SAPONINS AND PLANT DEFENSE RESPONSES

Saponins are secondary metabolites produced in healthy plants and derive their name from their soap-like properties. They are pre-formed antimicrobial agents in contrast to phytoalexins which are synthesized in response to pathogen attack (Osbourn et al., 1998). Saponins a glycosylated natural product present in plant exhibits antifungal activity as defense response against phytopathogenic fungi (Osbourn et al., 1998), they also play a role as defensive compound against insect (Nielson et al., 2010) and has molluscicidal effect (Huang et al., 2003). Saponins can be divided into three groups such as triterpenoid (aglycone), a steroid or a steroidal glycoalkaloid (Osbourn 1996 a). There are 11 main classes of saponin: dammaranes, tirucallanes, lupanes, hopanes, oleananes, taraxasteranes, ursanes, cycloartanes, lanostanes, cucurbitanes and steroids (Kregiel et al., 2017).  Triterpenoid is primarily found in dicotyledonous plants but may also be present in monocot. Steroid saponins mainly occurs in monocots example Liliaceae, Dioscoraceae and Agavaceae but is also present in certain dicots such as Foxglove (Osbourn 1996 a).  Oats (Avena sativa) contain both triterpenoid and steroid saponins (Osbourn 1996 a).  Oat kernel saponin is mainly present in endosperm (Onning et al., 1993).

Saponins are associated with defensive roles due to their cytotoxicity and are active against microorganisms (Colson et al., 2020). Saponins may have membranolytic, toxic and fungitoxic effects (Price et al., 1987). Antifungal saponins from oats and solanaceous plants are oat root saponin avenacin A-I (a triterpenoid) and α-tomatine as well as α-chaconine are both steroidal glycoalkaloids and are found in tomato and potato respectively (Morrissey and Osbourn 1999). The mechanisms of antifungal activity of saponins is due to their ability to complex with sterols in fungal membranes and induce membrane disruption (Keukens et al., 1995). Glycoalkaloid is toxic to Cladospoprium fulvum (Dow and Callow 1978). Tomatine exerted both fungistatic and fungicidal effects and caused an irreversible leakage of electrolytes from hyphae (Dow and Callow 1978). Antifungal compounds are commonly sequestered in vacuoles or organelles of healthy plants and so necrotrophic pathogens may encounter fungitoxic levels of these compounds because they cause extensive tissue damage (Morrissey and Osbourn 1999). The antifungal steroidal, glycoalkaloid saponin, alpha-tomatine is present in uninfected tomato plants in substantial concentrations and may contribute to the protection of tomato plants against the attack by phytopathogenic fungi (Melton et al., 1998).  Many tomato pathogens has the ability to detoxify alpha-tomatine through the action of enzymes known as tomatinases. In contrast the biotrophic tomato pathogen Cladosporium fulvum is sensitive to alpha-tomatine and is unable to detoxify this saponin (Melton et al., 1998). Number of phytopathogenic fungi degrade the saponins of their respective host by hydrolysis of sugar molecules from sugar chain attached to C-3 of the saponin backbone. Fungi that succeed in breaching antimicrobial plant defences produce saponin detoxifying enzymes (Osbourn 1996 b). Root-infecting pathogen Gaeumannomyces graminis requires saponin detoxifying enzyme avenacinase for infection of oats, the increased disease susceptibility of oat variants lacking avenacins supports the significance of saponin resistance for fungal pathogenesis and to the notion that saponins play a role as antifungal phytoprotectants (Morrissey and Osbourn 1999).

Aescin a saponin has a strong antifungal activity and can also activate plant immunity and provides SA-dependent resistance against both fungi and bacterial pathogens (Trda et al., 2019). The fungistatic activity of saponins was demonstrated both in vivo and in vitro (Gruiz 1996).  Antifungal activity of saponins were evaluated in vitro against six pathogenic fungi and it was observed that saponins inhibited the growth of  Fusarium oxysporum f. sp. callistephi, Botrytis cinerea, Botrytis tulipae, Phoma narcissi, Fusarium oxysporum narcissi  (Saniewska et al., 2006). Trda et al.(2019) showed that aescin triggers plant defense by activating the SA pathway and oxidative burst ultimately leading to resistance of Brassica napus against the fungus Leptosphaeria maculans. The antimycotic activity of saponin A from Styrax and of its debenzoylated derivative saponin B was studied on number of plant pathogens and on Trichoderma viride. Saponin A demonstrated activity against Trichoderma viride, Fusarium oxysporum, Aspergillus niger and Rhizopus mucco. Saponin B had low activity on Trichoderma viride (Zehavi et al., 2008). Zehavi et al.(1993) studied the structure and antifungal activity of medicagenic acid saponins as well as included synthetic glycosides of mannose, galactose, cellobiose and lactose and furthermore 23α-hydroxymethyl analog of medicagenic acid on plant pathogens.  The native glucose-containing saponin was more effective antifungal agent. A carboxyl substituent at the 23α  position of the sapogenin showed higher fungistatic activity than a methyl carboxylate which in turn was more effective than hydroxymethyl group at the same position (Zehavi et al., 1993). Saponin rich extracts can control the phytopathogenic fungi especially under organic management (Chapagain et al, 2007). Saponins are effective against a wide range of plant pathogens and can be used as natural fungicide.

                                                                          See Part A for further information ………

References:

Chapagain, B. P., Wiesman, Z. and Tsror, L. 2007 In -Vitro Study of the Antifungal Activity of Saponin-Rich Extracts against Prevalent Phytopathogenic Fungi. Ind. Crops Prod.  26(2): 109 – 115

doi.org/10.1016/j.indcrop.2007.02.005

Colson, E., Savarino, P., Claereboudt, E. J. S., Cabrera-Barjas, G., Deleu, M., Lins, L., Eeckhaut, I., Flammang, P. and Gerbaux, P. 2020 Enhancing the Membranolytic Activity of Chenopodium quinoa Saponins by Fast Microwave Hydrolysis. Molecules 25(7): 1731

doi: 10.3390/molecules25071731

Dow, J. M. and Callow, J. A. 1978 A Possible Role for α-tomatine in the Varietal-Specific Resistance of Tomato to Cladosporium fulvum. Phytopathol.  Z.   92(3): 211 – 216

doi.org/10.1111/j.1439-0434.1978.tb03605.x

Gruiz, K. 1996 Fungitoxic Activity of Saponins: Practical Use and Fundamental Principles. In: “Saponins Used in Traditional and Modern Medicine”. Advances in Experimental Medicine and Biology. Waller, G. R., Yamasaki, K. (eds.). Springer, Boston, MA. 404: 527 – 534

doi.org/10.1007/978-1-4899-1367-8_43

Huang, H-C., Liao, S-C., Chang, F-R., Kuo, Y-H.  and Wu, Y-C. 2003 Molluscicidal Saponins from Sapindus mukorossi Inhibitory Agents of Golden Apple Snails Pomacea canaliculata. J. Agric. Food Chem. 51(17): 4916 – 4919

doi.org/10.1021/jf0301910

Keukens, E. A. J., de Vrije, T., van den Boom, C., de Waard, P., Plasman, H. H., Thiel, F., Chupin, V., Jongen, W. M. F. and de Kruijff, B. 1995 Molecular Basis of Glycoalkaloid Induced Membrane Disruption. Biochimica et Biophysica Acta (BBA) – Biomembranes 1240(2): 216 – 228

doi.org/10.1016/0005-2736(95)00186-7

Kregiel, D., Berlowska, J., Witonska, I. A., Antolak, H., Proestos, C., Babic, M., Babic, L. and Zhang, B. 2017 Saponin Based Biological- Active Surfactants from Plants. In: “Application and Characterization of Surfactants”. Najjar, R. (ed.). Publisher: In Tech. Edition 1st, Chapter 6: 183 – 205

doi.org/10.5772/68062

Melton, R. E., Flegg, L. M., Brown, J. K., Oliver, R. P., Daniels, M. J. and Osbourn, A. E. 1998 Heterologous Expression of Septoria lycopersici  tomatinase in Cladosporium fulvum: Effects on Compatible and Incompatible Interactions with Tomato Seedlings. Mol. Plant Microbe Interact. 11(3): 228 – 236

doi: 10.1094/MPMI.1998.11.3.228

Morrissey, J. P. and Osburn, A. E. 1999  Fungal Resistance to Plant Antibiotics as a Mechanism of Pathogenesis.  Microbiol. Mol. Biol. Rev. 63(3): 708 – 724

doi: 10.1128/MMBR.63.3.708-724.1999

Nielsen, J. K., Nagao, T., Okabe, H. and Shinoda, T. 2010 Resistance in the Plant Barbarea vulgaris and Counter-Adaptations in Flea Beetles Mediated by Saponins. J. Chem. Ecol. 36: 227 – 285

doi.org/10.1007/s10886-010-9758-6

Onning, G., Asp, N-G. and Sivik, B. 1993 Saponin Content in Different Oat Varieties and in Different Fractions of Oat Grain. Food Chemistry 48(3): 251 – 254

doi.org/10.1016/0308-8146(93)90135-3

Osbourn, A. E., Wubben, J. P., Melton, R. E., Carter, J. P. and Daniels, M. J. 1998 Saponins and Plant Defense. In: “Phytochemical Signals and Plant-Microbe Interactions”. Romeo, J. T.., Downum, K. R. and Verpoorte, R. (eds.). Springer, Boston MA.  Recent Advances in Phytochemistry (Proceedings of the Phytochemical Society of North America) 32: 1-15

doi.org/10.1007/978-1-4615-5329-8_1

Osbourn, A. E. 1996 a Preformed Antimicrobial Compounds and Plant Defense against Fungal Attack.  Plant Cell 8: 1821 – 1831

doi.org/10.1105/tpc.8.10.1821

Osbourn, A. 1996 b Saponins and Plant Defense – A Soap Story. Trends Plant Sci. 1(1): 4 – 9

doi.org/10.1016/S1360-1385(96)80016-1

Price, K. R., Johnson, I. T., Fenwick, G. R. and Malinow, M. R. 1987 The Chemistry and Biological Significance of Saponins in Foods and Feeding Stuffs, C R C Critical Reviews in Food Science and Nutrition 26(1): 27 – 135

doi: 10.1080/10408398709527461

Saniewska, A., Jarecka, A., Bialy, Z. and Jurzysta, M. 2006 Antifungal Activity of Saponins Originated from Medicago hybrida against Some Ornamental Plant Pathogens. Acta Agrobotanica 59(2): 51 – 58

doi.org/10.5586/aa.2006.061

Trda, L., Janda, M., Mackova, D., Pospichalova, R., Dobrev, P. I., Burketova, L. and Matusinsky, P. 2019 Dual Mode of the  Saponin Aescin in Plant Protection: Antifungal Agent and Plant Defense Elicitor. Front.  Plant Sci. 10: 1448

doi: 10.3389/fpls.2019.01448

Zehavi, U., Ziv-Fecht, O., Levy, M., Naim, M., Evron, R. and Polacheck, I. 1993 Synthesis and Antifungal Activity of Medicagenic Acid Saponins on Plant Pathogens: Modification of the Saccharide Moiety and the 23 Alpha Substitution. Carbohydr. Res. 244(1): 161 – 169

doi: 10.1016/0008-6215(93)80012-4

Zehavi, U., Levy, M. and Segal, R. 2008 Fungistatic Activity of Saponin A from Styrax officinalis L. on Plant Pathogens. J. Phytopath. 116(4): 338 – 343

doi: 10.1111/j.1439-0434.1986.tb00929.x

Leave a Reply

Fill in your details below or click an icon to log in:

WordPress.com Logo

You are commenting using your WordPress.com account. Log Out /  Change )

Google photo

You are commenting using your Google account. Log Out /  Change )

Twitter picture

You are commenting using your Twitter account. Log Out /  Change )

Facebook photo

You are commenting using your Facebook account. Log Out /  Change )

Connecting to %s