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Highly Glycosylated Flavonols at the Genistoid Boundary and The

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Highly Glycosylated Flavonols at the Genistoid Boundary and The South African Journal of Botany 89 (2013) 181–187 Contents lists available at ScienceDirect South African Journal of Botany journal homepage: www.elsevier.com/locate/sajb Highly glycosylated flavonols at the genistoid boundary and the systematic position of Dermatophyllum G.C. Kite a,⁎, N.C. Veitch a, M. Soto-Hernández b, G.P. Lewis a a Royal Botanic Gardens, Kew, Richmond, Surrey TW9 3AB, UK b Colegio de Postgraduados, Campus Montecillo, Texcoco, Estado de México 56230, Mexico article info abstract Available online 1 July 2013 Among papilionoid legumes known to express the phenotype of quinolizidine alkaloid production, only Dermatophyllum occurs outside of the genistoid clade in phylogenetic analyses of DNA sequence data. Analysis Edited by B-E Van Wyk of the foliar flavonoid glycosides of Dermatophyllum and possibly related clades, by liquid chromatography-UV spectrophotometry-mass spectrometry, revealed that taxa sampled from Dermatophyllum, Amphimas and Keywords: the Cladrastis, lecointeoid and vataireoid clades contained mostly flavonol O-glycosides whereas taxa sampled Leguminosae from early-branching genistoid clades, the Andira clade and Aldina contained mostly flavone C-glycosides. Dermatophyllum Furthermore, leaves of Dermatophyllum secundiflorum and Dermatophyllum arizonicum contained, as their Calia fl fl α → α Genistoids main avonoids, two highly glycosylated avonols: kaempferol 3-O- -rhamnopyranosyl(1 2)[ - Flavonol glycosides rhamnopyranosyl(1 → 6)]-β-galactopyranoside-7-O-α-rhamnopyranoside and its quercetin analogue. These compounds also occurred in Cladrastis kentukea, Styphnolobium japonicum and Pickeringia montana in the Cladrastis clade, Uribea tamarindoides and some samples of Zollernia in the lecointeoid clade, and in Amphimas pterocarpoides (another genus of uncertain relationships). The alkaloid and flavonoid pheno- types of Dermatophyllum each suggest affinities to different groups — aconflict which is accommodated by the current phylogenetic hypothesis, based on molecular data, that the genus is a possible sister to the genistoid clade but not a member of it. © 2013 SAAB. Published by Elsevier B.V. All rights reserved. 1. Introduction et al., 2011). Quinolizidine alkaloids have been reported in leaves, stems, roots and seeds of Dermatophyllum secundiflorum (Ortega) Within Leguminosae subfamily Papilionoideae, phylogenetic anal- Gandhi & Reveal (Chavez and Sullivan, 1984; García-Mateos et al., yses of DNA sequence data (‘molecular analyses’) have generally re- 2007; Izaddoost et al., 1976; Ketter, 1975) and recently in leaves of solved a well-supported genistoid clade (Cardoso et al., 2012; Doyle Dermatophyllum arizonicum (S. Watson) Vincent and Dermatophyllum et al., 1997; Pennington et al., 2001; Wojciechowski et al., 2004). Stud- gypsophilum (B.L. Turner & A.M. Powell) Vincent (Lee et al., 2013). ies on the chemistry of members of this clade suggest that they share In molecular analyses to date, Dermatophyllum has been placed close the common phenotype of quinolizidine alkaloid production, except to the genistoid clade of other quinolizidine alkaloid-containing taxa for some genera in tribes Crotalarieae and Genisteae which instead but never within it. Initial trnL sequence analyses placed the genus produce pyrrolizidine alkaloids (Van Wyk, 2003). Although legume among several unresolved sister groups to the genistoids (Pennington taxa outside of the genistoid clade may possess the genes for et al., 2001). A subsequent matK analysis provided resolution of some quinolizidine alkaloid synthesis (Wink and Mohamed, 2003), only of these potential sister groups and placed members of the lecointeoid one genus, Dermatophyllum, is known to produce these metabolites clade between the genistoid clade (and other unresolved groups) and (García-Mateos et al., 2007; Ketter, 1975; Lee et al., 2013). Reports Dermatophyllum, although with only moderate support (Wojciechowski of other legume taxa outside of the genistoid clade accumulating et al., 2004). In the most recent family-wide analysis of matK sequence quinolizidine alkaloids have proved to be erroneous (Kite and data, which included increased sampling among taxa in the boundary Pennington, 2003). between the genistoid clade and related groups, phylogenetic resolution Dermatophyllum Scheele, formerly segregated as Calia Terán & again collapsed and Dermatophyllum was a monogeneric group among Berland from Sophora sensu lato, is a genus of four species of trees several well-supported but unresolved clades that comprised the large and shrubs occurring from south-western USA to Mexico (Gandhi unresolved 50 kb-inversion clade (containing most papilionoid le- gumes); this clade also included Amphimas Pierre ex Harms and Aldina Endl. as the two further unresolved genera (Cardoso et al., 2012). The ⁎ Corresponding author. Tel.: +44 208 332 5368; fax: +44 208 332 5310. similarity in alkaloid chemistry between Dermatophyllum and the E-mail address: [email protected] (G.C. Kite). genistoid clade, and the poor support in molecular data separating 0254-6299/$ – see front matter © 2013 SAAB. Published by Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.sajb.2013.06.003 182 G.C. Kite et al. / South African Journal of Botany 89 (2013) 181–187 them, creates uncertainty in the placement of Dermatophyllum within analogue, quercetin 3-O-α-rhamnopyranosyl(1 → 2)[α-rhamnopy- the papilionoid phylogeny. ranosyl(1 → 6)]-β-glucopyranoside-7-O-α-rhamnopyranoside (4), A new line of enquiry, using chemical characters, on the relation- was again isolated from leaves of S. japonicum (Kite et al., 2007). ships of Dermatophyllum was recently suggested following the de- Analysis by liquid chromatography-UV spectrophotometry-mass tection of highly glycosylated flavonols in leaves of D. secundiflorum spectrometry (LC-UV-MS) has shown that leaves of C. kentukea con- (Barrón-Yánez et al., 2011). These compounds were examples of tain all of 1–4 (Kite et al., 2011), so for convenience we will refer to tetraglycosides of kaempferol and quercetin bearing a branched tri- flavonol tetraglycosides with this glycosylation pattern as Cladrastis- saccharide at C-3 (glucose or galactose with both a (1 → 2) and a type highly glycosylated flavonols (CHGFs). (1 → 6) terminally linked rhamnose) and a rhamnose at C-7 (Fig. 1). To understand further the significance of the occurrence of CHGFs Although not particularly unusual in structural terms, flavonols with in Dermatophyllum, we have carried out a survey of the flavonoid these glycosylation patterns have not been widely reported in glycosides of 28 taxa selected from across the genistoid boundary; plants, indeed the first records were from legumes placed close to i.e. early-branching taxa of the genistoid clade and taxa from po- Dermatophyllum in molecular analyses. Kaempferol 3-O-α-rhamnopy- tential sister groups of the genistoid clade. Leaf extracts were ana- ranosyl(1 → 2)[α-rhamnopyranosyl(1 → 6)]-β-galactopyranoside-7- lysed by LC-UV-MS specifically for CHGFs 1–4, although the data O-α-rhamnopyranoside (1)wasfirst described from leaves of acquired could also be used to determine the general types of Zollernia ilicifolia (Brongn.) Vogel (Coelho et al., 2003), a member flavonoid glycoside present. While the flavonoid chemistry of of the lecointeoid clade, and the glucose analogue of this com- temperate members of the core genistoids is reasonably well pound, kaempferol 3-O-α-rhamnopyranosyl(1 → 2)[α-rhamnopy- known (e.g. Harborne, 1969), there have been fewer studies of the ranosyl(1 → 6)]-β-glucopyranoside-7-O-α-rhamnopyranoside (2), flavonoids of early-branching genistoid clades, as many are less was described from leaves of Styphnolobium japonicum (L.) Schott readily accessible tropical tree species (Van Wyk, 2003). Tropical (Kite et al., 2007), a member of the Cladrastis clade; these clades are woody taxa are also prevalent among potential sister groups to the the sister groups to Dermatophyllum in the analysis of Wojciechowski genistoid clade (Lewis et al., 2005), and their flavonoid chemistry is et al. (2004). Quercetin 3-O-α-rhamnopyranosyl(1 → 2)[α-rhamnopy- likewise poorly known. Thus the present study also aimed to com- ranosyl(1 → 6)]-β-galactopyranoside-7-O-α-rhamnopyranoside (3) pare the general profile of flavonoid glycosides of early-branching was detected in leaves of Cladrastis kentukea (Dum. Cours.) Rudd genistoids and potential sister groups, including Dermatophyllum. (Kite et al., 2011), although not formally described, while its glucose 2. Materials and methods 2.1. Plant material and sample preparation R 3' CH3 OH Details of the taxa analysed and the source of material are listed in HO 4' the Appendix 1. Dry leaf material (20–100 mg, weighed accurately) O O O HO 7 OH was powdered in a pestle and mortar with sand and transferred to O CH3 an Eppendorf tube. Aqueous 80% methanol was then added (1 μl per HO 3 O OH 5 OH mg of plant material) and the sample was left overnight (ca 18 h) at 7-O-Rha OH O O 1'' 2'' 2''-O-Rha room temperature (ca 22 °C). Following centrifugation, the superna- O OH tant was poured into a second Eppendorf tube and diluted with an Gal OH equal volume of water. After an hour standing at room temperature, CH3 any precipitate that had formed was removed by centrifugation and HO 6'' the supernatant was poured into an autosampler vial for LC–MS 6''-O-Rha O HO O analysis. HO 2.2. Analysis by LC-UV-MS 1 R = H 3 R = OH Samples were analysed using a Thermo Scientific LC-UV-MS system comprising an ‘Accela’ 1290 pump, autosampler and PDA de- R tector interfaced to an ‘LTQ-Orbitrap XL’ hybrid mass spectrometer 3' ‘ ’ CH3 OH via an Ion-Max electrospray source. Separation of the glucose and HO 4' galactose analogues of CHGFs 1 & 3 and 2 & 4 was achieved by O O O performing high resolution chromatography of 2 μl injections on a HO 7 OH O CH3 150 mm × 2.1 mm, 1.9 μm Hypersil GOLD C18 column (Thermo Sci- HO 3 OH fi μ 5 O OH enti c) using a 400 l/min mobile phase gradient of 95:0:5 to 0:95:5 7-O-Rha OH O O water/methanol/acetonitrile + 1% formic acid over 100 min, follow- 1'' 2'' 2''-O-Rha ing 3 min pre-injection equilibration in start conditions.
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