Italian saffron (Crocus sativus L.). Am J Plant Sci. 3(11), 1573–1580 (2012). https://doi.org/10.4236/ajps.2012.311190

    Article  Google Scholar 

  15. Zanella, L., Gismondi, A., Di Marco, G., Braglia, R., Scuderi, F., Redi, E.L., Galgani, A., Canini, A.: Induction of antioxidant metabolites in Moringa oleifera callus by abiotic stresses. J. Nat. Prod. 82(9), 2379–2386 (2019). https://doi.org/10.1021/acs.jnatprod.8b00801

    Article  Google Scholar 

  16. Singleton, V.L., Rossi, J.A.: Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagents. Am. J. Enol. Vitic. 16, 144–158 (1965)

    Google Scholar 

  17. Zhishen, J., Mengcheng, T., Jianming, W.: The determination of flavonoid contents in mulberry and their scavenging effects on super oxide radicals. Food Chem. 64(4), 555–559 (1999). https://doi.org/10.1016/S0308-8146(98)00102-2

    Article  Google Scholar 

  18. Kumaran, A., Karunakaran, R.J.: In vitro antioxidant activities of methanol extracts of five Phyllanthus species from India. LWT-Food Sci. Technol. 40(2), 344–352 (2007). https://doi.org/10.1016/j.lwt.2005.09.011

    Article  Google Scholar 

  19. Julkunen-Titto, R.: Phenolic constituents in the levels of northern willows: methods for precursors of clarified apple juice sediment. J. Food Sci. 33, 254–257 (1985)

    Google Scholar 

  20. Mole, S., Waterman, P.: A critical analysis of techniques for measuring tannins in ecological studies. Oecologia 72(1), 137–147 (1987)

    Article  Google Scholar 

  21. Wagner, G.J.: Content and vacuole/extra vacuole distribution of neutral sugars free amino acids, and anthocyanins in protoplast. Plant Physiol. 64, 88–93 (1979). https://doi.org/10.1104/pp.64.1.88

    Article  Google Scholar 

  22. Prieto, P., Pineda, M., Aguilar, M.: Spectrophotometric quantitation of antioxidant capacity through the formation of a phospho-molybdenum complex: specific application to the determination of vitamin E. Anal. Biochem. 269, 337–341 (1999). https://doi.org/10.1006/abio.1999.4019

    Article  Google Scholar 

  23. Sanchez-Moreno, C., Larrauri, J.: Main methods used in lipid oxidation determination. Food Sci. Technol. Int. 4, 391–399 (1998). https://doi.org/10.1177/108201329800400603

    Article  Google Scholar 

  24. Oyaizu, M.: Studies on products of browning reaction prepared from glucose amine. Jpn. J. Nutr. 44, 307–315 (1986). https://doi.org/10.5264/eiyogakuzashi.44.307

    Article  Google Scholar 

  25. Moure, A., Franco, D., Sineiro, J., Dominguez, H., Nunez, M.J., Lema, J.M.: Evaluation of extracts from Gevuina avellana hulls as antioxidants. J. Agri. Food Chem. 48, 3890–3897 (2000). https://doi.org/10.1021/jf000048w

    Article  Google Scholar 

  26. NCCLS, “National Committee for Clinical Laboratory Standards”: Performance standards for antimicrobial susceptibility testing: eleventh informational supplement. M100–S11. NCCLS, Wayne (2001)

    Google Scholar 

  27. NCCLS, “National Committee for Clinical Laboratory Standards”: Reference method for broth dilution antifungal susceptibility testing of yeasts: approved standard. NCCLS, Wayne (1997)

    Google Scholar 

  28. CLSI: Performance standards for antimicrobial disk susceptibility tests; Approved standard Twelfth Edition. CLSI document M02-A12. Clinical and Laboratory Standards Institute, Wayne (2015)

    Google Scholar 

  29. Belyagoubi-Benhammou, N., Belyagoubi, L., Gismondi, A., Di Marco, G., Canini, A., Atik-Bekkara, F.: GC/MS analysis, and antioxidant and antimicrobial activities of alkaloids extracted by polar and a polar solvents from the stems of Anabasis articulata. J. Med. Chem. Res. 28, 754–767 (2019). https://doi.org/10.1007/s00044-019-02332-6

    Article  Google Scholar 

  30. ISO 3632-1: Spices—Saffron (Crocus sativus L.). In: Part 1: Specification, 2nd edn. International Organization for Standardization, Genève (2011)

    Google Scholar 

  31. Lage, M., Cantrell, C.L.: Quantification of saffron (Crocus sativus L.) metabolites crocins, picrocrocin and safranal for quality determination of the spice grown under different environmental Moroccan conditions. Sci. Hortic. 121, 366–373 (2009). https://doi.org/10.1016/j.scienta.2009.02.017

    Article  Google Scholar 

  32. Caballero-Ortega, H., Pereda-Miranda, R., Riveron-Negrete, L., Hernandez, J.M., Medecigo-Rıos, M., Castillo-Villanueva, A.: Chemical composition of saffron (Crocus sativus L.) from four countries. In: Ferna´ ndez, J.A., Abdullaev, F.I. (eds.) Proceedings of the First International Symposium on Saffron Biology and Biotechnology, Acta Horticulture, pp. 321–326. International Society for Horticultural Science, Leuven (2004)

    Google Scholar 

  33. Sujata, V., Ravishankar, A., Venkataraman, L.V.: Methods for the analysis of the saffron metabolites crocin, crocetins, picrocrocin and safranal for the determination of the quality of the spice using thin-layer chromatography, high performance liquid chromatography and gas chromatography. J. Chromatogr. 624, 497–502 (1992). https://doi.org/10.1016/0021-9673(92)85699-T

    Article  Google Scholar 

  34. Atyane, L.H., Molinet, J., Serghini, M.A., Dupuy, N., Maimouni, E.L.: Influence of drying process on safranal content in the Taliouine Saffron (Morocco): quantification by gas chromatography. J. Mater. Environ. Sci. 8(S), 4597–4603 (2017)

    Google Scholar 

  35. Moratalla-López, N., Bouhadida, N., Bagur, M.J., García-Rodríguez, M.V., Oueslati, S., Alonso, G.L.: Comparing Tunisian and Spanish saffron regarding their bioactive metabolites using HPLC and GC methods. Acta Hortic. 1184, 279–286 (2017). https://doi.org/10.17660/ActaHortic.2017.1184.40

    Article  Google Scholar 

  36. Bononi, M., Milella, P., Tateo, F.: Gas chromatography of safranal as preferable method for the commercial grading of saffron (Crocus sativus L.). Food Chem. 176, 15–21 (2015). https://doi.org/10.1016/j.foodchem.2014.12.047

    Article  Google Scholar 

  37. Alonso, G.L., Salinas, M.R., Garijo, J., Sánchez-Fernánde, M.A.: Composition of crocins and picrocrocin from spanish saffron (Crocus sativus L.). J. Food Qual. 24, 219–233 (2001). https://doi.org/10.1111/j.1745-4557.2001.tb00604.x

    Article  Google Scholar 

  38. Menghini, L., Leporini, L., Vecchiotti, G., Locatelli, M., Carradori, S., Ferrante, C., Zengin, G., Recinella, L., Chiavaroli, A., Leone, S., Brunetti, L., Orlando, G.: Crocus sativus L. stigmas and byproducts: Qualitative fingerprint, antioxidant potentials and enzyme inhibitory activities. Food Res. Int. 109, 91–98 (2018). https://doi.org/10.1016/j.foodres.2018.04.028

    Article  Google Scholar 

  39. Vahedi, M., Kabiri, M., Salami, A., Rezadoost, S., Mirzaie, H., Reza Kanani, M.: M.: Quantitative HPLC-based metabolomics of some Iranian saffron (Crocus sativus L.) accessions. Ind Crops Prod. 118, 26–29 (2018). https://doi.org/10.1016/j.indcrop.2018.03.024

    Article  Google Scholar 

  40. Straubinger, M., Bau, B., Eckstein, S., Fink, M., Winterhalter, P.: Identification of novel glycosidic aroma precursors in saffron. J. Agric. Food Chem. 46, 3238–3243 (1998). https://doi.org/10.1021/jf980119f

    Article  Google Scholar 

  41. Carmona, M., Zalacain, A., Pardo, J.E., López, E., Alvarruiz, A., Alonso, G.L.: Influence of different drying and aging conditions on saffron constituents. Agric. Food Chem. 53, 3974–3979 (2005). https://doi.org/10.1021/jf0404748

    Article  Google Scholar 

  42. Chaouqi, S., Moratalla-López, N., Lage, M., Lorenzo, C., Alonso, G.L., Guedira, T.: Effect of drying and storage process on Moroccan saffron quality. Food Biosci. 22, 146–153 (2018). https://doi.org/10.1016/j.fbio.2018.02.003

    Article  Google Scholar 

  43. Tarantilis, P.A., Tsoupras, G., Polissiou, M.: Determination of saffron (Crocus sativus L.) components in crude plant extract using high-performance liquid chromatography-UV–visible photodiode-array detection-mass spectrometry. J. Chromatogr. 699, 107–118 (1995). https://doi.org/10.1016/0021-9673(95)00044-N

    Article  Google Scholar 

  44. Moratalla-Lopez, N., Sanchez, A.M., Lorenzo, C., Lopez-Corcoles, H., Alonso, G.L.: Quality determination of Crocus sativus L. flower by high-performance liquid chromatography. J. Food Compost. Anal. 93, 103613 (2020). https://doi.org/10.1016/j.jfca.2020.103613

    Article  Google Scholar 

  45. Vignolini, P., Heimler, D., Pinelli, P., Ieri, F., Sciullo, A., Romani, A.: Characterization of by-products of saffron (Crocus sativus L.) production. Nat. Prod. Commun. 3(12), 1959–1962 (2008). https://doi.org/10.1177/1934578X0800301203

    Article  Google Scholar 

  46. Termentzi, A., Kokkalou, E.: LC-DAD-MS (ESI+) analysis and antioxidant capacity of Crocus sativus petal extracts. Planta Med. 74, 573–581 (2008). https://doi.org/10.1055/s-2008-1074498

    Article  Google Scholar 

  47. Serrano-Díaz, J., Sánchez, A.M., Maggi, L., Martínez-Tomé, M., Garcia-Diz, L., Murcia, A., Alonso, M.: Increasing the applications of Crocus sativus flowers as natural antioxidants. J. Food Sci. 77(11), C1162–C1168 (2012). https://doi.org/10.1111/j.1750-3841.2012.02926.x

    Article  Google Scholar 

  48. Jadouali, S.M., Atifi, H., Bouzoubaa, Z., Majourhat, K., Gharby, S., Achemchem, F., Elmoslih, A., Laknifli, A., Mamouni, R.: Chemical characterization, antioxidant and antibacterial activity of Moroccan Crocus sativus L. petals and leaves. J. Mater. Environ. Sci. 9(1), 113–118 (2018). https://doi.org/10.26872/jmes.2018.9.1.14

    Article  Google Scholar 

  49. Jadouali, S.M., Atifi, H., Mamouni, R., Majourhat, K., Bouzoubaâ, Z., Laknifli, A., Faouzi, A.: Chemical characterization and antioxidant compounds of flower parts of Moroccan Crocus sativus L. J. Saudi Soc. Agric. Sci. 18, 476–480 (2019). https://doi.org/10.1016/j.jssas.2018.03.007

    Article  Google Scholar 

  50. Azizian–Shermeh, O., Valizadeh, M., Taherizadeh, M., Beigomi, M.: Phytochemical investigation and phytosynthesis of eco–friendly stable bioactive gold and silver nanoparticles using petal extract of saffron (Crocus sativus L.) and study of their antimicrobial activities. Appl. Nanosci. 10, 2921–2922 (2020). https://doi.org/10.1007/s13204-019-01059-5

    Article  Google Scholar 

  51. Babaei, A., Arshami, J., Haghparast, A., Danesh Mesgaran, M.: Effects of Saffron (Crocus sativus) petal ethanolic extract on hematology, antibody response, and spleen histology in rats. Avecina J. Phytomed. 4, 103–109 (2014)

    Google Scholar 

  52. Tanaka, Y., Sasaki, N., Ohmiya, A.: Biosynthesis of plant pigments: anthocyanins, betalains and carotenoids. Plant J 54(4), 733–749 (2008). https://doi.org/10.1111/j.1365-313X.2008.03447.x

    Article  Google Scholar 

  53. Serrano-Díaz, J., Sánchez, A.M., Martínez-Tomé, M., Winterhalter, P., Alonso, G.L.: Flavonoid determinationin the quality control of floral bioresidues from Crocus sativus L. J. Agric. Food Chem. 62, 3125–3133 (2014). https://doi.org/10.1021/jf4057023

    Article  Google Scholar 

  54. Cusano, E., Consonni, R., Petrakis, E.A., Astraka, K., Cagliani, L.R., Polissiou, M.G.: Integrated analytical methodology to investigate bioactive compounds in Crocus sativus L. flowers. Phytochem. Anal. 29(5), 1–11 (2018). https://doi.org/10.1002/pca.2753

    Article  Google Scholar 

  55. Moratalla-López, N., Bagur, M.J., Lorenzo, C., Martínez-Navarro, M.E., Salinas, M.R., Alonso, G.L.: Bioactivity and bioavailability of the major metabolites of Crocus sativus L. flower. Molecules 24(15), 2827 (2019). https://doi.org/10.3390/molecules24152827

    Article  Google Scholar 

  56. Lahmass, I., Ouahhoud, S., Elmansuri, M., Sabouni, A., Elyoubi, M., Benabbas, R., Choukri, M., Saalaoui, E.: Determination of antioxidant properties of six by-products of Crocus sativus L. (Saffron) plant products. Waste Biomass Valor. 9(8), 1349–1357 (2018). https://doi.org/10.1007/s12649-017-9851-y

    Article  Google Scholar 

  57. Lahmass, I., Ouahhoud, S., Elyoubi, M., Benabbas, R., Sabouni, A., Asehraou, A., Saalaoui, E.: Evaluation of antioxidant activities of saffron stigma and spath as by-product of Crocus sativus L. MOJ Biol Med. 3(4), 154–158 (2018). https://doi.org/10.15406/mojbm.2018.03.00091

    Article  Google Scholar 

  58. Asdaq, S.M., Inamdar, M.N.: Potential of Crocus sativus (saffron) and its constituent, crocin, as hypolipidemic and antioxidant in rats. Appl. Biochem. Biotechnol. 162(2), 358–372 (2010). https://doi.org/10.1007/s12010-009-8740-7

    Article  Google Scholar 

  59. Fazeli-Nasab, B.: Evaluation of antibacterial activities of hydroalcoholic extract of saffron petals on some bacterial pathogens. J. Med. Bacteriol. 8(5), 8–20 (2019)

    Google Scholar 

  60. Muzaffar, S., Rather, S.A., Khan, K.Z., Yildiz, F.: In vitro bactericidal and fungicidal activities of various extracts of saffron (Crocus sativus L.) stigmas from Jammu & Kashmir, India. Cogent. Food & Agric. 2(1), 1158999 (2016). https://doi.org/10.1080/23311932.2016.1158999

    Article  Google Scholar 

  61. Wali, A.F., Abou Alchamat, H.A., Hariri, H.K., Hariri, B.K., Menezes, G.A., Zehra, U., Rehman, M.U., Ahmad, P.: Antioxidant, antimicrobial, antidiabetic and cytotoxic activity of Crocus sativus L. petals. Appl. Sci. 10, 1519 (2020). https://doi.org/10.3390/app10041519

    Article  Google Scholar 

  62. De Monte, C., Bizzarri, B., Gidaro, M.C., Carradori, S., Mollica, A., Luisi, G., Granese, A., Alcaro, S., Costa, G., Basilico, N., Parapini, S., Scaltrito, M.M., Masia, C., Sisto, F.: Bioactive compounds of Crocus sativus L. and their semi-synthetic derivatives as promising anti-Helicobacter pylori, anti-malarial and anti-leishmanial agents. J. Enzyme Inhib. Med. Chem. 30(6), 1027–1033 (2015). https://doi.org/10.3109/14756366.2014.1001755

    Article  Google Scholar 

  63. Hussein, R.A., Salih, N.A., Nadhaif, E.T.: Bioactivity of crocin pigment of saffron plant. Plant Arch. 18(1), 357–364 (2018)

    Google Scholar 

  64. Buzzini, P., Arapitsas, P., Goretti, M., Branda, E., Turchetti, B., Pinelli, P., Ieri, F., Romani, A.: Antimicrobial and antiviral activity of hydrolysable tannins. Mini-Rev. Med. Chem. 8(12), 1179–1187 (2008). https://doi.org/10.2174/138955708786140990

    Article  Google Scholar 

  65. Sun, X.H., Zhou, T.T., Wei, C.H., Lan, W.Q., Zhao, Y., Pan, Y.J., Wu, V.C.H.: Antibacterial effect and mechanism of anthocyanin rich Chinese wild blueberry extract on various foodborne pathogens. Food Control. 94, 155–161 (2018). https://doi.org/10.1016/j.foodcont.2018.07.012

    Article  Google Scholar 

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Acknowledgements

The authors acknowledge the saffron producer in this region for providing plant material. The authors also thank Dr. BETTIOUI Reda for his help in statistical analysis with PCA.

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Belyagoubi, L., Loukidi, B., Belyagoubi-Benhammou, N. et al. Valorization of Algerian Saffron: Stigmas and Flowers as Source of Bioactive Compounds. Waste Biomass Valor 12, 6671–6683 (2021). https://doi.org/10.1007/s12649-021-01454-6

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