Abstract
A spirostane with an attached trisaccharide, (25R)-5α-spirostane-2α,3β,5α-triol 3-O-(O-α-l-rhamnopyranosyl-(1 → 2)-O-(β-d-galactopyranosyl-(1 → 3))-β-d-glucopyranoside), was isolated and identified from the aerial parts of Agapanthus africanus by activity-guided fractionation. Fungicidal properties of the crude extract, semi-purified fractions as well as the purified active saponin from A. africanus were screened in vitro against Fusarium oxysporum. At a concentration of 1 mg mL−1, the crude extract and semi-purified ethyl acetate and dichloromethane fractions showed significant antifungal activity. The purified saponin inhibited the in vitro mycelial growth of F. oxysporum completely (100 %) at a concentration of 125 µg mL−1. Furthermore, to verify previously observed induced resistance by crude extracts of A. africanus towards leaf rust, intercellular PR-protein activity was determined in wheat seedlings following foliar application of the purified saponin at 100 µg mL−1. In vitro peroxidase enzyme activity increased significantly (60 %) in wheat seedlings 48 h after treatment with the purified saponin, demonstrating its role as an elicitor to activate a defence reaction in wheat.
Similar content being viewed by others
References
Bohra NK, Purohit DK (2002) Effect of some aqueous plant extracts on toxigenic strain of Aspergillus flavus. Adv Plant Sci 15:103–106
Bowles DJ (1990) Defense-related proteins in higher plants. Annu Rev Biochem 59:873–907
Bronner R, Westphal E, Dreger F (1991) Enhanced peroxidase activity associated with the hypersensitive response of Solanum dulcamara to the gall mite Aceria cladophthirus (Acari: Eriophyoidea). Can J Bot 69:2192–2196
Caceres A, Fletes L, Aguilar L, Ramirez O, Figueroa L, Taracena AM, Samayoa B (1993) Plants used in Guatemala for the treatment of gastrointestinal disorders III. Confirmation of activity against enterobacteria of 16 plants. J Ethnopharmacol 38:31–38
Cawood ME, Pretorius JC, van der Westhuizen AJ, Pretorius ZA (2010) Disease development and PR-protein activity in wheat (Triticum aestivum) seedlings treated with plant extracts prior to leaf rust (Puccinia triticina) infection. Crop Prot 29:1311–1319
Cawood ME, Pretorius JC, Visser B, van der Westhuizen AJ (2013) Induced gene expression in wheat seedlings treated with a crude extract of Agapanthus africanus L. prior to leaf rust infection. Afr J Biotechnol 12(20):2876–2883
Cowan MM (1999) Plant products as antimicrobial agents. Clin Micrbiol Rev 12:564–582
Datta SK, Muthukrishnan S (1999) Pathogenesis-related proteins in plants. CRC Press LLC, Florida
Desta B (1993) Ethiopian traditional herbal drugs. Part II: antimicrobial activity of 63 medicinal plants. J Ethnopharmacol 39:129–139
Dixon RA, Lamb CJ (1990) Molecular communication in interactions between plants and microbial pathogens. Annu Rev Plant Physiol Plant Mol Biol 41:339–367
Duncan AC, Jäger AK, van Staden J (1999) Screening of Zulu medicinal plants for angiotensin converting enzyme (ACE) inhibitors. J Ethnopharmacol 68:63–70
Durrant WE, Dong X (2004) Systemic acquired resistance. Annu Rev Phytopathol 42:185–209
Ekpendu TO, Akah PA, Adesomoju AA, Okogun JI (1994) Antiinflammatory and antimicrobial activities of Mitracarpus scaber extracts. Int J Pharmacogn 32:192–196
El Gueddari NE, Moerschbacher BM (2003) A bioactivity matrix for chitosans as elicitors of disease resistance reactions in wheat. Adv Chitin Sci 7:56–59
Eloff JN, Mdee LK, Masoko P (2007) Invasive and weedy species can be used as a source of antifungal compounds to control plant fungal pathogens. S Afr J Bot 73:287
Felton GW, Workman J, Duffey SS (1992) Avoidance of antinutritive plant defense: role of midgut pH in Colorado potato beatle. J Chem Ecol 18:571–583
Gamoh K, Omote K, Okamoto N, Takatsuto S (1989) High-performance liquid-chromatography of brassinosteroids in plants with derivatization using 9-phenanthreneboronic acid. J Chromatogr A 469:424–428
González AG, Freire R, Francisco CG, Salazar JA, Suárez E (1974) 7-Dehydroagapanthagenin and 8(14)-dehydroagapanthagenin, two new spirostan sapogenins from Agapanthus africanus. Phytochemistry 13:627–632
González AG, Francisco CG, Freire R, Hernández R, Salazar JA, Suárez E (1975) 9(11)-Dehydroagapanthagenin, a new spirostan sapogenin from Agapanthus africanus. Phytochemistry 14:2259–2262
Gotthardt U, Grambow HJ (1992) Near-isogenic wheat suspension cultures: establishment, elicitor induced peroxidase activity and potential use in the study of host pathogen-interactions. J Plant Physiol 139:659–665
Hildebrand DF, Rodriguez JG, Legg CS, Brown GC, Bookjans G (1989) The effects of wounding and mite infestation on soybean leaf lipoxygenase levels. Z Naturforsch 44:655–659
Hintze JL (1999) Number cruncher statistical systems 2000. Kaysville, Utah, USA
Hostettmann KA, Marston A (1995) Saponins. Chemistry and pharmacology of natural products. Cambridge University Press, Cambridge
Jurzysta M, Bialy Z (1999) Antifungal and Haemolytic activity of roots of alfalfa (Medicago spp.) in relation to saponin composition. In: Lyr H, Russell PE, Dehne H-W, Siseer HD (eds) Modern fungicides and antifungal compounds II. 12th international reinhardsbrunn symposium, Friedrichroda, Thuringia, Germany, 24th–29th May 1998. Intercept Limited, pp 445–451
Kaido TL, Veale DJH, Havlik I, Rama DBK (1997) Preliminary screening of plants used in South Africa as traditional herbal remedies during pregnancy and labour. J Ethnopharmacol 55:185–191
Kessmann H, Staub T, Hofmann C, Maetzke T, Herzog J, Ward E, Uknes S, Ryals J (1994a) Induction of systemic acquired disease resistance in plants by chemicals. Annu Rev Phytopathol 32:439–459
Kessmann H, Staub T, Ligon J, Oostendorp M, Ryals J (1994b) Activation of systemic acquired disease resistance in plants. Eur J Plant Pathol 100:359–369
Kogel G, Beissmann B, Reisener HJ, Kogel KH (1988) A single glycoprotein from Puccinia graminis f. sp. tritici cell walls elicits the hypersensitive lignification response in wheat. Physiol Mol Plant Pathol 33:173–185
Magama S, Pretorius JC, Zietsman PC (2003) Antimicrobial properties of extracts from Euclea crispa subsp. Crispa (Ebenaceae) towards human pathogens. S Afr J Bot 69:193–198
Mahato SB, Ganguly AN, Sahu NP (1982) Steroid saponins. Phytochemistry 21:959–978
Marston A, Gafner F, Dossaji SF, Hostettmann K (1988) Fungicidal and molluscicidal saponins from Dolichos kilimandscharicus. Phytochemistry 27:1325–1326
Masoko P, Picard J, Eloff JN (2007) The antifungal activity of twenty-four southern African Combretum species (Combretaceae). S Afr J Bot 73:173–183
Mason RL, Gunst RF, Hess JL (1989) Statistical design and analysis of experiments with application to engineering and science. Wiley, Canada, p 692
Mehdy MC (1994) Active oxygen species in plant defense against pathogens. Plant Physiol 105:467–472
Morrissey JP, Osbour AE (1999) Fungal resistance to plant antibiotics as a mechanism of pathogenesis. Micrbiol Mol Biol Rev 63:708–724
Nakamura O, Mimaki Y, Sashida Y, Nikaido T, Ohmoto T (1993) Agapanthussaponins A-D, new potent cAMP-phosphodiesterase inhibitors from the underground parts of Agapanthus inapertus. Chem Pharm Bull 41:1784–1789
Osbourn AE (2003) Saponins in cereals. Phytochemistry 62:1–4
Pretorius JC, Zietsman PC, Eksteen D (2002) Fungitoxic properties of selected South African plant species against plant pathogens of economic importance in agriculture. Ann Appl Biol 141:117–124
Reichling J (1999) Plant-microbe interactions and secondary metabolites with antiviral, antibacterial and antifungal properties. In: Wink M (ed) Function of plant secondary metabolites and their exploitation in biotechnology. CRC Press, Florida, pp 187–273
Sato J, Goto K, Nanjo F, Kawai S, Murata K (2000) Antifungal activity of plant extracts against Arthrinium sacchari and Chaetomium funicola. J Biosci Bioeng 90:442–446
Schnabl H, Roth U, Friebe A (2001) Brassinosteroid-induced stress tolerances of plants. Recent Res Dev Phytochem 5:169–183
Singh DN, Verma N, Kulshreshtha DK (2007) Steroidal saponins from the rhizomes of Agapanthus africanus (Linn). Ind J Chem Sect B 46:1154–1158
Singh DN, Verma N, Raghuwanshi S, Shukla PK, Kulshreshtha DK (2008) Antifungal activity of Agapanthus africanus extractives. Fitoterapia 79:298–300
Somssich IE (2003) Closing another gap in the plant SAR puzzle. Cell 113:815–816
Steele RG, Torrie JH (1980) Principles and procedures of statistics, 2nd edn. McGraw-Hill, New York
Stephen T (1956) Saponins and sapogenins. Part IV. Agapanthagenin (22a-spirostan-2-α-3-ß-5-α-triol), a new sapogenin from Agapanthus species. J Chem Soc 1167–1169
Sticher L, Mauch-Mani B, Métraux JP (1997) Systemic acquired resistance. Annu Rev Phytopathol 35:235–270
Takechi M, Tanaka Y (1990) Structure-activity relationships of the saponin α-Hederin. Phytochemistry 29:451–452
Tegegne G, Pretorius JC, Swart WJ (2008) Antifungal properties of Agapanthus africanus L. extracts against plant pathogens. Crop Prot 27:1052–1060
Vasyukova NI, Paseshnichenko VA, Davydova MA, Chalenko GI (1977) Prikl Biokhim Mikrobiol 13:172
Wagner H, Bladt S (1996) Plant drug analysis. A thin layer chromatogrphy atlas. Springer, Berlin
Waller GR (1999) Recent advances in saponins used in foods, agriculture, and medicine. In: Cutler HG, Cutler SJ (eds) Biologically active natural products: agrochemicals. CRC Press, Boca Raton, pp 243–274
Zacheo G, Bleve-Zacheo T, Lamberti F (1982) Role of peroxidase and superoxidase dismutase activity in resistant and susceptible tomato cultivars infested by Meloidogyne incognita. Nematol Mediterr 10:75–80
Zehavi U, Polacheck I (1996) Saponins as antimycotic agents: glycosides of medicagenic acid. In: Waller GR, Yamasaki K (eds) Saponins used in traditional and modern medicine. Plenum publishing Co, New York, pp 535–546
Acknowledgments
Financial support by the South African National Research Foundation is gratefully acknowledged.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by E. Schleiff.
Rights and permissions
About this article
Cite this article
Cawood, M.E., Pretorius, J.C., van der Westhuizen, J.H. et al. A saponin isolated from Agapanthus africanus differentially induces apoplastic peroxidase activity in wheat and displays fungicidal properties. Acta Physiol Plant 37, 246 (2015). https://doi.org/10.1007/s11738-015-1992-7
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11738-015-1992-7