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Fccecd771cdbecfff2f2912320015 International Journal of Molecular Sciences Article Tissue-Specific Accumulation and Isomerization of Valuable Phenylethanoid Glycosides from Plantago and Forsythia Plants Moritz Zürn 1 , Gerg˝oTóth 2 , Tim Ausbüttel 1,3 , Zoltán Mucsi 4, Kata Horváti 5 , Szilvia B˝osze 5 , Magdolna Sütöri-Diószegi 6, Bernadett Pályi 7, Zoltán Kis 7,Béla Noszál 2 and Imre Boldizsár 1,* 1 Department of Plant Anatomy, Institute of Biology, Eötvös Loránd University, Pázmány Péter Sétány 1/C, 1117 Budapest, Hungary; [email protected] (M.Z.); [email protected] (T.A.) 2 Department of Pharmaceutical Chemistry, Semmelweis University, H˝ogyesEndre u. 9, 1092 Budapest, Hungary; [email protected] (G.T.); [email protected] (B.N.) 3 Department of Pharmacognosy, Semmelweis University, Üll˝oi út 26, 1085 Budapest, Hungary 4 Femtonics Ltd., T˝uzoltó u. 59, 1094 Budapest, Hungary; [email protected] 5 Research Group of Peptide Chemistry, Eötvös Loránd University, Eötvös Loránd Research Network (ELKH), Pázmány Péter Sétány 1/A, 1117 Budapest, Hungary; [email protected] (K.H.); [email protected] (S.B.) 6 Department of Floriculture and Dendrology, Faculty of Horticultural Science, Szent István University, Villányi út 29-43, 1119 Budapest, Hungary; [email protected] 7 National Biosafety Laboratory, National Public Health Center, Albert Flórián út 2-6, 1097 Budapest, Hungary; [email protected] (B.P.); [email protected] (Z.K.) * Correspondence: [email protected] Abstract: A comparative phytochemical study on the phenylethanoid glycoside (PhEG) composition Citation: Zürn, M.; Tóth, G.; of the underground organs of three Plantago species (P. lanceolata, P. major, and P. media) and that of the Ausbüttel, T.; Mucsi, Z.; Horváti, K.; fruit wall and seed parts of Forsythia suspensa and F. europaea fruits was performed. The leaves of these B˝osze,S.; Sütöri-Diószegi, M.; Pályi, Forsythia species and six cultivars of the hybrid F. × intermedia were also analyzed, demonstrating the B.; Kis, Z.; Noszál, B.; et al. tissue-specific accumulation and decomposition of PhEGs. Our analyses confirmed the significance Tissue-Specific Accumulation and of selected tissues as new and abundant sources of these valuable natural compounds. The optimized Isomerization of Valuable heat treatment of tissues containing high amounts of the PhEG plantamajoside (PM) or forsythoside Phenylethanoid Glycosides from Plantago and Forsythia Plants. Int. J. A (FA), which was performed in distilled water, resulted in their characteristic isomerizations. In Mol. Sci. 2021, 22, 3880. https:// addition to PM and FA, high amounts of the isomerization products could also be isolated after doi.org/10.3390/ijms22083880 heat treatment. The isomerization mechanisms were elucidated by molecular modeling, and the structures of PhEGs were identified by nuclear magnetic resonance spectroscopy (NMR) and high- Academic Editor: Purusotam Basnet resolution mass spectrometry (HR-MS) techniques, also confirming the possibility of discriminating regioisomeric PhEGs by tandem MS. The PhEGs showed no cytostatic activity in non-human primate Received: 13 March 2021 Vero E6 cells, supporting their safe use as natural medicines and allowing their antiviral potency to Accepted: 7 April 2021 be tested. Published: 9 April 2021 Keywords: Forsythia; Plantago; forsythoside; plantamajoside; acteoside; isomerization; Vero cells Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affil- iations. 1. Introduction To determine the novel plant sources of valuable phenylethanoid glycosides (PhEGs) showing no cytotoxicity against normal cells [1], we investigated various tissues of Plantago and Forsythia species. Copyright: © 2021 by the authors. From the large genus of Plantago (order Lamiales, family Plantaginaceae), comprising Licensee MDPI, Basel, Switzerland. about 200 species, Plantago lanceolata L. (ribwort plantain), P. major L. (broadleaf plantain), This article is an open access article P. media P. lanceolata distributed under the terms and and L. (hoary plantain) were involved in this study. Among them, conditions of the Creative Commons and P. major are widely distributed around the world, while P. media is common in Europe Attribution (CC BY) license (https:// and Asia but also locally in the USA [2]. These herbaceous perennial plants develop an creativecommons.org/licenses/by/ underground rhizome that bears roots, a solitary, erect flower stem, and leaves forming a 4.0/). rosette [3]. Among these three plant species, P. lanceolata and P. major are amongst the most Int. J. Mol. Sci. 2021, 22, 3880. https://doi.org/10.3390/ijms22083880 https://www.mdpi.com/journal/ijms Int. J. Mol. Sci. 2021, 22, x FOR PEER REVIEW 2 of 19 ditions of the Creative Commons At- underground rhizome that bears roots, a solitary, erect flower stem, and leaves forming a tribution (CC BY) license (http://cre- rosette [3]. Among these three plant species, P. lanceolata and P. major are amongst the ativecommons.org/licenses/by/4.0/). most commonly used medicinal herbs in the world. Various extracts of their aerial parts exhibit many beneficial effects on human health, including wound-healing, anti-inflam- matory, antioxidant, and chemopreventive effects [2]. Based on the therapeutic signifi- Int. J. Mol. Sci. 2021, 22, 3880 cance of the P. lanceolata leaf, it is listed as an official drug in the European2 of 18 Pharmacopoeia (Ph. Eur., 10th edition). Furthermore, the leaves of P. lanceolata [4] and P. major [5] are edible and can be used as vegetables. Despite being readily available in the nature, these commonly used medicinal herbs in the world. Various extracts of their aerial parts exhibit two plantain species are also crops cultivated in many countries [4,6]. many beneficial effects on human health, including wound-healing, anti-inflammatory, antioxidant,The genus and chemopreventive Forsythia (order effects Lamiales, [2]. Based onfamily the therapeutic Oleaceae) significance consists of of the about 10 species P.native lanceolata to leaf,eastern it is listed Asia, as with an official the drugsingle in exception the European of Pharmacopoeia F. europaea Degen (Ph. Eur., & Bald, which is 10thnative edition). to southeastern Furthermore, theEurope. leaves ofForsythiaP. lanceolata plants[4] and areP. deciduous major [5] are edibleshrubs and with can opposite leaves beand used yellow as vegetables. flowers Despite blooming being in readily early available spring before in the nature, the appearance these two plantain of leaves. The fruit, if species are also crops cultivated in many countries [4,6]. formed,The genus is a Forsythiacapsule (orderthat, at Lamiales, maturity, family splits Oleaceae) open consiststo release of about its numerous 10 species seeds [7]. Two nativeForsythia to eastern species, Asia, F. with suspensa the single Vahl exception and F. viridissima of F. europaea Lindl.,Degen and & Bald, particularly which is their hybrid F. native× intermedia to southeastern, are widely Europe. cultivatedForsythia plants as areornamentals deciduous shrubs for their with oppositeflowers leaves in temperate zones andworldwide. yellow flowers On bloomingthe contrary, in early F. springeuropaea before is not the commonly appearance of cultivated leaves. The and fruit, can if only be found formed, is a capsule that, at maturity, splits open to release its numerous seeds [7]. Two in special plant collections outside its habitat [7]. In our study, among the Forsythia species, Forsythia species, F. suspensa Vahl and F. viridissima Lindl., and particularly their hybrid F.F.× europaeaintermedia,, F.are suspensa widely cultivated, and F. as× ornamentalsintermedia, forwhich their are flowers also in available temperate zonesin botanical gardens worldwide.in Europe, On were the contrary, studied.F. europaeaThe fruitsis not and commonly leaves cultivated of F. suspensa and can have only bebeen found used for centuries inin special eastern plant medicine: collections the outside fruits its habitatas anti-inflamma [7]. In our study,tory among and thediureticForsythia agentsspecies, and the leaves as × F.health europaea tea, F. for suspensa colds, and [8].F. Theintermedia fruits are, which also listed are also as available an official in botanical drug in gardens the Chinese, Japanese, in Europe, were studied. The fruits and leaves of F. suspensa have been used for centuries inand eastern Korean medicine: Pharmacopoeias the fruits as anti-inflammatory [9]. and diuretic agents and the leaves as health teaThe for PhEG colds [8acteoside]. The fruits (AO) are also is listeda chemotaxon as an officialomic drug inmarker the Chinese, compound Japanese, of the order La- andmiales Korean [10]. Pharmacopoeias Thus, this compound [9]. is also present in many species of the genera Plantago andThe Forsythia PhEG acteoside. Structurally, (AO) is aAO chemotaxonomic consists of a marker centrally compound positioned of the β order-D-glucose Lami- that is linked ales [10]. Thus, this compound is also present in many species of the genera Plantago and Forsythiaat its C1,. Structurally, C3, and C4 AO hydroxyl consists of groups a centrally to hydroxytyrosol, positioned β-D-glucose α-L-rhamnose, that is linked and caffeic acid atunits, its C1, respectively. C3, and C4 hydroxyl Some groupsLamiales to hydroxytyrosol, plants also containα-L-rhamnose, (i) isomers and caffeic of AO, acid such as isoacteo- units,side respectively.(IsoAO), forsythoside
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