Anti-phytopathogen terpenoid glycosides from the root bark of Chytranthus macrobotrys and Radlkofera calodendron

Antimicrobials; Chytranthus macrobotrys; Esca disease; Farnesyl glycosides; Radlkofera calodendron; Sapindaceae; Triterpene saponins; Xylella fastidiosa

Abstract :

[en] Chytranthus macrobotrys and Radlkofera calodendron are two Sapindaceae characterized by a lack of phytochemical data. Both root barks from the two Sapindaceae species were processed by ethanol extraction followed by the isolation of their primary constituents by liquid chromatography. This process yielded four previously undescribed terpenoid glycosides together with eight known analogues. Extracts and isolated compounds from C. macrobotrys and R. calodendron were then screened for antimicrobial activity against fifteen phytopathogens. The biological screening also involved extracts and pure compounds from Blighia unijugata and Blighia welwitschii, two Sapindaceae previously studied by our group. Phytopathogens were chosen based on their economic impact on agriculture worldwide. The selection was composed primarily of fungal species including; Pyricularia oryzae, Gaeumannomyces graminis var. tritici, Zymoseptoria tritici, Fusarium oxysporum, Botrytis cinerea, Pythium spp., Trichoderma spp. and Rhizoctonia solani. Furthermore, pure terpenoid glycosides were tested for the first time against wood-inhabiting phytopathogens such as; Phaeomoniella chlamydospora, Phaeoacremonium minimum, Fomitiporia mediterranea, Eutype lata and Xylella fastidiosa. Raw extracts exhibited different levels of activity dependent on the organism. Some pure compounds, including 3-O-α-L-arabinopyranosyl-(1 → 4)-β-D-xylopyranosyl-(1 → 3)-α-L-rhamnopyranosyl-(1 → 2)-α-L-arabinopyranosylhederagenin, 3-O-α-L-rhamnopyranosyl-(1 → 2)-α-L-arabinopyranosylhederagenin (α-hederin), 3-O-β-D-glucopyranosyl-(1 → 3)-α-L-rhamnopyranosyl-(1 → 2)-α-L-arabinopyranosylhederagenin (macranthoside A) and 3-O-α-L-arabinopyranosyl-(1 → 3)-α-L-rhamnopyranosyl-(1 → 2)-α-L-arabinopyranosylhederagenin (clemontanoside C), exhibited significant growth inhibitions on Pyricularia oryzae, Gaeumannomyces graminis var. tritici, Fomitiporia mediterranea and Zymoseptoria tritici. Monodesmoside triterpene saponins, in particular, exhibited MIC (IC100) values as low as 25 μg/ml and IC50 values as low as 10 μg/ml against these phytopathogens. Structure-activity relationships, as well as plant-microbe interactions, were discussed.

Disciplines :

Pharmacy, pharmacology & toxicology

Author, co-author :

Petit, Bastien; Université de Bourgogne Franche-Comté

Mitaine-Offer, Anne-Claire; Université de Bourgogne Franche-Comté

Fischer, Jochen; Institut für Biotechnologie und Wirkstoff-Forschung

Schüffler, Anja; Institut für Biotechnologie und Wirkstoff-Forschung

Delaude, Clément ; Université de Liège - ULiège > Institut de chimie

Miyamoto, Tomofumi; Kyushu University

Tanaka, Chiaki; Kyushu University

Thines, Eckhard; Institut für Biotechnologie und Wirkstoff-Forschung

Lacaille-Dubois, Marie-Aleth; Université de Bourgogne Franche-Comté

Language :

English

Title :

Anti-phytopathogen terpenoid glycosides from the root bark of Chytranthus macrobotrys and Radlkofera calodendron

Publication date :

2021

Journal title :

Phytochemistry

ISSN :

0031-9422

eISSN :

1873-3700

Publisher :

Elsevier, Netherlands

Volume :

188

Pages :

112797

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 05 January 2022

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Bibliography

Abbruscato, P., Tosi, S., Crispino, L., Biazzi, E., Menin, B., Picco, A.M., Pecetti, L., Avato, P., Tava, A., Triterpenoid glycosides from Medicago sativa as antifungal agents against Pyricularia oryzae. J. Agric. Food Chem. 62 (2014), 11030–11036, 10.1021/jf5049063.
Adesanya, S.A., Martin, M.-T., Hill, B., Dumontet, V., Tri, M.V., Sévenet, T., Paıs, M., Rubiginoside, a farnesyl glycoside from Lepisanthes rubiginosa. Phytochemistry 51 (1999), 1039–1041, 10.1016/s0031-9422(98)00701-8.
Adeyemi, T.O., Ogundipe, O.T., Olowokudejo, J.D., Distribution and DNA conservation of Sapindaceae juss. In western africa. Int. J. Bot. 8 (2012), 31–37, 10.3923/ijb.2012.31.37.
Avato, P., Bucci, R., Tava, A., Vitali, C., Rosato, A., Bialy, Z., Jurzysta, M., Antimicrobial activity of saponins from Medicago sp.: structure-activity relationship. Phytother Res. 20 (2006), 454–457, 10.1002/ptr.1876.
Barile, E., Bonanomi, G., Antignani, V., Zolfaghari, B., Sajjadi, S.E., Scala, F., Lanzotti, V., Saponins from Allium minutiflorum with antifungal activity. Phytochemistry 68 (2007), 596–603, 10.1016/j.phytochem.2006.10.009.
Biang, A.E.M., Kamto, E.L.D., Simo, L.M., Antheaume, C., Lavedan, P., Vedrenne, M., Noté, O.P., Pegnyemb, D.E., Mbing, J.N., Haddad, M., Triterpenoid saponins from the stem barks of Chytranthus klaineanus Radlk. ex Engl. Phytochem. Lett. 37 (2020), 37–41, 10.1016/j.phytol.2020.04.006.
Bouarab, K., Melton, R., Peart, J., Baulcombe, D., Osbourn, A.E., A saponin-detoxifying enzyme mediates suppression of plant defences. Nature 418 (2002), 889–892, 10.1038/nature00950.
Braca, A., Autore, G., Simone, F.D., Marzocco, S., Morelli, I., Venturella, F., Tommasi, N.D., Cytotoxic saponins from Schefflera rotundifolia. Planta Med. 70 (2004), 960–966, 10.1055/s-2004-832623.
Buerki, S., Forest, F., Acevedo-Rodríguez, P., Callmander, M.W., Nylander, J.A.A., Harrington, M., Sanmartín, I., Küpfer, P., Alvarez, N., Plastid and nuclear DNA markers reveal intricate relationships at subfamilial and tribal levels in the soapberry family (Sapindaceae). Mol. Phylogenet. Evol. 51 (2009), 238–258, 10.1016/j.ympev.2009.01.012.
Cobos, R., Mateos, R.M., Álvarez-Pérez, J.M., Olego, M.A., Sevillano, S., González-García, S., Garzón-Jimeno, E., Coque, J.J.R., Effectiveness of natural antifungal compounds in controlling infection by grapevine trunk disease pathogens through pruning wounds. Appl. Environ. Microbiol. 81 (2015), 6474–6483, 10.1128/AEM.01818-15.
Delaude, C., Chemical study of the saponins of Sapindaceae. Identification of the saponin of Radlkofera calodendra. Bull. Soc. R. Sci. Liege 43 (1974), 693–696.
Delaude, C., Breyne, H., Welter, A., Contribution to the study of saponins contained in Sapindaceae. Study of the saponoside from Chytranthus macrobotrys (Gilg.) Exell & Mendonça and Lecaniodiscus cupanoides. Planch. Bull. Soc. R. Sci. Liège 45 (1976), 458–461.
Dong, S., Yang, X., Zhao, L., Zhang, F., Hou, Z., Xue, P., Antibacterial activity and mechanism of action saponins from Chenopodium quinoa Willd. husks against foodborne pathogenic bacteria. Ind. Crop. Prod., 149, 2020, 112350, 10.1016/j.indcrop.2020.112350.
Ekabo, O.A., Farnsworth, N.R., Henderson, T.O., Mao, G., Mukherjee, R., Antifungal and molluscicidal saponins from Serjania salzmanniana. J. Nat. Prod. 59 (1996), 431–435, 10.1021/np960208r.
Encarnación, R., Kenne, L., Samuelsson, G., Sandberg, F., Structural studies on some saponins from Lecaniodiscus cupanioides. Phytochemistry 20 (1981), 1939–1942, 10.1016/0031-9422(81)84039-3.
Faleye, F.J., Ajayi, C.B., Antioxidant potentials of the methanol seed and leaves extracts of Chytranthus macrobotrys (Gilg.) Exell & Mendonça. J. Chem. Biol. Phys. Sci. 8 (2018), 475–481, 10.24214/jcbps.B.8.2.47581.
Faleye, F.J., Ajayi, C.B., Akinwumi, O.A., Popoola, O.K., Evaluation of methanolic extract of Chytranthus macrobotrys seed (cms) for antimicrobial, α-glucosidase and α-amylase inhibitory activities. Int. J. Pharma Sci. Res. 10 (2019), 678–685, 10.13040/IJPSR.0975-8232.10(2).678-85.
Hara, S., Okabe, H., Mihashi, K., Gas-liquid chromatographic separation of aldose enantiomers as trimethylsilyl ethers of methyl 2- (polyhydroxyalkyl) -thiazolidine-4 (R) -carboxylates. Chem. Pharm. Bull. 35 (1987), 501–506, 10.1248/cpb.35.501.
Harrington, M., Edwards, K., Johnson, S., Chase, M., Gadek, P., Phylogenetic inference in Sapindaceae sensu lato using plastid matk and rbcl DNA sequences. Syst. Bot. 30 (2005), 366–382, 10.1600/0363644054223549.
Hernández-Montelongo, J., Nascimento, V.F., Murillo, D., Taketa, T.B., Sahoo, P., de Souza, A.A., Beppu, M.M., Cotta, M.A., Nanofilms of hyaluronan/chitosan assembled layer-by-layer: an antibacterial surface for Xylella fastidiosa. Carbohydr. Polym. 136 (2016), 1–11, 10.1016/j.carbpol.2015.08.076.
Hu, Q., Chen, Y.-Y., Jiao, Q.-Y., Khan, A., Li, F., Han, D.-F., Cao, G.-D., Lou, H.-X., Triterpenoid saponins from the pulp of Sapindus mukorossi and their antifungal activities. Phytochemistry 147 (2018), 1–8, 10.1016/j.phytochem.2017.12.004.
Ishii, H., Kitagawa, I., Matsushita, K., Shirakawa, K., Tori, K., Tozyo, T., Yoshikawa, M., Yoshimura, Y., The configuration and conformation of the arabinose moiety in platycodins, saponins isolated from Platycodon grandiflorum, and mi-saponins from Madhuca longifolia based on carbon-13 and hydrogen-1 nmr spectroscopic evidence: the total structures of the saponins. Tetrahedron Lett. 22 (1981), 1529–1532, 10.1016/S0040-4039(01)90369-7.
Kasai, R., Fujino, H., Kuzuki, T., Wong, W.-H., Goto, C., Yata, N., Tanaka, O., Yasuhara, F., Yamaguchi, S., Acyclic sesquiterpene oligoglycosides from pericarps of Sapindus mukurossi. Phytochemistry 25 (1986), 871–876, 10.1016/0031-9422(86)80019-X.
Kim, B., Han, J.W., Thi Ngo, M., Le Dang, Q., Kim, J.-C., Kim, H., Choi, G.J., Identification of novel compounds, oleanane- and ursane-type triterpene glycosides, from Trevesia palmata: their biocontrol activity against phytopathogenic fungi. Sci. Rep., 8, 2018, 14522, 10.1038/s41598-018-32956-4.
Lacaille-Dubois, M.-A., Delaude, C., Mitaine-Offer, A.-C., Triterpenoid saponins: a focus on Polygalaceae. Natural Products, 2013, Springer, Berlin, Heidelberg, 3205–3223.
Lavaud, C., Crublet, M.-L., Pouny, I., Litaudon, M., Sévenet, T., Triterpenoid saponins from the stem bark of Elattostachys apetala. Phytochemistry 57 (2001), 469–478, 10.1016/s0031-9422(01)00063-2.
Lunga, P.K., Qin, X.-J., Yang, X.W., Kuiate, J.-R., Du, Z.Z., Gatsing, D., Antimicrobial steroidal saponin and oleanane-type triterpenoid saponins from Paullinia pinnata. BMC Compl. Alternative Med., 14, 2014, 369, 10.1186/1472-6882-14-369.
Maddox, C.E., Laur, L.M., Tian, L., Antibacterial activity of phenolic compounds against the phytopathogen Xylella fastidiosa. Curr. Microbiol. 60 (2009), 53–58, 10.1007/s00284-009-9501-0.
Magid, A.A., Voutquenne-Nazabadioko, L., Litaudon, M., Lavaud, C., Acylated farnesyl diglycosides from Guioa crenulata. Phytochemistry 66 (2005), 2714–2718, 10.1016/j.phytochem.2005.09.009.
Mandal, P., Sinha Babu, S.P., Mandal, N.C., Antimicrobial activity of saponins from Acacia auriculiformis. Fitoterapia 76 (2005), 462–465, 10.1016/j.fitote.2005.03.004.
Mazzola, E.P., Parkinson, A., Kennelly, E.J., Coxon, B., Einbond, L.S., Freedberg, D.I., Utility of coupled-hsqc experiments in the intact structural elucidation of three complex saponins from Blighia sapida. Carbohydr. Res. 346 (2011), 759–768, 10.1016/j.carres.2011.02.019.
Mimaki, Y., Yokosuka, A., Hamanaka, M., Sakuma, C., Yamori, T., Sashida, Y., Triterpene saponins from the roots of Clematis chinensis. J. Nat. Prod. 67 (2004), 1511–1516, 10.1021/np040088k.
Njateng, G.S.S., Du, Z., Gatsing, D., Nanfack Donfack, A.R., Feussi Talla, M., Kamdem Wabo, H., Tane, P., Mouokeu, R.S., Luo, X., Kuiate, J.-R., Antifungal properties of a new terpernoid saponin and other compounds from the stem bark of Polyscias fulva Hiern (Araliaceae). BMC Compl. Alternative Med., 15, 2015, 25, 10.1186/s12906-015-0541-7.
Osbourn, A.E., Saponins in cereals. Phytochemistry 62 (2003), 1–4, 10.1016/s0031-9422(02)00393-x.
Osbourn, A.E., Clarke, B.R., Lunness, P., Scott, P.R., Daniels, M.J., An oat species lacking avenacin is susceptible to infection by Gaeumannomyces graminis var. tritici. Physiol. Mol. Plant Pathol. 45 (1994), 457–467, 10.1016/s0885-5765(05)80042-6.
Pensec, F., Les triterpénoïdes chez la vigne: quantifications, voies de biosynthèse et intérêt pour la lutte contre des bioagresseurs. Sciences agricoles. 2013, Université de Haute Alsace – Mulhouse.
Pertuit, D., Mitaine-Offer, A.-C., Miyamoto, T., Tanaka, C., Delaude, C., Lacaille-Dubois, M.-A., Terpenoid glycosides from the root's barks of Eriocoelum microspermum Radlk. ex Engl. Phytochemistry 152 (2018), 182–190, 10.1016/j.phytochem.2018.04.009.
Petit, B., Mitaine-Offer, A.-C., Delaude, C., Miyamoto, T., Tanaka, C., Lacaille-Dubois, M.-A., Hederagenin glycosides from the fruits of Blighia unijugata. Phytochemistry 162 (2019), 260–269, 10.1016/j.phytochem.2019.03.020.
Petit, B., Mitaine-Offer, A.-C., Real Fernandez, F., Papini, A.M., Delaude, C., Miyamoto, T., Tanaka, C., Rovero, P., Lacaille-Dubois, M.-A., Triterpene glycosides from Blighia welwitschii and evaluation of their antibody recognition capacity in multiple sclerosis. Phytochemistry, 176, 2020, 112392, 10.1016/j.phytochem.2020.112392.
Porsche, F.M., Molitor, D., Beyer, M., Charton, S., André, C., Kollar, A., Antifungal activity of saponins from the fruit pericarp of Sapindus mukorossi against Venturia inaequalis and Botrytis cinerea. Plant Dis. 102 (2018), 991–1000, 10.1094/pdis-06-17-0906-re.
Rezgui, A., Mitaine-Offer, A.-C., Miyamoto, T., Tanaka, C., Delemasure, S., Dutartre, P., Lacaille-Dubois, M.-A., Oleanolic acid and hederagenin glycosides from Weigela stelzneri. Phytochemistry 123 (2016), 40–47, 10.1016/j.phytochem.2015.12.016.
Roblin, G., Luini, E., Fleurat-Lessard, P., Larignon, P., Berjeaud, J.-M., Towards a preventive and/or curative treatment of esca in grapevine trunk disease: general basis in the elaboration of treatments to control plant pathogen attacks. Crop Protect. 116 (2019), 156–169, 10.1016/j.cropro.2018.10.016.
Saboora, A., Sajjadi, S.-T., Mohammadi, P., Fallahi, Z., Antibacterial activity of different composition of aglycone and glycosidic saponins from tuber of Cyclamen coum Miller. Ind. Crop. Prod., 140, 2019, 111662, 10.1016/j.indcrop.2019.111662.
Saha, S., Walia, S., Kumar, J., Parmar, B.S., Structure-biological activity relationships in triterpenic saponins: the relative activity of protobassic acid and its derivatives against plant pathogenic fungi. Pest Manag. Sci. 66 (2010), 825–831, 10.1002/ps.1947.
Saito, S., Sumita, S., Tamura, N., Nagamura, Y., Nishida, K., Ito, M., Ishiguro, I., Saponins from the leaves of Aralia elata seem. Araliaceae. Chem. Pharm. Bull. 38 (1990), 411–414, 10.1248/cpb.38.411.
Santiago, M.B., Moraes, T. da S., Massuco, J.E., Silva, L.O., Lucarini, R., Silva, D.F. da, Vieira, T.M., Crotti, A.E.M., Martins, C.H.G., In vitro evaluation of essential oils for potential antibacterial effects against Xylella fastidiosa. J. Phytopathol. 166 (2018), 790–798, 10.1111/jph.12762.
Santos, C., Fragoeiro, S., Oliveira, H., Phillips, A., Response of Vitis vinifera L. plants inoculated with Phaeoacremonium angustius and Phaeomoniella chlamydospora to thiabendazole, resveratrol and sodium arsenite. Sci. Hortic. 107 (2006), 131–136, 10.1016/j.scienta.2005.04.015.
The Angiosperm Phylogeny Group. An update of the angiosperm phylogeny group classification for the orders and families of flowering plants: APG IV. Bot. J. Linn. Soc. 181 (2016), 1–20, 10.1111/boj.12385.
Voutquenne, L., Guinot, P., Thoison, O., Sevenet, T., Lavaud, C., Oleanolic glycosides from Pometia ridleyi. Phytochemistry 64 (2003), 781–789, 10.1016/s0031-9422(03)00380-7.
Yu, Q.-T., Qi, L.-W., Li, P., Yi, L., Zhao, J., Bi, Z., Determination of seventeen main flavonoids and saponins in the medicinal plant huang-qi (Radix astragali) by hplc-dad-elsd. J. Separ. Sci. 30 (2007), 1292–1299, 10.1002/jssc.200600422.